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Adipose Tissue-Derived Mesenchymal Stem Cell and Angiogenesis in Ischemic Heart Disease

  • Lina BadimonEmail author
  • Blanca Oñate
  • Gemma Vilahur
Chapter
  • 1.6k Downloads
Part of the Advances in Biochemistry in Health and Disease book series (ABHD, volume 6)

Abstract

Acute myocardial infarction is one of the most important causes of death and disability worldwide. The limited capacity of the adult heart to self-regenerate and revascularize the ischemic damaged tissue leads to tissue loss, ventricular remodeling, and persistent deterioration in cardiac performance increasing the frequency of heart failure. Over the last several years, adult stem cells have appeared as one of the novel promising therapeutic approaches for the treatment of ischemic heart disease. However, the quest for the best cell type is still ongoing. This ideal cell type should be capable of differentiating into functional cardiomyocytes and of forming new vessels to nourish the damaged area. Recent studies have shown that adipose tissue contains multipotent stem cells (the so-called adipose tissue-derived stem cells or ASC) that are capable of regenerating injured myocardium by differentiating into cardiac resident cells or by secreting multiple angiogenic growth factors (paracrine effects). Moreover, due to ease of harvesting these cells in large numbers and low immunogenicity, white adipose tissue has become an attractive stem cell source. In this chapter, we review the principal characteristics of ASC as well as their capacity to repair cardiac damage in the setting of ischemic heart disease as compared with other adult stem cells, with special attention to their pro-­angiogenic mechanisms of action.

Keywords

Cell therapy Adipose tissue-derived stem cells Myocardial ­infarction Angiogenesis Cytokines 

Notes

Acknowledgements 

This work was supported by grants TERCEL, SAF 2010-16549, CIBEROBN CB06/03 and by the ENCITE (European Network for Cell Imaging and Tracking Expertise) project Cooperation Health-2007-1.2-4 In Vivo Image-guidance for Cell Therapy, Large-scale Integrating Project (to LB). We thank Fundacion Jesus Serra-FIC, Barcelona, for their continuous support. BO is a recipient of a predoctoral fellowship from Instituto Salud Carlos III, Madrid, and GV is a recipient of a contract from the Innovation and Science Spanish Ministry (RyC-2009-5495).

Disclosure No competing financial interests exist.

References

  1. 1.
    Armstrong L, Lako M, Buckley N et al (2012) Editorial: our top 10 developments in stem cell biology over the last 30 years. Stem Cells 30:2–9PubMedGoogle Scholar
  2. 2.
    Daher SR, Johnstone BH, Phinney DG, March KL (2008) Adipose stromal/stem cells: basic and translational advances: the IFATS collection. Stem Cells 26:2664–2665PubMedGoogle Scholar
  3. 3.
    Uccelli A, Moretta L, Pistoia V (2008) Mesenchymal stem cells in health and disease. Nat Rev Immunol 8:726–736PubMedGoogle Scholar
  4. 4.
    Bianco P, Robey PG, Simmons PJ (2008) Mesenchymal stem cells: revisiting history, ­concepts, and assays. Cell Stem Cell 2:313–319PubMedGoogle Scholar
  5. 5.
    Ranganath SH, Levy O, Inamdar MS, Karp JM (2012) Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 10:244–258PubMedGoogle Scholar
  6. 6.
    Dominici M, Le Blanc K, Mueller I et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317PubMedGoogle Scholar
  7. 7.
    Horwitz EM, Dominici M (2008) How do mesenchymal stromal cells exert their therapeutic benefit? Cytotherapy 10:771–774PubMedGoogle Scholar
  8. 8.
    Nadri S, Soleimani M (2007) Comparative analysis of mesenchymal stromal cells from murine bone marrow and amniotic fluid. Cytotherapy 9:729–737PubMedGoogle Scholar
  9. 9.
    Zuk PA, Zhu M, Ashjian P et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295PubMedGoogle Scholar
  10. 10.
    Shih DT, Lee DC, Chen SC et al (2005) Isolation and characterization of neurogenic mesenchymal stem cells in human scalp tissue. Stem Cells 23:1012–1020PubMedGoogle Scholar
  11. 11.
    Sarugaser R, Lickorish D, Baksh D et al (2005) Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23:220–229PubMedGoogle Scholar
  12. 12.
    Mazo M, Gavira JJ, Pelacho B, Prosper F (2011) Adipose-derived stem cells for myocardial infarction. J Cardiovasc Transl Res 4:145–153PubMedGoogle Scholar
  13. 13.
    Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24:150–154PubMedGoogle Scholar
  14. 14.
    Strawford A, Antelo F, Christiansen M, Hellerstein MK (2004) Adipose tissue triglyceride turnover, de novo lipogenesis, and cell proliferation in humans measured with 2H2O. Am J Physiol 286:E577–E588Google Scholar
  15. 15.
    Zuk PA, Zhu M, Mizuno H et al (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211–228PubMedGoogle Scholar
  16. 16.
    Schaffler A, Buchler C (2007) Concise review: adipose tissue-derived stromal cells—basic and clinical implications for novel cell-based therapies. Stem Cells 25:818–827PubMedGoogle Scholar
  17. 17.
    Miyahara Y, Nagaya N, Kataoka M et al (2006) Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 12:459–465PubMedGoogle Scholar
  18. 18.
    Williams KJ, Picou AA, Kish SL et al (2008) Isolation and characterization of porcine adipose tissue-derived adult stem cells. Cells Tissues Organs 188:251–258PubMedGoogle Scholar
  19. 19.
    De Ugarte DA, Alfonso Z, Zuk PA et al (2003) Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol Lett 89:267–270PubMedGoogle Scholar
  20. 20.
    Puissant B, Barreau C, Bourin P et al (2005) Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 129:118–129PubMedGoogle Scholar
  21. 21.
    Rodriguez AM, Pisani D, Dechesne CA et al (2005) Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med 201:1397–1405PubMedGoogle Scholar
  22. 22.
    Jurgens WJ, Oedayrajsingh-Varma MJ, Helder MN et al (2008) Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cell-based therapies. Cell Tissue Res 332:415–426PubMedGoogle Scholar
  23. 23.
    Fraser JK, Schreiber R, Strem B et al (2006) Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nat Clin Pract Cardiovasc Med 3(suppl 1):S33–S37PubMedGoogle Scholar
  24. 24.
    Nakagami H, Morishita R, Maeda K et al (2006) Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. J Atheroscler Thromb 13:77–81PubMedGoogle Scholar
  25. 25.
    Planat-Benard V, Silvestre JS, Cousin B et al (2004) Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109:656–663PubMedGoogle Scholar
  26. 26.
    Djouad F, Plence P, Bony C et al (2003) Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102:3837–3844PubMedGoogle Scholar
  27. 27.
    Nakagami H, Maeda K, Morishita R et al (2005) Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol 25:2542–2547PubMedGoogle Scholar
  28. 28.
    Bensinger W, Singer J, Appelbaum F et al (1993) Autologous transplantation with peripheral blood mononuclear cells collected after administration of recombinant granulocyte stimulating factor. Blood 81:3158–3163PubMedGoogle Scholar
  29. 29.
    Asahara T, Murohara T, Sullivan A et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967PubMedGoogle Scholar
  30. 30.
    Gronthos S, Franklin DM, Leddy HA et al (2001) Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 189:54–63PubMedGoogle Scholar
  31. 31.
    Festy F, Hoareau L, Bes-Houtmann S et al (2005) Surface protein expression between human adipose tissue-derived stromal cells and mature adipocytes. Histochem Cell Biol 124:113–121PubMedGoogle Scholar
  32. 32.
    Rehman J, Traktuev D, Li J et al (2004) Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109:1292–1298PubMedGoogle Scholar
  33. 33.
    Kern S, Eichler H, Stoeve J et al (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294–1301PubMedGoogle Scholar
  34. 34.
    Hombach-Klonisch S, Panigrahi S, Rashedi I et al (2008) Adult stem cells and their ­transdifferentiation potential-perspectives and therapeutic applications. J Mol Med 86(12):1301–1314PubMedGoogle Scholar
  35. 35.
    Sanz-Ruiz R, Fernandez-Santos E, Dominguez-Munoa M et al (2009) Early translation of adipose-derived cell therapy for cardiovascular disease. Cell Transplant 18:245–254PubMedGoogle Scholar
  36. 36.
    Casteilla L, Planat-Benard V, Cousin B et al (2005) Plasticity of adipose tissue: a promising therapeutic avenue in the treatment of cardiovascular and blood diseases? Arch Mal Coeur Vaiss 98:922–926PubMedGoogle Scholar
  37. 37.
    Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M et al (2006) Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy 8:166–177PubMedGoogle Scholar
  38. 38.
    Martínez-González J, Viñals M et al (1997) Mevalonate deprivation impairs IGF-I/insulin signaling in human vascular smooth cells. Atherosclerosis 135:213–223PubMedGoogle Scholar
  39. 39.
    Bai X, Alt E (2010) Myocardial regeneration potential of adipose tissue-derived stem cells. Biochem Biophys Res Commun 401:321–326PubMedGoogle Scholar
  40. 40.
    Sanz-Ruiz R, Santos ME, Munoa MD et al (2008) Adipose tissue-derived stem cells: the friendly side of a classic cardiovascular foe. J Cardiovasc Transl Res 1:55–63PubMedGoogle Scholar
  41. 41.
    Rodriguez AM, Elabd C, Amri E-Z et al (2005) The human adipose tissue is a source of multipotent stem cells. Biochimie 87:125–128PubMedGoogle Scholar
  42. 42.
    Locke M, Feisst V, Dunbar PR (2011) Concise review: human adipose-derived stem cells: separating promise from clinical need. Stem Cells 29:404–411PubMedGoogle Scholar
  43. 43.
    Fuster V, Badimon L, Badimon JJ, Chesebro JH (1992) The pathogenesis of coronary artery disease and the acute coronary syndromes (1). N Engl J Med 326:242–250PubMedGoogle Scholar
  44. 44.
    Fuster V, Badimon L, Badimon JJ, Chesebro JH (1992) The pathogenesis of coronary artery disease and the acute coronary syndromes (2). N Engl J Med 326:310–318PubMedGoogle Scholar
  45. 45.
    Beltrami AP, Urbanek K, Kajstura J et al (2001) Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 344:1750–1757PubMedGoogle Scholar
  46. 46.
    Condorelli G, Borello U, De Angelis L et al (2001) Cardiomyocytes induce endothelial cells to trans-differentiate into cardiac muscle: implications for myocardium regeneration. Proc Natl Acad Sci U S A 98:10733–10738PubMedGoogle Scholar
  47. 47.
    Kudo M, Wang Y, Wani MA et al (2003) Implantation of bone marrow stem cells reduces the infarction and fibrosis in ischemic mouse heart. J Mol Cell Cardiol 35:1113–1119PubMedGoogle Scholar
  48. 48.
    Smart N, Riley PR (2008) The stem cell movement. Circ Res 102:1155–1168PubMedGoogle Scholar
  49. 49.
    Sanchez PL, Villa A, Sanz R et al (2007) Present and future of stem cells for cardiovascular therapy. Ann Med 39:412–427PubMedGoogle Scholar
  50. 50.
    Orlic D, Kajstura J, Chimenti S et al (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410:701–705PubMedGoogle Scholar
  51. 51.
    Murry CE, Soonpaa MH, Reinecke H et al (2004) Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428:664–668PubMedGoogle Scholar
  52. 52.
    Balsam LB, Wagers AJ, Christensen JL et al (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428:668–673PubMedGoogle Scholar
  53. 53.
    Miller-Kasprzak E, Jagodzinski PP (2007) Endothelial progenitor cells as a new agent contributing to vascular repair. Arch Immunol Ther Exp 55:247–259Google Scholar
  54. 54.
    Rubart M, Field LJ (2006) Cardiac regeneration: repopulating the heart. Annu Rev Physiol 68:29–49PubMedGoogle Scholar
  55. 55.
    Narmoneva DA, Vukmirovic R, Davis ME et al (2004) Endothelial cells promote cardiac myocyte survival and spatial reorganization: implications for cardiac regeneration. Circulation 110:962–968PubMedGoogle Scholar
  56. 56.
    Makino S, Fukuda K, Miyoshi S et al (1999) Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 103:697–705PubMedGoogle Scholar
  57. 57.
    Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147PubMedGoogle Scholar
  58. 58.
    Murry CE, Field LJ, Menasche P (2005) Cell-based cardiac repair: reflections at the 10-year point. Circulation 112:3174–3183PubMedGoogle Scholar
  59. 59.
    Menasche P (2007) Skeletal myoblasts as a therapeutic agent. Prog Cardiovasc Dis 50:7–17PubMedGoogle Scholar
  60. 60.
    Shi X, Garry DJ (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev 20:1692–1708PubMedGoogle Scholar
  61. 61.
    Dowell JD, Rubart M, Pasumarthi KBS et al (2003) Myocyte and myogenic stem cell transplantation in the heart. Cardiovasc Res 58:336–350PubMedGoogle Scholar
  62. 62.
    Laflamme MA, Murry CE (2005) Regenerating the heart. Nat Biotechnol 23:845–856PubMedGoogle Scholar
  63. 63.
    Aicher A, Brenner W, Zuhayra M et al (2003) Assessment of the tissue distribution of ­transplanted human endothelial progenitor cells by radioactive labeling. Circulation 107:2134–2139PubMedGoogle Scholar
  64. 64.
    Dimmeler S, Zeiher AM, Schneider MD (2005) Unchain my heart: the scientific foundations of cardiac repair. J Clin Invest 115:572–583PubMedGoogle Scholar
  65. 65.
    Menasche P, Hagege AA, Vilquin JT et al (2003) Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol 41:1078–1083PubMedGoogle Scholar
  66. 66.
    Menasche P, Alfieri O, Janssens S et al (2008) The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 117:1189–1200PubMedGoogle Scholar
  67. 67.
    Barile L, Messina E, Giacomello A, Marban E (2007) Endogenous cardiac stem cells. Prog Cardiovasc Dis 50:31–48PubMedGoogle Scholar
  68. 68.
    Oh H, Bradfute SB, Gallardo TD et al (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100:12313–12318PubMedGoogle Scholar
  69. 69.
    Oettgen P (2006) Cardiac stem cell therapy: need for optimization of efficacy and safety monitoring. Circulation 114:353–358PubMedGoogle Scholar
  70. 70.
    Wang JS, Shum-Tim D, Galipeau J et al (2000) Marrow stromal cells for cellular cardiomyoplasty: feasibility and potential clinical advantages. J Thorac Cardiovasc Surg 120:999–1005PubMedGoogle Scholar
  71. 71.
    Wakitani S, Saito T, Caplan AI (1995) Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 18:1417–1426PubMedGoogle Scholar
  72. 72.
    Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74PubMedGoogle Scholar
  73. 73.
    Nagaya N, Fujii T, Iwase T et al (2004) Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am J Physiol Heart Circ Physiol 287:H2670–H2676PubMedGoogle Scholar
  74. 74.
    Strem BM, Zhu M, Alfonso Z et al (2005) Expression of cardiomyocytic markers on adipose tissue-derived cells in a murine model of acute myocardial injury. Cytotherapy 7:282–291PubMedGoogle Scholar
  75. 75.
    Strem BM, Jordan M, Kim J, Yang J, Anderson CD, Daniels E (2005) Adipose tissue-derived stem cells enhance cardiac function following surgically-induced myocardial infarction. Circulation 112(suppl II):274Google Scholar
  76. 76.
    Mazo M, Planat-Bénard V, Abizanda G et al (2008) Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction. Eur J Heart Fail 10:454–462PubMedGoogle Scholar
  77. 77.
    Cai L, Johnstone BH, Cook TG et al (2009) IFATS collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells 27:230–237PubMedGoogle Scholar
  78. 78.
    Léobon B, Roncalli J, Joffre C et al (2009) Adipose-derived cardiomyogenic cells: in vitro expansion and functional improvement in a mouse model of myocardial infarction. Cardiovasc Res 83:757–767PubMedGoogle Scholar
  79. 79.
    Schenke-Layland K, Strem BM, Jordan MC et al (2009) Adipose tissue-derived cells improve cardiac function following myocardial infarction. J Surg Res 153:217–223PubMedGoogle Scholar
  80. 80.
    van der Bogt KE, Schrepfer S, Yu J et al (2009) Comparison of transplantation of adipose tissue- and bone marrow-derived mesenchymal stem cells in the infarcted heart. Transplantation 87:642–652PubMedGoogle Scholar
  81. 81.
    Wang L, Deng J, Tian W et al (2009) 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 297:H1020–H1031PubMedGoogle Scholar
  82. 82.
    Zhu XY, Zhang XZ, Xu L et al (2009) Transplantation of adipose-derived stem cells overexpressing hHGF into cardiac tissue. Biochem Biophys Res Commun 379:1084–1090PubMedGoogle Scholar
  83. 83.
    Bai X, Yan Y, Song YH et al (2010) Both cultured and freshly isolated adipose tissue-derived stem cells enhance cardiac function after acute myocardial infarction. Eur Heart J 31:489–501PubMedGoogle Scholar
  84. 84.
    Bayes-Genis A, Soler-Botija C, Farré J et al (2010) Human progenitor cells derived from cardiac adipose tissue ameliorate myocardial infarction in rodents. J Mol Cell Cardiol 49:771–780PubMedGoogle Scholar
  85. 85.
    Danoviz ME, Nakamuta JS, Marques FL et al (2010) Rat adipose tissue-derived stem cells transplantation attenuates cardiac dysfunction post infarction and biopolymers enhance cell retention. PLoS One 5:e12077PubMedGoogle Scholar
  86. 86.
    Lin YC, Leu S, Sun CK et al (2010) Early combined treatment with sildenafil and adiposederived mesenchymal stem cells preserves heart function in rat dilated cardiomyopathy. J Transl Med 8:88PubMedGoogle Scholar
  87. 87.
    Okura H, Matsuyama A, Lee CM et al (2010) Cardiomyoblast-like cells differentiated from human adipose tissue-derived mesenchymal stem cells improve left ventricular dysfunction and survival in a rat myocardial infarction model. Tissue Eng Part C Methods 16:417–425PubMedGoogle Scholar
  88. 88.
    Zhang X, Wang H, Ma X et al (2010) Preservation of the cardiac function in infarcted rat hearts by the transplantation of adipose-derived stem cells with injectable fibrin scaffolds. Exp Biol Med (Maywood) 235:1505–1515PubMedGoogle Scholar
  89. 89.
    Bai X, Yan Y, Caleman M et al (2011) Tracking long-term survival of intramyocardially delivered human adipose tissue-derived stem cells using bioluminescence imaging. Mol Imaging Biol 13:633–645PubMedGoogle Scholar
  90. 90.
    Berardi GR, Rebelatto CK, Tavares HF et al (2011) Transplantation of SNAP-treated adipose tissue-derived stem cells improves cardiac function and induces neovascularization after myocardium infarct in rats. Exp Mol Pathol 90:149–156PubMedGoogle Scholar
  91. 91.
    Cai A, Zheng D, Dong Y et al (2011) Efficacy of Atorvastatin combined with adipose-derived mesenchymal stem cell transplantation on cardiac function in rats with acute myocardial infarction. Acta Biochim Biophys Sin (Shanghai) 43:857–866PubMedGoogle Scholar
  92. 92.
    Gaebel R, Furlani D, Sorg H et al (2011) Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. PLoS One 6:e15652PubMedGoogle Scholar
  93. 93.
    Hamdi H, Planat-Benard V, Bel A et al (2011) Epicardial adipose stem cell sheets results in greater post-infarction survival than intramyocardial injections. Cardiovasc Res 91:483–491PubMedGoogle Scholar
  94. 94.
    Ii M, Horii M, Yokoyama A et al (2011) Synergistic effect of adiposederived stem cell therapy and bone marrow progenitor recruitment in ischemic heart. Lab Invest 91:539–552PubMedGoogle Scholar
  95. 95.
    Paul A, Srivastava S, Cheng G et al (2011) Functional assessment of adipose stem cells for xenotransplantation using myocardial. Infarction immunocompetent models: comparison with bone marrow stem cells. Cell Biochem Biophys [Epub ahead of print]PubMedGoogle Scholar
  96. 96.
    van Dijk A, Naaijkens BA, Jurgens WJ et al (2011) 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 7:219–229PubMedGoogle Scholar
  97. 97.
    Bagno LL, Werneck-de-Castro JP, Oliveira PF et al (2012) Adipose-derived stromal cell therapy improves cardiac function after coronary occlusion in rats. Cell Transplant 21 (9):1985–1996PubMedGoogle Scholar
  98. 98.
    Otto Beitnes J, Oie E, Shahdadfar A et al (2012) Intramyocardial injections of human mesenchymal stem cells following acute myocardial infarction modulate scar formation and improve left ventricular function. Cell Transplant 21:1697–1709PubMedGoogle Scholar
  99. 99.
    Fang CH, Jin J, Joe JH et al (2012) In vivo differentiation of human amniotic epithelial cells into cardiomyocyte-like cells and cell transplantation effect on myocardial infarction in rats: comparison with cord blood and adipose tissue-derived mesenchymal stem cells. Cell Transplant 21:1687–1696PubMedGoogle Scholar
  100. 100.
    Hoke NN, Salloum FN, Dakks DA et al (2012) Preconditioning by phosphodiesterase-5 inhibition improves therapeutic efficacy of adipose-derived stem cells following myocardial infarction in mice. Stem Cells 30:326–335PubMedGoogle Scholar
  101. 101.
    Li TS, Cheng K, Malliaras K et al (2012) Direct comparison of different stem cell types and subpopulations reveals superior paracrine potency and myocardial repair efficacy with cardiosphere-­derived cells. J Am Coll Cardiol 59:942–953PubMedGoogle Scholar
  102. 102.
    Liu Z, Wang H, Wang Y et al (2012) The influence of chitosan hydrogel on stem cell engraftment, survival and homing in the ischemic myocardial microenvironment. Biomaterials 33:3093–3106PubMedGoogle Scholar
  103. 103.
    Paul A, Cheng G, Khan A et al (2012) Genipin-cross-linked microencapsulated human adipose stem cells augment transplant retention resulting in attenuation of chronically infarcted rat heart fibrosis and cardiac dysfunction. Cell Transplant 21:2735–2751PubMedGoogle Scholar
  104. 104.
    Shi CZ, Zhang XP, Lv ZW et al (2012) Adipose tissue-derived stem cells embedded with eNOS restore cardiac function in acute myocardial infarction model. Int J Cardiol 154:2–8PubMedGoogle Scholar
  105. 105.
    Zhang DZ, Gai LY, Liu HW et al (2007) Transplantation of autologous adipose-derived stem cells ameliorates cardiac function in rabbits with myocardial infarction. Chin Med J (Engl) 120:300–307Google Scholar
  106. 106.
    Yang JJ, Yang X, Liu ZQ et al (2012) Transplantation of adipose tissue-derived stem cells overexpressing heme oxygenase-1 improves functions and remodeling of infarcted myocardium in rabbits. Tohoku J Exp Med 226:231–241PubMedGoogle Scholar
  107. 107.
    Watanabe C (2004) Intracoronary adipose tissue derived stem cells therapy preserves left ventricular function in a porcine infarct model. Paper presented at Transvascular Cardiovascular Therapeutics Annual Meeting, September 2004, Washington DC, USAPubMedGoogle Scholar
  108. 108.
    Fotuhi P, Song YH, Alt E (2007) Electrophysiological consequence of adipose-derived stem cell transplantation in infarcted porcine myocardium. Europace 9:1218–1221PubMedGoogle Scholar
  109. 109.
    Valina C, Pinkernell K, Song YH et al (2007) Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J 28:2667–2677PubMedGoogle Scholar
  110. 110.
    Alt E, Pinkernell K, Scharlau M et al (2010) Effect of freshly isolated autologous tissue resident stromal cells on cardiac function and perfusion following acute myocardial infarction. Int J Cardiol 144:26–35PubMedGoogle Scholar
  111. 111.
    Rigol M, Solanes N, Farre J et al (2010) Effects of adipose tissue-derived stem cell therapy after myocardial infarction: impact of the route of administration. J Card Fail 16:357–366PubMedGoogle Scholar
  112. 112.
    Mazo M, Hernández S, Gavira JJ et al (2012) Treatment of reperfused ischemia with adiposederived stem cells in a preclinical Swine model of myocardial infarction. Cell Transplant 21:2723–2733PubMedGoogle Scholar
  113. 113.
    Kim YM, Jeon ES, Kim MR et al (2008) Angiotensin II-induced differentiation of adipose tissue-derived mesenchymal stem cells to smooth muscle-like cells. Int J Biochem Cell Biol 40:2482–2491PubMedGoogle Scholar
  114. 114.
    Rodriguez LV, Alfonso Z, Zhang R et al (2006) Clonogenic multipotent stem cells in human adipose tissue differentiate into functional smooth muscle cells. Proc Natl Acad Sci U S A 103:12167–12172PubMedGoogle Scholar
  115. 115.
    Ning H, Liu G, Lin G et al (2009) Fibroblast growth factor 2 promotes endothelial differentiation of adipose tissue-derived stem cells. J Sex Med 6:967–979PubMedGoogle Scholar
  116. 116.
    Jackson KA, Majka SM, Wang H et al (2001) Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395–1402PubMedGoogle Scholar
  117. 117.
    Laflamme MA, Myerson D, Saffitz JE, Murry CE (2002) Evidence for cardiomyocyte repopulation by extracardiac progenitors in transplanted human hearts. Circ Res 90:634–640PubMedGoogle Scholar
  118. 118.
    Gnecchi M, He H, Liang OD et al (2005) Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11:367–368PubMedGoogle Scholar
  119. 119.
    Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182–1186PubMedGoogle Scholar
  120. 120.
    Yanagisawa-Miwa A, Uchida Y, Nakamura F et al (1992) Salvage of infarcted myocardium by angiogenic action of basic fibroblast growth factor. Science 257:1401–1403PubMedGoogle Scholar
  121. 121.
    Takeshita S, Zheng LP, Brogi E et al (1994) Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest 93:662–670PubMedGoogle Scholar
  122. 122.
    Losordo DW, Dimmeler S (2004) Therapeutic angiogenesis and vasculogenesis for ischemic disease. Part I: angiogenic cytokines. Circulation 109:2487–2491PubMedGoogle Scholar
  123. 123.
    Freedman SB, Isner JM (2002) Therapeutic angiogenesis for coronary artery disease. Ann Intern Med 136:54–71PubMedGoogle Scholar
  124. 124.
    Losordo DW, Vale PR, Hendel RC et al (2002) Phase 1/2 placebo-controlled, double-blind, dose-escalating trial of myocardial vascular endothelial growth factor 2 gene transfer by catheter delivery in patients with chronic myocardial ischemia. Circulation 105:2012–2018PubMedGoogle Scholar
  125. 125.
    Henry TD, Annex BH, McKendall GR et al (2003) The VIVA trial: vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation 107:1359–1365PubMedGoogle Scholar
  126. 126.
    Lazarous DF, Shou M, Scheinowitz M et al (1996) Comparative effects of basic fibroblast growth factor and vascular endothelial growth factor on coronary collateral development and the arterial response to injury. Circulation 94:1074–1082PubMedGoogle Scholar
  127. 127.
    Takahashi T, Kalka C, Masuda H et al (1999) Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5:434–438PubMedGoogle Scholar
  128. 128.
    Yamaguchi J, Kusano KF, Masuo O et al (2003) Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107:1322–1328PubMedGoogle Scholar
  129. 129.
    Wang M, Crisostomo PR, Herring C et al (2006) Human progenitor cells from bone marrow or adipose tissue produce VEGF, HGF, and IGF-I in response to TNF by a p38 MAPKdependent mechanism. Am J Physiol Regul Integr Comp Physiol 291:R880–R884PubMedGoogle Scholar
  130. 130.
    Dernbach E, Urbich C, Brandes RP et al (2004) Antioxidative stress-associated genes in ­circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood 104:3591–3597PubMedGoogle Scholar
  131. 131.
    Kocher AA, Schuster MD, Szabolcs MJ et al (2001) Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7:430–436PubMedGoogle Scholar
  132. 132.
    Schuster MD, Kocher AA, Seki T et al (2004) Myocardial neovascularization by bone ­marrow angioblasts results in cardiomyocyte regeneration. Am J Physiol Heart Circ Physiol 287:H525–H532PubMedGoogle Scholar
  133. 133.
    Murohara T (2009) Autologous adipose tissue as a new source of progenitor cells for therapeutic angiogenesis. J Cardiol 53:155–163PubMedGoogle Scholar
  134. 134.
    Sadat S, Gehmert S, Song YH et al (2007) The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem Biophys Res Commun 363:674–679PubMedGoogle Scholar
  135. 135.
    Liles WC, Broxmeyer HE, Rodger E et al (2003) Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood 102:2728–2730PubMedGoogle Scholar
  136. 136.
    Tachibana K, Hirota S, Iizasa H et al (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393:591–594PubMedGoogle Scholar
  137. 137.
    Rasmussen JG, Frobert O, Pilgaard L et al (2011) Prolonged hypoxic culture and trypsinization increase the pro-angiogenic potential of human adipose tissue-derived stem cells. Cytotherapy 13:318–328PubMedGoogle Scholar
  138. 138.
    Suga H, Eto H, Aoi N et al (2010) Adipose tissue remodeling under ischemia: death of ­adipocytes and activation of stem/progenitor cells. Plast Reconstr Surg 126:1911–1923PubMedGoogle Scholar
  139. 139.
    Stubbs SL, Hsiao ST, Peshavariya HM et al (2012) Hypoxic preconditioning enhances survival of human adipose-derived stem cells and conditions endothelial cells in vitro. Stem Cells Dev 21:1887–1896PubMedGoogle Scholar
  140. 140.
    Tateishi-Yuyama E, Matsubara H, Murohara T et al (2002) Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 360:427–435PubMedGoogle Scholar
  141. 141.
    Jay SM, Shepherd BR, Bertram JP et al (2008) Engineering of multifunctional gels integrating highly efficient growth factor delivery with endothelial cell transplantation. FASEB J 22:2949–2956PubMedGoogle Scholar
  142. 142.
    Deuse T, Peter C, Fedak PW et al (2009) Hepatocyte growth factor or vascular endothelial growth factor gene transfer maximizes mesenchymal stem cell-based myocardial salvage after acute myocardial infarction. Circulation 120:S247–S254PubMedGoogle Scholar
  143. 143.
    Fitzpatrick JR III, Frederick JR, McCormick RC et al (2010) Tissue-engineered proangiogenic fibroblast scaffold improves myocardial perfusion and function and limits ventricular remodeling after infarction. J Thorac Cardiovasc Surg 140:667–676PubMedGoogle Scholar
  144. 144.
    Bhang SH, Cho SW, La WG et al (2011) Angiogenesis in ischemic tissue produced by spheroid grafting of human adipose-derived stromal cells. Biomaterials 32:2734–2747PubMedGoogle Scholar
  145. 145.
    Amos PJ, Shang H, Bailey AM et al (2008) IFATS collection: the role of human adiposederived stromal cells in inflammatory microvascular remodeling and evidence of a perivascular phenotype. Stem Cells 26:2682–2690PubMedGoogle Scholar
  146. 146.
    Zannettino AC, Paton S, Arthur A et al (2008) Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 214:413–421PubMedGoogle Scholar
  147. 147.
    Efimenko A, Starostina E, Kalinina N, Stolzing A (2011) Angiogenic properties of aged adipose derived mesenchymal stem cells after hypoxic conditioning. J Transl Med 9:10PubMedGoogle Scholar
  148. 148.
    Onate B, Vilahur G, Ferrer-Lorente R et al (2012) The subcutaneous adipose tissue reservoir of functionally active stem cells is reduced in obese patients. FASEB J 26(10):4327–4336PubMedGoogle Scholar
  149. 149.
    Hwangbo S, Kim J, Her S et al (2010) Therapeutic potential of human adipose stem cells in a rat myocardial infarction model. Yonsei Med J. 51:69–76PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Lina Badimon
    • 1
    • 2
    • 3
    Email author
  • Blanca Oñate
    • 1
    • 2
  • Gemma Vilahur
    • 1
    • 2
  1. 1.Cardiovascular Research Center, CSIC-ICCC, Hospital de la Santa Creu i Sant Pau, IIB-Sant PauBarcelonaSpain
  2. 2.CIBEROBN-Pathophysiology of Obesity and NutritionBarcelonaSpain
  3. 3.UABBarcelonaSpain

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