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


Cite item

Full Text

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.

About the authors

Goknur Yasan

Department of Oral and Maxillofacial Surgery, Hacettepe University

Author for correspondence.
Email: info@benthamscience.net

Aysen Gunel-Ozcan

Department of Stem Cell Sciences Center for Stem Cell Research and Development, Hacettepe University

Author for correspondence.
Email: info@benthamscience.net

References

  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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1002/jcb.20886 PMID: 16619257
  18. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007; 110(10): 3499-506. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1186/s13287-020-01853-x PMID: 31900237

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Bentham Science Publishers