Preconditioning of Hypoxic Culture Increases The Therapeutic Potential of Adipose Derived Mesenchymal Stem Cells

Authors

  • Tito Sumarwoto Doctoral Program, Faculty of Medicine, Airlangga University, Surabaya, Indonesia; Department of Orthopaedics and Traumatology, Faculty of Medicine, Prof Soeharso Orthopaedic Hospital, Sebelas Maret University, Surakarta, Indonesia
  • Heri Suroto Department of Orthopaedic and Traumatology, Faculty of Medicine, Dr. Soetomo General Hospital, Airlangga University, Surabaya, Indonesia https://orcid.org/0000-0002-9384-897X
  • Ferdiansyah Mahyudin Department of Orthopaedic and Traumatology, Faculty of Medicine, Dr. Soetomo General Hospital, Airlangga University, Surabaya, Indonesia
  • Dwikora Novembri Utomo Department of Orthopaedic and Traumatology, Faculty of Medicine, Dr. Soetomo General Hospital, Airlangga University, Surabaya, Indonesia
  • Romaniyanto Romaniyanto Department of Orthopaedics and Traumatology, Faculty of Medicine, Prof Soeharso Orthopaedic Hospital, Sebelas Maret University, Surakarta, Indonesia
  • Andhi Prijosedjati Department of Orthopaedics and Traumatology, Faculty of Medicine, Prof Soeharso Orthopaedic Hospital, Sebelas Maret University, Surakarta, Indonesia
  • Pamudji Utomo Department of Orthopaedics and Traumatology, Faculty of Medicine, Prof Soeharso Orthopaedic Hospital, Sebelas Maret University, Surakarta, Indonesia
  • Cita Rosita Sigit Prakoeswa Department of Dermatology and Venereology, Faculty of Medicine, Dr. Soetomo General Hospital, Airlangga University, Surabaya, Indonesia https://orcid.org/0000-0003-3232-095X
  • Fedik Abdul Rantam Department of Microbiology, Virology and Immunology Laboratory, Faculty of Veterinary Medicine, Airlangga University, Surabaya, Indonesia; Stem Cell Research and Development Center, Airlangga University, Surabaya, Indonesia
  • Damayanti Tinduh Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Dr. Soetomo General Hospital, Airlangga University, Surabaya, Indonesia
  • Hari Basuki Notobroto Faculty of Public Health, Airlangga University, Surabaya, Indonesia
  • Sholahuddin Rhatomy Department of Orthopaedics and Traumatology, Dr. Soeradji Tirtonegoro General Hospital, Klaten, Indonesia; Faculty of Medicine, Public Health, and Nursing, Gadjah Mada University, Yogyakarta, Indonesia

DOI:

https://doi.org/10.3889/oamjms.2021.5870

Keywords:

Hypoxic, Culture, Adipose Derived Mesenchymal Stem Cells

Abstract

Various in vitro preconditioning strategies have been implemented to increase the regenerative capacity of MSCs. Among them are modulation of culture atmosphere (hypoxia or anoxia), three-dimensional culture (3D), addition of trophic factors (in the form of growth factors, cytokines or hormones), lipopolysaccharides, and pharmacological agents. Preconditioning mesenchymal stem cells by culturing them in a hypoxic environment, which resembles the natural oxygen environment of the tissues (1% –7%) and not with standard culture conditions (21%), increases the survival of these cells via Hypoxia Inducible Factor-1α (HIF-1a) and via Akt-dependent mechanisms. In addition, the hypoxic precondition stimulates the secretion of pro-angiogenic growth factors, increases the expression of chemokines SDF-1 (stromal cell-derived factor-1) and its receptor CXCR4 (chemokine receptor type 4) - CXCR7 (chemokine receptor type 7) and increases engraftment of stem cell. This review aims to provide an overview of the preconditioned hypoxic treatment to increase the therapeutic potential of adipose-derived mesenchymal stem cells.

 

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Plum Analytics Artifact Widget Block

References

Zhang R, Rosen JM. The role of undifferentiated adiposederived stem cells in peripheral nerve repair. Neural Regen Res. 2018;13(5):757-63. https://doi.org/10.4103/1673-5374.232457 PMid:29862994 DOI: https://doi.org/10.4103/1673-5374.232457

Mazini L, Rochette L, Amine M, Malka G. Regenerative capacity of adipose derived stem cells (ADSCs), comparison with mesenchymal stem cells (MSCs). Int J Mol Sci. 2019;20(10):2523. https://doi.org/10.3390/ijms20102523 PMid:31121953 DOI: https://doi.org/10.3390/ijms20102523

Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation. 2002;105(1):93-8. https://doi.org/10.1161/hc0102.101442 PMid:11772882 DOI: https://doi.org/10.1161/hc0102.101442

Schäfer R, Spohn G, Baer PC. Mesenchymal stem/stromal cells in regenerative medicine: Can preconditioning strategies improve therapeutic efficacy? Transfus Med Hemother. 2016;43(4):256-67. https://doi.org/10.1159/000447458 PMid:27721701 DOI: https://doi.org/10.1159/000447458

Hu X, Yu SP, Fraser JL, Lu Z, Ogle ME, Wang JA, et al. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg. 2008;135(4):799-808. https://doi.org/10.1016/j.jtcvs.2007.07.071 PMid:18374759 DOI: https://doi.org/10.1016/j.jtcvs.2007.07.071

Hung S, Pochampally RR, Hsu S, Sanchez C, Chen SC, Spees J, et al. Short-term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PLoS One. 2007;5:e416. https://doi.org/10.1371/journal.pone.0000416 PMid:17476338 DOI: https://doi.org/10.1371/journal.pone.0000416

Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, et al. Clarification of the nomenclature for MSC: The international society for cellular therapy position statement. Cytotherapy. 2005;7(5):393-5. https://doi.org/10.1080/14653240500319234 PMid:16236628 DOI: https://doi.org/10.1080/14653240500319234

Jacobs SA, Pinxteren J, Roobrouck VD, Luyckx A, van’t Hof W, Deans R, et al. Human multipotent adult progenitor cells are nonimmunogenic and exert potent immunomodulatory effects on alloreactive T-cell responses. Cell Transplant. 2013;22(10):1915-28. https://doi.org/10.3727/096368912x657369 PMid:23031260 DOI: https://doi.org/10.3727/096368912X657369

Tsuji W, Rubin JP, Marra KG. Adipose-derived stem cells: Implications in tissue regeneration. World J Stem Cells. 2014;6(3):312-21. https://doi.org/10.4252/wjsc.v6.i3.312 PMid:25126381 DOI: https://doi.org/10.4252/wjsc.v6.i3.312

Meng F, Zhou D, Li W. Adipose-derived stem cells as a potential weapon for diabetic foot ulcers. Int J Clin Exp Med. 2017;10(12):15967-73.

Lee HC, An SG, Lee HW, Park JS, Cha KS, Hong TJ, et al. Safety and effect of adipose tissue-derived stem cell implantation in patients with critical limb ischemia: A pilot study. Circ J. 2012;76:1750-60. https://doi.org/10.1253/circj.cj-11-1135 PMid:22498564 DOI: https://doi.org/10.1253/circj.CJ-11-1135

Porada C, Zanjani E, Almeida-Porada G. Adult mesenchymal stem cells: A pluripotent population with multiple applications. Curr Stem Cell Res Ther. 2012;1(3):365-9. https://doi.org/10.2174/157488806778226821 PMid:18220880 DOI: https://doi.org/10.2174/157488806778226821

Zuk P. Adipose-derived stem cells in tissue regeneration: A review. ISRN Stem Cells. 2013;2013(1):1-35. https://doi.org/10.1155/2013/713959 DOI: https://doi.org/10.1155/2013/713959

Casadei A, Epis R, Ferroni L, Tocco I, Gardin C, Bressan E, et al. Adipose tissue regeneration: A state of the art. J Biomed Biotechnol. 2012;2012:462543. https://doi.org/10.1155/2012/462543 PMid:23193362 DOI: https://doi.org/10.1155/2012/462543

Fairbairn NG, Meppelink AM, Ng-Glazier J, Randolph MA, Winograd JM. Augmenting peripheral nerve regeneration using stem cells: A review of current opinion. World J Stem Cells. 2015;7(1):11-26. https://doi.org/10.4252/wjsc.v7.i1.11 PMid:25621102 DOI: https://doi.org/10.4252/wjsc.v7.i1.11

Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, et al. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng. 2001;7(2):211-28. https://doi.org/10.1089/107632701300062859 PMid:11304456 DOI: https://doi.org/10.1089/107632701300062859

Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002;13(12):4279-95. https://doi.org/10.1091/mbc.e02-02-0105 PMid:12475952 DOI: https://doi.org/10.1091/mbc.e02-02-0105

Gimble J, Guilak F. Adipose-derived stem cells: Isolation, characterization, and differentiation potential. Cytotherapy. 2003;5(5):362-9. https://doi.org/10.1080/14653240310003026 PMid:14578098 DOI: https://doi.org/10.1080/14653240310003026

Kim YJ, Kim HK, Cho HK, Bae YC, Suh KT, Jung JS. Direct comparison of human mesenchymal stem cells derived from adipose tissues and bone marrow in mediating neovascularization in response to vascular ischemia. Cell Physiol Biochem. 2007;20(6):867-76. https://doi.org/10.1159/000110447 PMid:17982269 DOI: https://doi.org/10.1159/000110447

Kingham PJ, Kolar MK, Novikova LN, Novikov LN, Wiberg M. Stimulating the neurotrophic and angiogenic properties of human adipose-derived stem cells enhances nerve repair. Stem Cells Dev. 2013;23(7):741-54. https://doi.org/10.1089/scd.2013.0396 PMid:24124760 DOI: https://doi.org/10.1089/scd.2013.0396

Kapur SK, Katz AJ. Review of the adipose derived stem cell secretome. Biochimie. 2013;95(12):2222-8. https://doi.org/10.1016/j.biochi.2013.06.001 PMid:23770442 DOI: https://doi.org/10.1016/j.biochi.2013.06.001

Kingham PJ, Kalbermatten DF, Mahay D, Armstrong SJ, Wiberg M, Terenghi G. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol. 2007;207(2):267-74. https://doi.org/10.1016/j.expneurol.2007.06.029 PMid:17761164 DOI: https://doi.org/10.1016/j.expneurol.2007.06.029

Chandra V, Swetha G, Muthyala S, Jaiswal AK, Bellare JR, Nair PD, et al. Islet-like cell aggregates generated from human adipose tissue derived stem cells ameliorate experimental diabetes in mice. PLoS One. 2011;6(6):e20615. https://doi.org/10.1371/journal.pone.0020615 PMid:21687731 DOI: https://doi.org/10.1371/journal.pone.0020615

Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F. Rapid hepatic fate specification of adipose-derived stem cells and their therapeutic potential for liver failure. J Gastroenterol Hepatol. 2009;24(1):70-7. https://doi.org/10.1111/j.1440-1746.2008.05496.x PMid:18624899 DOI: https://doi.org/10.1111/j.1440-1746.2008.05496.x

De Ugarte DA, Morizono K, Elbarbary A, Alfonso Z, Zuk PA, Zhu M, et al. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs. 2003;174(3):101-9. https://doi.org/10.1159/000071150 PMid:12835573 DOI: https://doi.org/10.1159/000071150

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. https://doi.org/10.1634/stemcells.2005-0342 PMid:16410387 DOI: https://doi.org/10.1634/stemcells.2005-0342

Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol. 2005;33(11):1402-16. https://doi.org/10.1016/j.exphem.2005.07.003 PMid:16263424 DOI: https://doi.org/10.1016/j.exphem.2005.07.003

Heo JS, Choi Y, Kim HS, Kim HO. Comparison of molecular profiles of human mesenchymal stem cells derived from bone marrow, umbilical cord blood, placenta and adipose tissue. Int J Mol Med. 2016;37(1):115-25. https://doi.org/10.3892/ijmm.2015.2413 PMid:26719857 DOI: https://doi.org/10.3892/ijmm.2015.2413

Carbone A, Rucci M, Luigi A, Portincasa A, Conese M. Adipose-derived stem cells and platelet-rich plasma: Inputs for regenerative medicine. Med Res Arch. 2017;5(10):1-12.

Oberbauer E, Steffenhagen C, Wurzer C, Gabriel C, Redl H, Wolbank S. Enzymatic and non-enzymatic isolation systems for adipose tissue-derived cells: Current state of the art. Cell Regen. 2015;4:7. https://doi.org/10.1186/s13619-015-0020-0 PMid:26435835 DOI: https://doi.org/10.1186/s13619-015-0020-0

Baldari S, di Rocco G, Piccoli M, Muraca M, Toietta G. Challenges and strategies for improving the regenerative effects of mesenchymal stromal cell-based therapies. Int J Mol Sci. 2017;18(10):2087. https://doi.org/10.3390/ijms18102087 PMid:28974046 DOI: https://doi.org/10.3390/ijms18102087

Doorn J, Moll G, Le Blanc K, van Blitterswijk C, de Boer J. Therapeutic applications of mesenchymal stromal cells: Paracrine effects and potential improvements. Tissue Eng Part B Rev. 2012;18(2):101-15. https://doi.org/10.1089/ten.teb.2011.0488 PMid:21995703 DOI: https://doi.org/10.1089/ten.teb.2011.0488

Wang X, Liu C, Li S, Xu Y, Chen P, Liu Y, et al. Hypoxia precondition promotes adipose-derived mesenchymal stem cells based repair of diabetic erectile dysfunction via augmenting angiogenesis and neuroprotection. PLoS One. 2015;10(3):e0118951. https://doi.org/10.1371/journal.pone.0118951 PMid:25790284 DOI: https://doi.org/10.1371/journal.pone.0118951

Sart S, Ma T, Li Y. Preconditioning stem cells for in vivo delivery. Biores Open Access. 2014;3(4):137-49. PMid:25126478 DOI: https://doi.org/10.1089/biores.2014.0012

Guo M, Cai C, Zhao G, Qiu X, Zhao H, Ma Q, et al. Hypoxia promotes migration and induces CXCR4 expression via HIF-1alpha activation in human osteosarcoma. PLoS One. 2014;9(3):e90518. https://doi.org/10.1371/journal.pone.0090518 PMid:24618817 DOI: https://doi.org/10.1371/journal.pone.0090518

Wei L, Fraser JL, Lu Z, Hu X, Ping S. transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats. Neurobiol Dis. 2012;46(3):635-45. https://doi.org/10.1016/j.nbd.2012.03.002 PMid:22426403 DOI: https://doi.org/10.1016/j.nbd.2012.03.002

Lennon DP, Edmison JM, Caplan AI. Cultivation of rat marrowderived mesenchymal stem cells in reduced oxygen tension: Effects on in vitro and in vivo osteochondrogenesis. J Cell Physiol. 2001;187(3):345-55. https://doi.org/10.1002/jcp.1081 PMid:11319758 DOI: https://doi.org/10.1002/jcp.1081

Geng YJ. Molecular mechanisms for cardiovascular stem cell apoptosis and growth in the hearts with atherosclerotic coronary disease and ischemic heart failure. Ann NY Acad Sci. 2003;1010:687-97. https://doi.org/10.1196/annals.1299.126 PMid:15033813 DOI: https://doi.org/10.1196/annals.1299.126

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. https://doi.org/10.1136/jcp.2003.015032 PMid:15452150 DOI: https://doi.org/10.1136/jcp.2003.015032

Martin AR, Ronco C, Demange L, Benhida R. Hypoxia inducible factor down-regulation, cancer and cancer stem cells (CSCs): Ongoing success stories. Medchemcomm. 2017;8(1):21-52. https://doi.org/10.1039/c6md00432f PMid:30108689 DOI: https://doi.org/10.1039/C6MD00432F

Sun X, Fang B, Zhao X, Zhang G, Ma H. Preconditioning of mesenchymal stem cells by sevoflurane to improve their therapeutic potential. PLoS One. 2014;9(3):e90667. https://doi.org/10.1371/journal.pone.0090667 PMid:24599264 DOI: https://doi.org/10.1371/journal.pone.0090667

Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003;3(10):721-32. PMid:13130303 DOI: https://doi.org/10.1038/nrc1187

Romain B, Hachet-Haas M, Rohr S, Brigand C, Galzi JL, Gaub MP, et al. Hypoxia differentially regulated CXCR4 and CXCR7 signaling in colon cancer. Mol Cancer. 2014;13:58. https://doi.org/10.1186/1476-4598-13-58 PMid:24629239 DOI: https://doi.org/10.1186/1476-4598-13-58

Abdolmohammadi K, Mahmoudi T, Nojehdehi S, Tayebi L, Hashemi SM, Noorbakhsh F, et al. Effect of hypoxia preconditioned adipose-derived mesenchymal stem cell conditioned medium on cerulein-induced acute pancreatitis in mice. Adv Pharm Bull. 2020;10(2):297-306. https://doi.org/10.34172/apb.2020.036 PMid:32373500 DOI: https://doi.org/10.34172/apb.2020.036

Xue Y, Li Z, Wang Y, Zhu X, Hu R, Xu W. Role of the HIF-1 α/SDF1/CXCR4 signaling axis in accelerated fracture healing after craniocerebral injury. Mol Med Rep. 2020;22(16):2767-74. https://doi.org/10.3892/mmr.2020.11361 PMid:32945380 DOI: https://doi.org/10.3892/mmr.2020.11361

Lee JW, Ko J. Hypoxia signaling in human diseases and therapeutic targets. Exp Mol Med. 2019;51(6):1-13. https://doi.org/10.1128/mcb.00409-10 PMid:31221962 DOI: https://doi.org/10.1038/s12276-019-0235-1

Culver C, Sundqvist A, Mudie S, Melvin A, Xirodimas D, Rocha S. Mechanism of hypoxia-induced NF-kappa B. Mol Cell Biol. 2010;30(20):4901-21. PMid:20696840 DOI: https://doi.org/10.1128/MCB.00409-10

Hu C, Wang L, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1 alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol. 2003;23(24):9361-74. https://doi.org/10.1128/mcb.23.24.9361-9374.2003 PMid:14645546 DOI: https://doi.org/10.1128/MCB.23.24.9361-9374.2003

Kang S, Kim S, Sung J. Cellular and molecular stimulation of adipose-derived stem cells under hypoxia. Cell Biol Int. 2014;38(5):553-62. https://doi.org/10.1002/cbin.10246 PMid:24446066 DOI: https://doi.org/10.1002/cbin.10246

Drela K, Sarnowska A, Siedlecka P, Szablowska-Gadomska I, Wielgos M, Jurga M, et al. Low oxygen atmosphere facilitates proliferation and maintains undifferentiated state of umbilical cord mesenchymal stem cells in an hypoxia inducible factordependent manner. Cytotherapy. 2014;16(7):881-92. https://doi.org/10.1016/j.jcyt.2014.02.009 PMid:24726658 DOI: https://doi.org/10.1016/j.jcyt.2014.02.009

Portalska KJ, Leferink A, Groen N, Fernandes H, Moroni L, van Blitterswijk C, et al. Endothelial differentiation of mesenchymal stromal cells. PLoS One. 2012;7(10):e46842. https://doi.org/10.1371/journal.pone.0046842 PMid:23056481 DOI: https://doi.org/10.1371/journal.pone.0046842

Chang W, Lee CY, Park JH, Park MS, Maeng LS, Yoon CS, et al. Survival of hypoxic human mesenchymal stem cells is enhanced by a positive feedback loop involving miR-210 and hypoxia-induced factor I. J Vet Sci. 2013;14(1):69-76. https://doi.org/10.4142/jvs.2013.14.1.69 PMid:23388440 DOI: https://doi.org/10.4142/jvs.2013.14.1.69

Kim JH, Park SG, Song S, Kim JK, Sung J. Reactive oxygen species-responsive miR-210 regulates proliferation and migration of adipose-derived stem cells via PTPN2. Cell Death Dis. 2013;4(4):e588. https://doi.org/10.1038/cddis.2013.117 PMid:23579275 DOI: https://doi.org/10.1038/cddis.2013.117

Kim JH, Park S, Park SG, Choi J, Xia Y, Sung J. The pivotal role of reactive oxygen species generation in the hypoxia-induced stimulation of adipose-derived stem cells. Stem Cells Dev. 2011;20(10):1753-61. https://doi.org/10.1089/scd.2010.0469 PMid:21265612 DOI: https://doi.org/10.1089/scd.2010.0469

Weijers EM, van den Broek LJ, Waaijman T, van Hinsbergh VW, Gibbs S, Koolwijk P. The influence of hypoxia and fibrinogen variants on the expansion and differentiation of adipose tissuederived mesenchymal stem cells. Tissue Eng Part A. 2011;17(21-22):2675-85. https://doi.org/10.1089/ten.tea.2010.0661 PMid:21830936 DOI: https://doi.org/10.1089/ten.tea.2010.0661

Yang J, Zhang H, Zhao L, Chen Y, Liu H, Zhang T. Human adipose tissue-derived stem cells protect impaired cardiomyocytes from hypoxia/reoxygenation injury through hypoxia-induced paracrine mechanism. Cell Biochem Funct. 2012;30(6):505-14. https://doi.org/10.1002/cbf.2829 PMid:22610511 DOI: https://doi.org/10.1002/cbf.2829

Kim JH, Song S, Park SG, Song SU, Xia Y, Sung J. Primary involvement of NADPH oxidase 4 in hypoxia-induced generation of reactive oxygen species in adipose-derived stem cells. Stem Cells Dev. 2012;21(12):2212-21. https://doi.org/10.1089/scd.2011.0561 PMid:22181007 DOI: https://doi.org/10.1089/scd.2011.0561

Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10(8):858-64. https://doi.org/10.1038/nm1075 PMid:15235597 DOI: https://doi.org/10.1038/nm1075

Fotia C, Massa A, Boriani F, Baldini N. Hypoxia enhances proliferation and stemness of human adipose-derived mesenchymal stem cells. Cytotechnology. 2015;67(6):1073-84. https://doi.org/10.1007/s10616-014-9731-2 PMid:24798810 DOI: https://doi.org/10.1007/s10616-014-9731-2

Bruno S, Grange C, Collino F, Deregibus MC, Cantaluppi V, Biancone L, et al. Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS One. 2012;7(3):e33115. https://doi.org/10.1371/journal.pone.0033115 PMid:22431999 DOI: https://doi.org/10.1371/journal.pone.0033115

Chistiakov DA, Chekhonin VP. Extracellular vesicles shed by glioma cells: Pathogenic role and clinical value. Tumour Biol. 2014;35(9):8425-38. https://doi.org/10.1007/s13277-014-2262-9 PMid:24969563 DOI: https://doi.org/10.1007/s13277-014-2262-9

Quesenberry PJ, Goldberg LR, Aliotta JM, Dooner MS, Pereira MG, Wen S, et al. Cellular phenotype and extracellular vesicles: Basic and clinical considerations. Stem Cells Dev. 2014;23(13):1429-36. https://doi.org/10.1089/scd.2013.0594 PMid:24564699 DOI: https://doi.org/10.1089/scd.2013.0594

Beegle J, Lakatos K, Kalomoiris S, Stewart H, Isseroff RR, Nolta JA, et al. Hypoxic preconditioning of mesenchymal stromal cells induces metabolic changes, enhances survival, and promotes cell retention in vivo. Stem Cells. 2015;33:1818-28. https://doi.org/10.1002/stem.1976 PMid:25702874 DOI: https://doi.org/10.1002/stem.1976

Stubbs SL, Hsiao ST, Peshavariya HM, Lim SY, Dusting GJ, Dilley RJ. Hypoxic preconditioning enhances survival of human adipose-derived stem cells and conditions endothelial cells in vitro. Stem Cells Dev. 2012;21(11):1887-96. https://doi.org/10.1089/scd.2011.0289 PMid:22165914 DOI: https://doi.org/10.1089/scd.2011.0289

Zhang W, Liu L, Huo Y, Yang Y, Wang Y. Hypoxia-pretreated human MSCs attenuate acute kidney injury through enhanced angiogenic and antioxidative capacities. Biomed Res Int. 2014;2014:462472. https://doi.org/10.1155/2014/462472 PMid:25133162 DOI: https://doi.org/10.1155/2014/462472

Wang L, Sanford MT, Xin Z, Lin G, Lue TF. Role of schwann cells in the regeneration of penile and peripheral nerves. Asian J Androl. 2015;17(5):776-82. https://doi.org/10.4103/1008-682x.154306 PMid:25999359 DOI: https://doi.org/10.4103/1008-682X.154306

Downloads

Published

2021-10-31

How to Cite

1.
Sumarwoto T, Suroto H, Mahyudin F, Utomo DN, Romaniyanto R, Prijosedjati A, Utomo P, Prakoeswa CRS, Rantam FA, Tinduh D, Notobroto HB, Rhatomy S. Preconditioning of Hypoxic Culture Increases The Therapeutic Potential of Adipose Derived Mesenchymal Stem Cells. Open Access Maced J Med Sci [Internet]. 2021 Oct. 31 [cited 2024 Nov. 22];9(F):505-1. Available from: https://oamjms.eu/index.php/mjms/article/view/5870

Issue

Vol. 9 No. F (2021): F - Review Articles

Section

Narrative Review Article

Categories

License

Copyright (c) 2021 Tito Sumarwoto, Heri Suroto, Ferdiansyah Mahyudin, Dwikora Novembri Utomo, Romaniyanto Romaniyanto, Andhi Prijosedjati, Pamudji Utomo, Cita Rosita Sigit Prakoeswa, Fedik Abdul Rantam, Damayanti Tinduh, Hari Basuki Notobroto, Sholahuddin Rhatomy (Author)

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

http://creativecommons.org/licenses/by-nc/4.0

Crossref
Scopus
Google Scholar
Europe PMC