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Biochemistry, Cell and Molecular Biology

Effects of hypoxia on stemness, survival and angiogenic capacity of muscle-derived stem/progenitor cells

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Pages 855-868 | Received 10 Feb 2021, Accepted 05 Jul 2021, Published online: 14 Sep 2021

References

  • Alessandri G, Pagano S, Bez A, Benetti A, Pozzi S, Iannolo G, Baronio M, Invernici G, Caruso A, Muneretto C, et al. 2004. Isolation and culture of human muscle-derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet. 364:1872–1883. Epub 2004/11/24.
  • An G, Guo F, Liu X, Wang Z, Zhu Y, Fan Y, Xuan C, Li Y, Wu H, Shi X, et al. 2020. Functional reconstruction of injured corpus cavernosa using 3D-printed hydrogel scaffolds seeded with HIF-1α-expressing stem cells. Nat Commun. 11:2687. Epub 2020/06/03.
  • Bellayr IH, Gharaibeh B, Huard J, Li Y. 2010. Skeletal muscle-derived stem cells differentiate into hepatocyte-like cells and aid in liver regeneration. Int J Clin Exp Pathol. 3:681–690. Epub 2010/09/11.
  • Bernhardt WM, Warnecke C, Willam C, Tanaka T, Wiesener MS, Eckardt KU. 2007. Organ protection by hypoxia and hypoxia-inducible factors. Methods Enzymol. 435:221–245. Epub 2007/11/14.
  • Boulahbel H, Durán RV, Gottlieb E. 2009. Prolyl hydroxylases as regulators of cell metabolism. Biochem Soc Trans. 37(Part 1):291–294. Epub 2009/01/16.
  • Calinescu AA, Yadav VN, Carballo E, Kadiyala P, Tran D, Zamler DB, Doherty R, Srikanth M, Lowenstein PR, Castro MG. 2017. Survival and proliferation of neural progenitor-derived glioblastomas under hypoxic stress is controlled by a CXCL12/CXCR4 autocrine-positive feedback mechanism. Clin Cancer Res. 23:1250–1262. Epub 2016/08/21.
  • Choi JR, Pingguan-Murphy B, Wan Abas WAB, Omar SZ, Chua KH, Mat Adenan NA, Wan Safwani WKZ. 2014. Hypoxia promotes growth and viability of human adipose-derived stem cells with increased growth factors secretion. J Asian Sci Res. 4:328–338.
  • Choi YJ, Lee JY, Lee SJ, Chung CP, Park YJ. 2012. Determination of osteogenic or adipogenic lineages in muscle-derived stem cells (MDSCs) by a collagen-binding peptide (CBP) derived from bone sialoprotein (BSP). Biochem Biophys Res Commun. 419:326–332. Epub 2012/02/22.
  • Csete M, Walikonis J, Slawny N, Wei Y, Korsnes S, Doyle JC, Wold B. 2001. Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in culture. J Cell Physiol. 189:189–196. Epub 2001/10/13.
  • Deasy BM, Gharaibeh BM, Pollett JB, Jones MM, Lucas MA, Kanda Y, Huard J. 2005. Long-term self-renewal of postnatal muscle-derived stem cells. Mol Biol Cell. 16:3323–3333. Epub 2005/05/06.
  • Faroni A, Mobasseri SA, Kingham PJ, Reid AJ. 2015. Peripheral nerve regeneration: experimental strategies and future perspectives. Adv Drug Deliv Rev. 82-83:160–167. Epub 2014/12/03.
  • Gharaibeh B, Lavasani M, Cummins JH, Huard J. 2011. Terminal differentiation is not a major determinant for the success of stem cell therapy – cross-talk between muscle-derived stem cells and host cells. Stem Cell Res Ther. 2:31. Epub 2011/07/13.
  • Gharaibeh B, Lu A, Tebbets J, Zheng B, Feduska J, Crisan M, Péault B, Cummins J, Huard J. 2008. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc. 3:1501–1509. Epub 2008/09/06.
  • Gonzalez-King H, García NA, Ontoria-Oviedo I, Ciria M, Montero JA, Sepúlveda P. 2017. Hypoxia inducible factor-1α potentiates jagged 1-mediated angiogenesis by mesenchymal stem cell-derived exosomes. Stem Cells. 35:1747–1759. Epub 2017/04/05.
  • Haider H, Ashraf M. 2010. Preconditioning and stem cell survival. J Cardiovasc Transl Res. 3:89–102. Epub 2010/06/19.
  • Han Y, Ren J, Bai Y, Pei X, Han Y. 2019. Exosomes from hypoxia-treated human adipose-derived mesenchymal stem cells enhance angiogenesis through VEGF/VEGF-R. Int J Biochem Cell Biol. 109:59–68. Epub 2019/02/03.
  • Hao D, He C, Ma B, Lankford L, Reynaga L, Farmer DL, Guo F, Wang A. 2019. Hypoxic preconditioning enhances survival and proangiogenic capacity of human first trimester chorionic villus-derived mesenchymal stem cells for fetal tissue engineering. Stem Cells Int. 2019:9695239. Epub 2019/11/30.
  • Haque N, Rahman MT, Abu Kasim NH, Alabsi AM. 2013. Hypoxic culture conditions as a solution for mesenchymal stem cell based regenerative therapy. Sci World J. 2013:632972. Epub 2013/09/27.
  • Ho SS, Hung BP, Heyrani N, Lee MA, Leach JK. 2018. Hypoxic preconditioning of mesenchymal stem cells with subsequent spheroid formation accelerates repair of segmental bone defects. Stem Cells. 36:1393–1403. Epub 2018/07/04.
  • Hoppeler H, Vogt M, Weibel ER, Flück M. 2003. Response of skeletal muscle mitochondria to hypoxia. Exp Physiol. 88:109–119. Epub 2003/01/15.
  • Ilic D, Ogilvie C. 2017. Concise review: human embryonic stem cells – what have we done? What are we doing? Where are we going? Stem Cells. 35:17–25. Epub 2016/06/29.
  • Jash S, Adhya S. 2015. Effects of transient hypoxia versus prolonged hypoxia on satellite cell proliferation and differentiation in vivo. Stem Cells Int. 2015:961307. Epub 2015/03/20.
  • Jiang RH, Wu CJ, Xu XQ, Lu SS, Zu QQ, Zhao LB, Wang J, Liu S, Shi HB. 2019. Hypoxic conditioned medium derived from bone marrow mesenchymal stromal cells protects against ischemic stroke in rats. J Cell Physiol. 234:1354–1368. Epub 2018/08/05.
  • Kawakami Y, Hambright WS, Takayama K, Mu X, Lu A, Cummins JH, Matsumoto T, Yurube T, Kuroda R, Kurosaka M, et al. 2019. Rapamycin rescues age-related changes in muscle-derived stem/progenitor cells from progeroid mice. Mol Therapy Methods Clin Develop. 14:64–76. Epub 2019/07/18.
  • Kazuno A, Maki D, Yamato I, Nakajima N, Seta H, Soeda S, Ozawa S, Uchiyama Y, Tamaki T. 2018. Regeneration of transected recurrent laryngeal nerve using hybrid-transplantation of skeletal muscle-derived stem cells and bioabsorbable scaffold. J Clin Med. 7:276–293. Epub 2018/09/15.
  • Kwon D, Kim Y, Pruchnic R, Jankowski R, Usiene I, de Miguel F, Huard J, Chancellor MB. 2006. Periurethral cellular injection: comparison of muscle-derived progenitor cells and fibroblasts with regard to efficacy and tissue contractility in an animal model of stress urinary incontinence. Urology. 68:449–454. Epub 2006/08/15.
  • Laumonier T, Bermont F, Hoffmeyer P, Kindler V, Menetrey J. 2017. Human myogenic reserve cells are quiescent stem cells that contribute to muscle regeneration after intramuscular transplantation in immunodeficient mice. Sci Rep. 7:3462. Epub 2017/06/16.
  • Lavasani M, Thompson SD, Pollett JB, Usas A, Lu A, Stolz DB, Clark KA, Sun B, Péault B, Huard J. 2014. Human muscle-derived stem/progenitor cells promote functional murine peripheral nerve regeneration. J Clin Invest. 124:1745–1756. Epub 2014/03/20.
  • Li H, Usas A, Poddar M, Chen CW, Thompson S, Ahani B, Cummins J, Lavasani M, Huard J. 2013. Platelet-rich plasma promotes the proliferation of human muscle derived progenitor cells and maintains their stemness. PLoS One. 8:e64923. Epub 2013/06/14.
  • Li X, Wang X, Zhang P, Zhu L, Zhao T, Liu S, Wu Y, Chen X, Fan M. 2012. Extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase pathway is involved in inhibition of myogenic differentiation of myoblasts by hypoxia. Exp Physiol. 97:257–264. Epub 2011/10/18.
  • Liu W, Wen Y, Bi P, Lai X, Liu XS, Liu X, Kuang S. 2012. Hypoxia promotes satellite cell self-renewal and enhances the efficiency of myoblast transplantation. Development. 139:2857–2865. Epub 2012/07/06.
  • Ma Z, Han D, Zhang P, Yang JF, Wang Y, Zhang Y, Yang D, Liu J. 2012. Utilizing muscle-derived stem cells to enhance long-term retention and aesthetic outcome of autologous fat grafting: pilot study in mice. Aesthetic Plast Surg. 36:186–192. Epub 2011/05/25.
  • McManis PG, Low PA. 1988. Factors affecting the relative viability of centrifascicular and subperineurial axons in acute peripheral nerve ischemia. Exp Neurol. 99:84–95. Epub 1988/01/01.
  • Meng SS, Xu XP, Chang W, Lu ZH, Huang LL, Xu JY, Liu L, Qiu HB, Yang Y, Guo FM. 2018. LincRNA-p21 promotes mesenchymal stem cell migration capacity and survival through hypoxic preconditioning. Stem Cell Res Ther. 9:280. Epub 2018/10/26.
  • Mitutsova V, Yeo WWY, Davaze R, Franckhauser C, Hani EH, Abdullah S, Mollard P, Schaeffer M, Fernandez A, Lamb NJC. 2017. Adult muscle-derived stem cells engraft and differentiate into insulin-expressing cells in pancreatic islets of diabetic mice. Stem Cell Res Ther. 8:86. Epub 2017/04/20.
  • Muscari C, Giordano E, Bonafè F, Govoni M, Pasini A, Guarnieri C. 2013. Priming adult stem cells by hypoxic pretreatments for applications in regenerative medicine. J Biomed Sci. 20:63. Epub 2013/08/30.
  • Oshima H, Payne TR, Urish KL, Sakai T, Ling Y, Gharaibeh B, Tobita K, Keller BB, Cummins JH, Huard J. 2005. Differential myocardial infarct repair with muscle stem cells compared to myoblasts. Mol Therapy. 12:1130–1141. Epub 2005/08/30.
  • Park HS, Choi GH, Hahn S, Yoo YS, Jung IM, Lee T. 2014. Tracking the fate of muscle-derived stem cells: an insight into the distribution and mode of action. Vasc Specialist Int. 30:11–18. Epub 2014/03/01.
  • Payne TR, Oshima H, Okada M, Momoi N, Tobita K, Keller BB, Peng H, Huard J. 2007. A relationship between vascular endothelial growth factor, angiogenesis, and cardiac repair after muscle stem cell transplantation into ischemic hearts. J Am Coll Cardiol. 50:1677–1684. Epub 2007/10/24.
  • Proto JD, Tang Y, Lu A, Chen WC, Stahl E, Poddar M, Beckman SA, Robbins PD, Nidernhofer LJ, Imbrogno K, et al. 2015. NF-κB inhibition reveals a novel role for HGF during skeletal muscle repair. Cell Death Dis. 6:e1730. Epub 2015/04/24.
  • Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, Mytinger J, Cao B, Gates C, Wernig A, et al. 2002. Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol. 157:851–864. Epub 2002/05/22.
  • Redshaw Z, Loughna PT. 2012. Oxygen concentration modulates the differentiation of muscle stem cells toward myogenic and adipogenic fates. Differentiation. 84:193–202. Epub 2012/07/14.
  • Rouwkema J, Khademhosseini A. 2016. Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. 34:733–745. Epub 2016/04/02.
  • Rugowska A, Wiernicki B, Maczewski M, Mackiewicz U, Chojnacka K, Bednarek-Rajewska K, Kluk A, Majewski P, Kolanowski T, Malcher A, et al. 2019. Human skeletal muscle-derived stem/progenitor cells modified with connexin-43 prevent arrhythmia in rat post-infarction hearts and influence gene expression in the myocardium. J Physiol Pharmacol. 70:917–933. Epub 2020/03/24.
  • Sakushima K, Yoshikawa M, Osaki T, Miyamoto N, Hashimoto T. 2020. Moderate hypoxia promotes skeletal muscle cell growth and hypertrophy in C2C12 cells. Biochem Biophys Res Commun. 525:921–927. Epub 2020/03/17.
  • Santos PM. 2000. A functional model system of an hypoxic nerve injury and its evaluation. Laryngoscope. 110:845–853. Epub 2000/05/12.
  • Scheib J, Höke A. 2013. Advances in peripheral nerve regeneration. Nat Rev Neurol. 9:668–676. Epub 2013/11/13.
  • Schneider C, Krischke G, Rascher W, Gassmann M, Trollmann R. 2012. Systemic hypoxia differentially affects neurogenesis during early mouse brain maturation. Brain Dev. 4:261–273. Epub 2011/08/10.
  • Sheu ML, Cheng FC, Su HL, Chen YJ, Chen CJ, Chiang CM, Chiu WT, Sheehan J, Pan HC. 2012. Recruitment by SDF-1α of CD34-positive cells involved in sciatic nerve regeneration. J Neurosurg. 116:432–444. Epub 2011/08/23.
  • Sinha KM, Tseng C, Guo P, Lu A, Pan H, Gao X, Andrews R, Eltzschig H, Huard J. 2019. Hypoxia-inducible factor 1α (HIF-1α) is a major determinant in the enhanced function of muscle-derived progenitors from MRL/MpJ mice. FASEB J. 33:8321–8334. Epub 2019/04/11.
  • Song M, Lavasani M, Thompson SD, Lu A, Ahani B, Huard J. 2013. Muscle-derived stem/progenitor cell dysfunction in Zmpste24-deficient progeroid mice limits muscle regeneration. Stem Cell Res Ther. 4:33. Epub 2013/03/28.
  • Stubbs SL, Hsiao ST, Peshavariya HM, Lim SY, Dusting GJ, Dilley RJ. 2012. Hypoxic preconditioning enhances survival of human adipose-derived stem cells and conditions endothelial cells in vitro. Stem Cells Dev. 21:1887–1896. Epub 2011/12/15.
  • Tamaki T. 2017. Therapeutic capacities of human and mouse skeletal muscle-derived stem cells for a long gap peripheral nerve injury. Neural Regen Res. 12:1811–1813. Epub 2017/12/15.
  • Vogel C, Marcotte EM. 2012. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet. 13:227–232. Epub 2012/03/14.
  • Wang H, Zhang D, Jia S, Huang S, Xiao L, Ma L, Liu G, Gong K, Xu L. 2018a. Effect of sustained hypoxia on autophagy of genioglossus muscle-derived stem cells. Med Sci Monit. 24:2218–2224. Epub 2018/04/14.
  • Wang HD, Guo Q, Quan A, Lopez J, Alonso-Escalante JC, Lough DM, Lee WPA, Brandacher G, Kumar AR. 2017. Vascular endothelial growth factor induction of muscle-derived stem cells enhances vascular phenotype while preserving myogenic potential. Ann Plast Surg. 79:404–409. Epub 2017/06/02.
  • Wang J, Zhang F, Yang H, Wu H, Cui R, Zhao Y, Jiao C, Wang X, Liu X, Wu L, et al. 2018b. Effect of TEAD4 on multilineage differentiation of muscle-derived stem cells. Am J Transl Res. 10:998–1011. Epub 2018/04/11.
  • Wan Safwani WKZ, Choi JR, Yong KW, Ting I, Mat Adenan NA, Pingguan-Murphy B. 2017. Hypoxia enhances the viability, growth and chondrogenic potential of cryopreserved human adipose-derived stem cells. Cryobiology. 75:91–99. Epub 2017/01/22.
  • Wei Y, Li Y, Chen C, Stoelzel K, Kaufmann AM, Albers AE. 2011. Human skeletal muscle-derived stem cells retain stem cell properties after expansion in myosphere culture. Exp Cell Res. 317:1016–1027. Epub 2011/02/01.
  • Werle SB, Chagastelles P, Pranke P, Casagrande L. 2019. Hypoxia upregulates the expression of the pluripotency markers in the stem cells from human deciduous teeth. Clin Oral Investig. 23:199–207. Epub 2018/04/08.
  • Wu X, Wang S, Chen B, An X. 2010. Muscle-derived stem cells: isolation, characterization, differentiation, and application in cell and gene therapy. Cell Tissue Res. 340:549–567. Epub 2010/05/25.
  • Xu W, Xu R, Li Z, Wang Y, Hu R. 2019. Hypoxia changes chemotaxis behaviour of mesenchymal stem cells via HIF-1α signalling. J Cell Mol Med. 23:1899–1907. Epub 2019/01/11.
  • Yang J, Wang X, Wang Y, Guo ZX, Luo DZ, Jia J, Wang XM. 2012. Dopaminergic neuronal conversion from adult rat skeletal muscle-derived stem cells in vitro. Neurochem Res. 37:1982–1992. Epub 2012/06/23.
  • Zagórska A, Dulak J. 2004. HIF-1: the knowns and unknowns of hypoxia sensing. Acta Biochim Pol. 51:563–585. Epub 2004/09/28.
  • Zhang T, Yang X, Liu T, Shao J, Fu N, Yan A, Geng K, Xia W. 2017. Adjudin-preconditioned neural stem cells enhance neuroprotection after ischemia reperfusion in mice. Stem Cell Res Ther. 8:248. Epub 2017/11/09.
  • Zhang Y, Ma L, Su Y, Su L, Lan X, Wu D, Han S, Li J, Kvederis L, Corey S, et al. 2019. Hypoxia conditioning enhances neuroprotective effects of aged human bone marrow mesenchymal stem cell-derived conditioned medium against cerebral ischemia in vitro. Brain Res. 1725:146432. Epub 2019/09/07.
  • Zhilai Z, Biling M, Sujun Q, Chao D, Benchao S, Shuai H, Shun Y, Hui Z. 2016. Preconditioning in lowered oxygen enhances the therapeutic potential of human umbilical mesenchymal stem cells in a rat model of spinal cord injury. Brain Res. 1642:426–435. Epub 2016/04/18.
  • Zimna A, Wiernicki B, Kolanowski T, Malcher A, Rozwadowska N, Labedz W, Kubaszewski L, Kurpisz M. 2018. Influence of hypoxia prevailing in post-infarction heart on proangiogenic gene expression and biological features of human myoblast cells applied as a pro-regenerative therapeutic tool. J Physiol Pharmacol. 69:859–874. Epub 2019/03/23.