Korean Circulation Journal

The Korean Society of Cardiology (대한심장학회)
권호 표지
DOI QR코드

DOI QR Code

Adipose Tissue-Derived Stem Cells for Myocardial Regeneration

  • Joo, Hyung Joon (Department of Cardiology, Cardiovascular Center, Korea University Anam Hospital) ;
  • Kim, Jong-Ho (Department of Cardiology, Cardiovascular Center, Korea University Anam Hospital) ;
  • Hong, Soon Jun (Department of Cardiology, Cardiovascular Center, Korea University Anam Hospital)
  • Received : 2016.05.18
  • Accepted : 2016.07.15
  • Published : 2017.03.31
⟨ Previous Next ⟩

Abstract

Over the past decade, stem cell therapy has been extensively studied for clinical application for heart diseases. Among various stem cells, adipose tissue-derived stem cell (ADSC) is still an attractive stem cell resource due to its abundance and easy accessibility. In vitro studies showed the multipotent differentiation potentials of ADSC, even differentiation into cardiomyocytes. Many pre-clinical animal studies have also demonstrated promising therapeutic results of ADSC. Furthermore, there were several clinical trials showing the positive results in acute myocardial infarction using ADSC. The present article covers the brief introduction, the suggested therapeutic mechanisms, application methods including cell dose and delivery, and human clinical trials of ADSC for myocardial regeneration.

Keywords

Acknowledgement

Supported by : Korea Health Industry Development Institute (KHIDI), National Research Foundation of Korea (NRF)

References

  1. Moran AE, Forouzanfar MH, Roth GA, et al. Temporal trends in ischemic heart disease mortality in 21 world regions, 1980 to 2010: the Global Burden of Disease 2010 study. Circulation 2014;129:1483-92. https://doi.org/10.1161/CIRCULATIONAHA.113.004042
  2. Bourin P, Bunnell BA, Casteilla L, et al. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 2013;15:641-8. https://doi.org/10.1016/j.jcyt.2013.02.006
  3. Hong SJ, Traktuev DO, March KL. Therapeutic potential of adiposederived stem cells in vascular growth and tissue repair. Curr Opin Organ Transplant 2010;15:86-91. https://doi.org/10.1097/MOT.0b013e328334f074
  4. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001;7:211-28. https://doi.org/10.1089/107632701300062859
  5. Halvorsen YD, Franklin D, Bond AL, et al. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 2001;7:729-41. https://doi.org/10.1089/107632701753337681
  6. Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 2002;290:763-9. https://doi.org/10.1006/bbrc.2001.6270
  7. Gimble J, Guilak F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 2003;5:362-9. https://doi.org/10.1080/14653240310003026
  8. De Francesco F, Tirino V, Desiderio V, et al. Human CD34/CD90 ASCs are capable of growing as sphere clusters, producing high levels of VEGF and forming capillaries. PLoS One 2009;4:e6537. https://doi.org/10.1371/journal.pone.0006537
  9. Kim JH, Lim IR, Joo HJ, et al. Sphere formation of adipose stem cell engineered by poly-2-hydroxyethyl methacrylate induces in vitro angiogenesis through fibroblast growth factor 2. Biochem Biophys Res Commun 2015;468:372-9. https://doi.org/10.1016/j.bbrc.2015.10.083
  10. Hong SJ, Rogers PI, Kihlken J, et al. Intravenous xenogeneic transplantation of human adipose-derived stem cells improves left ventricular function and microvascular integrity in swine myocardial infarction model. Catheter Cardiovasc Interv 2015;86:E38-48. https://doi.org/10.1002/ccd.25566
  11. 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;8:315-7. https://doi.org/10.1080/14653240600855905
  12. Maumus M, Peyrafitte JA, D'Angelo R, et al. Native human adipose stromal cells: localization, morphology and phenotype. Int J Obes (Lond) 2011;35:1141-53. https://doi.org/10.1038/ijo.2010.269
  13. Rodbell M. Localization of lipoprotein lipase in fat cells of rat adipose tissue. J Biol Chem 1964;239:753-5.
  14. Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13:4279-95. https://doi.org/10.1091/mbc.e02-02-0105
  15. Nicoletti GF, De Francesco F, D'Andrea F, Ferraro GA. Methods and procedures in adipose stem cells: state of the art and perspective for translation medicine. J Cell Physiol 2015;230:489-95. https://doi.org/10.1002/jcp.24837
  16. D'Andrea F, De Francesco F, Ferraro GA, et al. Large-scale production of human adipose tissue from stem cells: a new tool for regenerative medicine and tissue banking. Tissue Eng Part C Methods 2008;14:233-42. https://doi.org/10.1089/ten.tec.2008.0108
  17. Yu G, Floyd ZE, Wu X, et al. Adipogenic differentiation of adiposederived stem cells. Methods Mol Biol 2011;702:193-200.
  18. Kroeze RJ, Knippenberg M, Helder MN. Osteogenic differentiation strategies for adipose-derived mesenchymal stem cells. Methods Mol Biol 2011;702:233-48.
  19. Cheng SL, Yang JW, Rifas L, Zhang SF, Avioli LV. Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone. Endocrinology 1994;134:277-86. https://doi.org/10.1210/endo.134.1.8275945
  20. Huang JI, Zuk PA, Jones NF, et al. Chondrogenic potential of multipotential cells from human adipose tissue. Plast Reconstr Surg 2004;113:585-94. https://doi.org/10.1097/01.PRS.0000101063.27008.E1
  21. Planat-Benard V, Silvestre JS, Cousin B, et al. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 2004;109:656-63. https://doi.org/10.1161/01.CIR.0000114522.38265.61
  22. Janeczek Portalska K, Leferink A, Groen N, et al. Endothelial differentiation of mesenchymal stromal cells. PLoS One 2012;7:e46842. https://doi.org/10.1371/journal.pone.0046842
  23. Mizuno H, Zuk PA, Zhu M, Lorenz HP, Benhaim P, Hedrick MH. Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg 2002;109:199-209; discussion 210-1. https://doi.org/10.1097/00006534-200201000-00030
  24. Planat-Benard V, Menard C, Andre M, et al. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res 2004;94:223-9. https://doi.org/10.1161/01.RES.0000109792.43271.47
  25. Rehman J, Traktuev D, Li J, et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004;109:1292-8. https://doi.org/10.1161/01.CIR.0000121425.42966.F1
  26. Katz AJ, Tholpady A, Tholpady SS, Shang H, Ogle RC. Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells 2005;23:412-23. https://doi.org/10.1634/stemcells.2004-0021
  27. Nakagami H, Morishita R, Maeda K, Kikuchi Y, Ogihara T, Kaneda Y. Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. J Atheroscler Thromb 2006;13:77-81. https://doi.org/10.5551/jat.13.77
  28. Varma MJ, Breuls RG, Schouten TE, et al. Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells Dev 2007;16:91-104. https://doi.org/10.1089/scd.2006.0026
  29. Li CY, Wu XY, Tong JB, et al. Comparative analysis of human mesenchymal stem cells from bone marrow and adipose tissue under xeno-free conditions for cell therapy. Stem Cell Res Ther 2015;6:55. https://doi.org/10.1186/s13287-015-0066-5
  30. Jin HJ, Bae YK, Kim M, et al. Comparative analysis of human mesenchymal stem cells from bone marrow, adipose tissue, and umbilical cord blood as sources of cell therapy. Int J Mol Sci 2013;14:17986-8001. https://doi.org/10.3390/ijms140917986
  31. Kern S, Eichler H, Stoeve J, Kluter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006;24:1294-301. https://doi.org/10.1634/stemcells.2005-0342
  32. Ullah I, Subbarao RB, Rho GJ. Human mesenchymal stem cells - current trends and future prospective. Biosci Rep 2015;35. pii: e00191.
  33. Bai X, Yan Y, Song YH, et al. Both cultured and freshly isolated adipose tissue-derived stem cells enhance cardiac function after acute myocardial infarction. Eur Heart J 2010;31:489-501. https://doi.org/10.1093/eurheartj/ehp568
  34. Chang JC, Lee PC, Lin YC, Lee KW, Hsu SH. Primary adipose-derived stem cells enriched by growth factor treatment improves cell adaptability toward cardiovascular differentiation in a rodent model of acute myocardial infarction. J Stem Cells 2011;6:21-37.
  35. Wang L, Deng J, Tian W, et al. Adipose-derived stem cells are an effective cell candidate for treatment of heart failure: an MR imaging study of rat hearts. Am J Physiol Heart Circ Physiol 2009;297:H1020-31. https://doi.org/10.1152/ajpheart.01082.2008
  36. Acquistapace A, Bru T, Lesault PF, et al. Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer. Stem Cells 2011;29:812-24. https://doi.org/10.1002/stem.632
  37. Yang D, Wang W, Li L, et al. The relative contribution of paracine effect versus direct differentiation on adipose-derived stem cell transplantation mediated cardiac repair. PLoS One 2013;8:e59020. https://doi.org/10.1371/journal.pone.0059020
  38. Mazo M, Planat-Benard V, Abizanda G, et al. Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction. Eur J Heart Fail 2008;10:454-62. https://doi.org/10.1016/j.ejheart.2008.03.017
  39. Madonna R, Geng YJ, De Caterina R. Adipose tissue-derived stem cells: characterization and potential for cardiovascular repair. Arterioscler Thromb Vasc Biol 2009;29:1723-9. https://doi.org/10.1161/ATVBAHA.109.187179
  40. Meliga E, Strem BM, Duckers HJ, Serruys PW. Adipose-derived cells. Cell Transplant 2007;16:963-70. https://doi.org/10.3727/096368907783338190
  41. Chen L, Qin F, Ge M, Shu Q, Xu J. Application of adipose-derived stem cells in heart disease. J Cardiovasc Transl Res 2014;7:651-63. https://doi.org/10.1007/s12265-014-9585-1
  42. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008;103:1204-19. https://doi.org/10.1161/CIRCRESAHA.108.176826
  43. Kondo K, Shintani S, Shibata R, et al. Implantation of adipose-derived regenerative cells enhances ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol 2009;29:61-6. https://doi.org/10.1161/ATVBAHA.108.166496
  44. Hao C, Shintani S, Shimizu Y, et al. Therapeutic angiogenesis by autologous adipose-derived regenerative cells: comparison with bone marrow mononuclear cells. Am J Physiol Heart Circ Physiol 2014;307:H869-79. https://doi.org/10.1152/ajpheart.00310.2014
  45. Puissant B, Barreau C, Bourin P, et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005;129:118-29. https://doi.org/10.1111/j.1365-2141.2005.05409.x
  46. Rasmussen JG, Frobert O, Holst-Hansen C, et al. Comparison of human adipose-derived stem cells and bone marrow-derived stem cells in a myocardial infarction model. Cell Transplant 2014;23:195-206. https://doi.org/10.3727/096368912X659871
  47. Paul A, Srivastava S, Chen G, Shum-Tim D, Prakash S. Functional assessment of adipose stem cells for xenotransplantation using myocardial infarction immunocompetent models: comparison with bone marrow stem cells. Cell Biochem Biophys 2013;67:263-73. https://doi.org/10.1007/s12013-011-9323-0
  48. Hong SJ, Kihlken J, Choi SC, March KL, Lim DS. Intramyocardial transplantation of human adipose-derived stromal cell and endothelial progenitor cell mixture was not superior to individual cell type transplantation in improving left ventricular function in rats with myocardial infarction. Int J Cardiol 2013;164:205-11. https://doi.org/10.1016/j.ijcard.2011.06.128
  49. Naaijkens BA, van Dijk A, Kamp O, Krijnen PA, Niessen HW, Juffermans LJ. Therapeutic application of adipose derived stem cells in acute myocardial infarction: lessons from animal models. Stem Cell Rev 2014;10:389-98.
  50. Fischer UM, Harting MT, Jimenez F, et al. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev 2009;18:683-92. https://doi.org/10.1089/scd.2008.0253
  51. Zhu XY, Zhang XZ, Xu L, Zhong XY, Ding Q, Chen YX. Transplantation of adipose-derived stem cells overexpressing hHGF into cardiac tissue. Biochem Biophys Res Commun 2009;379:1084-90. https://doi.org/10.1016/j.bbrc.2009.01.019
  52. van Dijk A, Naaijkens BA, Jurgens WJ, et al. Reduction of infarct size by intravenous injection of uncultured adipose derived stromal cells in a rat model is dependent on the time point of application. Stem Cell Res 2011;7:219-29. https://doi.org/10.1016/j.scr.2011.06.003
  53. Valina C, Pinkernell K, Song YH, et al. Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J 2007;28:2667-77. https://doi.org/10.1093/eurheartj/ehm426
  54. Yang JJ, Yang X, Liu ZQ, et al. Transplantation of adipose tissuederived stem cells overexpressing heme oxygenase-1 improves functions and remodeling of infarcted myocardium in rabbits. Tohoku J Exp Med 2012;226:231-41. https://doi.org/10.1620/tjem.226.231
  55. Alt E, Pinkernell K, Scharlau M, et al. Effect of freshly isolated autologous tissue resident stromal cells on cardiac function and perfusion following acute myocardial infarction. Int J Cardiol 2010;144:26-35. https://doi.org/10.1016/j.ijcard.2009.03.124
  56. De Siena R, Balducci L, Blasi A, et al. Omentum-derived stromal cells improve myocardial regeneration in pig post-infarcted heart through a potent paracrine mechanism. Exp Cell Res 2010;316:1804-15. https://doi.org/10.1016/j.yexcr.2010.02.009
  57. Rigol M, Solanes N, Farre J, et al. Effects of adipose tissue-derived stem cell therapy after myocardial infarction: impact of the route of administration. J Card Fail 2010;16:357-66. https://doi.org/10.1016/j.cardfail.2009.12.006
  58. Mazo M, Hernandez S, Gavira JJ, et al. Treatment of reperfused ischemia with adipose-derived stem cells in a preclinical Swine model of myocardial infarction. Cell Transplant 2012;21:2723-33. https://doi.org/10.3727/096368912X638847
  59. Hong SJ, Hou D, Brinton TJ, et al. Intracoronary and retrograde coronary venous myocardial delivery of adipose-derived stem cells in swine infarction lead to transient myocardial trapping with predominant pulmonary redistribution. Catheter Cardiovasc Interv 2014;83:E17-25. https://doi.org/10.1002/ccd.24659
  60. Wang H, Shi J, Wang Y, et al. Promotion of cardiac differentiation of brown adipose derived stem cells by chitosan hydrogel for repair after myocardial infarction. Biomaterials 2014;35:3986-98. https://doi.org/10.1016/j.biomaterials.2014.01.021
  61. Sun CK, Zhen YY, Leu S, et al. Direct implantation versus platelet-rich fibrin-embedded adipose-derived mesenchymal stem cells in treating rat acute myocardial infarction. Int J Cardiol 2014;173:410-23. https://doi.org/10.1016/j.ijcard.2014.03.015
  62. Ishii M, Shibata R, Shimizu Y, et al. Multilayered adipose-derived regenerative cell sheets created by a novel magnetite tissue engineering method for myocardial infarction. Int J Cardiol 2014;175:545-53. https://doi.org/10.1016/j.ijcard.2014.06.034
  63. Yeh TS, Fang YH, Lu CH, et al. Baculovirus-transduced, VEGFexpressing adipose-derived stem cell sheet for the treatment of myocardium infarction. Biomaterials 2014;35:174-84. https://doi.org/10.1016/j.biomaterials.2013.09.080
  64. Ishida O, Hagino I, Nagaya N, et al. Adipose-derived stem cell sheet transplantation therapy in a porcine model of chronic heart failure. Transl Res 2015;165:631-9. https://doi.org/10.1016/j.trsl.2014.12.005
  65. Pavo N, Charwat S, Nyolczas N, et al. Cell therapy for human ischemic heart diseases: critical review and summary of the clinical experiences. J Mol Cell Cardiol 2014;75:12-24. https://doi.org/10.1016/j.yjmcc.2014.06.016
  66. Houtgraaf JH, den Dekker WK, van Dalen BM, et al. First experience in humans using adipose tissue-derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction. J Am Coll Cardiol 2012;59:539-40. https://doi.org/10.1016/j.jacc.2011.09.065
  67. Perin EC, Sanz-Ruiz R, Sanchez PL, et al. Adipose-derived regenerative cells in patients with ischemic cardiomyopathy: The PRECISE Trial. Am Heart J 2014;168:88-95.e2. https://doi.org/10.1016/j.ahj.2014.03.022
  68. Henry TD, Pepine C, Lambert C, et al. The Athena Trials: Autologous Adipose-Derived Regenerative Cells (ADRCs) for Refractory Chronic Myocardial Ischemia with Left Ventricular Dysfunction. Catheter Cardiovasc Interv 2017:1;89:169-77. https://doi.org/10.1002/ccd.26601
  69. Qayyum AA, Haack-Sorensen M, Mathiasen AB, Jorgensen E, Ekblond A, Kastrup J. Adipose-derived mesenchymal stromal cells for chronic myocardial ischemia (MyStromalCell Trial): study design. Regen Med 2012;7:421-8. https://doi.org/10.2217/rme.12.17
  70. Follin B, Tratwal J, Haack-Sorensen M, Elberg JJ, Kastrup J, Ekblond A. Identical effects of VEGF and serum-deprivation on phenotype and function of adipose-derived stromal cells from healthy donors and patients with ischemic heart disease. J Transl Med 2013;11:219. https://doi.org/10.1186/1479-5876-11-219

Cited by

  1. Mesenchymal Stem/Stromal Cell-Based Therapy for Heart Failure ― What Is the Best Source? ― vol.82, pp.9, 2018, https://doi.org/10.1253/circj.cj-18-0786
  2. Plasticity of Adipose Tissue-Derived Stem Cells and Regulation of Angiogenesis vol.9, pp.None, 2017, https://doi.org/10.3389/fphys.2018.01656
  3. Platelet-rich plasma enhances the proliferation of human adipose stem cells through multiple signaling pathways vol.9, pp.1, 2017, https://doi.org/10.1186/s13287-018-0851-z
  4. Insulin gene enhancer binding protein 1 induces adipose tissue‑derived stem cells to differentiate into pacemaker‑like cells vol.43, pp.2, 2017, https://doi.org/10.3892/ijmm.2018.4002
  5. An updated review of adipose derived-mesenchymal stem cells and their applications in musculoskeletal disorders vol.19, pp.3, 2017, https://doi.org/10.1080/14712598.2019.1563069
  6. A new combination of transcription factors increases the harvesting efficiency of pacemaker-like cells vol.19, pp.5, 2019, https://doi.org/10.3892/mmr.2019.10012
  7. Therapeutic Cell Protective Role of Histochrome under Oxidative Stress in Human Cardiac Progenitor Cells vol.17, pp.6, 2017, https://doi.org/10.3390/md17060368
  8. Adipose Tissue Stem Cells for Therapy: An Update on the Progress of Isolation, Culture, Storage, and Clinical Application vol.8, pp.7, 2019, https://doi.org/10.3390/jcm8070917
  9. Animal‐ and human‐based evidence for the protective effects of stem cell therapy against cardiovascular disorders vol.234, pp.9, 2017, https://doi.org/10.1002/jcp.28330
  10. Adipose-Derived Stem Cells: Current Applications and Future Directions in the Regeneration of Multiple Tissues vol.2020, pp.None, 2020, https://doi.org/10.1155/2020/8810813
  11. Adipose-derived mesenchymal stem cells promote the malignant phenotype of cervical cancer vol.10, pp.1, 2017, https://doi.org/10.1038/s41598-020-69907-x
  12. Adipose derived mesenchymal stem cells along with Alpinia oxyphylla extract alleviate mitochondria-mediated cardiac apoptosis in aging models and cardiac function in aging rats vol.264, pp.None, 2017, https://doi.org/10.1016/j.jep.2020.113297
  13. Cell and Cell Free Therapies in Osteoarthritis vol.9, pp.11, 2017, https://doi.org/10.3390/biomedicines9111726
  14. Nanofat: A therapeutic paradigm in regenerative medicine vol.13, pp.11, 2021, https://doi.org/10.4252/wjsc.v13.i11.1733
  15. Nanofat: A therapeutic paradigm in regenerative medicine vol.13, pp.11, 2021, https://doi.org/10.4252/wjsc.v13.i11.1736
  16. Immune modulation via adipose derived Mesenchymal Stem cells is driven by donor sex in vitro vol.11, pp.1, 2017, https://doi.org/10.1038/s41598-021-91870-4