Skip to main content

Advertisement

SpringerLink
Log in

Associations of circulating advanced glycation end products and their soluble receptors with cancer risk: A systematic review and meta-analysis of observational studies

  • Review
  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Advanced glycation end products (AGE) in complex with their receptors (RAGE) cause a chronic inflammatory state in the body, which is the major mechanism in cancer development. This study aimed to conduct a systematic review and meta-analysis on the observational studies investigating the association between AGEs / sRAGE and cancer incidence. The PubMed, Scopus, and Web of Science databases were comprehensively searched to identify papers focused on the associations of sRAGE and AGEs with cancer incidence up to May 2023. Eight studies with a total of 7690 participants were included in the analysis to evaluate the association between circulating sRAGE and cancer incidence. The results indicated that circulating sRAGE (per 100 ng/L) had a significant inverse association with cancer incidence (RR 0.977; 95% CI 0.956, 0.999; p = 0.036; I 2 = 73.3%). The association between AGEs and cancer incidence was evaluated in 8 studies with a total of 3718 individuals. Serum concentrations of AGEs (per 100 µg/L) were not associated with the risk of cancer incidence (RR 0.988; 95% CI 0.974, 1.002; p = 0.08; I2 = 78.8%). Our findings revealed that a higher circulating sRAGE may have a protective effect against cancer incidence.

Graphical Abstract

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

AGEs:

Advanced glycation end-products

BMI:

Body mass index

CML:

Carboxy-methyl lysine

cRAGE:

Proteolytic cleavage of RAGE

esRAGE:

Endogenous secretory major splice variant of RAGE

HMGB1:

High mobility group box-1

ROS:

Reactive oxygen species

RAGE:

Receptors for AGEs

sRAGE:

Soluble forms of RAGE

References

  1. World Health Organization. "International agency for research on cancer" (2019)

  2. Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R.L., Torre, L.A., Jemal, A.: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 68(6), 394–424 (2018)

    Article  PubMed  Google Scholar 

  3. Katzke, V.A., Kaaks, R., Kühn, T.: Lifestyle and cancer risk. Cancer J. 21(2), 104–110 (2015)

    Article  PubMed  Google Scholar 

  4. Khansari, N., Shakiba, Y., Mahmoudi, M.: Chronic inflammation and oxidative stress as a major cause of age-related diseases and cancer. Recent Pat. Inflamm. Allergy Drug Discov. 3(1), 73–80 (2009)

    Article  CAS  PubMed  Google Scholar 

  5. Liou, G.-Y., Storz, P.: Reactive oxygen species in cancer. Free Radical Res. 44(5), 479–496 (2010)

    Article  CAS  Google Scholar 

  6. Cai, W., Gao, Q.-D., Zhu, L., Peppa, M., He, C., Vlassara, H.: Oxidative stress-inducing carbonyl compounds from common foods: novel mediators of cellular dysfunction. Mol. Med. 8, 337–346 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Sharifi-Zahabi, E., Sharafabad, F.H., Abdollahzad, H., Malekahmadi, M., Rad, N.B.: Circulating advanced glycation end products and their soluble receptors in relation to all-cause and cardiovascular mortality: a systematic review and meta-analysis of prospective observational studies. Adv. Nutr. 12(6), 2157–2171 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Goldin, A., Beckman, J.A., Schmidt, A.M., Creager, M.A.: Advanced glycation end products: sparking the development of diabetic vascular injury. Circ. 114(6), 597–605 (2006)

    Article  CAS  Google Scholar 

  9. Singh, R., Barden, A., Mori, T., Beilin, L.: Advanced glycation end-products: a review. Diabetol. 44, 129–146 (2001)

    Article  CAS  Google Scholar 

  10. Goldberg, T., Cai, W., Peppa, M., Dardaine, V., Baliga, B.S., Uribarri, J., Vlassara, H.: Advanced glycoxidation end products in commonly consumed foods. J. Am. Diet. Assoc. 104(8), 1287–1291 (2004)

    Article  CAS  PubMed  Google Scholar 

  11. Nicholl, I., Bucala, R.: Advanced glycation endproducts and cigarette smoking. Cell. Mol. Biol. (Noisy-le-grand) 44(7), 1025–1033 (1998)

    CAS  PubMed  Google Scholar 

  12. Aglago, E.K., Mayén, A.-L., Knaze, V., Freisling, H., Fedirko, V., Hughes, D.J., Jiao, L., Eriksen, A.K., Tjønneland, A., Boutron-Ruault, M.-C.: Dietary advanced glycation end-products and colorectal cancer risk in the European prospective investigation into cancer and nutrition (EPIC) study. Nutrients 13(9), 3132 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Turner, D.P.: Advanced glycation end-products: a biological consequence of lifestyle contributing to cancer disparity. Can. Res. 75(10), 1925–1929 (2015)

    Article  CAS  Google Scholar 

  14. Younessi, P., Yoonessi, A.: Advanced glycation end-products and their receptor-mediated roles: inflammation and oxidative stress. Iran. J. Med. Sci. 36(3), 154 (2011)

    PubMed  PubMed Central  Google Scholar 

  15. Ott, C., Jacobs, K., Haucke, E., Santos, A.N., Grune, T., Simm, A.: Role of advanced glycation end products in cellular signaling. Redox Biol. 2, 411–429 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Tang, D., Kang, R., Coyne, C.B., Zeh, H.J., Lotze, M.T.: PAMP s and DAMP s: signal 0s that spur autophagy and immunity. Immunol. Rev. 249(1), 158–175 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chuah, Y.K., Basir, R., Talib, H., Tie, T.H., Nordin, N.: Receptor for advanced glycation end products and its involvement in inflammatory diseases. Int. J. Inflam. 2013, article ID 403460, 15 pages (2013)

  18. Ahmad, S., Khan, H., Siddiqui, Z., Khan, M.Y., Rehman, S., Shahab, U., Godovikova, T., Silnikov, V.: AGEs, RAGEs and s-RAGE; friend or foe for cancer. Seminars in cancer biology. 49, 44–55 (2018)

  19. Yonekura, H., Yamamoto, Y., Sakurai, S., Petrova, R.G., Abedin, M.J., Li, H., Yasui, K., Takeuchi, M., Makita, Z., Takasawa, S.: Novel splice variants of the receptor for advanced glycation end-products expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury. Biochem. J. 370(3), 1097–1109 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Raucci, A., Cugusi, S., Antonelli, A., Barabino, S.M., Monti, L., Bierhaus, A., Reiss, K., Saftig, P., Bianchi, M.E.: A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). Faseb J. 22(10), 3716–3727 (2008)

    Article  CAS  PubMed  Google Scholar 

  21. Vazzana, N., Santilli, F., Cuccurullo, C., Davì, G.: Soluble forms of RAGE in internal medicine. Intern. Emerg. Med. 4, 389–401 (2009)

    Article  PubMed  Google Scholar 

  22. Li, T., Qin, W., Liu, Y., Li, S., Qin, X., Liu, Z.: Effect of RAGE gene polymorphisms and circulating sRAGE levels on susceptibility to gastric cancer: a case-control study. Cancer Cell. Int. 17, 19 (2017). https://doi.org/10.1186/s12935-017-0391-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Chen, Z., Hong, Q.: Correlation of serum IGF-1, AGEs and their receptors with the risk of colorectal cancer in patients with type 2 diabetes mellitus. Front. Oncol. 13, 1125745 (2023). https://doi.org/10.3389/fonc.2023.1125745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Tesařová, P., Kalousová, M., Jáchymová, M., Mestek, O., Petruzelka, L., Zima, T.: Receptor for advanced glycation end products (RAGE) - Soluble form (sRAGE) and gene polymorphisms in patients with breast cancer. Cancer Invest. 25(8), 720–725 (2007). https://doi.org/10.1080/07357900701560521

    Article  CAS  PubMed  Google Scholar 

  25. Jiao, L., Chen, L., Alsarraj, A., Ramsey, D., Duan, Z., El-Serag, H.B.: Plasma soluble receptor for advanced glycation end-products and risk of colorectal adenoma. Int. J. Mol. Epidemiol. Genet. 3(4), 294–304 (2012)

    PubMed  PubMed Central  Google Scholar 

  26. Jiao, L., Weinstein, S.J., Albanes, D., Taylor, P.R., Graubard, B.I., Virtamo, J., Stolzenberg-Solomon, R.Z.: Evidence that serum levels of the soluble receptor for advanced glycation end products are inversely associated with pancreatic cancer risk: a prospective study. Can. Res. 71(10), 3582–3589 (2011). https://doi.org/10.1158/0008-5472.can-10-2573

    Article  CAS  Google Scholar 

  27. White, D.L., Hoogeveen, R.C., Chen, L., Richardson, P., Ravishankar, M., Shah, P., Tinker, L., Rohan, T., Whitsel, E.A., El-Serag, H.B., Jiao, L.: A prospective study of soluble receptor for advanced glycation end products and adipokines in association with pancreatic cancer in postmenopausal women. Cancer Med. 7(5), 2180–2191 (2018). https://doi.org/10.1002/cam4.1426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Allegra, A., Pace, E., Tartarisco, G., Innao, V., E, D.I.S., Allegra, A.G., Ferraro, M., Musolino, C., Gangemi, S.: Changes in Serum Interleukin-8 and sRAGE Levels in Multiple Myeloma Patients. Anticancer Res. 40(3), 1443–1449 (2020). https://doi.org/10.21873/anticanres.14086

  29. He, L., Bao, H., Xue, J., Zheng, L., Zhang, Q., Sun, L., Pan, H.: Circulating soluble advanced glycation end product is inversely associated with the significant risk of developing cancer: evidence from a meta-analysis. Tumour biology : the journal of the International Society for Oncodevelopmental Biology and Medicine 35(9), 8749–8755 (2014). https://doi.org/10.1007/s13277-014-2122-7

    Article  CAS  PubMed  Google Scholar 

  30. Chan, Y.X., Alfonso, H., Fegan, P.G., Flicker, L., Yeap, B.B.: Neither Hormonal Factors Nor AGEs Explain Lower Prostate Cancer Risk in Older Men with Diabetes Mellitus. J. Clin. Endocrinol. Metab. 104(12), 6017–6024 (2019). https://doi.org/10.1210/jc.2019-01142

    Article  PubMed  Google Scholar 

  31. Grote, V.A., Nieters, A., Kaaks, R., Tjønneland, A., Roswall, N., Overvad, K., Nielsen, M.R., Clavel-Chapelon, F., Boutron-Ruault, M.C., Racine, A., Teucher, B., Lukanova, A., Boeing, H., Drogan, D., Trichopoulou, A., Trichopoulos, D., Lagiou, P., Palli, D., Sieri, S., Tumino, R., Vineis, P., Mattiello, A., Argüelles Suárez, M.V., Duell, E.J., Sánchez, M.J., Dorronsoro, M., Huerta Castaño, J.M., Barricarte, A., Jeurnink, S.M., Peeters, P.H., Sund, M., Ye, W., Regner, S., Lindkvist, B., Khaw, K.T., Wareham, N., Allen, N.E., Crowe, F.L., Fedirko, V., Jenab, M., Romaguera, D., Siddiq, A., Bueno-de-Mesquita, H.B., Rohrmann, S.: The associations of advanced glycation end products and its soluble receptor with pancreatic cancer risk: a case-control study within the prospective EPIC Cohort. Cancer Epidemiol. Biomark. Prevention Publication Am. Assoc. Cancer Res. Cosponsored Am. Soc. Prev. Oncol. 21(4), 619–628 (2012). https://doi.org/10.1158/1055-9965.epi-11-1139

    Article  CAS  Google Scholar 

  32. Moy, K.A., Jiao, L., Freedman, N.D., Weinstein, S.J., Sinha, R., Virtamo, J., Albanes, D., Stolzenberg-Solomon, R.Z.: Soluble receptor for advanced glycation end products and risk of liver cancer. Hepatol. (Baltimore, Md.) 57(6), 2338–2345 (2013). https://doi.org/10.1002/hep.26264

  33. Yang, S., Pinney, S.M., Mallick, P., Ho, S.M., Bracken, B., Wu, T.: Impact of Oxidative Stress Biomarkers and Carboxymethyllysine (an Advanced Glycation End Product) on Prostate Cancer: A Prospective Study. Clin. Genitourin. Cancer 13(5), e347–e351 (2015). https://doi.org/10.1016/j.clgc.2015.04.004

    Article  PubMed  PubMed Central  Google Scholar 

  34. Jiao, L., Taylor, P.R., Weinstein, S.J., Graubard, B.I., Virtamo, J., Albanes, D., Stolzenberg-Solomon, R.Z.: Advanced glycation end products, soluble receptor for advanced glycation end products, and risk of colorectal cancer. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 20(7), 1430–1438 (2011). https://doi.org/10.1158/1055-9965.epi-11-0066

    Article  CAS  Google Scholar 

  35. Aglago, E.K., Schalkwijk, C.G., Freisling, H., Fedirko, V., Hughes, D.J., Jiao, L., Dahm, C.C., Olsen, A., Tjønneland, A., Katzke, V., Johnson, T., Schulze, M.B., Aleksandrova, K., Masala, G., Sieri, S., Simeon, V., Tumino, R., Macciotta, A., Bueno-De-Mesquita, B., Skeie, G., Gram, I.T., Sandanger, T., Jakszyn, P., Sánchez, M.J., Amiano, P., Colorado-Yohar, S.M., Gurrea, A.B., Perez-Cornago, A., Mayén, A.L., Weiderpass, E., Gunter, M.J., Heath, A.K., Jenab, M.: Plasma concentrations of advanced glycation end-products and colorectal cancer risk in the EPIC study. Carcinogenesis 42(5), 705–713 (2021). https://doi.org/10.1093/carcin/bgab026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kong, S.Y., Takeuchi, M., Hyogo, H., McKeown-Eyssen, G., Yamagishi, S.I., Chayama, K., O'Brien, P.J., Ferrari, P., Overvad, K., Olsen, A., Tjønneland, A., Boutron-Ruault, M.C., Bastide, N., Carbonnel, F., Kühn, T., Kaaks, R., Boeing, H., Aleksandrova, K., Trichopoulou, A., Lagiou, P., Vasilopoulou, E., Masala, G., Pala, V., De Magistris, M.S., Tumino, R., Naccarati, A., Bueno-De-Mesquita, H.B., Peeters, P.H., Weiderpass, E., Quiŕos, J.R., Jakszyn, P., ͆anchez, M.J., Dorronsoro, M., Gavrila, D., Ardanaz, E., Rutegård, M., Nyström, H., Wareham, N.J., Khaw, K.T., Bradbury, K.E., Romieu, I., Freisling, H., Stavropoulou, F., Gunter, M.J., Cross, A.J., Riboli, E., Jenab, M., Bruce, W.R.: The association between glyceraldehyde-derived advanced glycation end-products and colorectal cancer risk. Cancer Epidemiol. Biomark. Prevention. 24(12), 1855–1863 (2015). https://doi.org/10.1158/1055-9965.EPI-15-0422

  37. Chen, L., Duan, Z., Tinker, L., Sangi-Haghpeykar, H., Strickler, H., Ho, G.Y., Gunter, M.J., Rohan, T., Logsdon, C., White, D.L., Royse, K., El-Serag, H.B., Jiao, L.: A prospective study of soluble receptor for advanced glycation end-products and colorectal cancer risk in postmenopausal women. Cancer Epidemiol. 42, 115–123 (2016). https://doi.org/10.1016/j.canep.2016.04.004

    Article  PubMed  PubMed Central  Google Scholar 

  38. Aglago, E.K., Rinaldi, S., Freisling, H., Jiao, L., Hughes, D.J., Fedirko, V., Schalkwijk, C.G., Weiderpass, E., Dahm, C.C., Overvad, K., Eriksen, A.K., Kyrø, C., Boutron-Ruault, M.C., Rothwell, J.A., Severi, G., Katzke, V., Kühn, T., Schulze, M.B., Aleksandrova, K., Masala, G., Krogh, V., Panico, S., Tumino, R., Naccarati, A., Bueno-de-Mesquita, B., van Gils, C.H., Sandanger, T.M., Gram, I.T., Skeie, G., Quirós, J.R., Jakszyn, P., Sánchez, M.J., Amiano, P., Huerta, J.M., Ardanaz, E., Johansson, I., Harlid, S., Perez-Cornago, A., Mayén, A.L., Cordova, R., Gunter, M.J., Vineis, P., Cross, A.J., Riboli, E., Jenab, M.: Soluble Receptor for Advanced Glycation End-products (sRAGE) and Colorectal Cancer Risk: A Case-Control Study Nested within a European Prospective Cohort. Cancer Epidemiol, Biomark. Prevention Publication Am. Assoc. Cancer Res. Cosponsored Am. Soc. Prev. Oncol. 30(1), 182–192 (2021). https://doi.org/10.1158/1055-9965.epi-20-0855

    Article  Google Scholar 

  39. Zhou, X., Lin, N., Zhang, M., Wang, X., An, Y., Su, Q., Du, P., Li, B., Chen, H.: Circulating soluble receptor for advanced glycation end products and other factors in type 2 diabetes patients with colorectal cancer. BMC Endocr. Disord. 20(1), 170 (2020). https://doi.org/10.1186/s12902-020-00647-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Leclerc, E., Fritz, G., Vetter, S.W., Heizmann, C.W.: Binding of S100 proteins to RAGE: an update. Biochim. Biophys. Acta. Mol. Cell. Res. 1793(6), 993–1007 (2009)

  41. Dariya, B., Nagaraju, G.P.: Advanced glycation end products in diabetes, cancer and phytochemical therapy. Drug Discov. Today 25(9), 1614–1623 (2020)

    Article  CAS  PubMed  Google Scholar 

  42. Santilli, F., Vazzana, N., Bucciarelli, L.G., Davi, G.: Soluble forms of RAGE in human diseases: clinical and therapeutical implications. Curr. Med. Chem. 16(8), 940–952 (2009)

    Article  CAS  PubMed  Google Scholar 

  43. Liliensiek, B., Weigand, M.A., Bierhaus, A., Nicklas, W., Kasper, M., Hofer, S., Plachky, J., Gröne, H.-J., Kurschus, F.C., Schmidt, A.M.: Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J. Clin. Investig. 113(11), 1641–1650 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wagner, N.B., Weide, B., Reith, M., Tarnanidis, K., Kehrel, C., Lichtenberger, R., Pflugfelder, A., Herpel, E., Eubel, J., Ikenberg, K.: Diminished levels of the soluble form of RAGE are related to poor survival in malignant melanoma. Int. J. Cancer 137(11), 2607–2617 (2015)

    Article  CAS  PubMed  Google Scholar 

  45. Taguchi, A., Blood, D.C., del Toro, G., Canet, A., Lee, D.C., Qu, W., Tanji, N., Lu, Y., Lalla, E., Fu, C.: Blockade of RAGE–amphoterin signalling suppresses tumour growth and metastases. Nature 405(6784), 354–360 (2000)

    Article  CAS  PubMed  Google Scholar 

  46. Chen, Y., Yan, S.S., Colgan, J., Zhang, H.-P., Luban, J., Schmidt, A.M., Stern, D., Herold, K.C.: Blockade of late stages of autoimmune diabetes by inhibition of the receptor for advanced glycation end products. J. Immunol. 173(2), 1399–1405 (2004)

    Article  CAS  PubMed  Google Scholar 

  47. Heier, M., Margeirsdottir, H.D., Gaarder, M., Stensæth, K.H., Brunborg, C., Torjesen, P.A., Seljeflot, I., Hanssen, K.F., Dahl-Jørgensen, K.: Soluble RAGE and atherosclerosis in youth with type 1 diabetes: a 5-year follow-up study. Cardiovasc. Diabetol. 14(1), 1–8 (2015)

    Article  Google Scholar 

  48. Lee, J., Yun, J.-S., Ko, S.-H.: Advanced glycation end products and their effect on vascular complications in type 2 Diabetes mellitus. Nutrients 14(15), 3086 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Hudson, B.I., Stickland, M.H., Grant, P.J., Futers, T.S.: Characterization of allelic and nucleotide variation between the RAGE gene on chromosome 6 and a homologous pseudogene sequence to its 5′ regulatory region on chromosome 3: implications for polymorphic studies in diabetes. Diabetes 50(12), 2646–2651 (2001)

    Article  CAS  PubMed  Google Scholar 

  50. Hofmann, M., Drury, S., Hudson, B., Gleason, M., Qu, W., Lu, Y., Lalla, E., Chitnis, S., Monteiro, J., Stickland, M.: RAGE and arthritis: the G82S polymorphism amplifies the inflammatory response. Genes Immun. 3(3), 123–135 (2002)

    Article  CAS  PubMed  Google Scholar 

  51. Xu, Y., Lu, Z., Shen, N., Wang, X.: Association of RAGE rs1800625 polymorphism and cancer risk: a meta-analysis of 18 case-control studies. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res. 25, 7026 (2019)

    CAS  Google Scholar 

  52. Geduk, A., Oztas, B., Eryılmaz, B.H., Demirsoy, E.T., Menguc, M.U., Unal, S., Mersin, S., Polat, M.G., Aygun, K., Yenihayat, E.M., Albayrak, H., Erol, H.A., Balcı, S., Mehtap1, O., Tarkun1, P., Hacihanefioglu1, A.: Effects of AGEs, sRAGE and HMGB1 on Clinical Outcomes in Multiple MyelomaIn. Indian J. Hematol. Blood. Transfus. 39, 220–227 (2023). https://doi.org/10.1007/s12288-022-01574-6

  53. Cho, C.H., Cha, J.: Analysis of neutrophil gelatinase-associated lipocalin, vascular endothelial growth factor, and soluble receptor for advanced glycation end-products in bone marrow supernatant in hematologic malignancies. Clin. Biochem. 80, 19–24 (2020). https://doi.org/10.1016/j.clinbiochem.2020.04.002

    Article  CAS  PubMed  Google Scholar 

  54. Krechler, T., Jáchymová, M., Mestek, O., Zák, A., Zima, T., Kalousová, M.: Soluble receptor for advanced glycation end-products (sRAGE) and polymorphisms of RAGE and glyoxalase I genes in patients with pancreas cancer. Clin. Biochem. 43(10–11), 882–886 (2010). https://doi.org/10.1016/j.clinbiochem.2010.04.004

    Article  CAS  PubMed  Google Scholar 

  55. Kan, H., Yamagishi, S.I., Ojima, A., Fukami, K., Ueda, S., Takeuchi, M., Hyogo, H., Aikata, H., Chayama, K.: Elevation of Serum Levels of Advanced Glycation End Products in Patients With Non-B or Non-C Hepatocellular Carcinoma. J. Clin. Lab. Anal. 29(6), 480–484 (2015). https://doi.org/10.1002/jcla.21797

    Article  CAS  PubMed  Google Scholar 

  56. Heidari, F., Rabizadeh, S., Ali Mansournia, M., Mirmiranpoor, H., Salehi, S.S., Akhavan, S., Esteghamati, A., Nakhjavani, M.: Inflammatory, oxidative stress and anti-oxidative markers in patients with endometrial carcinoma and diabetes. Cytokine 120, 186–190 (2019). https://doi.org/10.1016/j.cyto.2019.05.007

    Article  CAS  PubMed  Google Scholar 

  57. Zińczuk, J., Maciejczyk, M., Zaręba, K., Romaniuk, W., Markowski, A., Kędra, B., Zalewska, A., Pryczynicz, A., Matowicka-Karna, J., Guzińska-Ustymowicz, K.: Antioxidant barrier, redox status, and oxidative damage to biomolecules in patients with colorectal cancer. Can malondialdehyde and catalase be markers of colorectal cancer advancement? Biomol 9(10), 637 (2019). https://doi.org/10.3390/biom9100637

  58. Felicetti, F., Aimaretti, E., Dal Bello, F., Gatti, F., Godono, A., Saba, F., Einaudi, G., Collino, M., Fagioli, F., Aragno, M., Brignardello, E.: Advanced glycation end products and their related signaling cascades in adult survivors of childhood Hodgkin lymphoma: A possible role in the onset of late complications. Free Radical Biol. Med. 178, 76–82 (2022). https://doi.org/10.1016/j.freeradbiomed.2021.11.036

    Article  CAS  Google Scholar 

  59. Khan, H., Alouffi, S., Alatar, A.A., Qahtan, A.A., Faisal, M., Ahmad, S.: Glycoxidative profile of cancer patient serum: A clinical result to associate glycation to cancer. Glycobiol. 30(3), 152–158 (2021). https://doi.org/10.1093/GLYCOB/CWZ093

    Article  Google Scholar 

  60. Gaens, K.H., Goossens, G.H., Niessen, P.M., van Greevenbroek, M.M., van der Kallen, C.J., Niessen, H.W., Rensen, S.S., Buurman, W.A., Greve, J.W.M., Blaak, E.E.: Nε-(carboxymethyl) lysine-receptor for advanced glycation end product axis is a key modulator of obesity-induced dysregulation of adipokine expression and insulin resistance. Arterioscler. Thromb. Vasc. Biol. 34(6), 1199–1208 (2014)

    Article  CAS  PubMed  Google Scholar 

  61. Koschinsky, T., He, C.-J., Mitsuhashi, T., Bucala, R., Liu, C., Buenting, C., Heitmann, K., Vlassara, H.: Orally absorbed reactive glycation products (glycotoxins): an environmental risk factor in diabetic nephropathy. Proc. Natl. Acad. Sci. 94(12), 6474–6479 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kizer, J.R., Benkeser, D., Arnold, A.M., Ix, J.H., Mukamal, K.J., Djousse, L., Tracy, R.P., Siscovick, D.S., Psaty, B.M., Zieman, S.J.: Advanced glycation/glycoxidation endproduct carboxymethyl-lysine and incidence of coronary heart disease and stroke in older adults. Atherosclerosis 235(1), 116–121 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Jiao, L., Stolzenberg-Solomon, R., Zimmerman, T.P., Duan, Z., Chen, L., Kahle, L., Risch, A., Subar, A.F., Cross, A.J., Hollenbeck, A.: Dietary consumption of advanced glycation end products and pancreatic cancer in the prospective NIH-AARP Diet and Health Study. Am. J. Clin. Nutr. 101(1), 126–134 (2015)

    Article  CAS  PubMed  Google Scholar 

  64. Omofuma, O.O., Turner, D.P., Peterson, L.L., Merchant, A.T., Zhang, J., Steck, S.E.: Dietary advanced glycation end-products (AGE) and risk of breast cancer in the prostate, lung, colorectal and ovarian cancer screening trial (PLCO). Cancer Prev. Res. 13(7), 601–610 (2020)

    Article  CAS  Google Scholar 

Download references

Funding

This study was funded by Urmia University of Medical Sciences, Urmia, Iran.

Author information

Authors and Affiliations

  1. Patient Safety Research Center, Clinical Research Institute, Urmia University of Medical Sciences, Urmia, Iran

    Fatemeh Hajizadeh-Sharafabad, Farzad Gerami & Mohammad Reza Pashaei

  2. Colorectal Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

    Sara Shojaei-Zarghani

  3. Student Research Committee, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Elham Sharifi-Zahabi

  4. Department of Internal Medicine, School of Medicine, Urmia University of Medical Sciences, Urmia, Iran

    Mohammad Reza Pashaei

Authors
  1. Fatemeh Hajizadeh-Sharafabad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sara Shojaei-Zarghani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elham Sharifi-Zahabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Farzad Gerami
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammad Reza Pashaei
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FHS: Contributed to the study conception, design and data collection, and interpretation and drafting the manuscript. SSZ: Contributed to the data extraction, interpretation and drafting the manuscript. ESZ: Contributed to the data collection and drafting the manuscript. FG: Participated in the interpretation and drafting the manuscript. MP: Participated in revising the paper critically and approving the version of the manuscript being submitted.

Corresponding author

Correspondence to Mohammad Reza Pashaei.

Ethics declarations

Conflict of interest

The authors declare no financial or non-financial conflicts of interest.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 13 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hajizadeh-Sharafabad, F., Shojaei-Zarghani, S., Sharifi-Zahabi, E. et al. Associations of circulating advanced glycation end products and their soluble receptors with cancer risk: A systematic review and meta-analysis of observational studies. Glycoconj J 41, 35–46 (2024). https://doi.org/10.1007/s10719-024-10147-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-024-10147-w

Keywords

Search

Navigation