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Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Review Article

Hypoxia and Hypoxia Mimetic Agents As Potential Priming Approaches to Empower Mesenchymal Stem Cells

Author(s): Goknur Topaloglu Yasan* and Aysen Gunel-Ozcan*

Volume 19, Issue 1, 2024

Published on: 07 February, 2023

Page: [33 - 54] Pages: 22

DOI: 10.2174/1574888X18666230113143234

Price: $65

Abstract

Mesenchymal stem cells (MSC) exhibit self-renewal capacity and multilineage differentiation potential, making them attractive for research and clinical application. The properties of MSC can vary depending on specific micro-environmental factors. MSC resides in specific niches with low oxygen concentrations, where oxygen functions as a metabolic substrate and a signaling molecule. Conventional physical incubators or chemically hypoxia mimetic agents are applied in cultures to mimic the original low oxygen tension settings where MSC originated.

This review aims to focus on the current knowledge of the effects of various physical hypoxic conditions and widely used hypoxia-mimetic agents-PHD inhibitors on mesenchymal stem cells at a cellular and molecular level, including proliferation, stemness, differentiation, viability, apoptosis, senescence, migration, immunomodulation behaviors, as well as epigenetic changes.

Graphical Abstract

[1]
Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006; 24(5): 1294-301.
[http://dx.doi.org/10.1634/stemcells.2005-0342] [PMID: 16410387]
[2]
Braun RD, Lanzen JL, Snyder SA, Dewhirst MW. Comparison of tumor and normal tissue oxygen tension measurements using OxyLite or microelectrodes in rodents. Am J Physiol Heart Circ Physiol 2001; 280(6): H2533-44.
[http://dx.doi.org/10.1152/ajpheart.2001.280.6.H2533] [PMID: 11356608]
[3]
Erecińska M, Silver IA. Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 2001; 128(3): 263-76.
[http://dx.doi.org/10.1016/S0034-5687(01)00306-1] [PMID: 11718758]
[4]
Cipolleschi MG, Dello Sbarba P, Olivotto M. The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 1993; 82(7): 2031-7.
[http://dx.doi.org/10.1182/blood.V82.7.2031.2031] [PMID: 8104535]
[5]
Teti G, Focaroli S, Salvatore V, et al. The hypoxia-mimetic agent cobalt chloride differently affects human mesenchymal stem cells in their chondrogenic potential. Stem Cells Int 2018; 2018: 1-9.
[http://dx.doi.org/10.1155/2018/3237253] [PMID: 29731777]
[6]
Muñoz-Sánchez J, Chánez-Cárdenas ME. The use of cobalt chloride as a chemical hypoxia model. J Appl Toxicol 2019; 39(4): 556-70.
[http://dx.doi.org/10.1002/jat.3749] [PMID: 30484873]
[7]
Elks PM, Renshaw SA, Meijer AH, Walmsley SR, van Eeden FJ. Exploring the HIFs, buts and maybes of hypoxia signalling in disease: lessons from zebrafish models. Dis Model Mech 2015; 8(11): 1349-60.
[http://dx.doi.org/10.1242/dmm.021865] [PMID: 26512123]
[8]
Epstein ACR, Gleadle JM, McNeill LA, et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001; 107(1): 43-54.
[http://dx.doi.org/10.1016/S0092-8674(01)00507-4] [PMID: 11595184]
[9]
Ren H, Cao Y, Zhao Q, et al. Proliferation and differentiation of bone marrow stromal cells under hypoxic conditions. Biochem Biophys Res Commun 2006; 347(1): 12-21.
[http://dx.doi.org/10.1016/j.bbrc.2006.05.169] [PMID: 16814746]
[10]
Huang Y, Du K-M, Xue Z-H, et al. Cobalt chloride and low oxygen tension trigger differentiation of acute myeloid leukemic cells: possible mediation of hypoxia-inducible factor-1α. Leukemia 2003; 17(11): 2065-73.
[http://dx.doi.org/10.1038/sj.leu.2403141] [PMID: 14523474]
[11]
Yuan Y, Hilliard G, Ferguson T, Millhorn DE. Cobalt inhibits the interaction between hypoxia-inducible factor-α and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-α. J Biol Chem 2003; 278(18): 15911-6.
[http://dx.doi.org/10.1074/jbc.M300463200] [PMID: 12606543]
[12]
Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284(5411): 143-7.
[13]
Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.
[http://dx.doi.org/10.1080/14653240600855905] [PMID: 16923606]
[14]
Chung DJ, Choi CB, Lee SH, et al. Intraarterially delivered human umbilical cord blood-derived mesenchymal stem cells in canine cerebral ischemia. J Neurosci Res 2009; 87(16): 3554-67.
[http://dx.doi.org/10.1002/jnr.22162] [PMID: 19642203]
[15]
Lund P, Pilgaard L, Duroux M, Fink T, Zachar V. Effect of growth media and serum replacements on the proliferation and differentiation of adipose-derived stem cells. Cytotherapy 2009; 11(2): 189-97.
[http://dx.doi.org/10.1080/14653240902736266] [PMID: 19241196]
[16]
Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 2003; 18(4): 696-704.
[http://dx.doi.org/10.1359/jbmr.2003.18.4.696] [PMID: 12674330]
[17]
Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98(5): 1076-84.
[http://dx.doi.org/10.1002/jcb.20886] [PMID: 16619257]
[18]
Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007; 110(10): 3499-506.
[http://dx.doi.org/10.1182/blood-2007-02-069716] [PMID: 17664353]
[19]
Martens TP, See F, Schuster MD, et al. Mesenchymal lineage precursor cells induce vascular network formation in ischemic myocardium. Nat Clin Pract Cardiovasc Med 2006; 3 (Suppl. 1): S18-22.
[http://dx.doi.org/10.1038/ncpcardio0404] [PMID: 16501624]
[20]
Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3(3): 301-13.
[http://dx.doi.org/10.1016/j.stem.2008.07.003] [PMID: 18786417]
[21]
Zannettino ACW, Paton S, Arthur A, et al. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008; 214(2): 413-21.
[http://dx.doi.org/10.1002/jcp.21210] [PMID: 17654479]
[22]
Miura M, Gronthos S, Zhao M, et al. SHED: Stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 2003; 100(10): 5807-12.
[http://dx.doi.org/10.1073/pnas.0937635100] [PMID: 12716973]
[23]
Harrison JS, Rameshwar P, Chang V, Bandari P. Oxygen saturation in the bone marrow of healthy volunteers. Blood 2002; 99(1): 394-4.
[http://dx.doi.org/10.1182/blood.V99.1.394] [PMID: 11783438]
[24]
Pasarica M, Sereda OR, Redman LM, et al. Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes 2009; 58(3): 718-25.
[http://dx.doi.org/10.2337/db08-1098] [PMID: 19074987]
[25]
Matsumoto A, Matsumoto S, Sowers AL, et al. Absolute oxygen tension (pO2) in murine fatty and muscle tissue as determined by EPR. Magn Reson Med 2005; 54(6): 1530-5.
[http://dx.doi.org/10.1002/mrm.20714] [PMID: 16276490]
[26]
Kwon SY, Chun SY, Ha YS, et al. Hypoxia enhances cell properties of human mesenchymal stem cells. Tissue Eng Regen Med 2017; 14(5): 595-604.
[http://dx.doi.org/10.1007/s13770-017-0068-8] [PMID: 30603513]
[27]
Hwang OK, Noh YW, Hong JT, Lee JW. Hypoxia pretreatment promotes chondrocyte differentiation of human adipose-derived stem cells via vascular endothelial growth factor. Tissue Eng Regen Med 2020; 17(3): 335-50.
[http://dx.doi.org/10.1007/s13770-020-00265-5] [PMID: 32451775]
[28]
Ivanovic Z. Hypoxia or in situ normoxia: The stem cell paradigm. J Cell Physiol 2009; 219(2): 271-5.
[http://dx.doi.org/10.1002/jcp.21690] [PMID: 19160417]
[29]
Carreau A, Hafny-Rahbi BE, Matejuk A, Grillon C, Kieda C. Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J Cell Mol Med 2011; 15(6): 1239-53.
[http://dx.doi.org/10.1111/j.1582-4934.2011.01258.x] [PMID: 21251211]
[30]
Bahsoun S, Coopman K, Forsyth NR, Akam EC. The role of dissolved oxygen levels on human mesenchymal stem cell culture success, regulatory compliance, and therapeutic potential. Stem Cells Dev 2018; 27(19): 1303-21.
[http://dx.doi.org/10.1089/scd.2017.0291] [PMID: 30003826]
[31]
Wenger R, Kurtcuoglu V, Scholz C, Marti H, Hoogewijs D. Frequently asked questions in hypoxia research. Hypoxia (Auckl) 2015; 3: 35-43.
[http://dx.doi.org/10.2147/HP.S92198] [PMID: 27774480]
[32]
Jones DL, Wagers AJ. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 2008; 9(1): 11-21.
[http://dx.doi.org/10.1038/nrm2319] [PMID: 18097443]
[33]
Li L, Xie T. Stem Cell Niche: Structure and function. Annu Rev Cell Dev Biol 2005; 21(1): 605-31.
[http://dx.doi.org/10.1146/annurev.cellbio.21.012704.131525] [PMID: 16212509]
[34]
Scadden DT. The stem-cell niche as an entity of action. Nature 2006; 441(7097): 1075-9.
[http://dx.doi.org/10.1038/nature04957] [PMID: 16810242]
[35]
Jones NM, Kardashyan L, Callaway JK, Lee EM, Beart PM. Long-term functional and protective actions of preconditioning with hypoxia, cobalt chloride, and desferrioxamine against hypoxic-ischemic injury in neonatal rats. Pediatr Res 2008; 63(6): 620-4.
[http://dx.doi.org/10.1203/PDR.0b013e31816d9117] [PMID: 18317402]
[36]
Sharp FR, Bernaudin M. HIF1 and oxygen sensing in the brain. Nat Rev Neurosci 2004; 5(6): 437-48.
[http://dx.doi.org/10.1038/nrn1408] [PMID: 15152194]
[37]
Grayson WL, Zhao F, Izadpanah R, Bunnell B, Ma T. Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. J Cell Physiol 2006; 207(2): 331-9.
[http://dx.doi.org/10.1002/jcp.20571] [PMID: 16331674]
[38]
Dos Santos F, Andrade PZ, Boura JS, Abecasis MM, da Silva CL, Cabral JM. Ex vivo expansion of human mesenchymal stem cells: a more effective cell proliferation kinetics and metabolism under hypoxia. J Cell Physiol 2010; 223(1): 27-35.
[PMID: 20020504]
[39]
Lavrentieva A, Majore I, Kasper C, Hass R. Effects of hypoxic culture conditions on umbilical cord-derived human mesenchymal stem cells. Cell Commun Signal 2010; 8(1): 18.
[http://dx.doi.org/10.1186/1478-811X-8-18] [PMID: 20637101]
[40]
Wang DW, Fermor B, Gimble JM, Awad HA, Guilak F. Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J Cell Physiol 2005; 204(1): 184-91.
[http://dx.doi.org/10.1002/jcp.20324] [PMID: 15754341]
[41]
Laksana K, Sooampon S, Pavasant P, Sriarj W. Cobalt chloride enhances the stemness of human dental pulp cells. J Endod 2017; 43(5): 760-5.
[http://dx.doi.org/10.1016/j.joen.2017.01.005] [PMID: 28343926]
[42]
Ahmed NEMB, Murakami M, Kaneko S, Nakashima M. The effects of hypoxia on the stemness properties of human dental pulp stem cells (DPSCs). Sci Rep 2016; 6(1): 35476.
[http://dx.doi.org/10.1038/srep35476] [PMID: 27739509]
[43]
Youn SW, Kim DS, Cho HJ, et al. Cellular senescence induced loss of stem cell proportion in the skin in vitro. J Dermatol Sci 2004; 35(2): 113-23.
[http://dx.doi.org/10.1016/j.jdermsci.2004.04.002] [PMID: 15265523]
[44]
Eliasson P, Jönsson JI. The hematopoietic stem cell niche: Low in oxygen but a nice place to be. J Cell Physiol 2010; 222(1): 17-22.
[http://dx.doi.org/10.1002/jcp.21908] [PMID: 19725055]
[45]
Panchision DM. The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol 2009; 220(3): 562-8.
[http://dx.doi.org/10.1002/jcp.21812] [PMID: 19441077]
[46]
Spencer JA, Ferraro F, Roussakis E, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 2014; 508(7495): 269-73.
[http://dx.doi.org/10.1038/nature13034] [PMID: 24590072]
[47]
Goossens GH, Blaak EE. Adipose tissue oxygen tension. Curr Opin Clin Nutr Metab Care 2012; 15(6): 539-46.
[http://dx.doi.org/10.1097/MCO.0b013e328358fa87] [PMID: 23037900]
[48]
Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992; 80(2): 283-5.
[PMID: 1635745]
[49]
Zhou S, Cui Z, Urban JPG. Factors influencing the oxygen concentration gradient from the synovial surface of articular cartilage to the cartilage-bone interface: A modeling study. Arthritis Rheum 2004; 50(12): 3915-24.
[http://dx.doi.org/10.1002/art.20675] [PMID: 15593204]
[50]
Yu CY, Boyd NM, Cringle SJ, Alder VA, Yu DY. Oxygen distribution and consumption in rat lower incisor pulp. Arch Oral Biol 2002; 47(7): 529-36.
[http://dx.doi.org/10.1016/S0003-9969(02)00036-5] [PMID: 12208077]
[51]
Kozam G. Oxygen tension of rabbit incisor pulp. J Dent Res 1967; 46(2): 352-8.
[http://dx.doi.org/10.1177/00220345670460020701] [PMID: 5228068]
[52]
Simon MC, Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 2008; 9(4): 285-96.
[http://dx.doi.org/10.1038/nrm2354] [PMID: 18285802]
[53]
Wagner W, Horn P, Castoldi M, et al. Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 2008; 3(5): e2213.
[http://dx.doi.org/10.1371/journal.pone.0002213] [PMID: 18493317]
[54]
Haque N, Rahman MT, Abu Kasim NH, Alabsi AM. Hypoxic culture conditions as a solution for mesenchymal stem cell based regenerative therapy. ScientificWorldJournal 2013; 2013: 632972.
[http://dx.doi.org/10.1155/2013/632972] [PMID: 24068884]
[55]
Bork S, Pfister S, Witt H, et al. DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells. Aging Cell 2010; 9(1): 54-63.
[http://dx.doi.org/10.1111/j.1474-9726.2009.00535.x] [PMID: 19895632]
[56]
Fehrer C, Brunauer R, Laschober G, et al. Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell 2007; 6(6): 745-57.
[http://dx.doi.org/10.1111/j.1474-9726.2007.00336.x] [PMID: 17925003]
[57]
Kim DS, Ko YJ, Lee MW, et al. Effect of low oxygen tension on the biological characteristics of human bone marrow mesenchymal stem cells. Cell Stress Chaperones 2016; 21(6): 1089-99.
[http://dx.doi.org/10.1007/s12192-016-0733-1] [PMID: 27565660]
[58]
Busuttil RA, Rubio M, Dollé MET, Campisi J, Vijg J. Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture. Aging Cell 2003; 2(6): 287-94.
[http://dx.doi.org/10.1046/j.1474-9728.2003.00066.x] [PMID: 14677631]
[59]
Wiseman H, Halliwell B. Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J 1996; 313(1): 17-29.
[http://dx.doi.org/10.1042/bj3130017] [PMID: 8546679]
[60]
Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55(1): 373-99.
[http://dx.doi.org/10.1146/annurev.arplant.55.031903.141701] [PMID: 15377225]
[61]
Golstein P, Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 2007; 32(1): 37-43.
[http://dx.doi.org/10.1016/j.tibs.2006.11.001] [PMID: 17141506]
[62]
Ali SS, Hsiao M, Zhao HW, Dugan LL, Haddad GG, Zhou D. Hypoxia-adaptation involves mitochondrial metabolic depression and decreased ROS leakage. PLoS One 2012; 7(5): e36801.
[http://dx.doi.org/10.1371/journal.pone.0036801] [PMID: 22574227]
[63]
Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 1993; 90(9): 4304-8.
[http://dx.doi.org/10.1073/pnas.90.9.4304] [PMID: 8387214]
[64]
Semenza GL. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007; 2007(407): P. cm8.
[http://dx.doi.org/10.1126/stke.4072007cm8] [PMID: 17925579]
[65]
Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA 1997; 94(9): 4273-8.
[http://dx.doi.org/10.1073/pnas.94.9.4273] [PMID: 9113979]
[66]
Gu Y-Z, Moran SM, Hogenesch JB, Wartman L, Bradfield CA. Molecular characterization and chromosomal localization of a third α-class hypoxia inducible factor subunit, HIF3α. Gene Expr 1998; 7(3): 205-13.
[PMID: 9840812]
[67]
Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 1995; 270(3): 1230-7.
[http://dx.doi.org/10.1074/jbc.270.3.1230] [PMID: 7836384]
[68]
Zhang P, Yao Q, Lu L, Li Y, Chen PJ, Duan C. Hypoxia-inducible factor 3 is an oxygen-dependent transcription activator and regulates a distinct transcriptional response to hypoxia. Cell Rep 2014; 6(6): 1110-21.
[http://dx.doi.org/10.1016/j.celrep.2014.02.011] [PMID: 24613356]
[69]
Maynard MA, Qi H, Chung J, et al. Multiple splice variants of the human HIF-3 α locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J Biol Chem 2003; 278(13): 11032-40.
[http://dx.doi.org/10.1074/jbc.M208681200] [PMID: 12538644]
[70]
Lando D, Peet DJ, Whelan DA, Gorman JJ, Whitelaw ML. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 2002; 295(5556): 858-61.
[http://dx.doi.org/10.1126/science.1068592] [PMID: 11823643]
[71]
Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001; 294(5545): 1337-40.
[http://dx.doi.org/10.1126/science.1066373] [PMID: 11598268]
[72]
Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008; 30(4): 393-402.
[http://dx.doi.org/10.1016/j.molcel.2008.04.009] [PMID: 18498744]
[73]
Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 1992; 12(12): 5447-54.
[PMID: 1448077]
[74]
Huang LE, Arany Z, Livingston DM, Bunn HF. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its α subunit. J Biol Chem 1996; 271(50): 32253-9.
[http://dx.doi.org/10.1074/jbc.271.50.32253] [PMID: 8943284]
[75]
Forsythe JA, Jiang BH, Iyer NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996; 16(9): 4604-13.
[http://dx.doi.org/10.1128/MCB.16.9.4604] [PMID: 8756616]
[76]
Jiang BH, Rue E, Wang GL, Roe R, Semenza GL. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 1996; 271(30): 17771-8.
[http://dx.doi.org/10.1074/jbc.271.30.17771] [PMID: 8663540]
[77]
Semenza GL, Roth PH, Fang HM, Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 1994; 269(38): 23757-63.
[http://dx.doi.org/10.1016/S0021-9258(17)31580-6] [PMID: 8089148]
[78]
Firth JD, Ebert BL, Pugh CW, Ratcliffe PJ. Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc Natl Acad Sci USA 1994; 91(14): 6496-500.
[http://dx.doi.org/10.1073/pnas.91.14.6496] [PMID: 8022811]
[79]
Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 2004; 5(5): 343-54.
[http://dx.doi.org/10.1038/nrm1366] [PMID: 15122348]
[80]
Wilkins SE, Abboud MI, Hancock RL, Schofield CJ. Targeting protein-protein interactions in the HIF system. ChemMedChem 2016; 11(8): 773-86.
[http://dx.doi.org/10.1002/cmdc.201600012] [PMID: 26997519]
[81]
Rankin EB, Wu C, Khatri R, et al. The HIF signaling pathway in osteoblasts directly modulates erythropoiesis through the production of EPO. Cell 2012; 149(1): 63-74.
[http://dx.doi.org/10.1016/j.cell.2012.01.051] [PMID: 22464323]
[82]
Kapitsinou PP, Liu Q, Unger TL, et al. Hepatic HIF-2 regulates erythropoietic responses to hypoxia in renal anemia. Blood 2010; 116(16): 3039-48.
[http://dx.doi.org/10.1182/blood-2010-02-270322] [PMID: 20628150]
[83]
Lambertini E, Penolazzi L, Angelozzi M, et al. Hypoxia preconditioning of human MSCs: a direct evidence of HIF-1α and collagen type XV correlation. Cell Physiol Biochem 2018; 51(5): 2237-49.
[http://dx.doi.org/10.1159/000495869] [PMID: 30537732]
[84]
Yu X, Lu C, Liu H, et al. Hypoxic preconditioning with cobalt of bone marrow mesenchymal stem cells improves cell migration and enhances therapy for treatment of ischemic acute kidney injury. PLoS One 2013; 8(5): e62703.
[http://dx.doi.org/10.1371/journal.pone.0062703] [PMID: 23671625]
[85]
Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 1995; 92(12): 5510-4.
[http://dx.doi.org/10.1073/pnas.92.12.5510] [PMID: 7539918]
[86]
Post DE, Van Meir EG. A novel hypoxia-inducible factor (HIF) activated oncolytic adenovirus for cancer therapy. Oncogene 2003; 22(14): 2065-72.
[http://dx.doi.org/10.1038/sj.onc.1206464] [PMID: 12687009]
[87]
Freshney RI. Culture of animal cells: a manual of basic technique and specialized applications. John Wiley & Sons 2015.
[88]
Osathanon T, Vivatbutsiri P, Sukarawan W, Sriarj W, Pavasant P, Sooampon S. Cobalt chloride supplementation induces stem-cell marker expression and inhibits osteoblastic differentiation in human periodontal ligament cells. Arch Oral Biol 2015; 60(1): 29-36.
[http://dx.doi.org/10.1016/j.archoralbio.2014.08.018] [PMID: 25244616]
[89]
Chen R, Forsyth N. the development of new classes of hypoxia mimetic agents for clinical use. Front Cell Dev Biol 2019; 7: 120.
[http://dx.doi.org/10.3389/fcell.2019.00120] [PMID: 31297372]
[90]
Yeh TL, Leissing TM, Abboud MI, et al. Molecular and cellular mechanisms of HIF prolyl hydroxylase inhibitors in clinical trials. Chem Sci (Camb) 2017; 8(11): 7651-68.
[http://dx.doi.org/10.1039/C7SC02103H] [PMID: 29435217]
[91]
Baek JH, Mahon PC, Oh J, et al. OS-9 interacts with hypoxia-inducible factor 1α and prolyl hydroxylases to promote oxygen-dependent degradation of HIF-1α. Mol Cell 2005; 17(4): 503-12.
[http://dx.doi.org/10.1016/j.molcel.2005.01.011] [PMID: 15721254]
[92]
Lee SH, Bae SC, Kim KW, Lee YM. RUNX3 inhibits hypoxia-inducible factor-1α protein stability by interacting with prolyl hydroxylases in gastric cancer cells. Oncogene 2014; 33(11): 1458-67.
[http://dx.doi.org/10.1038/onc.2013.76] [PMID: 23542169]
[93]
Zhang CS, Liu Q, Li M, et al. RHOBTB3 promotes proteasomal degradation of HIFα through facilitating hydroxylation and suppresses the Warburg effect. Cell Res 2015; 25(9): 1025-42.
[http://dx.doi.org/10.1038/cr.2015.90] [PMID: 26215701]
[94]
Nguyen LK, Cavadas MAS, Scholz CC, et al. A dynamic model of the hypoxia-inducible factor 1-alpha (HIF-1α) network. J Cell Sci 2013; 126(Pt 6): jcs.119974.
[http://dx.doi.org/10.1242/jcs.119974] [PMID: 23390316]
[95]
Wang GL, Semenza GL. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 1993; 82(12): 3610-5.
[PMID: 8260699]
[96]
Tian YM, Yeoh KK, Lee MK, et al. Differential sensitivity of hypoxia inducible factor hydroxylation sites to hypoxia and hydroxylase inhibitors. J Biol Chem 2011; 286(15): 13041-51.
[http://dx.doi.org/10.1074/jbc.M110.211110] [PMID: 21335549]
[97]
Yang S-J, Pyen J, Lee I, Lee H, Kim Y, Kim T. Cobalt chloride-induced apoptosis and extracellular signal-regulated protein kinase 1/2 activation in rat C6 glioma cells. J Biochem Mol Biol 2004; 37(4): 480-6.
[PMID: 15469737]
[98]
Badr GA, Zhang JZ, Tang J, Kern TS, Ismail-Beigi F. Glut1 and Glut3 expression, but not capillary density, is increased by cobalt chloride in rat cerebrum and retina. Brain Res Mol Brain Res 1999; 64(1): 24-33.
[http://dx.doi.org/10.1016/S0169-328X(98)00301-5] [PMID: 9889305]
[99]
Brittenham GM. Iron-chelating therapy for transfusional iron overload. N Engl J Med 2011; 364(2): 146-56.
[http://dx.doi.org/10.1056/NEJMct1004810] [PMID: 21226580]
[100]
Shen X, Wan C, Ramaswamy G, et al. Prolyl hydroxylase inhibitors increase neoangiogenesis and callus formation following femur fracture in mice. J Orthop Res 2009; 27(10): 1298-305.
[http://dx.doi.org/10.1002/jor.20886] [PMID: 19338032]
[101]
Ren X, Dorrington KL, Maxwell PH, Robbins PA. Effects of desferrioxamine on serum erythropoietin and ventilatory sensitivity to hypoxia in humans. J Appl Physiol 2000; 89(2): 680-6.
[http://dx.doi.org/10.1152/jappl.2000.89.2.680] [PMID: 10926654]
[102]
Potier E, Ferreira E, Dennler S, et al. Desferrioxamine‐driven upregulation of angiogenic factor expression by human bone marrow stromal cells. J Tissue Eng Regen Med 2008; 2(5): 272-8.
[http://dx.doi.org/10.1002/term.92] [PMID: 18512268]
[103]
Donneys A, Weiss DM, Deshpande SS, et al. Localized deferoxamine injection augments vascularity and improves bony union in pathologic fracture healing after radiotherapy. Bone 2013; 52(1): 318-25.
[http://dx.doi.org/10.1016/j.bone.2012.10.014] [PMID: 23085084]
[104]
Wang L, Jia P, Shan Y, et al. Synergistic protection of bone vasculature and bone mass by desferrioxamine in osteoporotic mice. Mol Med Rep 2017; 16(5): 6642-9.
[http://dx.doi.org/10.3892/mmr.2017.7451] [PMID: 28901524]
[105]
Chan MC, Holt-Martyn JP, Schofield CJ, Ratcliffe PJ. Pharmacological targeting of the HIF hydroxylases - A new field in medicine development. Mol Aspects Med 2016; 47-48: 54-75.
[http://dx.doi.org/10.1016/j.mam.2016.01.001] [PMID: 26791432]
[106]
Singh A, Wilson JW, Schofield CJ, Chen R. Hypoxia-inducible factor (HIF) prolyl hydroxylase inhibitors induce autophagy and have a protective effect in an in-vitro ischaemia model. Sci Rep 2020; 10(1): 1597.
[http://dx.doi.org/10.1038/s41598-020-58482-w] [PMID: 31913322]
[107]
Chen RL, Ogunshola OO, Yeoh KK, et al. HIF prolyl hydroxylase inhibition prior to transient focal cerebral ischaemia is neuroprotective in mice. J Neurochem 2014; 131(2): 177-89.
[http://dx.doi.org/10.1111/jnc.12804] [PMID: 24974727]
[108]
Reischl S, Li L, Walkinshaw G, Flippin LA, Marti HH, Kunze R. Inhibition of HIF prolyl-4-hydroxylases by FG-4497 reduces brain tissue injury and edema formation during ischemic stroke. PLoS One 2014; 9(1): e84767.
[http://dx.doi.org/10.1371/journal.pone.0084767] [PMID: 24409307]
[109]
Zhou J, Li J, Rosenbaum DM, et al. The prolyl 4-hydroxylase inhibitor GSK360A decreases post-stroke brain injury and sensory, motor, and cognitive behavioral deficits. PLoS One 2017; 12(9): e0184049.
[http://dx.doi.org/10.1371/journal.pone.0184049] [PMID: 28880966]
[110]
Besarab A, Provenzano R, Hertel J, et al. Randomized placebo-controlled dose-ranging and pharmacodynamics study of roxadustat (FG-4592) to treat anemia in nondialysis-dependent chronic kidney disease (NDD-CKD) patients. Nephrol Dial Transplant 2015; 30(10): 1665-73.
[http://dx.doi.org/10.1093/ndt/gfv302] [PMID: 26238121]
[111]
Li X, Cui XX, Chen YJ, et al. Therapeutic potential of a prolyl hydroxylase inhibitor FG-4592 for Parkinson’s diseases in vitro and in vivo: regulation of redox biology and mitochondrial function. Front Aging Neurosci 2018; 10: 121.
[http://dx.doi.org/10.3389/fnagi.2018.00121] [PMID: 29755339]
[112]
Bouchie A. First-in-class anemia drug takes aim at Amgen’s dominion. Nat Biotechnol 2013; 31(11): 948-9.
[http://dx.doi.org/10.1038/nbt1113-948b] [PMID: 24213751]
[113]
Wu Y, Li X, Xie W, Jankovic J, Le W, Pan T. Neuroprotection of deferoxamine on rotenone-induced injury via accumulation of HIF-1α and induction of autophagy in SH-SY5Y cells. Neurochem Int 2010; 57(3): 198-205.
[http://dx.doi.org/10.1016/j.neuint.2010.05.008] [PMID: 20546814]
[114]
Zheng X, Zhai B, Koivunen P, et al. Prolyl hydroxylation by EglN2 destabilizes FOXO3a by blocking its interaction with the USP9x deubiquitinase. Genes Dev 2014; 28(13): 1429-44.
[http://dx.doi.org/10.1101/gad.242131.114] [PMID: 24990963]
[115]
Rodriguez J, Pilkington R, Garcia Munoz A, et al. Substrate-trapped interactors of PHD3 and FIH cluster in distinct signaling pathways. Cell Rep 2016; 14(11): 2745-60.
[http://dx.doi.org/10.1016/j.celrep.2016.02.043] [PMID: 26972000]
[116]
Ullah K, Rosendahl AH, Izzi V, et al. Hypoxia-inducible factor prolyl-4-hydroxylase-1 is a convergent point in the reciprocal negative regulation of NF-κB and p53 signaling pathways. Sci Rep 2017; 7(1): 17220.
[http://dx.doi.org/10.1038/s41598-017-17376-0] [PMID: 28127051]
[117]
Holzwarth C, Vaegler M, Gieseke F, et al. Low physiologic oxygen tensions reduce proliferation and differentiation of human multipotent mesenchymal stromal cells. BMC Cell Biol 2010; 11(1): 11.
[http://dx.doi.org/10.1186/1471-2121-11-11] [PMID: 20109207]
[118]
Antebi B, Rodriguez LA II, Walker KP III, et al. Short-term physiological hypoxia potentiates the therapeutic function of mesenchymal stem cells. Stem Cell Res Ther 2018; 9(1): 265.
[http://dx.doi.org/10.1186/s13287-018-1007-x] [PMID: 30305185]
[119]
Taheem DK, Foyt DA, Loaiza S, et al. Differential regulation of human bone marrow mesenchymal stromal cell chondrogenesis by hypoxia inducible factor-1α hydroxylase inhibitors. Stem Cells 2018; 36(9): 1380-92.
[http://dx.doi.org/10.1002/stem.2844] [PMID: 29726060]
[120]
Berniakovich I, Giorgio M. Low oxygen tension maintains multipotency, whereas normoxia increases differentiation of mouse bone marrow stromal cells. Int J Mol Sci 2013; 14(1): 2119-34.
[http://dx.doi.org/10.3390/ijms14012119] [PMID: 23340651]
[121]
Grayson WL, Zhao F, Bunnell B, Ma T. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 2007; 358(3): 948-53.
[http://dx.doi.org/10.1016/j.bbrc.2007.05.054] [PMID: 17521616]
[122]
Chang CP, Chio CC, Cheong CU, Chao CM, Cheng BC, Lin MT. Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Clin Sci (Lond) 2013; 124(3): 165-76.
[http://dx.doi.org/10.1042/CS20120226] [PMID: 22876972]
[123]
Bobyleva PI, Andreeva ER, Gornostaeva AN, Buravkova LB. Tissue-related hypoxia attenuates proinflammatory effects of allogeneic PBMCS on adipose-derived stromal cells in vitro. Stem Cells Int 2016; 2016: 4726267.
[124]
Choi JR, Pingguan-Murphy B, Wan Abas WAB, et al. In situ normoxia enhances survival and proliferation rate of human adipose tissue-derived stromal cells without increasing the risk of tumourigenesis. PLoS One 2015; 10(1): e0115034.
[http://dx.doi.org/10.1371/journal.pone.0115034] [PMID: 25615717]
[125]
Roemeling-van Rhijn M, Mensah FKF, Korevaar SS, et al. Effects of hypoxia on the immunomodulatory properties of adipose tissue-derived mesenchymal stem cells. Front Immunol 2013; 4: 203.
[http://dx.doi.org/10.3389/fimmu.2013.00203] [PMID: 23882269]
[126]
Zhu W, Chen J, Cong X, Hu S, Chen X. Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells. Stem Cells 2006; 24(2): 416-25.
[http://dx.doi.org/10.1634/stemcells.2005-0121] [PMID: 16253984]
[127]
Casciaro F, Borghesan M, Beretti F, et al. Prolonged hypoxia delays aging and preserves functionality of human amniotic fluid stem cells. Mech Ageing Dev 2020; 191: 111328.
[http://dx.doi.org/10.1016/j.mad.2020.111328] [PMID: 32800796]
[128]
Xu Z, Lin L, Fan Y, et al. Secretome of mesenchymal stem cells from consecutive hypoxic cultures promotes resolution of lung inflammation by reprogramming anti-inflammatory macrophages. Int J Mol Sci 2022; 23(8): 4333.
[http://dx.doi.org/10.3390/ijms23084333] [PMID: 35457151]
[129]
Hung SP, Ho JH, Shih YRV, Lo T, Lee OK. Hypoxia promotes proliferation and osteogenic differentiation potentials of human mesenchymal stem cells. J Orthop Res 2012; 30(2): 260-6.
[http://dx.doi.org/10.1002/jor.21517] [PMID: 21809383]
[130]
D’Ippolito G, Diabira S, Howard GA, Roos BA, Schiller PC. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 2006; 39(3): 513-22.
[http://dx.doi.org/10.1016/j.bone.2006.02.061] [PMID: 16616713]
[131]
Iida K, Takeda-Kawaguchi T, Tezuka Y, Kunisada T, Shibata T, Tezuka K. Hypoxia enhances colony formation and proliferation but inhibits differentiation of human dental pulp cells. Arch Oral Biol 2010; 55(9): 648-54.
[http://dx.doi.org/10.1016/j.archoralbio.2010.06.005] [PMID: 20630496]
[132]
Sakdee JB, White RR, Pagonis TC, Hauschka PV. Hypoxia-amplified proliferation of human dental pulp cells. J Endod 2009; 35(6): 818-23.
[http://dx.doi.org/10.1016/j.joen.2009.03.001] [PMID: 19482178]
[133]
Yamamoto Y, Fujita M, Tanaka Y, et al. Low oxygen tension enhances proliferation and maintains stemness of adipose tissue-derived stromal cells Biores Open Access 2013; 2(3): 199-205.
[http://dx.doi.org/10.1089/biores.2013.0004] [PMID: 23741631]
[134]
Xu Y, Malladi P, Chiou M, Bekerman E, Giaccia AJ, Longaker MT. In vitro expansion of adipose-derived adult stromal cells in hypoxia enhances early chondrogenesis. Tissue Eng 2007; 13(12): 2981-93.
[http://dx.doi.org/10.1089/ten.2007.0050] [PMID: 17916040]
[135]
Nguyen VT, Canciani B, Cirillo F, Anastasia L, Peretti GM, Mangiavini L. Effect of chemically induced hypoxia on osteogenic and angiogenic differentiation of bone marrow mesenchymal stem cells and human umbilical vein endothelial cells in direct coculture. Cells 2020; 9(3): 757.
[http://dx.doi.org/10.3390/cells9030757] [PMID: 32204578]
[136]
Zeng HL, Zhong Q, Qin YL, et al. Hypoxia-mimetic agents inhibit proliferation and alter the morphology of human umbilical cord-derived mesenchymal stem cells. BMC Cell Biol 2011; 12(1): 32.
[http://dx.doi.org/10.1186/1471-2121-12-32] [PMID: 21827650]
[137]
Chen Y, Zhao Q, Yang X, Yu X, Yu D, Zhao W. Effects of cobalt chloride on the stem cell marker expression and osteogenic differentiation of stem cells from human exfoliated deciduous teeth. Cell Stress Chaperones 2019; 24(3): 527-38.
[http://dx.doi.org/10.1007/s12192-019-00981-5] [PMID: 30806897]
[138]
Zan T, Du Z, Li H, Li Q, Gu B. Cobalt chloride improves angiogenic potential of CD133+ cells. Front Biosci 2012; 17(7): 2247-58.
[http://dx.doi.org/10.2741/4048] [PMID: 22652775]
[139]
Fujisawa K, Takami T, Okada S, et al. Analysis of metabolomic changes in mesenchymal stem cells on treatment with desferrioxamine as a hypoxia mimetic compared with hypoxic conditions. Stem Cells 2018; 36(8): 1226-36.
[http://dx.doi.org/10.1002/stem.2826] [PMID: 29577517]
[140]
Jiang L, Peng WW, Li LF, et al. Effects of deferoxamine on the repair ability of dental pulp cells in vitro. J Endod 2014; 40(8): 1100-4.
[http://dx.doi.org/10.1016/j.joen.2013.12.016] [PMID: 25069915]
[141]
Lui GYL, Kovacevic Z, Richardson V, Merlot AM, Kalinowski DS, Richardson DR. Targeting cancer by binding iron: Dissecting cellular signaling pathways. Oncotarget 2015; 6(22): 18748-79.
[http://dx.doi.org/10.18632/oncotarget.4349] [PMID: 26125440]
[142]
Hoffbrand AV, Ganeshaguru K, Hooton JWL, Tattersall MHN. Effect of iron deficiency and desferrioxamine on DNA synthesis in human cells. Br J Haematol 1976; 33(4): 517-26.
[http://dx.doi.org/10.1111/j.1365-2141.1976.tb03570.x] [PMID: 1009024]
[143]
Furukawa T, Naitoh Y, Kohno H, Tokunaga R, Taketani S. Iron deprivation decreases ribonucleotide reductase activity and DNA synthesis. Life Sci 1992; 50(26): 2059-65.
[http://dx.doi.org/10.1016/0024-3205(92)90572-7] [PMID: 1608289]
[144]
Bomford A, Isaac J, Roberts S, Edwards A, Young S, Williams R. The effect of desferrioxamine on transferrin receptors, the cell cycle and growth rates of human leukaemic cells. Biochem J 1986; 236(1): 243-9.
[http://dx.doi.org/10.1042/bj2360243] [PMID: 3790074]
[145]
Ezashi T, Das P, Roberts RM. Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 2005; 102(13): 4783-8.
[http://dx.doi.org/10.1073/pnas.0501283102] [PMID: 15772165]
[146]
Tsai CC, Su PF, Huang YF, Yew TL, Hung SC. Oct4 and Nanog directly regulate Dnmt1 to maintain self-renewal and undifferentiated state in mesenchymal stem cells. Mol Cell 2012; 47(2): 169-82.
[http://dx.doi.org/10.1016/j.molcel.2012.06.020] [PMID: 22795133]
[147]
Potier E, Ferreira E, Andriamanalijaona R, et al. Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone 2007; 40(4): 1078-87.
[http://dx.doi.org/10.1016/j.bone.2006.11.024] [PMID: 17276151]
[148]
Pattappa G, Thorpe SD, Jegard NC, Heywood HK, de Bruijn JD, Lee DA. Continuous and uninterrupted oxygen tension influences the colony formation and oxidative metabolism of human mesenchymal stem cells. Tissue Eng Part C Methods 2013; 19(1): 68-79.
[http://dx.doi.org/10.1089/ten.tec.2011.0734] [PMID: 22731854]
[149]
Malladi P, Xu Y, Chiou M, Giaccia AJ, Longaker MT. Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol Cell Physiol 2006; 290(4): C1139-46.
[http://dx.doi.org/10.1152/ajpcell.00415.2005] [PMID: 16291817]
[150]
Crisostomo PR, Wang Y, Markel TA, Wang M, Lahm T, Meldrum DR. Human mesenchymal stem cells stimulated by TNF-α, LPS, or hypoxia produce growth factors by an NFκB- but not JNK-dependent mechanism. Am J Physiol Cell Physiol 2008; 294(3): C675-82.
[http://dx.doi.org/10.1152/ajpcell.00437.2007] [PMID: 18234850]
[151]
Yoo HI, Moon YH, Kim MS. Effects of CoCl 2 on multi-lineage differentiation of C3H/10T1/2 mesenchymal stem cells. Korean J Physiol Pharmacol 2016; 20(1): 53-62.
[http://dx.doi.org/10.4196/kjpp.2016.20.1.53] [PMID: 26807023]
[152]
Lan A-P, Xiao L-C, Yang Z-L, et al. Interaction between ROS and p38MAPK contributes to chemical hypoxia-induced injuries in PC12 cells. Mol Med Rep 2012; 5(1): 250-5.
[PMID: 21993612]
[153]
Zhang W, Li G, Deng L, Qiu S, Deng R. New bone formation in a true bone ceramic scaffold loaded with desferrioxamine in the treatment of segmental bone defect: a preliminary study. J Orthop Sci 2012; 17(3): 289-98.
[http://dx.doi.org/10.1007/s00776-012-0206-z] [PMID: 22526711]
[154]
Farberg AS, Jing XL, Monson LA, et al. Deferoxamine reverses radiation induced hypovascularity during bone regeneration and repair in the murine mandible. Bone 2012; 50(5): 1184-7.
[http://dx.doi.org/10.1016/j.bone.2012.01.019] [PMID: 22314387]
[155]
Qu ZH, Zhang XL, Tang TT, Dai KR. Promotion of osteogenesis through β-catenin signaling by desferrioxamine. Biochem Biophys Res Commun 2008; 370(2): 332-7.
[http://dx.doi.org/10.1016/j.bbrc.2008.03.092] [PMID: 18375202]
[156]
Suárez G. Effect of desferrioxamine and deferiprone on osteocalcin secretion in osteoblast-type cells. Nefrologia 2003; 23: 27-31.
[157]
Diaz M, Elorriaga R, Canteros A, Cannata Andía JB. Effect of desferrioxamine and deferiprone (L1) on the proliferation of MG-63 bone cells and on phosphatase alkaline activity. Nephrol Dial Transplant 1998; 13(90003) (Suppl. 3): 23-8.
[http://dx.doi.org/10.1093/ndt/13.suppl_3.23] [PMID: 9568816]
[158]
Mu S, Guo S, Wang X, et al. Effects of deferoxamine on the osteogenic differentiation of human periodontal ligament cells. Mol Med Rep 2017; 16(6): 9579-86.
[http://dx.doi.org/10.3892/mmr.2017.7810] [PMID: 29039615]
[159]
Schipani E, Ryan HE, Didrickson S, Kobayashi T, Knight M, Johnson RS. Hypoxia in cartilage: HIF-1α is essential for chondrocyte growth arrest and survival. Genes Dev 2001; 15(21): 2865-76.
[http://dx.doi.org/10.1101/gad.934301] [PMID: 11691837]
[160]
Provot S, Zinyk D, Gunes Y, et al. Hif-1α regulates differentiation of limb bud mesenchyme and joint development. J Cell Biol 2007; 177(3): 451-64.
[http://dx.doi.org/10.1083/jcb.200612023] [PMID: 17470636]
[161]
Robins JC, Akeno N, Mukherjee A, et al. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9. Bone 2005; 37(3): 313-22.
[http://dx.doi.org/10.1016/j.bone.2005.04.040] [PMID: 16023419]
[162]
Duval E, Baugé C, Andriamanalijaona R, et al. Molecular mechanism of hypoxia-induced chondrogenesis and its application in in vivo cartilage tissue engineering. Biomaterials 2012; 33(26): 6042-51.
[http://dx.doi.org/10.1016/j.biomaterials.2012.04.061] [PMID: 22677190]
[163]
Amarilio R, Viukov SV, Sharir A, Eshkar-Oren I, Johnson RS, Zelzer E. HIF1α regulation of Sox9 is necessary to maintain differentiation of hypoxic prechondrogenic cells during early skeletogenesis. Development 2007; 134(21): 3917-28.
[164]
Thoms BL, Dudek KA, Lafont JE, Murphy CL. Hypoxia promotes the production and inhibits the destruction of human articular cartilage. Arthritis Rheum 2013; 65(5): 1302-12.
[http://dx.doi.org/10.1002/art.37867] [PMID: 23334958]
[165]
Cheng M-s, Yi X, Zhou Q. Overexpression of HIF-1alpha in bone marrow mesenchymal stem cells promote the repair of mandibular condylar osteochondral defect in a rabbit model. J Oral and Maxillofacial Surg 2021; 79(2): 345-e1.e15.
[166]
Adesida AB, Mulet-Sierra A, Jomha NM. Hypoxia mediated isolation and expansion enhances the chondrogenic capacity of bone marrow mesenchymal stromal cells. Stem Cell Res Ther 2012; 3(2): 9.
[http://dx.doi.org/10.1186/scrt100] [PMID: 22385573]
[167]
Sathy BN, Daly A, Gonzalez-Fernandez T, et al. Hypoxia mimicking hydrogels to regulate the fate of transplanted stem cells. Acta Biomater 2019; 88: 314-24.
[http://dx.doi.org/10.1016/j.actbio.2019.02.042] [PMID: 30825603]
[168]
Falcon JM, Chirman D, Veneziale A, et al. DMOG negatively impacts tissue engineered cartilage development. Cartilage 2021; 13 (2 Suppl): 722S-33S.
[http://dx.doi.org/10.1177/1947603520967060] [PMID: 33100027]
[169]
Jeon ES, Shin JH, Hwang SJ, Moon GJ, Bang OY, Kim HH. Cobalt chloride induces neuronal differentiation of human mesenchymal stem cells through upregulation of microRNA-124a. Biochem Biophys Res Commun 2014; 444(4): 581-7.
[http://dx.doi.org/10.1016/j.bbrc.2014.01.114] [PMID: 24491559]
[170]
Bader AM, Klose K, Bieback K, et al. Hypoxic preconditioning increases survival and pro-angiogenic capacity of human cord blood mesenchymal stromal cells in vitro. PLoS One 2015; 10(9): e0138477.
[http://dx.doi.org/10.1371/journal.pone.0138477] [PMID: 26380983]
[171]
Khoshlahni N, Sagha M, Mirzapour T, Zarif MN, Mohammadzadeh-Vardin M. Iron depletion with deferoxamine protects bone marrow-derived mesenchymal stem cells against oxidative stress-induced apoptosis. Cell Stress Chaperones 2020; 25(6): 1059-69.
[http://dx.doi.org/10.1007/s12192-020-01142-9] [PMID: 32729002]
[172]
Greijer AE, van der Wall E. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J Clin Pathol 2004; 57(10): 1009-14.
[http://dx.doi.org/10.1136/jcp.2003.015032] [PMID: 15452150]
[173]
Salim A, Nacamuli RP, Morgan EF, Giaccia AJ, Longaker MT. Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts. J Biol Chem 2004; 279(38): 40007-16.
[http://dx.doi.org/10.1074/jbc.M403715200] [PMID: 15263007]
[174]
Utting JC, Robins SP, Brandao-Burch A, Orriss IR, Behar J, Arnett TR. Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts. Exp Cell Res 2006; 312(10): 1693-702.
[http://dx.doi.org/10.1016/j.yexcr.2006.02.007] [PMID: 16529738]
[175]
Zhang Z, Yang C, Shen M, et al. Autophagy mediates the beneficial effect of hypoxic preconditioning on bone marrow mesenchymal stem cells for the therapy of myocardial infarction. Stem Cell Res Ther 2017; 8(1): 89.
[http://dx.doi.org/10.1186/s13287-017-0543-0] [PMID: 28420436]
[176]
Liu J, Hao H, Huang H, et al. Hypoxia regulates the therapeutic potential of mesenchymal stem cells through enhanced autophagy. Int J Low Extrem Wounds 2015; 14(1): 63-72.
[http://dx.doi.org/10.1177/1534734615573660] [PMID: 25759412]
[177]
Lee SG, Joe YA. Autophagy mediates enhancement of proangiogenic activity by hypoxia in mesenchymal stromal/stem cells. Biochem Biophys Res Commun 2018; 501(4): 941-7.
[http://dx.doi.org/10.1016/j.bbrc.2018.05.086] [PMID: 29772235]
[178]
Kusuma GD, Carthew J, Lim R, Frith JE. Effect of the microenvironment on mesenchymal stem cell paracrine signaling: opportunities to engineer the therapeutic effect. Stem Cells Dev 2017; 26(9): 617-31.
[http://dx.doi.org/10.1089/scd.2016.0349] [PMID: 28186467]
[179]
Daneshmandi L, Shah S, Jafari T, et al. Emergence of the stem cell secretome in regenerative engineering. Trends Biotechnol 2020; 38(12): 1373-84.
[http://dx.doi.org/10.1016/j.tibtech.2020.04.013] [PMID: 32622558]
[180]
Wobma HM, Tamargo MA, Goeta S, Brown LM, Duran-Struuck R, Vunjak-Novakovic G. The influence of hypoxia and IFN-γ on the proteome and metabolome of therapeutic mesenchymal stem cells. Biomaterials 2018; 167: 226-34.
[http://dx.doi.org/10.1016/j.biomaterials.2018.03.027] [PMID: 29574308]
[181]
Linero I, Chaparro O. Paracrine effect of mesenchymal stem cells derived from human adipose tissue in bone regeneration. PLoS One 2014; 9(9): e107001.
[http://dx.doi.org/10.1371/journal.pone.0107001] [PMID: 25198551]
[182]
Hsiao ST, Lokmic Z, Peshavariya H, et al. Hypoxic conditioning enhances the angiogenic paracrine activity of human adipose-derived stem cells. Stem Cells Dev 2013; 22(10): 1614-23.
[http://dx.doi.org/10.1089/scd.2012.0602] [PMID: 23282141]
[183]
Bousnaki M, Bakopoulou A, Pich A, Papachristou E, Kritis A, Koidis P. Mapping the secretome of dental pulp stem cells under variable microenvironmental conditions. Stem Cell Rev Rep 2021; 2021: 1-36.
[PMID: 34553309]
[184]
Paquet J, Deschepper M, Moya A, Logeart-Avramoglou D, Boisson-Vidal C, Petite H. Oxygen tension regulates human mesenchymal stem cell paracrine functions. Stem Cells Transl Med 2015; 4(7): 809-21.
[http://dx.doi.org/10.5966/sctm.2014-0180] [PMID: 25979862]
[185]
Saraswati S, Guo Y, Atkinson J, Young PP. Prolonged hypoxia induces monocarboxylate transporter-4 expression in mesenchymal stem cells resulting in a secretome that is deleterious to cardiovascular repair. Stem Cells 2015; 33(4): 1333-44.
[http://dx.doi.org/10.1002/stem.1935] [PMID: 25537659]
[186]
Yang Y, Lee EH, Yang Z. Hypoxia-conditioned mesenchymal stem cells in tissue regeneration application. Tissue Eng Part B Rev 2022; 28(5): 966-77.
[http://dx.doi.org/10.1089/ten.teb.2021.0145] [PMID: 34569290]
[187]
Yu H, Xu Z, Qu G, et al. Hypoxic preconditioning enhances the efficacy of mesenchymal stem cells-derived conditioned medium in switching microglia toward anti-inflammatory polarization in ischemia/reperfusion. Cell Mol Neurobiol 2021; 41(3): 505-24.
[http://dx.doi.org/10.1007/s10571-020-00868-5] [PMID: 32424775]
[188]
Philipp D, Suhr L, Wahlers T, Choi YH, Paunel-Görgülü A. Preconditioning of bone marrow-derived mesenchymal stem cells highly strengthens their potential to promote IL-6-dependent M2b polarization. Stem Cell Res Ther 2018; 9(1): 286.
[http://dx.doi.org/10.1186/s13287-018-1039-2] [PMID: 30359316]
[189]
Lan YW, Choo KB, Chen CM, et al. Hypoxia-preconditioned mesenchymal stem cells attenuate bleomycin-induced pulmonary fibrosis. Stem Cell Res Ther 2015; 6(1): 97.
[http://dx.doi.org/10.1186/s13287-015-0081-6] [PMID: 25986930]
[190]
Jiang CM, Liu J, Zhao JY, et al. Effects of hypoxia on the immunomodulatory properties of human gingiva-derived mesenchymal stem cells. J Dent Res 2015; 94(1): 69-77.
[http://dx.doi.org/10.1177/0022034514557671] [PMID: 25403565]
[191]
Zhilai Z, Biling M, Sujun Q, et al. Preconditioning in lowered oxygen enhances the therapeutic potential of human umbilical mesenchymal stem cells in a rat model of spinal cord injury. Brain Res 2016; 1642: 426-35.
[http://dx.doi.org/10.1016/j.brainres.2016.04.025] [PMID: 27085204]
[192]
Petrenko Y, Vackova I, Kekulova K, et al. A comparative analysis of multipotent mesenchymal stromal cells derived from different sources, with a focus on neuroregenerative potential. Sci Rep 2020; 10(1): 4290.
[http://dx.doi.org/10.1038/s41598-020-61167-z] [PMID: 32152403]
[193]
Bhandi S, Al Kahtani A, Mashyakhy M, et al. Modulation of the dental pulp stem cell secretory profile by hypoxia induction using cobalt chloride. J Pers Med 2021; 11(4): 247.
[http://dx.doi.org/10.3390/jpm11040247] [PMID: 33808091]
[194]
Kwak J, Choi SJ, Oh W, Yang YS, Jeon HB, Jeon ES. Cobalt chloride enhances the anti-inflammatory potency of human umbilical cord blood-derived mesenchymal stem cells through the ERK-HIF-1α-microRNA-146a-mediated signaling pathway. Stem Cells Int 2018; 2018: 4978763.
[http://dx.doi.org/10.1155/2018/4978763] [PMID: 30254683]
[195]
Bidkhori HR, Ahmadiankia N, Matin MM, et al. Chemically primed bone-marrow derived mesenchymal stem cells show enhanced expression of chemokine receptors contributed to their migration capability. Iran J Basic Med Sci 2016; 19(1): 14-9.
[PMID: 27096059]
[196]
Heirani-Tabasi A, Naderi-Meshkin H, Matin MM, et al. Augmented migration of mesenchymal stem cells correlates with the subsidiary CXCR4 variant. Cell Adhes Migr 2018; 12(2): 1-9.
[http://dx.doi.org/10.1080/19336918.2016.1243643] [PMID: 29466916]
[197]
Mazzinghi B, Ronconi E, Lazzeri E, et al. Essential but differential role for CXCR4 and CXCR7 in the therapeutic homingof human renal progenitor cells. J Exp Med 2008; 205(2): 479-90.
[http://dx.doi.org/10.1084/jem.20071903] [PMID: 18268039]
[198]
Oses C, Olivares B, Ezquer M, et al. Preconditioning of adipose tissue-derived mesenchymal stem cells with deferoxamine increases the production of pro-angiogenic, neuroprotective and anti-inflammatory factors: Potential application in the treatment of diabetic neuropathy. PLoS One 2017; 12(5): e0178011.
[http://dx.doi.org/10.1371/journal.pone.0178011] [PMID: 28542352]
[199]
Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. nature 2000; 408(6809): 239-47.
[200]
Yasui Y, Chijimatsu R, Hart DA, et al. Preparation of scaffold-free tissue-engineered constructs derived from human synovial mesenchymal stem cells under low oxygen tension enhances their chondrogenic differentiation capacity. Tissue Eng Part A 2016; 22(5-6): 490-500.
[http://dx.doi.org/10.1089/ten.tea.2015.0458] [PMID: 26974507]
[201]
Liu J, He J, Ge L, et al. Hypoxic preconditioning rejuvenates mesenchymal stem cells and enhances neuroprotection following intracerebral hemorrhage via the miR-326-mediated autophagy. Stem Cell Res Ther 2021; 12(1): 413.
[http://dx.doi.org/10.1186/s13287-021-02480-w] [PMID: 34294127]
[202]
Isik B, Thaler R, Goksu BB, et al. Hypoxic preconditioning induces epigenetic changes and modifies swine mesenchymal stem cell angiogenesis and senescence in experimental atherosclerotic renal artery stenosis. Stem Cell Res Ther 2021; 12(1): 240.
[http://dx.doi.org/10.1186/s13287-021-02310-z] [PMID: 33853680]
[203]
Polonis K, Becari C, Chahal CAA, et al. Chronic intermittent hypoxia triggers a senescence-like phenotype in human white preadipocytes. Sci Rep 2020; 10(1): 6846.
[http://dx.doi.org/10.1038/s41598-020-63761-7] [PMID: 32321999]
[204]
Lunyak VV, Amaro-Ortiz A, Gaur M. Mesenchymal stem cells secretory responses: senescence messaging secretome and immunomodulation perspective. Front Genet 2017; 8: 220.
[http://dx.doi.org/10.3389/fgene.2017.00220] [PMID: 29312442]
[205]
Coppé JP, Patil CK, Rodier F, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008; 6(12): e301.
[http://dx.doi.org/10.1371/journal.pbio.0060301] [PMID: 19053174]
[206]
Kuilman T, Peeper DS. Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 2009; 9(2): 81-94.
[http://dx.doi.org/10.1038/nrc2560] [PMID: 19132009]
[207]
Rodier F, Coppé JP, Patil CK, et al. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 2009; 11(8): 973-9.
[http://dx.doi.org/10.1038/ncb1909] [PMID: 19597488]
[208]
van Vliet T, Varela-Eirin M, Wang B, Borghesan M, Brandenburg SM, Franzin R, et al. Physiological hypoxia restrains the senescence-associated secretory phenotype via AMPK-mediated mTOR suppression. Mol Cell 2021; 81(9): 2041-52.
[209]
Freund A, Orjalo AV, Desprez PY, Campisi J. Inflammatory networks during cellular senescence: causes and consequences. Trends Mol Med 2010; 16(5): 238-46.
[http://dx.doi.org/10.1016/j.molmed.2010.03.003] [PMID: 20444648]
[210]
Ritschka B, Storer M, Mas A, et al. The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration. Genes Dev 2017; 31(2): 172-83.
[http://dx.doi.org/10.1101/gad.290635.116] [PMID: 28143833]
[211]
Vassilieva IO, Reshetnikova GF, Shatrova AN, et al. Senescence-messaging secretome factors trigger premature senescence in human endometrium-derived stem cells. Biochem Biophys Res Commun 2018; 496(4): 1162-8.
[http://dx.doi.org/10.1016/j.bbrc.2018.01.163] [PMID: 29397942]
[212]
Xu M, Pirtskhalava T, Farr JN, et al. Senolytics improve physical function and increase lifespan in old age. Nat Med 2018; 24(8): 1246-56.
[http://dx.doi.org/10.1038/s41591-018-0092-9] [PMID: 29988130]
[213]
González A, Hall MN, Lin SC, Hardie DG. AMPK and TOR: the yin and yang of cellular nutrient sensing and growth control. Cell Metab 2020; 31(3): 472-92.
[http://dx.doi.org/10.1016/j.cmet.2020.01.015] [PMID: 32130880]
[214]
Avgustinova A, Benitah SA. Epigenetic control of adult stem cell function. Nat Rev Mol Cell Biol 2016; 17(10): 643-58.
[http://dx.doi.org/10.1038/nrm.2016.76] [PMID: 27405257]
[215]
Yin B, Yu F, Wang C, Li B, Liu M, Ye L. Epigenetic control of mesenchymal stem cell fate decision via histone methyltransferase Ash1l. Stem Cells 2019; 37(1): 115-27.
[http://dx.doi.org/10.1002/stem.2918] [PMID: 30270478]
[216]
Dobrynin G, McAllister TE, Leszczynska KB, et al. KDM4A regulates HIF-1 levels through H3K9me3. Sci Rep 2017; 7(1): 11094.
[http://dx.doi.org/10.1038/s41598-017-11658-3] [PMID: 28894274]
[217]
Choudhry H, Harris AL. Advances in hypoxia-inducible factor biology. Cell Metab 2018; 27(2): 281-98.
[http://dx.doi.org/10.1016/j.cmet.2017.10.005] [PMID: 29129785]
[218]
Hsu KF, Wilkins SE, Hopkinson RJ, et al. Hypoxia and hypoxia mimetics differentially modulate histone post-translational modifications. Epigenetics 2021; 16(1): 14-27.
[http://dx.doi.org/10.1080/15592294.2020.1786305] [PMID: 32609604]
[219]
Liu W, Li L, Rong Y, et al. Hypoxic mesenchymal stem cell-derived exosomes promote bone fracture healing by the transfer of miR-126. Acta Biomater 2020; 103: 196-212.
[http://dx.doi.org/10.1016/j.actbio.2019.12.020] [PMID: 31857259]
[220]
Peltzer J, Lund K, Goriot ME, et al. Interferon-γ and hypoxia priming have limited effect on the miRNA landscape of human mesenchymal stromal cells-derived extracellular vesicles. Front Cell Dev Biol 2020; 8: 581436.
[http://dx.doi.org/10.3389/fcell.2020.581436] [PMID: 33384991]
[221]
Gervin E, Shin B, Opperman R, et al. Chemically induced hypoxia enhances miRNA functions in breast cancer. Cancers (Basel) 2020; 12(8): 2008.
[http://dx.doi.org/10.3390/cancers12082008] [PMID: 32707933]
[222]
He J, Huang Y, Liu J, et al. Hypoxic conditioned promotes the proliferation of human olfactory mucosa mesenchymal stem cells and relevant lncRNA and mRNA analysis. Life Sci 2021; 265: 118861.
[http://dx.doi.org/10.1016/j.lfs.2020.118861] [PMID: 33301811]
[223]
Vrtačnik P, Marc J, Ostanek B. Hypoxia mimetic deferoxamine influences the expression of histone acetylation- and DNA methylation-associated genes in osteoblasts. Connect Tissue Res 2015; 56(3): 228-35.
[http://dx.doi.org/10.3109/03008207.2015.1017573] [PMID: 25674819]
[224]
Ahani-Nahayati M, Solali S, Shams Asenjan K, et al. Promoter methylation status of survival-related genes in MOLT-4 cells co-cultured with bone marrow mesenchymal stem cells under hypoxic conditions. Cell J 2018; 20(2): 188-94.
[PMID: 29633596]
[225]
Schmitz C, Pepelanova I, Seliktar D, et al. Live reporting for hypoxia: Hypoxia sensor-modified mesenchymal stem cells as in vitro reporters. Biotechnol Bioeng 2020; 117(11): 3265-76.
[http://dx.doi.org/10.1002/bit.27503] [PMID: 32667700]
[226]
Ishiuchi N, Nakashima A, Doi S, et al. Hypoxia-preconditioned mesenchymal stem cells prevent renal fibrosis and inflammation in ischemia-reperfusion rats. Stem Cell Res Ther 2020; 11(1): 130.
[http://dx.doi.org/10.1186/s13287-020-01642-6] [PMID: 32197638]
[227]
Liu L, Gao J, Yuan Y, Chang Q, Liao Y, Lu F. Hypoxia preconditioned human adipose derived mesenchymal stem cells enhance angiogenic potential via secretion of increased VEGF and bFGF. Cell Biol Int 2013; 37(6): 551-60.
[http://dx.doi.org/10.1002/cbin.10097] [PMID: 23505143]
[228]
Choi JR, Pingguan-Murphy B, Abas WABW, et al. Hypoxia promotes growth and viability of human adipose-derived stem cells with increased growth factors secretion. J Asian Sci Res 2014; 4(7): 328-38.
[229]
Chai M, Gu C, Shen Q, et al. Hypoxia alleviates dexamethasone-induced inhibition of angiogenesis in cocultures of HUVECs and rBMSCs via HIF-1α. Stem Cell Res Ther 2020; 11(1): 343.
[http://dx.doi.org/10.1186/s13287-020-01853-x] [PMID: 31900237]

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