Skip to main content

Advertisement

SpringerLink
Log in

The role of oxygen tension in cell fate and regenerative medicine: implications of hypoxia/hyperoxia and free radicals

  • Full Length Paper
  • Published:
Cell and Tissue Banking Aims and scope Submit manuscript

Abstract

Oxygen pressure plays an integral role in regulating various aspects of cellular biology. Cell metabolism, proliferation, morphology, senescence, metastasis, and angiogenesis are some instances that are affected by different tensions of oxygen. Hyperoxia or high oxygen concentration, enforces the production of reactive oxygen species (ROS) that disturbs physiological homeostasis, and consequently, in the absence of antioxidants, cells and tissues are directed to an undesired fate. On the other side, hypoxia or low oxygen concentration, impacts cell metabolism and fate strongly through inducing changes in the expression level of specific genes. Thus, understanding the precise mechanism and the extent of the implication of oxygen tension and ROS in biological events is crucial to maintaining the desired cell and tissue function for application in regenerative medicine strategies. Herein, a comprehensive literature review has been performed to find out the impacts of oxygen tensions on the various behaviors of cells or tissues.

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
Fig. 4

Similar content being viewed by others

References

  • Achuthan S, Santhoshkumar TR, Prabhakar J, Nair SA, Pillai MR (2011) Drug-induced senescence generates chemoresistant stemlike cells with low reactive oxygen species. J Biol Chem 286(43):37813–37829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adelibieke Y, Shimizu H, Muteliefu G, Bolati D, Niwa T (2012) Indoxyl sulfate induces endothelial cell senescence by increasing reactive oxygen species production and p53 activity. J Ren Nutr 22(1):86–89

    Article  CAS  PubMed  Google Scholar 

  • Ahmed NE-MB, Murakami M, Kaneko S, Nakashima M (2016) The effects of hypoxia on the stemness properties of human dental pulp stem cells (DPSCs). Sci Rep 6:35476

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Al Tameemi W, Dale TP, Al-Jumaily RMK, Forsyth NR (2019) Hypoxia-modified cancer cell metabolism. Front Cell Dev Biol 7:4

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Ali MH, Schlidt SA, Chandel NS, Hynes KL, Schumacker PT, Gewertz BL (1999) Endothelial permeability and IL-6 production during hypoxia: role of ROS in signal transduction. Am J Physiol Lung Cell Mol Physiol 277(5):L1057–L1065

    Article  CAS  Google Scholar 

  • Allen J, Winterford C, Axelsen RA, GobÉ GC (1992) Effects of hypoxia on morphological and biochemical characteristics of renal epithelial cell and tubule cultures. Ren Fail 14(4):453–460

    Article  CAS  PubMed  Google Scholar 

  • Azad MB, Chen Y, Gibson SB (2009) Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 11(4):777–790

    Article  CAS  PubMed  Google Scholar 

  • Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120(4):483–495

    Article  CAS  PubMed  Google Scholar 

  • Bals R, Hiemstra P (2004) Innate immunity in the lung: how epithelial cells fight against respiratory pathogens. Eur Respir J 23(2):327–333

    Article  CAS  PubMed  Google Scholar 

  • Bandarra D, Rocha S (2013) Tale of two transcription factors: NF-кB and HIF crosstalk. OA Mol Cell Biol 1(1):1–7

    Article  Google Scholar 

  • Bandarra D, Biddlestone J, Mudie S, Müller H-AJ, Rocha S (2015) HIF-1α restricts NF-κB-dependent gene expression to control innate immunity signals. Dis Model Mech 8(2):169–181

    PubMed  Google Scholar 

  • Barazzone-Argiroffo C, Muzzin P, Donati YR, Kan C-D, Aubert ML, Piguet P-F (2001) Hyperoxia increases leptin production: a mechanism mediated through endogenous elevation of corticosterone. Am J Physiol Lung Cell Mol Physiol 281(5):L1150–L1156

    Article  CAS  PubMed  Google Scholar 

  • Bardaweel SK, Gul M, Alzweiri M, Ishaqat A, ALSalamat HA, Bashatwah RM (2018) Reactive oxygen species: the dual role in physiological and pathological conditions of the human body. Eurasian J Med 50(3):193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bäumer AT, Ten Freyhaus H, Sauer H, Wartenberg M, Kappert K, Schnabel P et al (2008) Phosphatidylinositol 3-kinase-dependent membrane recruitment of Rac-1 and p47phox is critical for α-platelet-derived growth factor receptor-induced production of reactive oxygen species. J Biol Chem 283(12):7864–7876

    Article  PubMed  Google Scholar 

  • Benderro GF, Sun X, Kuang Y, LaManna JC (2012) Decreased VEGF expression and microvascular density, but increased HIF-1 and 2α accumulation and EPO expression in chronic moderate hyperoxia in the mouse brain. Brain Res 1471:46–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolisetty S, Jaimes EA (2013) Mitochondria and reactive oxygen species: physiology and pathophysiology. Int J Mol Sci 14(3):6306–6344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bragg R, Gilbert W, Elmansi AM, Isales CM, Hamrick MW, Hill WD et al (2019) Stromal cell-derived factor-1 as a potential therapeutic target for osteoarthritis and rheumatoid arthritis. Ther Adv Chron Dis 10:2040622319882531

    CAS  Google Scholar 

  • Brown BN, Ratner BD, Goodman SB, Amar S, Badylak SF (2012) Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine. Biomaterials 33(15):3792–3802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brueckl C, Kaestle S, Kerem A, Habazettl H, Krombach F, Kuppe H et al (2006) Hyperoxia-induced reactive oxygen species formation in pulmonary capillary endothelial cells in situ. Am J Respir Cell Mol Biol 34(4):453–463

    Article  CAS  PubMed  Google Scholar 

  • Busuttil RA, Rubio M, Dollé ME, Campisi J, Vijg J (2003) Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture. Aging Cell 2(6):287–294

    Article  CAS  PubMed  Google Scholar 

  • Cameron C, Harding F, Hu W-S, Kaufman DS (2008) Activation of hypoxic response in human embryonic stem cell–derived embryoid bodies. Exp Biol Med 233(8):1044–1057

    Article  CAS  Google Scholar 

  • Carreau A, Hafny-Rahbi BE, Matejuk A, Grillon C, Kieda C (2011) Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J Cell Mol Med 15(6):1239–1253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaddha A, Broytman O, Teodorescu M (2020) Effects of allergic airway inflammation and chronic intermittent hypoxia on systemic blood pressure. Am J Physiol Regul Integr Comp Physiol 319(5):R566–R574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L-W, Egan L, Li Z-W, Greten FR, Kagnoff MF, Karin M (2003) The two faces of IKK and NF-κB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat Med 9(5):575–581

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Andresen BT, Hill M, Zhang J, Booth F, Zhang C (2008) Role of reactive oxygen species in tumor necrosis factor-alpha induced endothelial dysfunction. Curr Hypertens Rev 4(4):245–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen CC, Hsia CW, Ho CW, Liang CM, Chen CM, Huang KL et al (2017) Hypoxia and hyperoxia differentially control proliferation of rat neural crest stem cells via distinct regulatory pathways of the HIF1α–CXCR4 and TP53–TPM1 proteins. Dev Dyn 246(3):162–185

    Article  CAS  PubMed  Google Scholar 

  • Choudhry H, Harris AL (2018) Advances in Hypoxia-Inducible Factor Biology. Cell Metab 27(2):281–298

    Article  CAS  PubMed  Google Scholar 

  • Cipolleschi MG, Dello Sbarba P, Olivotto M (1993) The role of hypoxia in the maintenance of hematopoietic stem cells

  • Colavitti R, Finkel T (2005) Reactive oxygen species as mediators of cellular senescence. IUBMB Life 57(4–5):277–281

    Article  CAS  PubMed  Google Scholar 

  • Coppé J-P, Patil CK, Rodier F, Krtolica A, Beauséjour CM, Parrinello S et al (2010) A human-like senescence-associated secretory phenotype is conserved in mouse cells dependent on physiological oxygen. PLoS ONE 5(2):e9188

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Corcoran SE, O’Neill LA (2016) HIF1α and metabolic reprogramming in inflammation. J Clin Investig 126(10):3699–3707

    Article  PubMed  PubMed Central  Google Scholar 

  • Cowden Dahl KD, Fryer BH, Mack FA, Compernolle V, Maltepe E, Adelman DM et al (2005) Hypoxia-inducible factors 1α and 2α regulate trophoblast differentiation. Mol Cell Biol 25(23):10479–10491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Csete M (2005) Oxygen in the cultivation of stem cells. Ann N Y Acad Sci 1049(1):1–8

    Article  ADS  MathSciNet  CAS  PubMed  Google Scholar 

  • Cubero FJ, Nieto N (2012) Arachidonic acid stimulates TNFα production in Kupffer cells via a reactive oxygen species-pERK1/2-Egr1-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 303(2):G228–G239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das R, Jahr H, van Osch GJ, Farrell E (2010) The role of hypoxia in bone marrow–derived mesenchymal stem cells: considerations for regenerative medicine approaches. Tissue Eng Part B Rev 16(2):159–168

    Article  CAS  PubMed  Google Scholar 

  • Desmarquest P, Chadelat K, Corroyer S, Cazals V, Clement A (1998) Effect of hyperoxia on human macrophage cytokine response. Respir Med 92(7):951–960

    Article  CAS  PubMed  Google Scholar 

  • Dewhirst MW, Cao Y, Moeller B (2008) Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat Rev Cancer 8(6):425–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Girolamo FG, Fiotti N, Sisto UG, Nunnari A, Colla S, Mearelli F et al (2022) Skeletal muscle in hypoxia and inflammation: insights on the COVID-19 pandemic. Front Nutr 9:865402

    Article  PubMed  PubMed Central  Google Scholar 

  • Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82(1):47–95

    Article  PubMed  Google Scholar 

  • Dvornikova KA, Platonova ON, Bystrova EY (2023) Hypoxia and intestinal inflammation: common molecular mechanisms and signaling pathways. Int J Mol Sci 24(3):2425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Efimenko A, Starostina E, Kalinina N, Stolzing A (2011) Angiogenic properties of aged adipose derived mesenchymal stem cells after hypoxic conditioning. J Transl Med 9(1):1–13

    Article  Google Scholar 

  • Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eren, M. K. (2023) Hypoxia and senescence: role of oxygen in modulation of tumor suppression. In: Hypoxia in cancer: significance and impact on cancer therapy, pp 89–117

  • Fan F, Sun L, Zhang D, Zhu L, Wang S, Wang D (2018) Effects of red blood cell supernatants on hypoxia/reoxygenation injury in H9C2 cells. Int J Clin Exp Med 11(4):3612–3619

    Google Scholar 

  • Fang J, Seki T, Maeda H (2009) Therapeutic strategies by modulating oxygen stress in cancer and inflammation. Adv Drug Deliv Rev 61(4):290–302

    Article  CAS  PubMed  Google Scholar 

  • Fattahi R, Soleimani M, Khani M-M, Rasouli M, Hosseinzadeh S (2023) A three-dimensional structure with osteoconductive function made of O-carboxymethyl chitosan using aspirin as a cross-linker. Int J Polym Mater Polym Biomat 1–17

  • Finkel T (1998) Oxygen radicals and signaling. Curr Opin Cell Biol 10(2):248–253

    Article  CAS  PubMed  Google Scholar 

  • Fong G-H (2009) Regulation of angiogenesis by oxygen sensing mechanisms. J Mol Med 87(6):549–560

    Article  CAS  PubMed  Google Scholar 

  • Forsyth NR, Musio A, Vezzoni P, Simpson AHR, Noble BS, McWhir J (2006) Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities. Cloning Stem Cells 8(1):16–23

    Article  CAS  PubMed  Google Scholar 

  • Furuta C, Miyamoto T, Takagi T, Noguchi Y, Kaneko J, Itoh S et al (2015) Transforming growth factor-β signaling enhancement by long-term exposure to hypoxia in a tumor microenvironment composed of L Ewis lung carcinoma cells. Cancer Sci 106(11):1524–1533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genbacev O, Zhou Y, Ludlow JW, Fisher SJ (1997) Regulation of human placental development by oxygen tension. Science 277(5332):1669–1672

    Article  CAS  PubMed  Google Scholar 

  • Ghaffari S (2008) Oxidative stress in the regulation of normal and neoplastic hematopoiesis. Antioxid Redox Signal 10(11):1923–1940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glass JJ, Phillips PA, Gunning PW, Stehn JR (2015) Hypoxia alters the recruitment of tropomyosins into the actin stress fibres of neuroblastoma cells. BMC Cancer 15:712

    Article  PubMed  PubMed Central  Google Scholar 

  • Grayson WL, Zhao F, Bunnell B, Ma T (2007) Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 358(3):948–953

    Article  CAS  PubMed  Google Scholar 

  • Greenwald AC, Licht T, Kumar S, Oladipupo SS, Iyer S, Grunewald M et al (2019) VEGF expands erythropoiesis via hypoxia-independent induction of erythropoietin in noncanonical perivascular stromal cells. J Exp Med 216(1):215–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grocott MP, Martin DS, Levett DZ, McMorrow R, Windsor J, Montgomery HE (2009) Arterial blood gases and oxygen content in climbers on Mount Everest. N Engl J Med 360(2):140–149

    Article  CAS  PubMed  Google Scholar 

  • Guitart A, Debeissat C, Hermitte F, Villacreces A, Ivanovic Z, Boeuf H et al (2011) Very low oxygen concentration (0.1%) reveals two FDCP-Mix cell subpopulations that differ by their cell cycling, differentiation and p27 KIP1 expression. Cell Death Differ 18(1):174–182

    Article  CAS  PubMed  Google Scholar 

  • Gupta SC, Hevia D, Patchva S, Park B, Koh W, Aggarwal BBJA et al (2012) Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 16(11):1295–1322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris AL (2002) Hypoxia—a key regulatory factor in tumour growth. Nat Rev Cancer 2(1):38–47

    Article  CAS  PubMed  Google Scholar 

  • Harrison JS, Rameshwar P, Chang V, Bandari P (2002) Oxygen saturation in the bone marrow of healthy volunteers. Blood J Am Soc Hematol 99(1):394–394

    CAS  Google Scholar 

  • Hartmann G, Tschöp M, Fischer R, Bidlingmaier C, Riepl R, Tschöp K et al (2000) High altitude increases circulating interleukin-6, interleukin-1 receptor antagonist and C-reactive protein. Cytokine 12(3):246–252

    Article  CAS  PubMed  Google Scholar 

  • Hielscher A, Qiu C, Porterfield J, Smith Q, Gerecht S (2013) Hypoxia affects the structure of breast cancer cell-derived matrix to support angiogenic responses of endothelial cells. J Carcinog Mutagen 005

  • Hsu Y-H, Lin R-M, Chiu Y-S, Liu W-L, Huang K-Y (2020) Effects of IL-1β, IL-20, and BMP-2 on intervertebral disc inflammation under hypoxia. J Clin Med 9(1):140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu X, Yu SP, Fraser JL, Lu Z, Ogle ME, Wang J-A et al (2008) Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 135(4):799–808

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Zitta K, Bein B, Steinfath M, Albrecht M (2013) An insert-based enzymatic cell culture system to rapidly and reversibly induce hypoxia: investigations of hypoxia-induced cell damage, protein expression and phosphorylation in neuronal IMR-32 cells. Dis Model Mech 6(6):1507–1514

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang D, Fang F, Xu F (2016) Hyperoxia induces inflammation and regulates cytokine production in alveolar epithelium through TLR2/4-NF-κB-dependent mechanism. Eur Rev Med Pharmacol Sci 20(7):1399–1410

    CAS  PubMed  Google Scholar 

  • Hubbi ME, Semenza GL (2015) Regulation of cell proliferation by hypoxia-inducible factors. Am J Physiol Cell Physiol 309(12):C775-782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue M, Sato EF, Nishikawa M, Park A-M, Kira Y, Imada I et al (2003) Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr Med Chem 10(23):2495–2505

    Article  CAS  PubMed  Google Scholar 

  • Isik B, Thaler R, Goksu BB, Conley SM, Al-Khafaji H, Mohan A et al (2021) Hypoxic preconditioning induces epigenetic changes and modifies swine mesenchymal stem cell angiogenesis and senescence in experimental atherosclerotic renal artery stenosis. Stem Cell Res Ther 12(1):1–13

    Article  Google Scholar 

  • Izyumov D, Domnina L, Nepryakhina O, Avetisyan A, Golyshev S, Ivanova OY et al (2010) Mitochondria as source of reactive oxygen species under oxidative stress. Study with novel mitochondria-targeted antioxidants—the “Skulachev-ion” derivatives. Biochemistry 75(2):123–129

    CAS  PubMed  Google Scholar 

  • Jamieson D, Chance B, Cadenas E, Boveris A (1986) The relation of free radical production to hyperoxia. Annu Rev Physiol 48(1):703–719

    Article  CAS  PubMed  Google Scholar 

  • Janssen A, Bosman C, Kruidenier L, Griffioen G, Lamers C, Van Krieken J et al (1999) Superoxide dismutases in the human colorectal cancer sequence. J Cancer Res Clin Oncol 125(6):327–335

    Article  CAS  PubMed  Google Scholar 

  • Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y et al (2005) Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 11(11):1173–1179

    Article  CAS  PubMed  Google Scholar 

  • Jin Z, El-Deiry WS (2005) Overview of cell death signaling pathways. Cancer Biol Ther 4(2):147–171

    Article  Google Scholar 

  • Jones DP, Sies H (2015) The redox code. Antioxid Redox Signal 23(9):734–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kammerer T, Faihs V, Hulde N, Stangl M, Brettner F, Rehm M et al (2020) Hypoxic-inflammatory responses under acute hypoxia: in Vitro experiments and prospective observational expedition trial. Int J Mol Sci 21(3):1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karhausen J, Furuta GT, Tomaszewski JE, Johnson RS, Colgan SP, Haase VH (2004) Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J Clin Invest 114:1098–1106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kendall AC, Whatmore JL, Harries LW, Winyard PG, Smerdon GR, Eggleton P (2012) Changes in inflammatory gene expression induced by hyperbaric oxygen treatment in human endothelial cells under chronic wound conditions. Exp Cell Res 318(3):207–216

    Article  CAS  PubMed  Google Scholar 

  • Kim DS, Ko YJ, Lee MW, Park HJ, Park YJ, Kim D-I et al (2016) Effect of low oxygen tension on the biological characteristics of human bone marrow mesenchymal stem cells. Cell Stress Chaperones 21(6):1089–1099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kingham PJ, McLean WG, Walsh M-T, Fryer AD, Gleich GJ, Costello RW (2003) Effects of eosinophils on nerve cell morphology and development: the role of reactive oxygen species and p38 MAP kinase. Am J Physiol Lung Cell Mol Physiol 285(4):L915–L924

    Article  CAS  PubMed  Google Scholar 

  • Klimkiewicz K, Weglarczyk K, Collet G, Paprocka M, Guichard A, Sarna M et al (2017) A 3D model of tumour angiogenic microenvironment to monitor hypoxia effects on cell interactions and cancer stem cell selection. Cancer Lett 396:10–20

    Article  CAS  PubMed  Google Scholar 

  • Kofoed H, Sjøntoft E, Siemssen SO, Olesen HP (1985) Bone marrow circulation after osteotomy: blood flow, po2, pCO2, and pressure studied in dogs. Acta Orthop Scand 56(5):400–403

    Article  CAS  PubMed  Google Scholar 

  • Kong Q, Beel J, Lillehei K (2000) A threshold concept for cancer therapy. Med Hypotheses 55(1):29–35

    Article  CAS  PubMed  Google Scholar 

  • Kuhlicke J, Frick JS, Morote-Garcia JC, Rosenberger P, Eltzschig HK (2007) Hypoxia inducible factor (HIF)-1 coordinates induction of Toll-like receptors TLR2 and TLR6 during hypoxia. PLoS ONE 2(12):e1364

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Kumari S, Badana AK, Malla R (2018) Reactive oxygen species: a key constituent in cancer survival. Biomark Insights 13:1177271918755391

    Article  PubMed  PubMed Central  Google Scholar 

  • Kwak DJ, Kwak SD, Gauda EB (2006) The effect of hyperoxia on reactive oxygen species (ROS) in rat petrosal ganglion neurons during development using organotypic slices. Pediatr Res 60(4):371–376

    Article  CAS  PubMed  Google Scholar 

  • Lacza Z, Snipes JA, Zhang J, Horváth EM, Figueroa JP, Szabó C et al (2003) Mitochondrial nitric oxide synthase is not eNOS, nNOS or iNOS. Free Radical Biol Med 35(10):1217–1228

    Article  CAS  Google Scholar 

  • Lambert AJ, Boysen HM, Buckingham JA, Yang T, Podlutsky A, Austad SN et al (2007) Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell 6(5):607–618

    Article  CAS  PubMed  Google Scholar 

  • Lange C, Turrero Garcia M, Decimo I, Bifari F, Eelen G, Quaegebeur A et al (2016) Relief of hypoxia by angiogenesis promotes neural stem cell differentiation by targeting glycolysis. EMBO J 35(9):924–941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lassègue B, San Martín A, Griendling KK (2012) Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res 110(10):1364–1390

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis J, Lee J, Underwood J, Harris A, Lewis C (1999) Macrophage responses to hypoxia: relevance to disease mechanisms. J Leukoc Biol 66(6):889–900

    Article  CAS  PubMed  Google Scholar 

  • Li TS, Marbán E (2010) Physiological levels of reactive oxygen species are required to maintain genomic stability in stem cells. Stem Cells 28(7):1178–1185

    Article  CAS  PubMed  Google Scholar 

  • Lim H-J, Han J, Woo D-H, Kim S-E, Kim S-K, Kang H-G et al (2011) Biochemical and morphological effects of hypoxic environment on human embryonic stem cells in long-term culture and differentiating embryoid bodies. Mol Cells 31(2):123–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin Y-J, Chien B-YC, Lee Y-H (2022) Injectable and thermoresponsive hybrid hydrogel with Antibacterial, Anti-inflammatory, oxygen Transport, and enhanced cell growth activities for improved diabetic wound healing. Eur Polym J 175:111364

    Article  CAS  Google Scholar 

  • Lu T, Finkel T (2008) Free radicals and senescence. Exp Cell Res 314(9):1918–1922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lugano R, Ramachandran M, Dimberg A (2020) Tumor angiogenesis: Causes, consequences, challenges and opportunities. Cell Mol Life Sci 77(9):1745–1770

    Article  CAS  PubMed  Google Scholar 

  • Luis A, Sandalio LM, Palma J, Bueno P, Corpas J (1992) Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Radic Biol Med 13(5):557–580

    Article  Google Scholar 

  • Ma T, Grayson WL, Fröhlich M, Vunjak-Novakovic G (2009) Hypoxia and stem cell-based engineering of mesenchymal tissues. Biotechnol Prog 25(1):32–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma T, Hao Y, Li S, Xia B, Gao X, Zheng Y et al (2022) Sequential oxygen supply system promotes peripheral nerve regeneration by enhancing Schwann cells survival and angiogenesis. Biomaterials 289:121755

    Article  CAS  PubMed  Google Scholar 

  • Macip S, Igarashi M, Berggren P, Yu J, Lee SW, Aaronson SA (2003) Influence of induced reactive oxygen species in p53-mediated cell fate decisions. Mol Cell Biol 23(23):8576–8585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacMillan-Crow LA, Crow JP, Thompson JA (1998) Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37(6):1613–1622

    Article  CAS  PubMed  Google Scholar 

  • Malladi P, Xu Y, Chiou M, Giaccia AJ, Longaker MT (2006) Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol Cell Physiol 290(4):C1139–C1146

    Article  CAS  PubMed  Google Scholar 

  • Martindale JL, Holbrook NJ (2002) Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 192(1):1–15

    Article  CAS  PubMed  Google Scholar 

  • Martínez JA, Cordero P, Campión J, Milagro FI (2012) Interplay of early-life nutritional programming on obesity, inflammation and epigenetic outcomes. Proc Nutr Soc 71(2):276–283

    Article  PubMed  Google Scholar 

  • Matés JM, Sánchez-Jiménez FM (2000) Role of reactive oxygen species in apoptosis: implications for cancer therapy. Int J Biochem Cell Biol 32(2):157–170

    Article  PubMed  Google Scholar 

  • Matsuoka J, Yashiro M, Doi Y, Fuyuhiro Y, Kato Y, Shinto O et al (2013) Hypoxia stimulates the EMT of gastric cancer cells through autocrine TGFβ signaling. PLoS ONE 8(5):e62310

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Medzhitov R (2008) Origin and physiological roles of inflammation. Nature 454(7203):428–435

    Article  ADS  CAS  PubMed  Google Scholar 

  • Miller JT, Bartley JH, Wimborne HJ, Walker AL, Hess DC, Hill WD et al (2005) The neuroblast and angioblast chemotaxic factor SDF-1 (CXCL12) expression is briefly up regulated by reactive astrocytes in brain following neonatal hypoxic-ischemic injury. BMC Neurosci 6(1):1–11

    Article  Google Scholar 

  • Mohd Ali N, Boo L, Yeap SK, Ky H, Satharasinghe DA, Liew WC et al (2016) Probable impact of age and hypoxia on proliferation and microRNA expression profile of bone marrow-derived human mesenchymal stem cells. PeerJ 4:e1536

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy CL, Polak JM (2004) Control of human articular chondrocyte differentiation by reduced oxygen tension. J Cell Physiol 199(3):451–459

    Article  CAS  PubMed  Google Scholar 

  • Nath A, Chakrabarti P, Sen S, Barui A (2022) Reactive oxygen species in modulating intestinal stem cell dynamics and function. Stem Cell Rev Rep 18(7):2328–2350

    Article  CAS  PubMed  Google Scholar 

  • Näthke I, Rocha S (2011) Antagonistic crosstalk between APC and HIF-1α. Cell Cycle 10(10):1545–1547

    Article  PubMed  PubMed Central  Google Scholar 

  • Nayadu S, Kaur G, Gudi G, Addepalli V (2012) The potentials of selected therapeutic targets for inflammation: a snapshot. Recent Pat Inflamm Allergy Drug Discov 6(2):137–146

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa M (2008) Reactive oxygen species in tumor metastasis. Cancer Lett 266(1):53–59

    Article  CAS  PubMed  Google Scholar 

  • Oeseburg H, de Boer RA, Buikema H, van der Harst P, van Gilst WH, Silljé HH (2010) Glucagon-like peptide 1 prevents reactive oxygen species-induced endothelial cell senescence through the activation of protein kinase A. Arterioscler Thromb Vasc Biol 30(7):1407–1414

    Article  CAS  PubMed  Google Scholar 

  • Ozben T (2007) Oxidative stress and apoptosis: impact on cancer therapy. J Pharm Sci 96(9):2181–2196

    Article  CAS  PubMed  Google Scholar 

  • Panieri E, Gogvadze V, Norberg E, Venkatesh R, Orrenius S, Zhivotovsky B (2013) Reactive oxygen species generated in different compartments induce cell death, survival, or senescence. Free Radic Biol Med 57:176–187

    Article  CAS  PubMed  Google Scholar 

  • Park TY, Jeon EY, Kim HJ, Choi B-H, Cha HJ (2019) Prolonged cell persistence with enhanced multipotency and rapid angiogenesis of hypoxia pre-conditioned stem cells encapsulated in marine-inspired adhesive and immiscible liquid micro-droplets. Acta Biomater 86:257–268

    Article  CAS  PubMed  Google Scholar 

  • Passos JF, Von Zglinicki T (2006) Oxygen free radicals in cell senescence: are they signal transducers? Free Radic Res 40(12):1277–1283

    Article  CAS  PubMed  Google Scholar 

  • Passos JF, Nelson G, Wang C, Richter T, Simillion C, Proctor CJ et al (2010) Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol Syst Biol 6(1):347

    Article  PubMed  PubMed Central  Google Scholar 

  • Peck SH, Bendigo JR, Tobias JW, Dodge GR, Malhotra NR, Mauck RL et al (2021) Hypoxic preconditioning enhances bone marrow-derived mesenchymal stem cell survival in a low oxygen and nutrient-limited 3D microenvironment. Cartilage 12(4):512–525

    Article  CAS  PubMed  Google Scholar 

  • Peixoto A, Fernandes E, Gaiteiro C, Lima L, Azevedo R, Soares J et al (2016) Hypoxia enhances the malignant nature of bladder cancer cells and concomitantly antagonizes protein O-glycosylation extension. Oncotarget 7(39):63138

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng L, Shu X, Lang C, Yu X (2016) Effects of hypoxia on proliferation of human cord blood-derived mesenchymal stem cells. Cytotechnology 68(4):1615–1622

    Article  CAS  PubMed  Google Scholar 

  • Pulido-Escribano V, Torrecillas-Baena B, Camacho-Cardenosa M, Dorado G, Gálvez-Moreno M, Casado-Díaz A (2022) Role of hypoxia preconditioning in therapeutic potential of mesenchymal stem-cell-derived extracellular vesicles. World J Stem Cells 14(7):453–472

    Article  PubMed  PubMed Central  Google Scholar 

  • Quintero P, Gonzalez-Muniesa P, Garcia-Diaz DF, Martinez JA (2012) Effects of hyperoxia exposure on metabolic markers and gene expression in 3T3-L1 adipocytes. J Physiol Biochem 68(4):663–669

    Article  CAS  PubMed  Google Scholar 

  • Radisic M, Park H, Chen F, Salazar-Lazzaro JE, Wang Y, Dennis R et al (2006) Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 12(8):2077–2091

    Article  CAS  PubMed  Google Scholar 

  • Rasouli M, Rahimi A, Soleimani M, Keshel SH (2021) The interplay between extracellular matrix and progenitor/stem cells during wound healing: Opportunities and future directions. Acta Histochem 123(7):151785

    Article  CAS  PubMed  Google Scholar 

  • Rasouli M, Vakilian F, Ranjbari J (2022) Therapeutic and protective potential of mesenchymal stem cells, pharmaceutical agents and current vaccines against COVID-19. Curr Stem Cell Res Ther 17(2):166–185

    Article  CAS  PubMed  Google Scholar 

  • Rasouli M, Hosseinzadeh S, Mortazavi SM, Fattahi R, Ranjbari J, Soleimani M (2023a) Do carboxymethyl cellulose and pal-KTTKS make bacterial cellulose a superior wound dressing or skin scaffold? Polym Plast Tech Mat 62(8):974–988

    CAS  Google Scholar 

  • Rasouli M, Naeimzadeh Y, Hashemi N, Hosseinzadeh S (2023b) Age-related alterations in mesenchymal stem cell function: understanding mechanisms and seeking opportunities to bypass the cellular aging. Curr Stem Cell Res Ther. Epub ahead of print. https://doi.org/10.2174/1574888X18666230113144016

  • Rasouli M, Soleimani M, Hosseinzadeh S, Ranjbari J (2023c) Bacterial cellulose as potential dressing and scaffold material: toward improving the antibacterial and cell adhesion properties. J Polym Environ. Epub ahead of print. https://doi.org/10.1007/s10924-023-02779-0

  • Raza MH, Siraj S, Arshad A, Waheed U, Aldakheel F, Alduraywish S et al (2017) ROS-modulated therapeutic approaches in cancer treatment. J Cancer Res Clin Oncol 143(9):1789–1809

    Article  CAS  PubMed  Google Scholar 

  • Redza-Dutordoir M, Averill-Bates DA (2016) Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta (BBA) Mol Cell Res 1863(12):2977–2992

    Article  CAS  Google Scholar 

  • Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE et al (2004) Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109(10):1292–1298

    Article  PubMed  Google Scholar 

  • Rhee SG, Bae YS, Lee S-R, Kwon J (2000) Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE 2000(53):pe1

    Article  CAS  PubMed  Google Scholar 

  • Rhoads RP, Johnson RM, Rathbone CR, Liu X, Temm-Grove C, Sheehan SM et al (2009) Satellite cell-mediated angiogenesis in vitro coincides with a functional hypoxia-inducible factor pathway. Am J Physiol Cell Physiol 296(6):C1321–C1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizvi SFA, Wasim B, Usman S, Borges KJJ, Sahibdad I, Salim A et al (2022) Zinc and hypoxic preconditioning: a strategy to enhance the functionality and therapeutic potential of bone marrow-derived mesenchymal stem cells. Mol Cell Biochem 477(12):2735–2749

    Article  CAS  PubMed  Google Scholar 

  • Rosenberger P, Schwab JM, Mirakaj V, Masekowsky E, Mager A, Morote-Garcia JC et al (2009) Hypoxia-inducible factor–dependent induction of netrin-1 dampens inflammation caused by hypoxia. Nat Immunol 10(2):195–202

    Article  CAS  PubMed  Google Scholar 

  • Ruigrok MJ, Tomar J, Frijlink HW, Melgert BN, Hinrichs WL, Olinga P (2019) The effects of oxygen concentration on cell death, anti-oxidant transcription, acute inflammation, and cell proliferation in precision-cut lung slices. Sci Rep 9(1):1–13

    Article  CAS  Google Scholar 

  • Sadat S, Gehmert S, Song Y-H, Yen Y, Bai X, Gaiser S et al (2007) The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem Biophys Res Commun 363(3):674–679

    Article  CAS  PubMed  Google Scholar 

  • Salminen A, Kaarniranta K, Kauppinen A (2012) Inflammaging: disturbed interplay between autophagy and inflammasomes. Aging (albany NY) 4(3):166

    Article  CAS  PubMed  Google Scholar 

  • Salvemini D, Ischiropoulos H, Cuzzocrea S (2003) Roles of nitric oxide and superoxide in inflammation. Inflammation Protocols. Springer, pp 291–303

    Google Scholar 

  • Samal JRK, Rangasami VK, Samanta S, Varghese OP, Oommen OP (2021) Discrepancies on the role of oxygen gradient and culture condition on mesenchymal stem cell fate. Adv Healthc Mater 10(6):e2002058

    Article  PubMed  Google Scholar 

  • Schumacker PT (2006) Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell 10(3):175–176

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (2000) HIF-1 and human disease: one highly involved factor. Genes Dev 14(16):1983–1991

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (2009a) Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Seminars in cancer biology. Elsevier

    Google Scholar 

  • Semenza GL (2009b) Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology 24(2):97–106

    Article  CAS  PubMed  Google Scholar 

  • Sharifpanah F, Behr S, Wartenberg M, Sauer H (2016) Mechanical strain stimulates vasculogenesis and expression of angiogenesis guidance molecules of embryonic stem cells through elevation of intracellular calcium, reactive oxygen species and nitric oxide generation. Biochim Biophys Acta (BBA) Mol Cell Res. 1863(12):3096–3105

    Article  CAS  Google Scholar 

  • Sharkey JV (2020) Effect of acute low oxygen exposure on the proliferation rate, viability, and gene expression of C2C12 myoblasts in vitro. BioRxiv

  • Sheridan J, Bishop C, Simmons R (1984) Effects of hypoxia on the kinetic and morphological characteristics of human melanoma cells grown as colonies in semi-solid agar medium. Br J Exp Pathol 65(2):171

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shirbaghaee Z, Keshel SH, Rasouli M, Valizadeh M, Nazari SSH, Hassani M et al (2023) Report of a phase 1 clinical trial for safety assessment of human placental mesenchymal stem cells therapy in patients with Critical limb ischemia (CLI)

  • Siegrist J, Sies H (2017) Disturbed redox homeostasis in oxidative distress: a molecular link from chronic psychosocial work stress to coronary heart disease? Circ Res 121(2):103–105

    Article  CAS  PubMed  Google Scholar 

  • Sies H (2017) Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress. Redox Biol 11:613–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sies H, Jones DP (2020) Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat Rev Mol Cell Biol 21(7):363–383

    Article  CAS  PubMed  Google Scholar 

  • Sies H, Belousov VV, Chandel NS, Davies MJ, Jones DP, Mann GE et al (2022) Defining roles of specific reactive oxygen species (ROS) in cell biology and physiology. Nat Rev Mol Cell Biol 23(7):499–515

    Article  CAS  PubMed  Google Scholar 

  • Sohal R, Sohal BH (1991) Hydrogen peroxide release by mitochondria increases during aging. Mech Ageing Dev 57(2):187–202

    Article  CAS  PubMed  Google Scholar 

  • Song J, Miermont A, Lim CT, Kamm RD (2018) A 3D microvascular network model to study the impact of hypoxia on the extravasation potential of breast cell lines. Sci Rep 8(1):1–11

    Article  Google Scholar 

  • Studer L, Csete M, Lee S-H, Kabbani N, Walikonis J, Wold B et al (2000) Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 20(19):7377–7383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suematsu N, Tsutsui H, Wen J, Kang D, Ikeuchi M, Ide T et al (2003) Oxidative stress mediates tumor necrosis factor-α–induced mitochondrial DNA damage and dysfunction in cardiac myocytes. Circulation 107(10):1418–1423

    Article  CAS  PubMed  Google Scholar 

  • Taylor CT (2008) Interdependent roles for hypoxia inducible factor and nuclear factor-κB in hypoxic inflammation. J Physiol 586(17):4055–4059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor CT, Colgan SP (2007) Hypoxia and gastrointestinal disease. J Mol Med 85(12):1295–1300

    Article  PubMed  Google Scholar 

  • Thangarajah H, Vial IN, Chang E, El-Ftesi S, Januszyk M, Chang EI et al (2009) IFATS collection: adipose stromal cells adopt a proangiogenic phenotype under the influence of hypoxia. Stem Cells 27(1):266–274

    Article  CAS  PubMed  Google Scholar 

  • Tiidus PM (1998) Radical species in inflammation and overtraining. Can J Physiol Pharmacol 76(5):533–538

    Article  CAS  PubMed  Google Scholar 

  • Tottey S, Corselli M, Jeffries EM, Londono R, Peault B, Badylak SF (2011) Extracellular matrix degradation products and low-oxygen conditions enhance the regenerative potential of perivascular stem cells. Tissue Eng Part A 17(1–2):37–44

    Article  CAS  PubMed  Google Scholar 

  • Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H et al (2006) Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by β-phenylethyl isothiocyanate. Cancer Cell 10(3):241–252

    Article  CAS  PubMed  Google Scholar 

  • Uchikura K, Wada T, Hoshino S, Nagakawa Y, Aiko T, Bulkley GB et al (2004) Lipopolysaccharides induced increases in fas ligand expression by kupffer cells via mechanisms dependent on reactive oxygen species. Am J Physiol Gastrointest Liver Physiol 287(3):G620–G626

    Article  CAS  PubMed  Google Scholar 

  • Ushio-Fukai M, Nakamura Y (2008) Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett 266(1):37–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vallabhapurapu S, Karin M (2009) Regulation and function of NF-κB transcription factors in the immune system. Annu Rev Immunol 27:693–733

    Article  CAS  PubMed  Google Scholar 

  • Van Uden P, Kenneth NS, Rocha S (2008) Regulation of hypoxia-inducible factor-1α by NF-κB. Biochem J 412(3):477–484

    Article  PubMed  Google Scholar 

  • Villarroya F, Iglesias R, Giralt M (2007) PPARs in the control of uncoupling proteins gene expression. PPAR research 2007

  • Wang C, Liu W, Liu Z, Chen L, Liu X, Kuang S (2015) Hypoxia inhibits myogenic differentiation through p53 protein-dependent induction of Bhlhe40 protein. J Biol Chem 290(50):29707–29716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Jiang H, Duan J, Chen J, Wang Q, Liu X et al (2018) Exploration of acute phase proteins and inflammatory cytokines in early stage diagnosis of acute mountain sickness. High Alt Med Biol 19(2):170–177

    Article  CAS  PubMed  Google Scholar 

  • Waris G, Ahsan H (2006) Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 5:14

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan G-J, Li Q-W, Shan S-L, Wang W-M, Jiang S, Xu X-M (2012) Hyperthermia inhibits hypoxia-induced epithelial-mesenchymal transition in HepG2 hepatocellular carcinoma cells. World J Gastroenterol WJG 18(34):4781

    Article  CAS  PubMed  Google Scholar 

  • Yun Z, Maecker HL, Johnson RS, Giaccia AJ (2002) Inhibition of PPARγ2 gene expression by the HIF-1-regulated gene DEC1/Stra13: a mechanism for regulation of adipogenesis by hypoxia. Dev Cell 2(3):331–341

    Article  CAS  PubMed  Google Scholar 

  • Zangl Q, Martignoni A, Jackson SH, Ohta A, Klaunberg B, Kaufmann I et al (2014) Postoperative hyperoxia (60%) worsens hepatic injury in mice. Anesthesiol J Am Soc Anesthesiol. 121(6):1217–1225

    Google Scholar 

  • Zhang J, Ahn KS, Kim C, Shanmugam MK, Siveen KS, Arfuso F et al (2016) Nimbolide-induced oxidative stress abrogates STAT3 signaling cascade and inhibits tumor growth in transgenic adenocarcinoma of mouse prostate model. Antioxid Redox Signal 24(11):575–589

    Article  CAS  PubMed  Google Scholar 

  • Zhang N, Hong B, Zhou C, Du X, Chen S, Deng X et al (2017) Cobalt chloride-induced hypoxia induces epithelial-mesenchymal transition in renal carcinoma cell lines. Ann Clin Lab Sci 47(1):40–46

    CAS  PubMed  Google Scholar 

  • Zhou R, Yazdi AS, Menu P, Tschopp J (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469(7329):221–225

    Article  ADS  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study is related to the project No. 1400/62981 from Student Research Committee, Shahid Beheshti University of Medical Sciences, Tehran, Iran. We also appreciate the “Student Research Committee” and “Research & Technology Chancellor” in Shahid Beheshti University of Medical Sciences for their financial support of this study.

Author information

Authors and Affiliations

  1. Student Research Committee, Department of Tissue Engineering and Applied Cell Science, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Mehdi Rasouli

  2. Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, 1985717443, Iran

    Roya Fattahi, Ghader Nuoroozi, Zeinab Hajmohammadi & Simzar Hosseinzadeh

  3. Department of Applied Cell Sciences, School of Advanced Technologies in Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

    Zeinab Zarei-Behjani

  4. Engineering Department, Faculty of Chemical Engineering, Zanjan University, Zanjan, Iran

    Maliheh Yaghoobi

  5. Medical Nanotechnology and Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Simzar Hosseinzadeh

Authors
  1. Mehdi Rasouli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roya Fattahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ghader Nuoroozi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zeinab Zarei-Behjani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maliheh Yaghoobi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zeinab Hajmohammadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Simzar Hosseinzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simzar Hosseinzadeh.

Additional information

Publisher's Note

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

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

Rasouli, M., Fattahi, R., Nuoroozi, G. et al. The role of oxygen tension in cell fate and regenerative medicine: implications of hypoxia/hyperoxia and free radicals. Cell Tissue Bank 25, 195–215 (2024). https://doi.org/10.1007/s10561-023-10099-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10561-023-10099-9

Keywords

Search

Navigation