Skip to main content
Log in

Formation of Supplementary Metal-Binding Centers in Proteins under Stress Conditions

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

In many proteins, supplementary metal-binding centers appear under stress conditions. They are known as aberrant or atypical sites. Physico-chemical properties of proteins are significantly changed after such metal binding, and very stable protein aggregates are formed, in which metals act as “cross-linking” agents. Supplementary metal-binding centers in proteins often arise as a result of posttranslational modifications caused by reactive oxygen and nitrogen species and reactive carbonyl compounds. New chemical groups formed as a result of these modifications can act as ligands for binding metal ions. Special attention is paid to the role of cysteine SH-groups in the formation of supplementary metal-binding centers, since these groups are the main target for the action of reactive species. Supplementary metal binding centers may also appear due to unmasking of amino acid residues when protein conformation changing. Appearance of such centers is usually considered as a pathological process. Such unilateral approach does not allow to obtain an integral view of the phenomenon, ignoring cases when formation of metal complexes with altered proteins is a way to adjust protein properties, activity, and stability under the changed redox conditions. The role of metals in protein aggregation is being studied actively, since it leads to formation of non-membranous organelles, liquid condensates, and solid conglomerates. Some proteins found in such aggregates are typical for various diseases, such as Alzheimer’s and Huntington’s diseases, amyotrophic lateral sclerosis, and some types of cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Abbreviations

α-Syn:

alpha-synuclein

AD:

Alzheimer’s disease

ADAM10:

a disintegrin and metalloproteinase domain-containing protein 10

ALS:

amyotrophic lateral sclerosis

APP:

amyloid-beta precursor protein

Hb:

hemoglobin

Lb:

leghemoglobin

Mb:

myoglobin

MT3:

metallothionein 3

DNICs:

dinitrosyl iron complexes

PD:

Parkinson’s disease

RNS:

reactive nitrogen species

ROS:

reactive oxygen species

SOD1:

copper-zinc superoxide dismutase 1

References

  1. Dutta, A., and Bahar, I. (2010) Metal-binding sites are designed to achieve optimal mechanical and signaling properties, Structure, 18, 1140-1148, https://doi.org/10.1016/j.str.2010.06.013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Wong, B. S., Chen, S. G., Colucci, M., Xie, Z., Pan, T., Liu, T., Li, R., Gambetti, P., Sy, M. S., and Brown, D. R. (2001) Aberrant metal binding by prion protein in human prion disease, J. Neurochem., 78, 1400-1408, https://doi.org/10.1046/j.1471-4159.2001.00522.x.

    Article  CAS  PubMed  Google Scholar 

  3. Leal, S. S., Cristóvão, J. S., Biesemeier, A., Cardoso, I., and Gomes, C. M. (2015) Aberrant zinc binding to immature conformers of metal-free copper-zinc superoxide dismutase triggers amorphous aggregation, Metallomics, 7, 333-346, https://doi.org/10.1039/C4MT00278D.

    Article  CAS  PubMed  Google Scholar 

  4. Kosmachevskaya, O. V., and Topunov, A. F. (2018) Alternate and additional functions of erythrocyte hemoglobin, Biochemistry (Moscow), 83, 1575-1593, https://doi.org/10.1134/S0006297918120155.

    Article  CAS  PubMed  Google Scholar 

  5. Pieniazek, A., and Gwozdzinski, K. (2015) Changes in the conformational state of hemoglobin in hemodialysed patients with chronic renal failure, Oxid. Med. Cell. Longev., 2015, e783073, https://doi.org/10.1155/2015/783073.

    Article  Google Scholar 

  6. Pieniazek, A., Gwozdzinski, L., Zbrog, Z., and Gwozdzinski, K. (2018) Alterations in conformational state of albumin in plasma in chronic hemodialyzed patients, PLoS One, 13, e0192268, https://doi.org/10.1371/journal.pone.0192268.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Harding, M. M. (2004) The architecture of metal coordination groups in proteins, Acta Crystallogr. D Biol. Crystallogr., 60, 849-859, https://doi.org/10.1107/S0907444904004081.

    Article  CAS  PubMed  ADS  Google Scholar 

  8. Schipper, H. M. (2009) Metal accumulation during aging, Encyclopedia Neurosci., 5, 811-818, https://doi.org/10.1016/B978-008045046-9.00132-7.

    Article  Google Scholar 

  9. Mezzaroba, L., Alfieri, D. F., Simão, A. N. C., and Reiche, E. M. V. (2019) The role of zinc, copper, manganese and iron in neurodegenerative diseases, Neurotoxicology, 74, 230-241, https://doi.org/10.1016/j.neuro.2019.07.007.

    Article  CAS  PubMed  Google Scholar 

  10. Kothapalli, C. R. (2021) Differential impact of heavy metals on neurotoxicity during development and in aging central nervous system, Curr. Opin. Toxicol., 26, 33-38, https://doi.org/10.1016/j.cotox.2021.04.003.

    Article  CAS  Google Scholar 

  11. Vielee, S. T., and Wise, J. P., Jr. (2023) Among gerontogens, heavy metals are a class of their own: a review of the evidence for cellular senescence, Brain Sci., 13, e500, https://doi.org/10.3390/brainsci13030500.

    Article  CAS  Google Scholar 

  12. Garipova, M. I., Il’ina, O. S., Butorina, O. L., Veselov, S. Yu., Shigapova, A. I., Novoselova, E. I., Garipov, O. S., Zinatullina, L. G., Tsvetkov, V. O. (2013) A rise in blood total zinc cation concentration and a decline in labile zinc concentration in patients with type I diabetes mellitus [in Russian], Fundamental'nye Issledovaniya, 2013, 368-370.

    Google Scholar 

  13. Wang, R., Long, T., He, J., Xu, Y., Wei, Y., Zhang, Y., He, X., and He, M. (2022) Associations of multiple plasma metals with chronic kidney disease in patients with diabetes, Ecotoxicol. Environ. Saf., 244, e114048, https://doi.org/10.1016/j.ecoenv.2022.114048.

    Article  CAS  Google Scholar 

  14. Shumaev, K. B., Kosmachevskaya, O. V., Timoshin, A. A., Vanin, A. F., and Topunov, A. F. (2008) Dinitrosyl iron complexes bound with haemoglobin as markers of oxidative stress, Methods Enzymol., 436, 445-461, https://doi.org/10.1016/S0076-6879(08)36025-X.

    Article  CAS  PubMed  Google Scholar 

  15. Shumaev, K. B., Gubkin, A. A., Serezhenkov, V. A., Lobysheva, I. I., Kosmachevskaya, O. V., Ruuge, E. K., Lankin, V. Z., Topunov, A. F., and Vanin, A. F. (2008) Interaction of reactive oxygen and nitrogen species with albumin – and hemoglobin bound dinitrosyl iron complexes, Nitric Oxide, 18, 37-46, https://doi.org/10.1016/j.niox.2007.09.085.

    Article  CAS  PubMed  Google Scholar 

  16. Kosmachevskaya, O. V., Nasybullina, E. I., Shumaev, K. B., Novikova, N. N., and Topunov, A. F. (2021) Protective effect of dinitrosyl iron complexes bound with hemoglobin on oxidative modification by peroxynitrite, Int. J. Mol. Sci., 22, e13649, https://doi.org/10.3390/ijms222413649.

    Article  CAS  Google Scholar 

  17. Kosmachevskaya, O. V., Nasybullina, E. I., Shumaev, K. B., and Topunov, A. F. (2021) Expressed soybean leghemoglobin: effect on Escherichia coli at oxidative and nitrosative stress, Molecules, 26, e7207, https://doi.org/10.3390/molecules26237207.

    Article  CAS  Google Scholar 

  18. Shumaev, K. B., Petrova, N. E., Zabbarova, I. V., Vanin, A. F., Topunov, A. F., Lankin, V. Z., and Ruuge, E. K. (2004) Interaction of oxoferrylmyoglobin and dinitrosyl-iron complexes, Biochemistry (Moscow), 69, 569-574, https://doi.org/10.1023/B:BIRY.0000029856.67884.c5.

    Article  CAS  PubMed  Google Scholar 

  19. Shumaev, K. B., Kosmachevskaya, O. V., Grachev, D. I., Timoshin, A. A., Topunov, A. F., Lankin, V. Z., and Ruuge, E. K. (2021) A possible mechanism of the antioxidant action of dinitrosyl iron complexes, Biomed. Khim., 15, 313-319, https://doi.org/10.1134/S1990750821040090.

    Article  Google Scholar 

  20. Kosmachevskaya, O. B., Nasybullina, E. I., Shumaev, K. B., Chumikina, L. V., Arabova, L. I., Yaglova, N. V., Obernikhin, S. S., and Topunov, A. F. (2021) Dinitrosyl iron complexes with glutathione ligands intercept peroxynitrite and protect hemoglobin from oxidative modification, Appl. Biochem. Microbiol., 57, 411-420, https://doi.org/10.1134/S0003683821040098.

    Article  CAS  Google Scholar 

  21. Kosmachevskaya, O. V., and Topunov, A. F. (2021) Nonenzymatic reactions in metabolism: their role in evolution and adaptation, Appl. Biochem. Microbiol., 57, 543-555, https://doi.org/10.1134/S0003683821050100.

    Article  CAS  Google Scholar 

  22. Vanin, A. F. (2016) Dinitrosyl iron complexes with thiol-containing ligands as a “working form” of endogenous nitric oxide, Nitric Oxide, 54, 15-29, https://doi.org/10.1016/j.niox.2016.01.006.

    Article  CAS  PubMed  Google Scholar 

  23. Hsiao, H. Y., Chung, C. W., Santos, J. H., Villaflores, O. B., and Lu, T. T. (2019) Fe in biosynthesis, translocation, and signal transduction of NO: toward bioinorganic engineering of dinitrosyl iron complexes into NO-delivery scaffolds for tissue engineering, Dalton Trans., 48, 9431-9453, https://doi.org/10.1039/C9DT00777F.

    Article  CAS  PubMed  Google Scholar 

  24. Lobysheva, I. I., Serezhenkov, V. A., and Vanin, A. F. (1999) Interaction of peroxynitrite and hydrogen peroxide with dinitrosyl iron complexes containing thiol ligands in vitro, Biochemistry (Moscow), 64, 153-158.

    CAS  PubMed  Google Scholar 

  25. Shumaev, K. B., Gorudko, I. V., Kosmachevskaya, O. V., Grigoryeva, D. V., Panasenko, O. M., Vanin, A. F., Topunov, A. F., Terekhova, M. S., Sokolov, A. V., Cherenkevich, S. N., and Ruuge, E. K. (2019) Protective effect of dinitrosyl iron complexes with glutathione in red blood cell lysisinduced by hypochlorous acid, Oxid. Med. Cell. Longev., 2019, e2798154, https://doi.org/10.1155/2019/2798154.

    Article  CAS  Google Scholar 

  26. Dudylina, A. L., Ivanova, M. V., Shumaev, K. B., and Ruuge, E. K. (2016) The generation of superoxide radicals by complex III in heart mitochondria and the antioxidant effect of dinitrosyl iron complexes at different partial pressures of oxygen, Biophysics, 61, 257-261, https://doi.org/10.1134/S0006350916020032.

    Article  CAS  Google Scholar 

  27. Vanin, A. F. (2015) Nitrosyl Iron Complexes with Thiol-Containing Ligands: Physical Chemistry, Biology, Medicine [in Russian], Institute of Computer Research, Moscow, 219 p.

  28. Shumaev, K. B., Gubkina, S. A., Vanin, A. F., Burbaev, D. Sh., Mokh, V. P., Topunov, A. V., and Ruuge, E. K. (2013) Formation of a new type of dinitrosyl iron complexes bound to cysteine modified with methylglyoxal, Biophysics, 58, 172-177, https://doi.org/10.1134/S000635091302019X.

    Article  CAS  Google Scholar 

  29. Shumaev, K. B., Kosmachevskaya, O. V., Nasybullina, E. I., Gromov, S. V., Novikov, A. A., and Topunov, A. F. (2017) New dinitrosyl iron complexes bound with physiologically active dipeptide carnosine, J. Biol. Inorg. Chem., 22, 153-160, https://doi.org/10.1007/s00775-016-1418-z.

    Article  CAS  PubMed  Google Scholar 

  30. Shumaev, K. B., Kosmachevskaya, O. V., Nasybullina, E. I., Ruuge, E. K., and Topunov, A. F. (2023) Role of nitric oxide-derived metabolites in reactions of methylglyoxal with lysine and lysine-rich protein leghemoglobin, Int. J. Mol. Sci., 24, e168, https://doi.org/10.3390/ijms24010168.

    Article  CAS  Google Scholar 

  31. Kosmachevskaya, O. V., Nasybullina, E. I., Shumaev, K. B., Novikova, N. N., and Topunov, A. F. (2020) Effect of iron-nitric oxide complexes on the reactivity of hemoglobin cysteines, Appl. Biochem. Microbiol., 56, 512-520, https://doi.org/10.1134/S0003683820050099.

    Article  CAS  Google Scholar 

  32. Brewer, G. J., and Prasad, A. S. (1977) Zinc Metabolism, Current Aspects in Health and Disease, Alan R. Liss Publ., New York, 378 p.

  33. Rifkind, J. M. (1983) Zinc and its role in biology and nutrition, Metal Ions Biol. Systems, 15, 275-309.

    CAS  Google Scholar 

  34. Rifkind, J. M., and Heim, J. M. (1977) Interaction of zinc and hemoglobin: binding of zinc and the oxygen affinity, Biochemistry, 16, 4438-4443, https://doi.org/10.1021/bi00639a017.

    Article  CAS  PubMed  Google Scholar 

  35. Gilman, J. G., and Brewer, G. J. (1978) The oxygen-linked zinc-binding site of human haemoglobin, Biochem. J., 169, 625-632, https://doi.org/10.1042/bj1690625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Oelshlegel, F. J. Jr., Brewer, G. J., Knutsen, C., Prasad, A. S., and Schoomaker, E. B. (1974) Studies on the interaction of zinc with human hemoglobin, Arch. Biochem. Biophys., 163, 742-748, https://doi.org/10.1016/0003-9861(74)90536-0.

    Article  CAS  PubMed  Google Scholar 

  37. Khromova, V. S., and Myshkin, A. E. (2002) Coagulation of zinc-modified hemoglobin, Russ. J. Gen. Chem., 72, 1645-1649, https://doi.org/10.1023/A:1023356221708.

    Article  CAS  Google Scholar 

  38. Cann, J. R. (1964) Kinetics of the reversible reaction of sperm whale myoglobin with zinc, Biochemistry, 3, 714-722, https://doi.org/10.1021/bi00893a020.

    Article  CAS  PubMed  Google Scholar 

  39. Hunter, C. L., Maurus, R., Mauk, M. R., Lee, H., Raver, E. L., Tong, H., Nguyen, N., Smith, M., Brayer, G. D., and Mauk, A. G. (2003) Introduction and characterization of a functionally linked metal ion binding site at the exposed heme edge of myoglobin, Proc. Natl. Acad. Sci. USA, 100, 3647-3652, https://doi.org/10.1073/pnas.0636702100.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  40. Banaszak, L. J., Watson, H. C., and Kendrew, J. C. (1965) The binding of cupric and zinc ions to crystalline sperm whale myoglobin, J. Mol. Biol., 12, 130-137, https://doi.org/10.1016/S0022-2836(65)80287-X.

    Article  CAS  PubMed  Google Scholar 

  41. Lepeshkevich, S. V., and Dzhagarov, B. M. (2009) Effect of zinc and cadmium ions on structure and function of myoglobin, Biochim. Biophys., 1794, 103-109, https://doi.org/10.1016/j.bbapap.2008.09.024.

    Article  CAS  Google Scholar 

  42. Simons, T. J. (1991) Intracellular free zinc and zinc buffering in human red blood cells, J. Membr. Biol., 123, 63-71, https://doi.org/10.1007/BF01993964.

    Article  CAS  PubMed  Google Scholar 

  43. Taylor, J. A., Acharya, J., Pearson, T. C., and Thompson, R. P. (1991) Zinc improves the filterability of sickle erythrocytes at intermediate oxygen partial pressures, Clin. Sci. (Lond), 81, 433-438, https://doi.org/10.1042/cs0810433.

    Article  CAS  PubMed  Google Scholar 

  44. Kruckeber, W. C., Oelshlegel, F. J., Jr., Shore, S. H., Smouse, P. E., and Brewer, G. J. (1977) The effects of zinc on the morphology of sickle red blood cell ghosts as observed by scanning electron microscopy, Res. Exp. Med. (Berl.), 170, 149-159, https://doi.org/10.1007/BF01851386.

    Article  Google Scholar 

  45. Hider, R. C., Ejim, L., Taylor, P. D., Gale, R., Huehns, E., and Porter, J. B. (1990) Facilitated uptake of zinc into human erythrocytes. Relevance to the treatment of sickle-cell anaemia, Biochem. Pharmacol., 39, 1005-1012, https://doi.org/10.1016/0006-2952(90)90278-S.

    Article  CAS  PubMed  Google Scholar 

  46. Son, S. Y., and Yoon, H. C. (2009) Zinc ion-mediated concentration of glycated hemoglobin for electrochemical biosensing, Biochip J., 3, 164-170.

    Google Scholar 

  47. Silva, A. M. N., and Rangel, M. (2022) The (bio)chemistry of non-transferrin-bound iron, Molecules, 27, e1784, https://doi.org/10.3390/molecules27061784.

    Article  CAS  Google Scholar 

  48. Shumaev, K. B., Gubkin, A. A., Gubkina, S. A., Gudkov, L. L., Lakomkin, V. L., Topunov, A. F., Vanin, A. F., and Ruuge, E. K. (2007) Interaction between albumin-bound dinitrosyl iron complexes and reactive oxygen species, Biophysics, 52, 336-339, https://doi.org/10.1134/S0006350907030141.

    Article  Google Scholar 

  49. Bal, W., Sokołowska, M., Kurowska, E., and Faller, P. (2013) Binding of transition metal ions to albumin: sites, affinities and rates, Biochim. Biophys. Acta, 1830, 5444-5455, https://doi.org/10.1016/j.bbagen.2013.06.018.

    Article  CAS  PubMed  Google Scholar 

  50. Al-Harthi, S., Chandra, K., and Jaremko, Ł. (2022) Lipoic acid restores binding of zinc ions to human serum albumin, Front. Chem., 10, e942585, https://doi.org/10.3389/fchem.2022.942585.

    Article  CAS  ADS  Google Scholar 

  51. Bal, W., Christodoulou, J., Sadler, P. J., and Tucker, A. (1998) Multi-metal binding site of serum albumin, J. Inorg. Biochem., 70, 33-39, https://doi.org/10.1016/S0162-0134(98)00010-5.

    Article  CAS  PubMed  Google Scholar 

  52. Blindauer, C. A., Harvey, I., Bunyan, K. E., Stewart, A. J., Sleep, D., Harrison, D. J., Berezenko, S., and Sadler, P. J. (2009) Structure, properties, and engineering of the major zinc binding site on human albumin, J. Biol. Chem., 284, 23116-23124, https://doi.org/10.1074/jbc.M109.003459.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Handing, K. B., van Shabalin, I. G., Kassaar, O., Khazaipoul, S., Blindauer, C. A., Stewart, A. J., Chruszcz, M., and Minor, W. (2016) Circulatory zinc transport is controlled by distinct interdomain sites on mammalian albumins, Chem. Sci., 7, 6635-6648, https://doi.org/10.1039/C6SC02267G.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Fasano, M., Curry, S., Terreno, E., Galliano, M., Fanali, G., Narciso, P., Notari, S., and Ascenzi, P. (2005) The extraordinary ligand binding properties of human serum albumin, IUBMB Life, 57, 787-796, https://doi.org/10.1080/15216540500404093.

    Article  CAS  PubMed  Google Scholar 

  55. Blindauer, C. A., Khazaipoul, S., Yu, R., and Stewart, A. J. (2016) Fatty acid-mediated inhibition of metal binding to the multi-metal site on serum albumin: implications for cardiovascular disease, Curr. Top. Med. Chem., 16, 3021-3032, https://doi.org/10.2174/1568026616666160216155927.

    Article  CAS  PubMed  Google Scholar 

  56. Novikova, N. N., Yakunin, S. N., Koval’chuk, M. V., Yur’eva, E. A., Stepina, N. D., Rogachev, A. V., Kremennaya, M. A., Yalovega, G. E., Kosmachevskaya, O. V., and Topunov, A. F. (2019) Possibilities of X-ray absorption spectroscopy in the total external reflection geometry for studying protein films on liquids, Crystallogr. Rep., 64, 952-957, https://doi.org/10.1134/S1063774519060130.

    Article  CAS  ADS  Google Scholar 

  57. Novikova, N. N., Kovalchuk, M. V., Yurieva, E. A., Konovalov, O. V., Stepina, N. D., Rogachev, A. V., Yalovega, G. E., Kosmachevskaya, O. V., Topunov, A. F., and Yakunin, S. N. (2019) The enhancement of metal-binding properties in hemoglobin: the role of mild damaging factors, J. Phys. Chem. B, 123, 8370-8377, https://doi.org/10.1021/acs.jpcb.9b06571.

    Article  CAS  PubMed  Google Scholar 

  58. Bui, V.-M., Weng, S.-L., Lu, C.-T., Chang, T.-H., Weng, J. T.-Y., and Lee, T.-Y. (2016) SOHsite: incorporating evolutionary information and physicochemical properties to identify protein S-sulfenylation sites, BMC Genomics, 17, e9, https://doi.org/10.1186/s12864-015-2299-1.

    Article  CAS  Google Scholar 

  59. Jia, P. W., Buehler, R. A., Boykins, R. M., Venable, R. M., and Alayash, I. (2007) Structural basis of peroxide mediated changes in human hemoglobin: a novel oxidative pathway, J. Biol. Chem., 282, 4894-4907, https://doi.org/10.1074/jbc.M609955200.

    Article  CAS  PubMed  Google Scholar 

  60. Giles, N. M., Watts, A. B., Giles, G. I., Fry, F. H., Littlechild, J. A., and Jacob, C. (2003) Metal and redox modulation of cysteine protein function, Chem. Biol., 10, 677-693, https://doi.org/10.1016/S1074-5521(03)00174-1.

    Article  CAS  PubMed  Google Scholar 

  61. Bonnet, D., Stevens, J. M., de Sousa, R. A., Sari, M. A., Mansuy, D., and Artaud, I. (2001) New inhibitors of iron-containing nitrile important biological control mechanisms ranging from hydratases, J. Biochem., 130, 227-233, https://doi.org/10.1093/oxfordjournals.jbchem.a002976.

    Article  CAS  PubMed  Google Scholar 

  62. Ge, W., Clifton, I. J., Stok, J. E., Adlington, R. M., Baldwin, J. E., and Rutledge, P. J. (2008) Isopenicillin N-synthase mediates thiolate oxidation to sulfenate in a depsipeptide substrate analogue: implications for oxygen binding and a link to nitrile hydratase? J. Am. Chem. Soc., 130, 10096-10102, https://doi.org/10.1021/ja8005397.

    Article  CAS  PubMed  Google Scholar 

  63. Arakawa, T., Kawano, Y., Katayama, Y., Nakayama, H., Dohmae, N., Yohda, M., and Odaka, M. (2009) Structural basis for catalytic activation of thiocyanate hydrolase involving metal-ligated cysteine modification, J. Am. Chem. Soc., 131, 14838-14843, https://doi.org/10.1021/ja903979s.

    Article  CAS  PubMed  Google Scholar 

  64. Sieracki, N. A., Tian, S., Hadt, R. G., Zhang, J.-L., Woertink, J. S., Nilges, M. J., Sun, F., Solomon, E. I., and Lu, Y. (2014) Copper-sulfenate complex from oxidation of a cavity mutant of Pseudomonas aeruginosa azurin, Proc. Natl. Acad. Sci. USA, 111, 924-929, https://doi.org/10.1073/pnas.1316483111.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  65. Poole, L. B., Karplus, P. A., and Claiborne, A. (2004) Protein sulfenic acids in redox signaling, Annu. Rev. Pharmacol. Toxicol., 44, 325-347, https://doi.org/10.1146/annurev.pharmtox.44.101802.121735.

    Article  CAS  PubMed  Google Scholar 

  66. Martinez, S., Wu, R., Sanishvili, R., Liu, D., and Holz, R. (2014) The active site sulfenic acid ligand in nitrile hydratases can function as a nucleophile, J. Am. Chem. Soc., 136, 1186-1189, https://doi.org/10.1021/ja410462j.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Rubino, F. M. (2021) The redox potential of the β-93-cysteine thiol group in human hemoglobin estimated from in vitro oxidant challenge experiments, Molecules, 26, e2528, https://doi.org/10.3390/molecules26092528.

    Article  CAS  Google Scholar 

  68. Turell, L., Carballal, S., Botti, H., Radi, R., and Alvarez, B. (2009) Oxidation of the albumin thiol to sulfenic acid and its implications in the intravascular compartment, Braz. J. Med. Biol. Res., 42, 305-311, https://doi.org/10.1590/S0100-879X2009000400001.

    Article  CAS  PubMed  Google Scholar 

  69. Nagumo, K., Tanaka, M., Chuang, V. T., Setoyama, H., Watanabe, H., Yamada, N., Kubota, K., Tanaka, M., Matsushita, K., Yoshida, A., Jinnouchi, H., Anraku, M., Kadowaki, D., Ishima, Y., Sasaki, Y., Otagiri, M., and Maruyama, T. (2014) Cys34-cysteinylated human serum albumin is a sensitive plasma marker in oxidative stress-related chronic diseases, PLoS One, 9, e85216, https://doi.org/10.1371/journal.pone.0085216.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  70. Musante, L., Bruschi, M., Candiano, G., Petretto, A., Dimasi, N., Del Boccio, P., Urbani, A., Rialdi, G., and Ghiggeri, G. M. (2006) Characterization of oxidation end product of plasma albumin in vivo, Biochem. Biophys. Res. Commun., 349, 668-673, https://doi.org/10.1016/j.bbrc.2006.08.079.

    Article  CAS  PubMed  Google Scholar 

  71. Terawaki, H., Yoshimura, K., Hasegawa, T, Matsuyama, Y., Negawa, T., Yamada, K., Matsushima, M., Nakayama, M., Hosoya, T., and Era, S. (2004) Oxidative stress is enhanced in correlation with renal dysfunction: examination with the redox state of albumin, Kidney Int., 66, 1988-1993, https://doi.org/10.1111/j.1523-1755.2004.00969.x.

    Article  CAS  PubMed  Google Scholar 

  72. Musante, L., Candiano, G., Petretto, A., Bruschi, M., Dimasi, N., Caridi, G., Pavone, B., Del Boccio, P., Galliano, M., Urbani, A., Scolari, F., Vincenti, F., and Ghiggeri, G. M. (2007) Active focal segmental glomerulosclerosis is associated with massive oxidation of plasma albumin, J. Am. Soc. Nephrol., 8, 799-810, https://doi.org/10.1681/ASN.2006090965.

    Article  CAS  Google Scholar 

  73. Oettl, K., Stadlbauer, V., Petter, F., Greilberger, J., Putz-Bankuti, C., Hallstrom, S., Lackner, C., and Stauber, R. E. (2008) Oxidative damage of albumin in advanced liver disease, Biochim. Biophys. Acta, 1782, 469-473, https://doi.org/10.1016/j.bbadis.2008.04.002.

    Article  CAS  PubMed  Google Scholar 

  74. Spinella, R., Sawhney, R., and Jalan, R. (2016) Albumin in chronic liver disease: structure, functions and therapeutic implications, Hepatol. Int., 10, 124-132, https://doi.org/10.1007/s12072-015-9665-6.

    Article  PubMed  Google Scholar 

  75. Suzuki, E., Yasuda, K., Takeda, N., Sakata, S., Era, S., Kuwata, K., Sogami, M., and Miura, K. (1992) Increased oxidized form of human serum albumin in patients with diabetes mellitus, Diabetes Res. Clin. Pract., 18, 153-158, https://doi.org/10.1016/0168-8227(92)90140-M.

    Article  CAS  PubMed  Google Scholar 

  76. Hayashi, T., Era, S., Kawai, K., Imai, H., Nakamura, K., and Onda, E. (2000) Observation for redox state of human serum and aqueous humor albumin from patients with senile cataract, Pathophysiology, 6, 237-243, https://doi.org/10.1016/S0928-4680(99)00022-X.

    Article  CAS  Google Scholar 

  77. Hayakawa, A., Kuwata, K., Era, S., Sogami, M., Shimonaka, H., Yamamoto, M., Dohi, S., and Hirose, H. (1997) Alteration of redox state of human serum albumin in patients under anesthesia and invasive surgery, J. Chromatogr. B Biomed. Sci. Appl., 698, 27-33, https://doi.org/10.1016/S0378-4347(97)00274-0.

    Article  CAS  PubMed  Google Scholar 

  78. Era, S., Hamaguchi, T., Sogami, M., Kuwata, K., Suzuki, E., Miura, K., Kawai, K., Kitazawa, Y., Okabe, H., Noma, A., and Miyata, S. (1988) Further studies on the resolution of human mercapt- and nonmercaptalbumin and on human serum albumin in the elderly by high-performance liquid chromatography, Int. J. Pept. Protein Res., 31, 435-442, https://doi.org/10.1111/j.1399-3011.1988.tb00900.x.

    Article  CAS  PubMed  Google Scholar 

  79. Giustarini, D., Dalle-Donne, I., Lorenzini, S., Milzani, A., and Rossi, R. (2006) Age-related influence on thiol, disulfide, and protein-mixed disulfide levels in human plasma, J. Gerontol. A Biol. Sci. Med. Sci., 61, 1030-1038, https://doi.org/10.1093/gerona/61.10.1030.

    Article  PubMed  Google Scholar 

  80. Imai, H., Hayashi, T., Negawa, T., Nakamura, K., Tomida, M., Koda, K., Suda, K., and Era, S. (2002) Strenuous exercise-induced change in redox state of human serum albumin during intensive kendo training, Jpn. J. Physiol., 52, 135-140, https://doi.org/10.2170/jjphysiol.52.135.

    Article  CAS  PubMed  Google Scholar 

  81. Salmeen, A., Andersen, J. N., Myers, M. P., Meng, T. C., Hinks, J. A., Tonks, N. K., and Barford, D. (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate, Nature, 423, 769-773, https://doi.org/10.1038/nature01680.

    Article  CAS  PubMed  ADS  Google Scholar 

  82. Nakamura, T., Yamamoto, T., Abe, M., Matsumura, H., Hagihara, Y., Goto, T., Yamaguchi, T., and Inoue, T. (2008) Oxidation of archaeal peroxiredoxin involves a hypervalent sulfur intermediate, Proc. Natl. Acad. Sci. USA, 105, 6238-6242, https://doi.org/10.1073/pnas.0709822105.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  83. Bromberg, Y., Aptekmann, A. A., Mahlich, Y., Cook, L., Senn, S., Miller, M., Nanda, V., Ferreiro, D. U., and Falkowski, P. G. (2022) Quantifying structural relationships of metal-binding sites suggests origins of biological electron transfer, Sci. Adv., 8, eabj3984, https://doi.org/10.1126/sciadv.abj3984.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  84. Torrance, J. W., Macarthur, M. W., and Thornton, J. M. (2008) Evolution of binding sites for zinc and calcium ions playing structural roles, Protein, 71, 813-830, https://doi.org/10.1002/prot.21741.

    Article  CAS  Google Scholar 

  85. Van der Gulik, P., Massar, S., Gilis, D., Buhrman, H., and Rooman, M. (2009) The first peptides: the evolutionary transition between prebiotic amino acids and early proteins, J. Theor. Biol., 261, 531-539, https://doi.org/10.1016/j.jtbi.2009.09.004.

    Article  CAS  PubMed  ADS  Google Scholar 

  86. Rudenko, A. P. (1995) Self-organization and progressive evolution in natural processes within the concept of evolutionary catalysis [in Russian], Ross. Khim. Zhurn., 39, 55-71.

    CAS  Google Scholar 

  87. Ireland, S. M., and Martin, A. C. R. (2019) ZincBind – the database of zinc binding sites, Database (Oxford), 2019, baz006, https://doi.org/10.1093/database/baz006.

    Article  CAS  PubMed  Google Scholar 

  88. Padjasek, M., Kocyła, A., Kluska, K., Kerber, O., BaTran, J., and Krężel, A. (2020) Structural zinc binding sites shaped for greater works: structure-function relations in classical zinc finger, hook and clasp domains, J. Inorg. Biochem., 204, e110955, https://doi.org/10.1016/j.jinorgbio.2019.110955.

    Article  CAS  Google Scholar 

  89. Vallee, B. L., and Auld, D. S. (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins, Biochemistry, 29, 5647-5659, https://doi.org/10.1021/bi00476a001.

    Article  CAS  PubMed  Google Scholar 

  90. Auld, D. S. (2009) The ins and outs of biological zinc sites, Biometals, 22, 141-148, https://doi.org/10.1007/s10534-008-9184-1.

    Article  CAS  PubMed  Google Scholar 

  91. Andreini, C., Banci, L., Bertini, I., and Rosato, A. (2006) Zinc through the three domains of life, J. Proteome Res., 5, 3173-3178, https://doi.org/10.1021/pr0603699.

    Article  CAS  PubMed  Google Scholar 

  92. Parkin, G. (2004) Synthetic analogues relevant to the structure and function of zinc enzymes, Chem. Rev., 104, 699-767, https://doi.org/10.1021/cr0206263.

    Article  CAS  PubMed  Google Scholar 

  93. Hristova, V. A., Beasley, S. A., Rylett, R. J., and Shaw, G. S. (2009) Identification of a novel Zn2+-binding domain in the autosomal recessive juvenile Parkinson-related E3 ligase Parkin, J. Biol. Chem., 284, 14978-14986, https://doi.org/10.1074/jbc.M808700200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Saini, N., and Schaffner, W. (2010) Short communication zinc supplement greatly improves the condition of parkin mutant Drosophila, J. Biol. Chem., 391, 513-518, https://doi.org/10.1515/bc.2010.052.

    Article  CAS  Google Scholar 

  95. Konovalov, O. V., Novikova, N. N., Kovalchuk, M. V., Yalovega, G. E., Topunov, A. F., Kosmachevskaya, O. V., Yurieva, E. A., Rogachev, A. V., Trigub, A. L., Kremennaya, M. A., Borshchevskiy, V. I., Vakhrameev, D. D., and Yakunin, S. N. (2020) XANES measurements for studies of adsorbed protein layers at liquid interfaces, Materials, 13, e4635, https://doi.org/10.3390/ma13204635.

    Article  CAS  ADS  Google Scholar 

  96. Novikova, N., Kovalchuk, M., Stepina, N., Gaynutdinov, R., Chukhraic, E., and Yurieva, E. (2015) Distinct effect of xenobiotics on the metal-binding properties of protein molecules, J. Synchrotron Radiat., 22, 1001-1007, https://doi.org/10.1107/S1600577515005627.

    Article  CAS  PubMed  Google Scholar 

  97. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The protein data bank, Nucleic Acids Res., 28, 235-242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Rosato, A., Valasatava, Y., and Andreini, C. (2016) Minimal functional sites in metalloproteins and their usage in structural bioinformatics, Int. J. Mol. Sci., 17, e671, https://doi.org/10.3390/ijms17050671.

    Article  CAS  Google Scholar 

  99. Kocyła, A., Tran, J. B., and Krężel, A. (2021) Galvanization of protein–protein interactions in a dynamic zinc interactome, Trends Biochem. Sci., 46, 64-79, https://doi.org/10.1016/j.tibs.2020.08.011.

    Article  CAS  PubMed  Google Scholar 

  100. Bray, T. M., and Bettger, W. J. (1990) The physiological role of zinc as an antioxidant, Free Radic. Biol. Med., 8, 281-291, https://doi.org/10.1016/0891-5849(90)90076-U.

    Article  CAS  PubMed  Google Scholar 

  101. Gibbs, P. N. B., Gore, M. G., and Jordan, P. M. (1985) Investigation of the effect of metal ions on the reactivity of thiol groups in humans: aminolevulinate dehydratase, Biochem. J., 225, 573-580, https://doi.org/10.1042/bj2250573.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Powell, S. R. (1994) Salicylate trapping of OH as a tool for studying post-ischemic oxidative injury in the isolated rat heart, Free Radic. Res., 21, 355-370, https://doi.org/10.3109/10715769409056588.

    Article  CAS  PubMed  Google Scholar 

  103. Powell, S. R., Gurzenda, E. M., Wingertzohan, M. A., and Wapnir, R. A. (1999) Promotion of copper excretion from the isolated perfused rat heart attenuates postischemic cardiac oxidative injury, Am. J. Physiol., 277, 956-962, https://doi.org/10.1152/ajpheart.1999.277.3.H956.

    Article  Google Scholar 

  104. Marreiro, D. D., Cruz, K. J., Morais, J. B., Beserra, J. B., Severo, J. S., and de Oliveira, A. R. (2017) Zinc and oxidative stress: current mechanisms, Antioxidants, 6, e24, https://doi.org/10.3390/antiox6020024.

    Article  CAS  Google Scholar 

  105. Oteiza, P. I. (2012) Zinc and the modulation of redox homeostasis, Free Radic. Biol. Med., 53, 1748-1759, https://doi.org/10.1016/j.freeradbiomed.2012.08.568.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Mammadova-Bach, E., and Braun, A. (2019) Zinc homeostasis in platelet-related diseases, Int. J. Mol. Sci., 20, e5258, https://doi.org/10.3390/ijms20215258.

    Article  CAS  Google Scholar 

  107. Hübner, C., and Haase, H. (2021) Interactions of zinc- and redox-signaling pathways, Redox Biol., 41, e101916, https://doi.org/10.1016/j.redox.2021.101916.

    Article  CAS  Google Scholar 

  108. Powell, S. R. (2000) The antioxidant properties of zinc, J. Nutr., 130, 1447S-1454S, https://doi.org/10.1093/jn/130.5.1447S.

    Article  CAS  PubMed  Google Scholar 

  109. Ellis, R. J. (2001) Macromolecular crowding: obvious but underappreciated, Trends Biochem. Sci., 26, 597-604, https://doi.org/10.1016/S0968-0004(01)01938-7.

    Article  CAS  PubMed  Google Scholar 

  110. Kuriyan, J., and Eisenberg, D. (2007) The origin of protein interactions and allostery in colocalization, Nature, 450, 983-990, https://doi.org/10.1038/nature06524.

    Article  CAS  PubMed  ADS  Google Scholar 

  111. Alberti, S., and Hyman, A. A. (2021) Biomolecular condensates at the nexus of cellular stress, protein aggregation disease and ageing, Nat. Rev. Mol. Cell Biol., 22, 196-213, https://doi.org/10.1038/s41580-020-00326-6.

    Article  CAS  PubMed  Google Scholar 

  112. Vazquez, D. S., Toledo, P. L., Gianotti, A. R., and Ermácora, M. R. (2022) Protein conformation and biomolecular condensates, Curr. Res. Struct. Biol., 4, 285-307, https://doi.org/10.1016/j.crstbi.2022.09.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Garcia-Seisdedos, H., Villegas, J. A., and Levy, E. D. (2019) Infinite assembly of folded proteins in evolution, disease, and engineering, Angew. Chem. Int. Ed. Engl., 58, 5514-5531, https://doi.org/10.1002/anie.201806092.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. O’Connell, J. D., Zhao, A., Ellington, A. D., and Marcotte, E. M. (2012) Dynamic reorganization of metabolic enzymes into intracellular bodies, Annu. Rev. Cell Dev. Biol., 28, 89-111, https://doi.org/10.1146/annurev-cellbio-101011-155841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Petrovska, I., Nüske, E., Munder, M. C., Kulasegaran, G., Malinovska, L., Kroschwald, S., Richter, D., Fahmy, K., Gibson, K., and Verbavatz, J.-M. (2014) Filament formation by metabolic enzymes is a specific adaptation to an advanced state of cellular starvation, eLife, 3, e02409, https://doi.org/10.7554/eLife.02409.

    Article  PubMed  PubMed Central  Google Scholar 

  116. Munder, M. C., Midtvedt, D., Franzmann, T., Nüske, E., Otto, O., Herbig, M., Ulbricht, E., Müller, P., Taubenberger, A., Maharana, S., Malinovska, L., Richter, D., Guck, J., Zaburdaev, V., and Alberti, S. (2016) A pH-driven transition of the cytoplasm from a fluid- to a solid-like state promotes entry into dormancy, eLife, 5, e09347, https://doi.org/10.7554/eLife.09347.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Minsky, A., Shimoni, E., and Frenkiel-Krispin, D. (2002) Stress, order and survival, Nat. Rev. Mol. Cell Biol., 3, 50-60, https://doi.org/10.1038/nrm700.

    Article  CAS  PubMed  Google Scholar 

  118. Rabouille, C., and Alberti, S. (2017) Cell adaptation upon stress: the emerging role of membrane-less compartments, Curr. Opin. Cell Biol., 47, 34-42, https://doi.org/10.1016/j.ceb.2017.02.006.

    Article  CAS  PubMed  Google Scholar 

  119. Parry, B. R., Surovtsev, I. V., Cabeen, M. T., O’Hern, C. S., Dufresne, E. R., and Jacobs-Wagner, C. (2014) The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity, Cell, 156, 183-194, https://doi.org/10.1016/j.cell.2013.11.028.

    Article  CAS  PubMed  Google Scholar 

  120. Salgado, E. N., Ambroggio, X. I., Brodin, J. D., Lewis, R. A., Kuhlman, B., and Tezcan, F. A. (2010) Metal templated design of protein interfaces, Proc. Natl. Acad. Sci. USA, 107, 1827-1832, https://doi.org/10.1073/pnas.0906852107.

    Article  PubMed  ADS  Google Scholar 

  121. Degtyar, E., Harrington, M. J., Politi, Y., and Fratzl, P. (2014) The mechanical role of metal ions in biogenic protein based materials, Angew. Chem. Int. Ed. Engl., 53, 12026-12044, https://doi.org/10.1002/anie.201404272.

    Article  CAS  PubMed  Google Scholar 

  122. Yang, Y. J., Holmberg, A. L., and Olsen, B. D. (2017) Artificially engineered protein polymers, Annu. Rev. Chem. Biomol. Eng., 8, 549-575, https://doi.org/10.1146/annurev-chembioeng-060816-101620.

    Article  CAS  PubMed  Google Scholar 

  123. Soraruf, D., Roosen-Runge, F., Grimaldo, M., and Zanini, F. (2014) Protein cluster formation in aqueous solution in the presence of multivalent metal ions – a light scattering study, Soft Matter, 10, 894-902, https://doi.org/10.1039/C3SM52447G.

    Article  CAS  PubMed  ADS  Google Scholar 

  124. Wolf, M. (2015) Effective Interactions in Liquid-Liquid Phase Separated Protein Solutions Induced by Multivalent Ions, Thesis for PhD. Tubingen, Germany, Eberhard Karls University, 176 p., https://doi.org/10.15496/publikation-4822.

  125. Lee, B. P., Messersmith, P. B., Israelachvili, J. N., and Waite, J. H. (2011) Mussel-inspired adhesives and coatings, Annu. Rev. Mater. Res., 41, 99-132, https://doi.org/10.1146/annurev-matsci-062910-100429.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  126. Zhang, F., Zocher, G., Sauter, A., Stehle, T., and Schreiber, F. (2011) Novel approach to controlled protein crystallization through ligandation of yttrium cations, J. Appl. Cryst., 44, 755-762, https://doi.org/10.1107/S0021889811017997.

    Article  CAS  ADS  Google Scholar 

  127. Zhang, F., Roth, R., Wolf, M., Roosen-Runge, F., Skoda, M. W. A., Jacobs, R. M. J., Sztucki, M., and Schreiber, F. (2012) Charge-controlled metastable liquid-liquid phase separation in protein solutions as a universal pathway towards crystallization, Soft Matter, 8, e1313, https://doi.org/10.1039/c2sm07008a.

    Article  CAS  ADS  Google Scholar 

  128. Hong, K., Song, D., and Jung, Y. (2020) Behavior control of membrane-less protein liquid condensates with metal ion-induced phase separation, Nat. Commun., 11, e5554, https://doi.org/10.1038/s41467-020-19391-8.

    Article  CAS  ADS  Google Scholar 

  129. Monette, A., and Mouland, A. J. (2020) Zinc and copper ions differentially regulate prion-like phase separation dynamics of pan-virus nucleocapsid biomolecular condensates, Viruses, 12, e1179, https://doi.org/10.3390/v12101179.

    Article  CAS  Google Scholar 

  130. Wiech, A., Tarczewska, A., Ożyhar, A., and Orłowski, M. (2021) Metal ions induce liquid condensate formation by the F domain of Aedes aegypti ecdysteroid receptor. New perspectives of nuclear receptor studies, Cells, 10, e571, https://doi.org/10.3390/cells10030571.

    Article  CAS  Google Scholar 

  131. Song, W. J., Pamela, A. S., Ambroggio, X. I., and Tezcan, F. A. (2014) Metals in protein–protein Interfaces, Annu. Rev. Biophys., 43, 409-431, https://doi.org/10.1146/annurev-biophys-051013-023038.

    Article  CAS  PubMed  Google Scholar 

  132. Kim, N. H., Choi, H., Shahzad, Z. M., Ki, H., Lee, J., Chae, H., and Kim, Y. H. (2022) Supramolecular assembly of protein building blocks: from folding to function, Nano Converg., 9, e4, https://doi.org/10.1186/s40580-021-00294-3.

    Article  CAS  Google Scholar 

  133. Bailey, J. B., Subramanian, R. H., Churchfield, L. A., and Tezcan, F. A. (2016) Metal-directed design of supramolecular protein assemblies, Methods Enzymol., 580, 223-250, https://doi.org/10.1016/bs.mie.2016.05.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Chalkley, M. J., Mann, S. I., and DeGrado, W. F. (2022) De novo metalloprotein design, Nat. Rev. Chem., 6, 31-50, https://doi.org/10.1038/s41570-021-00339-5.

    Article  CAS  PubMed  Google Scholar 

  135. Peacock, A. F. A. (2013) Incorporating metals into de novo proteins, Curr. Opin. Chem. Biol., 17, 934-939, https://doi.org/10.1016/j.cbpa.2013.10.015.

    Article  CAS  PubMed  Google Scholar 

  136. Slope, L. N., and Peacock, A. F. A. (2016) De novo design of xeno-metallo coiled coils, Chem. Asian J., 11, 660-666, https://doi.org/10.1002/asia.201501173.

    Article  CAS  PubMed  Google Scholar 

  137. Aleksandrov, V. Ya. (1985) Cell Reactivity and Proteins [in Russian], Nauka, Leningrad, 318 p.

  138. Matveev, V. V. (2005) Protoreaction of protoplasm, Cell Mol. Biol. (Noisy-le-grand), 51, 715-723.

    CAS  PubMed  Google Scholar 

  139. Agutter, P. S. (2007) Cell mechanics and stress: from molecular details to the ‘universal cell reaction’ and hormesis, Bioessays, 29, 324-333, https://doi.org/10.1002/bies.20550.

    Article  CAS  PubMed  Google Scholar 

  140. Bychkova, V. E., Basova, L. V., and Balobanov, V. A., (2014) How membrane surface affects protein structure, Biochemistry (Moscow), 79, 1483-1514, https://doi.org/10.1134/S0006297914130045.

    Article  CAS  PubMed  Google Scholar 

  141. Bychkova, V. E., Semisotnov, G. V., Balobanov, V. A., and Finkelstein, A. V. (2018) The molten globule concept: 45 years later, Biochemistry (Moscow), 83, S33-S47, https://doi.org/10.1134/S0006297918140043.

    Article  CAS  PubMed  Google Scholar 

  142. Bychkova, V. E., Dolgikh, D. A., Balobanov, V. A., and Finkelstein, A. V. (2022) The molten globule state of a globular protein in a cell is more or less frequent case rather than an exception, Molecules, 27, e4361, https://doi.org/10.3390/molecules27144361.

    Article  CAS  Google Scholar 

  143. Gupta, M. N., and Uversky, V. N. (2023) Pre-molten, wet, and dry molten globules en route to the functional state of proteins, Int. J. Mol. Sci., 24, e2424, https://doi.org/10.3390/ijms24032424.

    Article  CAS  Google Scholar 

  144. Bhowmick, J., Chandra, S., and Varadarajan, R. (2023) Deep mutational scanning to probe specificity determinants in proteins, Structure and Intrinsic Disorder in Enzymology, Elsevier, Amsterdam, pp. 31-71, https://doi.org/10.1016/B978-0-323-99533-7.00005-4.

  145. Gupta, M., Pandey, S., Ehtesham, N. Z., and Hasnain, S. E. (2019) Medical implications of protein moonlighting, Ind. J. Med. Res., 149, 322-325, https://doi.org/10.4103/ijmr.IJMR_2192_18.

    Article  CAS  Google Scholar 

  146. Es-haghi, A., Moghaddam, M. J., and Shahpasand, K. (2019) Role of pre-molten globule structure in protein amyloid fibril formation, Avicenna J. Med. Biochem., 7, 35-42, https://doi.org/10.34172/ajmb.2019.07.

    Article  Google Scholar 

  147. Blundell, T. L., Gupta, M. N., and Hasnain, S. E. (2020) Intrinsic disorder in proteins: Relevance to protein assemblies, drug design and host-pathogen interactions, Prog. Biophys. Mol. Biol., 156, 34-42, https://doi.org/10.1016/j.pbiomolbio.2020.06.004.

    Article  CAS  PubMed  Google Scholar 

  148. Iram, A., Alam, T., Khan, J. M., Khan, T. A., Khan, R. H., and Naeem, A. (2013) Molten globule of hemoglobin proceeds into aggregates and advanced glycated end products, PLoS One, 8, e72075, https://doi.org/10.1371/journal.pone.0072075.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  149. Dave, S., Mahajan, S., Chandra, V., and Gupta, P. (2011) Trifluoroethanol stabilizes the molten globule state and induces non-amyloidic turbidity in stem bromelain near its isoelectric point, Int. J. Biol. Macromol., 49, 536-542, https://doi.org/10.1016/j.ijbiomac.2011.06.006.

    Article  CAS  PubMed  Google Scholar 

  150. Banerjee, S. (2021) Long-term incubation of myoglobin with glyoxal induces amyloid like aggregation of the heme protein: implications of advanced glycation end products in protein conformational disorders, J. Mol. Liquids, 326, e115256, https://doi.org/10.1016/j.molliq.2020.115256.

    Article  CAS  Google Scholar 

  151. Blum, O., Haiek, A., Cwikel, D., and Gray, H. B. (1998) Isolation of a myoglobin molten globule by selective cobalt(III)-induced unfolding, Proc. Natl. Acad. Sci. USA, 95, 6659-6662, https://doi.org/10.1073/pnas.95.12.6659.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  152. Mukhopadhyay, A., Basu, S., Singha, S., and Patra, H. K. (2018) Inner-view of nanomaterial incited protein conformational changes: insights into designable interaction, Research (Wash. D C), 2018, e9712832, https://doi.org/10.1155/2018/9712832.

    Article  Google Scholar 

  153. Bhattacharya, J., Choudhuri, U., Siwach, O., Sen, P., and Dasgupta, A. K. (2006) Interaction of hemoglobin and copper nanoparticles: Implications in hemoglobinopathy, Nanomedicine, 2, 191-199, https://doi.org/10.1016/j.nano.2006.07.001.

    Article  CAS  PubMed  Google Scholar 

  154. Muzammil, S., Kumar, Y., and Tayyab, S. (1999) Molten globule-like state of human serum albumin at low pH, Eur. J. Biochem., 266, 26-32, https://doi.org/10.1046/j.1432-1327.1999.00810.x.

    Article  CAS  PubMed  Google Scholar 

  155. Kumar, Y., Tayyab, S., and Muzammil, S. (2004) Molten-globule like partially folded states of human serum albumin induced by fluoro and alkyl alcohols at low pH, Arch. Biochem. Biophys., 426, 3-10, https://doi.org/10.1016/j.abb.2004.03.025.

    Article  CAS  PubMed  Google Scholar 

  156. Sen, P., Ahmad, B., and Khan, R. H. (2008) Formation of a molten globule like state in bovine serum albumin at alkaline pH, Eur. Biophys. J., 37, 1303-1308, https://doi.org/10.1007/s00249-008-0335-7.

    Article  CAS  PubMed  Google Scholar 

  157. Farruggia, B., and Picó, G. A. (1999) Thermodynamic features of the chemical and thermal denaturations of human serum albumin, Int. J. Biol. Macromol., 26, 317-323, https://doi.org/10.1016/S0141-8130(99)00054-9.

    Article  CAS  PubMed  Google Scholar 

  158. Hekmat, A., Hajebrahimi, Z., and Motamedzade, A. (2017) Structural changes of human serum albumin (HSA) in simulated microgravity, Protein Pept. Lett., 24, 1030-1039, https://doi.org/10.2174/0929866524666170918111038.

    Article  CAS  PubMed  Google Scholar 

  159. Sattarahmady, N., Moosavi-Movahedi, A. A., Ahmad, F., Hakimelahi, G. H., Habibi-Rezaei, M., Saboury, A. A., and Sheibani, N. (2007) Formation of the molten globule-like state during prolonged glycation of human serum albumin, Biochim. Biophys. Acta, 1770, 933-942, https://doi.org/10.1016/j.bbagen.2007.02.001.

    Article  CAS  PubMed  Google Scholar 

  160. Bohlooli, M., Moosavi-Movahedi, A. A., Taghavi, F., Habibi-Rezaei, M., Seyedarabi, A., Saboury, A. A., and Ahmad, F. (2013) Thermodynamics of a molten globule state of human serum albumin by 3-β-hydroxybutyrate as a ketone body, Int. J. Biol. Macromol., 54, 258-263, https://doi.org/10.1016/j.ijbiomac.2012.12.018.

    Article  CAS  PubMed  Google Scholar 

  161. Muralidhara, B. K., and Prakash, V. (2002) Molten globule intermediates of human serum albumin in low concentration of urea, Ind. J. Biochem. Biophys., 39, 318-324.

    CAS  Google Scholar 

  162. Lee, J. Y., and Hirose, M. (1992) Partially folded state of the disulfide-reduced form of human serum albumin as an intermediate for reversible denaturation, J. Biol. Chem., 267, 14753-14758, https://doi.org/10.1016/S0021-9258(18)42104-7.

    Article  CAS  PubMed  Google Scholar 

  163. Islam, F., Shohag, S., Akhter, S., Islam, Md. R., Sultana, S., Mitra, S., Chandran, D., Khandaker, M. U., Ashraf, G., Idris, A. M., Emran, T. B., and Cavalu, S. (2022) Exposure of metal toxicity in Alzheimer’s disease: an extensive review, Front. Pharmacol., 13, e903099, https://doi.org/10.3389/fphar.2022.903099.

    Article  CAS  Google Scholar 

  164. Vendruscolo, M., and Fuxreiter, M. (2022) Protein condensation diseases: therapeutic opportunities, Nat. Commun., 13, e5550, https://doi.org/10.1038/s41467-022-32940-7.

    Article  CAS  ADS  Google Scholar 

  165. Cristóvão, J. S., Santos, R., and Gomes, C. M. (2015) Metals and neuronal metal binding proteins implicated in Alzheimer’s disease, Oxid. Med. Cell. Longev., 2016, e9812178, https://doi.org/10.1155/2016/9812178.

    Article  CAS  Google Scholar 

  166. Basu, S., Moha, M. L., Luo, X., Kundu, B., Kong, Q., and Singh, N. (2007) Modulation of proteinase K-resistant prion protein in cells and infectious brain homogenate by redox iron: implications for prion replication and disease pathogenesis, Mol. Biol. Cell, 18, 3302-3312, https://doi.org/10.1091/mbc.e07-04-0317.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Caito, S., and Aschner, M. (2015) Neurotoxicity of metals, Handb. Clin. Neurol., 131, 169-189, https://doi.org/10.1016/B978-0-444-62627-1.00011-1.

    Article  PubMed  Google Scholar 

  168. Devi, S., Chaturvedi, M., Fatima, S., and Priya, S. (2022) Environmental factors modulating protein conformations and their role in protein aggregation diseases, Toxicology, 465, e153049, https://doi.org/10.1016/j.tox.2021.153049.

    Article  CAS  Google Scholar 

  169. Toni, M., Massimino, M. L., De Mario, A., Angiulli, E., and Spisni, E. (2017) Metal dyshomeostasis and their pathological role in prion and prion-like diseases: the basis for a nutritional approach, Front. Neurosci., 11, e3, https://doi.org/10.3389/fnins.2017.00003.

    Article  Google Scholar 

  170. Li, M., Fan, Y., Li, Q., Wang, X., Zhao, L., and Zhu, M. (2022) Liquid-liquid phase separation promotes protein aggregation and its implications in ferroptosis in Parkinson’s disease dementia, Oxid. Med. Cell. Longev., 2022, e7165387, https://doi.org/10.1155/2022/7165387.

    Article  CAS  Google Scholar 

  171. Zatta, P., Drago, D., Bolognin, S., and Sensi, S. L. (2009) Alzheimer’s disease, metal ions and metal homeostatic therapy, Trends Pharmacol. Sci., 30, 346-355, https://doi.org/10.1016/j.tips.2009.05.002.

    Article  CAS  PubMed  Google Scholar 

  172. Duce, J. A., Tsatsanis, A., Cater, M. A., James, S. A., Robb, E., Wikhe, K., Leong, S. L., Perez, K., Johanssen, T., Greenough, M. A., Cho, H.-H., Galatis, D., Moir, R. D., Masters, C. L., McLean, C., Tanzi, R. E., Cappai, R., Barnham, K. J., Ciccotosto, G. D., Rogers, J. T., and Bush, A. I. (2010) Iron-export ferroxidase activity of β-amyloid precursor protein is inhibited by zinc in Alzheimer’s disease, Cell, 142, 857-867, https://doi.org/10.1016/j.cell.2010.08.014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. La Mendola, D., and Rizzarelli, E. (2014) Evolutionary implications of metal binding features in different species’ prion protein: an inorganic point of view, Biomolecules, 4, 546-565, https://doi.org/10.3390/biom4020546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Chen, W.-T., Liao, Y.-H., Yu, H.-M., Cheng, I. H., and Chen, Y.-R. (2011) Distinct effects of Zn2+, Cu2+, Fe3+, and Al3+ on amyloid-β stability, oligomerization, and aggregation: amyloid-β destabilization promotes annular protofibril formation, J. Biol. Chem., 286, 9646-9656, https://doi.org/10.1074/jbc.M110.177246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Bolognin, S., Messori, L., Drago, D., Gabbiani, C., Cendron, L., and Zatta, P. (2011) Aluminum, copper, iron and zinc differentially alter amyloid-Aβ(1-42) aggregation and toxicity, Int. J. Biochem. Cell Biol., 43, 877-885, https://doi.org/10.1016/j.biocel.2011.02.009.

    Article  CAS  PubMed  Google Scholar 

  176. Liu, B., Moloney, A., Meehan, S., Morris, K., Thomas, S. E., Serpell, L. C., Hider, R., Marciniak, S. J., Lomas, D. A., and Crowther, D. C. (2011) Iron promotes the toxicity of amyloid β peptide by impeding its ordered aggregation, J. Biol. Chem., 286, 4248-4256, https://doi.org/10.1074/jbc.M110.158980.

    Article  CAS  PubMed  Google Scholar 

  177. Rival, T., Page, R. M., Chandraratna, D. S., Sendall, T. J., Ryder, E., Liu, B., Lewis, H., Rosahl, T., Hider, R., Camargo, L. M., Shearman, M. S., Crowther, D. C., and Lomas, D. A. (2009) Fenton chemistry and oxidative stress mediate the toxicity of the β-amyloid peptide in a Drosophila model of Alzheimer’s disease, Eur. J. Neurosci., 29, 1335-1347, https://doi.org/10.1111/j.1460-9568.2009.06701.x.

    Article  PubMed  PubMed Central  Google Scholar 

  178. Spoerri, L., Vella, L. J., Pham, C. L. L., Barnham, K. J., and Cappai, R. (2012) The amyloid precursor protein copper binding domain histidine residues 149 and 151 mediate APP stability and metabolism, J. Biol. Chem., 287, 26840-26853, https://doi.org/10.1074/jbc.M112.355743.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Dahms, S. O., Könnig, I., Roeser, D., Gührs, K.-H., Mayer, M. C., Kaden, D., Multhaup, G., and Than, M. E. (2012) Metal binding dictates conformation and function of the amyloid precursor protein (APP) E2 domain, J. Mol. Biol., 416, 438-452, https://doi.org/10.1016/j.jmb.2011.12.057.

    Article  CAS  PubMed  Google Scholar 

  180. Maeda, S., Sahara, N., Saito, Y., Murayama, M., Yoshiike, Y., Kim, H., Miyasaka, T., Murayama, S., Ikai, A., and Takashima, A. (2007) Granular tau oligomers as intermediates of tau filaments, Biochemistry, 46, 3856-3861, https://doi.org/10.1021/bi061359o.

    Article  CAS  PubMed  Google Scholar 

  181. Mo, Z.-Y., Zhu, Y.-Z., Zhu, H.-L., Fan, J.-B., Chen, J., and Liang, Y. (2009) Low micromolar zinc accelerates the fibrillization of human Tau via bridging of Cys-291 and Cys-322, J. Biol. Chem., 284, 34648-34657, https://doi.org/10.1074/jbc.M109.058883.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Yamamoto, A., Shin, R.-W., Hasegawa, K., Naiki, H., Sato, H., Yoshimasu, F., and Kitamoto, T. (2002) Iron (III) induces aggregation of hyperphosphorylated tau and its reduction to iron (II) reverses the aggregation: implications in the formation of neurofibrillary tangles of Alzheimer’s disease, J. Neurochem., 82, 1137-1147, https://doi.org/10.1046/j.1471-4159.2002.t01-1-01061.x.

    Article  CAS  PubMed  Google Scholar 

  183. Kitazawa, M., Cheng, D., and Laferla, F. M. (2009) Chronic copper exposure exacerbates both amyloid and tau pathology and selectively dysregulates cdk5 in a mouse model of AD, J. Neurochem., 108, 1550-1560, https://doi.org/10.1111/j.1471-4159.2009.05901.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Crouch, P. J., Lin, W. H., Adlard, P. A., and Barnham, K. J. (2009) Increasing Cu bioavailability inhibits Aβ oligomers and tau phosphorylation, Proc. Natl. Acad. Sci. USA, 106, 381-386, https://doi.org/10.1073/pnas.0809057106.

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  185. Boyko, S., and Surewicz, W. K. (2022) Tau liquid-liquid phase separation in neurodegenerative diseases, Trends Cell Biol., 32, 611-623, https://doi.org/10.1016/j.tcb.2022.01.011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Singh, A., Isaac, A. O., Luo, X., Mohan, M. L., Cohen, M. L., Chen, F., Kong, Q., Bartz, J., and Singh, N. (2009) Abnormal brain iron homeostasis in human and animal prion disorders, PLoS Pathog., 5, e1000336, https://doi.org/10.1371/journal.ppat.1000336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Gao, Y. Y., Zhong, T., Wang, L. Q., Zhang, N., Zeng, Y., Hu, J. Y., Dang, H. B., Chen, J., and Liang, Y. (2022) Zinc enhances liquid-liquid phase separation of Tau protein and aggravates mitochondrial damages in cells, Int. J. Biol. Macromol., 209, 703-715, https://doi.org/10.1016/j.ijbiomac.2022.04.034.

    Article  CAS  PubMed  Google Scholar 

  188. Donato, R., Cannon, B. R., Sorci, G., Riuzzi, F., Hsu, K., Weber, D. J., and Geczy, C. L. (2013) Functions of S100 proteins, Curr. Mol. Med., 13, 24-57, https://doi.org/10.2174/156652413804486214.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Vogl, T., Gharibyan, A. L., and Morozova-Roche, L. A. (2012) Pro-inflammatory S100A8 and S100A9 proteins: Self-assembly into multifunctional native and amyloid complexes, Int. J. Mol. Sci., 13, 2893-2917, https://doi.org/10.3390/ijms13032893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Selinfreund, R. H., Barger, S. W., Pledger, W. J., and Van Eldik, L. J. (1991) Neurotrophic protein S100 beta stimulates glial cell proliferation, Proc. Natl. Acad. Sci. USA, 88, 3554-3558, https://doi.org/10.1073/pnas.88.9.3554.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  191. Cai, Z., Liu, N., Wang, C., Qin, B., Zhou, Y., Xiao, M., Chang, L., Yan, L.-J., and Zhao, B. (2016) Role of RAGE in Alzheimer’s disease, Cell. Mol. Neurobiol., 36, 483-495, https://doi.org/10.1007/s10571-015-0233-3.

    Article  CAS  PubMed  Google Scholar 

  192. Van Eldik, L. J., and Wainwright, M. S. (2003) The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain, Restor. Neurol. Neurosci., 21, 97-108.

    CAS  PubMed  Google Scholar 

  193. Wang, Y., Li, J., Sheng, J. G., Li, Y., Wang, J., Sheng, J. G., Liu, L., Barger, S. W., Jones, R. A., Van Eldik, L. J., Mrak, R. E., and Griffin, W. S. (1998) S100β increases levels of β-amyloid precursor protein and its encoding mRNA in rat neuronal cultures, J. Neurochem., 71, 1421-1428, https://doi.org/10.1046/j.1471-4159.1998.71041421.x.

    Article  PubMed  Google Scholar 

  194. Sirangelo, I., and Iannuzzi, C. (2017) The role of metal binding in the amyotrophic lateral sclerosis-related aggregation of copper-zinc superoxide dismutase, Molecules, 22, e1429, https://doi.org/10.3390/molecules22091429.

    Article  CAS  Google Scholar 

  195. Xu, W. C., Liang, J. Z., Li, C., He, Z. X., Yuan, H. Y., Huang, B. Y., Liu, X. L., Tang, B., Pang, D. W., Du, H. N., Yang, Y., Chen, J., Wang, L., Zhang, M., and Liang, Y. (2018) Pathological hydrogen peroxide triggers the fibrillization of wild-type SOD1 via sulfenic acid modification of Cys-111, Cell Death Dis., 9, e67, https://doi.org/10.1038/s41419-017-0106-4.

    Article  CAS  Google Scholar 

  196. Sanghai, N., and Tranmer, G. K. (2021) Hydrogen peroxide and amyotrophic lateral sclerosis: from biochemistry to pathophysiology, Antioxidants, 11, e52, https://doi.org/10.3390/antiox11010052.

    Article  CAS  Google Scholar 

  197. Takashima, C., Kosuge, Y., Inoue, M., Ono, S. I., and Tokuda, E. (2021) A metal-free, disulfide oxidized form of superoxide dismutase 1 as a primary misfolded species with prion-like properties in the extracellular environments surrounding motor neuron-like cells, Int. J. Mol. Sci., 22, e4155, https://doi.org/10.3390/ijms22084155.

    Article  CAS  Google Scholar 

  198. Das, B., Roychowdhury, S., Mohanty, P., Rizuan, A., Chakraborty, J., Mittal, J., and Chattopadhyay, K. (2022) A Zn-dependent structural transition of SOD1 modulates its ability to undergo phase separation, EMBO J., 42, e111185, https://doi.org/10.15252/embj.2022111185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Mukherjee, S., Sakunthala, A., Gadhe, L., Poudyal, M., Sawner, A. S., Kadu, P., and Maji, S. K. (2022) Liquid-liquid phase separation of α-synuclein: a new mechanistic insight for α-synuclein aggregation associated with Parkinson’s disease pathogenesis, J. Mol. Biol., 435, e167713, https://doi.org/10.1016/j.jmb.2022.167713.

    Article  CAS  Google Scholar 

  200. Huang, S., Xu, B., and Liu, Y. (2022) Calcium promotes α-synuclein liquid-liquid phase separation to accelerate amyloid aggregation, Biochem. Biophys. Res. Commun., 603, 13-20, https://doi.org/10.1016/j.bbrc.2022.02.097.

    Article  CAS  PubMed  Google Scholar 

  201. Xu, B., Huang, S., Liu, Y., Wan, C., Gu, Y., Wang, D., and Yu, H. (2022) Manganese promotes α-synuclein amyloid aggregation through the induction of protein phase transition, J. Biol. Chem., 298, e101469, https://doi.org/10.1016/j.jbc.2021.101469.

    Article  CAS  Google Scholar 

  202. Peggion, C., Bertoli, A., and Sorgato, M. C. (2016) Almost a century of prion protein(s): from pathology to physiology, and back to pathology, Biochem. Biophys. Res. Commun., 483, 1148-1155, https://doi.org/10.1016/j.bbrc.2016.07.118.

    Article  CAS  PubMed  Google Scholar 

  203. Brown, D. R. (2011) Prions and manganese: a maddening beast, Metallomics, 3, 229-238, https://doi.org/10.1039/C0MT00047G.

    Article  CAS  PubMed  Google Scholar 

  204. Benetti, F., Biarnés, X., Attanasio, F., Giachin, G., Rizzarelli, E., and Legname, G. (2014) Structural determinants in prion protein folding and stability, J. Mol. Biol., 426, 3796-3810, https://doi.org/10.1016/j.jmb.2014.09.017.

    Article  CAS  PubMed  Google Scholar 

  205. Canello, T., Friedman-Levi, Y., Mizrahi, M., Binyamin, O., Cohen, E., Frid, K., and Gabizon, R. (2012) Copper is toxic to PrP-ablated mice and exacerbates disease in a mouse model of E200K genetic prion disease, Neurobiol. Dis., 45, 1010-1017, https://doi.org/10.1016/j.nbd.2011.12.020.

    Article  CAS  PubMed  Google Scholar 

  206. Mitteregger, G., Korte, S., Shakarami, M., Herms, J., and Kretzschmar, H. A. (2009) Role of copper and manganese in prion disease progression, Brain Res., 1292, 155-164, https://doi.org/10.1016/j.brainres.2009.07.051.

    Article  CAS  PubMed  Google Scholar 

  207. Liu, M., Yu, S., Yang, J., Yin, X., and Zhao, D. (2007) RNA and CuCl2 induced conformational changes of therecombinant ovine prion protein, Mol. Cell. Biochem., 294, 197-203, https://doi.org/10.1007/s11010-006-9260-1.

    Article  CAS  PubMed  Google Scholar 

  208. Vassallo, N., and Herms, J. (2003) Cellular prion protein function in copper homeostasis and redox signalling at the synapse, J. Neurochem., 86, 538-544, https://doi.org/10.1046/j.1471-4159.2003.01882.x.

    Article  CAS  PubMed  Google Scholar 

  209. Brown, D. R. (2001) Prion and prejudice: normal protein and the synapse, Trends Neurosci., 24, 85-90, https://doi.org/10.1016/S0166-2236(00)01689-1.

    Article  CAS  PubMed  Google Scholar 

  210. Brown, D. R., Wong, B. S., Hafiz, F., Clive, C., Haswell, S. J., and Jones, I. M. (1999) Normal prion protein has an activity like that of superoxide dismutase, Biochem. J., 344, 1-5, https://doi.org/10.1042/bj3440001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Pass, R., Frudd, K., Barnett, J. P., Blindauer, C. A., and Brown, D. R. (2015) Prion infection in cells is abolished by a mutated manganese transporter but shows no relation to zinc, Mol. Cell. Neurosci., 68, 186-193, https://doi.org/10.1016/j.mcn.2015.08.004.

    Article  CAS  PubMed  Google Scholar 

  212. Choi, C. J., Anantharam, V., Saetveit, N. J., Houk, R. S., Kanthasamy, A., and Kanthasamy, A. G. (2007) Normal cellular prion protein protects against manganese-induced oxidative stress and apoptotic cell death, Toxicol. Sci., 98, 495-509, https://doi.org/10.1093/toxsci/kfm099.

    Article  CAS  PubMed  Google Scholar 

  213. Rana, A., Gnaneswari, D., Bansal, S., and Kundu, B. (2009) Prion metal interaction: is prion pathogenesis a cause or a consequence of metal imbalance? Chem. Biol. Interact., 181, 282-291, https://doi.org/10.1016/j.cbi.2009.07.021.

    Article  CAS  PubMed  Google Scholar 

  214. Watt, N. T., Griffiths, H. H., and Hooper, N. M. (2013) Neuronal zinc regulation and the prion protein, Prion, 7, 203-208, https://doi.org/10.4161/pri.24503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Kenward, A. G., Bartolotti, L. J., and Burns, C. S. (2007) Copper and zinc promote interactions between membrane-anchored peptides of the metal binding domain of the prion protein, Biochemistry, 46, 4261-4271, https://doi.org/10.1021/bi602473r.

    Article  CAS  PubMed  Google Scholar 

  216. Postnikova, G. B., and Shekhovtsova, E. A. (2016) Hemoglobin and myoglobin as reducing agents in biological systems. Redox reactions of globins with copper and iron salts and complexes, Biochemistry (Moscow), 81, 1735-1753, https://doi.org/10.1134/S0006297916130101.

    Article  CAS  PubMed  Google Scholar 

  217. Debnath, S., and Chakrabarti, A. (2020) Effects of free soluble iron on thermal aggregation of hemoglobin, Biophys. Chem., 269, e106527, https://doi.org/10.1016/j.bpc.2020.106527.

    Article  CAS  Google Scholar 

  218. Kozlova, E., Chernysh, A., Moroz, V., Sergunova, V., Gudkova, O., Fedorova, M., and Kuzovlev, A. (2012) Opposite effects of electroporation of red blood cell membranes under the influence of zinc ions, Acta Bioeng. Biomech., 14, 3-13.

    PubMed  Google Scholar 

  219. Lee, S. R. (2018) Critical role of zinc as either an antioxidant or a prooxidant in cellular systems, Oxid. Med. Cell. Longev., 2018, e9156285, https://doi.org/10.1155/2018/9156285.

    Article  CAS  Google Scholar 

  220. Kellis, J. T. Jr., Todd, R. J., and Arnold, F. H. (1991) Protein stabilization by engineered metal chelation, Biotechnology (NY), 10, 994-995, https://doi.org/10.1038/nbt1091-994.

    Article  Google Scholar 

  221. Chung, H.-S., Lee, S., and Park, S. J. (2016) Oxidation protection in metal-binding peptide motif and its application to antibody for site-selective conjugation, PLoS One, 11, e0159451, https://doi.org/10.1371/journal.pone.0159451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by ongoing institutional funding. No additional grants to carry out or direct this particular research were obtained.

Author information

Authors and Affiliations

Authors

Contributions

All authors equally contributed to designing and writing the manuscript.

Corresponding author

Correspondence to Alexey F. Topunov.

Ethics declarations

This work does not contain any studies involving human and animal subjects. The authors of this work declare that they have no conflicts of interest.

Additional information

Translated from Uspekhi Biologicheskoi Khimii, 2024, Vol. 64, pp. 349-396.

Publisher’s Note. Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kosmachevskaya, O.V., Novikova, N.N., Yakunin, S.N. et al. Formation of Supplementary Metal-Binding Centers in Proteins under Stress Conditions. Biochemistry Moscow 89 (Suppl 1), S180–S204 (2024). https://doi.org/10.1134/S0006297924140104

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297924140104

Keywords

Navigation