Adipose tissue: A new source for cardiovascular repair

Journal of Cardiovascular Medicine

Volumn 11, Issue 2, 2010, Pages 71-80

  Madonna, Rosalinda ^a   De Caterina, Raffaele ^a  

^a UNIVERSITY OF CHIETI   (Italy)

Author keywords

Adipose tissue; Adipose tissue derived stem cells; Angiogenesis; Bone marrow; Cell therapy; Myocardial regeneration; Myocardial repair; Myogenic differentiation; Stem cells; Stromal cells; Tissue engineering

Indexed keywords

VASCULOTROPIN;

ADIPOCYTE; ADIPOSE TISSUE; ADIPOSE TISSUE DERIVED STEM CELL; ADIPOSE TISSUE DERIVED STROMAL CELL; CAPILLARY DENSITY; CARTILAGE CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HUMAN; IN VIVO STUDY; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; MUSCLE CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; STEM CELL; STEM CELL TRANSPLANTATION;

ADIPOSE TISSUE; ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; CLINICAL TRIALS AS TOPIC; HEART DISEASES; HUMANS; MULTIPOTENT STEM CELLS; MYOCYTES, CARDIAC; STROMAL CELLS;

EID: 75149151470     PISSN: 15582027     EISSN: None     Source Type: Journal    
DOI: 10.2459/JCM.0b013e328330e9be     Document Type: Review

References (84)

1. Effect of metoprolol CR/XL in chronic heart failure: metoprolol CR/XL Randomised Intervention Trial in Congestive Heart Failure (MERIT-HF). Lancet 1999; 353:2001-2007.
2. Forrester JS, Price MJ, Makkar RR. Stem cell repair of infarcted myocardium: an overview for clinicians. Circulation 2003; 108:1139-1145.
3. Zimmermann WH, Didie M, Doker S, Melnychenko I, Naito H, Rogge C, et al. Heart muscle engineering: an update on cardiac muscle replacement therapy. Cardiovasc Res 2006; 71:419-429.
4. Sharma R, Raghubir R. Stem cell therapy: a hope for dying hearts. Stem Cells Dev 2007; 16:517-536.
5. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282:1145-1147.
6. Moore KE, Mills JF, Thornton MM. Alternative sources of adult stem cells: a possible solution to the embryonic stem cell debate. Gend Med 2006; 3:161-168.
7. 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; 7:211-228.
8. Lazar MA. Developmental biology. How now, brown fat? Science 2008; 321:1048-1049.
9. Psaltis PJ, Zannettino AC, Worthley SG, Gronthos S. Concise review: mesenchymal stromal cells: potential for cardiovascular repair. Stem Cells 2008; 26:2201-2210.
10. Rickard DJ, Kassem M, Hefferan TE, Sarkar G, Spelsberg TC, Riggs BL. Isolation and characterization of osteoblast precursor cells from human bone marrow. J Bone Miner Res 1996; 11:312-324.
11. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284:143-147.
12. 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; 290:763-769.
13. Safford KM, Hicok KC, Safford SD, Halvorsen YD, Wilkison WO, Gimble JM, Rice HE. Neurogenic differentiation of murine and human adiposederived stromal cells. Biochem Biophys Res Commun 2002; 294:371-379.
14. Gimble J, Guilak F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 2003; 5:362-369.
15. Gimble JM, Guilak F. Differentiation potential of adipose derived adult stem (ADAS) cells. Curr Top Dev Biol 2003; 58:137-160.
16. Planat-Benard V, Menard C, Andre M, Puceat M, Perez A, Garcia-Verdugo JM, et al. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res 2004; 94:223-229.
17. Bacou F, el Andalousi RB, Daussin PA, Micallef JP, Levin JM, Chammas M, et al. Transplantation of adipose tissue-derived stromal cells increases mass and functional capacity of damaged skeletal muscle. Cell Transplant 2004; 13:103-111.
18. Ashjian PH, Elbarbary AS, Edmonds B, DeUgarte D, Zhu M, Zuk PA, et al. In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plast Reconstr Surg 2003; 111:1922-1931.
19. Rangappa S, Fen C, Lee EH, Bongso A, Sim EK. Transformation of adult mesenchymal stem cells isolated from the fatty tissue into cardiomyocytes. Ann Thorac Surg 2003; 75:775-779.
20. Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006; 12:459-465.
21. Di Rocco G, Iachininoto MG, Tritarelli A, Straino S, Zacheo A, Germani A, et al. Myogenic potential of adipose-tissue-derived cells. J Cell Sci 2006; 119:2945-2952.
22. Madonna R, Willerson JT, Geng YJ. Myocardin a enhances telomerase activities in adipose tissue mesenchymal cells and embryonic stem cells undergoing cardiovascular myogenic differentiation. Stem Cells 2008; 26:202-211.
23. van Dijk A, Niessen HW, Zandieh Doulabi B, Visser FC, van Milligen FJ. Differentiation of human adipose-derived stem cells towards cardiomyocytes is facilitated by laminin. Cell Tissue Res 2008; 334:457-467.
24. Kim MR, Jeon ES, Kim YM, Lee JS, Kim JH. Thromboxane A2 induces differentiation of human mesenchymal stem cells to smooth muscle-like cells. Stem Cells 2008.
25. Aguiari P, Leo S, Zavan B, Vindigni V, Rimessi A, Bianchi K, et al. High glucose induces adipogenic differentiation of muscle-derived stem cells. Proc Natl Acad Sci USA 2008; 105:1226-1231.
26. Jeon ES, Park WS, Lee MJ, Kim YM, Han J, Kim JH. A Rho kinase/myocardin-related transcription factor-A-dependent mechanism underlies the sphingosylphosphorylcholine-induced differentiation of mesenchymal stem cells into contractile smooth muscle cells. Circ Res 2008; 103:635-642.
27. Schenke-Layland K, Strem B, Jordan M, Deemedio M, Hedrick M, Roos K, et al. Adipose tissue derived cells improve cardiac function following myocardial infarction. J Surg Res 2008; 153:217-233.
28. Miranville A, Heeschen C, Sengenes C, Curat CA, Busse R, Bouloumie A. Improvement of postnatal neovascularization by human adipose tissuederived stem cells. Circulation 2004; 110:349-355.
29. Estes BT, Wu AW, Guilak F. Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis Rheum 2006; 54:1222-1232. (Pubitemid 43672934)
30. Hicok KC, Du Laney TV, Zhou YS, Halvorsen YD, Hitt DC, Cooper LF, Gimble JM. Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Eng 2004; 10:371-380.
31. Halvorsen YD, Franklin D, Bond AL, Hitt DC, Auchter C, Boskey AL, et al. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 2001; 7:729-741.
32. Safford KM, Safford SD, Gimble JM, Shetty AK, Rice HE. Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp Neurol 2004; 187:319-328.
33. Planat-Benard V, Silvestre JS, Cousin B, Andre M, Nibbelink M, Tamarat R, et al. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 2004; 109:656-663.
34. Madonna R, De Caterina R. In vitro neovasculogenic potential of resident adipose tissue precursors. Am J Physiol Cell Physiol 2008; 295:C1271-1280.
35. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004; 109:1292-1298.
36. Song YH, Gehmert S, Sadat S, Pinkernell K, Bai X, Matthias N, Alt E. VEGF is critical for spontaneous differentiation of stem cells into cardiomyocytes. Biochem Biophys Res Commun 2007; 354:999-1003.
37. 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 210-1191 (Pubitemid 34056677)
38. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007; 100:1249-1260.
39. Fraser JK, Zhu M, Wulur I, Alfonso Z. Adipose-derived stem cells. Methods Mol Biol 2008; 449:59-67.
40. Suzdal'tseva YG, Burunova VV, Vakhrushev IV, Yarygin VN, Yarygin KN. Capability of human mesenchymal cells isolated from different sources to differentiation into tissues of mesodermal origin. Bull Exp Biol Med 2007; 143:114-121.
41. Billon N, Iannarelli P, Monteiro MC, Glavieux-Pardanaud C, Richardson WD, Kessaris N, et al. The generation of adipocytes by the neural crest. Development 2007; 134:2283-2292.
42. Billon N, Monteiro MC, Dani C. Developmental origin of adipocytes: new insights into a pending question. Biol Cell 2008; 100:563-575.
43. 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.
44. Kondo K, Shintani S, Shibata R, Murakami H, Murakami R, Imaizumi M, et al. Implantation of adipose-derived regenerative cells enhances ischemiainduced angiogenesis. Arterioscler Thromb Vasc Biol 2008; 29:61-66.
45. Jabbarzadeh E, Starnes T, Khan YM, Jiang T, Wirtel AJ, Deng M, et al. Induction of angiogenesis in tissue-engineered scaffolds designed for bone repair: a combined gene therapy-cell transplantation approach. Proc Natl Acad Sci USA 2008; 105:11099-11104.
46. Valina C, Pinkernell K, Song YH, Bai X, Sadat S, Campeau RJ, 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; 28:2667-2677.
47. Cai L, Johnstone BH, Cook TG, Tan J, Fishbein MC, Chen PS, March KL. IFATS Series: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells 2008; 27:230-237.
48. Mazo M, Planat-Benard V, Abizanda G, Pelacho B, Leobon B, Gavira JJ, 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; 10:454-462.
49. Cousin B, Andre M, Arnaud E, Penicaud L, Casteilla L. Reconstitution of lethally irradiated mice by cells isolated from adipose tissue. Biochem Biophys Res Commun 2003; 301:1016-1022.
50. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997; 90:5002-5012.
51. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000; 95:952-958.
52. Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M, et al. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 2000; 95:3106-3112.
53. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 2001; 7:1028-1034.
54. Scharenberg CW, Harkey MA, Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 2002; 99:507-512.
55. Martinez-Estrada OM, Munoz-Santos Y, Julve J, Reina M, Vilaro S. Human adipose tissue as a source of Flk-1+ cells: new method of differentiation and expansion. Cardiovasc Res 2005; 65:328-333.
56. De Ugarte DA, Morizono K, Elbarbary A, Alfonso Z, Zuk PA, Zhu M, et al. Comparison of multilineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003; 174:101-109. (Pubitemid 36819010)
57. Barry F, Boynton R, Murphy M, Haynesworth S, Zaia J. The SH-3 and SH-4 antibodies recognize distinct epitopes on CD73 from human mesenchymal stem cells. Biochem Biophys Res Commun 2001; 289:519-524.
58. Simmons PJ, Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 1991; 78:55-62.
59. Gronthos S, Graves SE, Ohta S, Simmons PJ. The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood 1994; 84:4164-4173.
60. Papayannopoulou T, Priestley GV, Nakamoto B, Zafiropoulos V, Scott LM. Molecular pathways in bone marrow homing: dominant role of alpha(4)beta(1) over beta(2)-integrins and selectins. Blood 2001; 98:2403-2411.
61. Sudhoff T, Sohngen D. Circulating endothelial adhesion molecules (sE-selectin, sVCAM-1 and sICAM-1) during rHuG-CSF-stimulated stem cell mobilization. J Hematother Stem Cell Res 2002; 11:147-151.
62. Kronenwett R, Martin S, Haas R. The role of cytokines and adhesion molecules for mobilization of peripheral blood stem cells. Stem Cells 2000; 18:320-330.
63. Huang JI, Beanes SR, Zhu M, Lorenz HP, Hedrick MH, Benhaim P. Rat extramedullary adipose tissue as a source of osteochondrogenic progenitor cells. Plast Reconstr Surg 2002; 109:1033-1041; discussion 1042-11033
64. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001; 410:701-705.
65. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005; 129:118-129.
66. McIntosh K, Zvonic S, Garrett S, Mitchell JB, Floyd ZE, Hammill L, et al. The immunogenicity of human adipose-derived cells: temporal changes in vitro. Stem Cells 2006; 24:1246-1253.
67. Morizono K, De Ugarte DA, Zhu M, Zuk P, Elbarbary A, Ashjian P, et al. Multilineage cells from adipose tissue as gene delivery vehicles. Hum Gene Ther 2003; 14:59-66.
68. Rao MS, Mattson MP. Stem cells and aging: expanding the possibilities. Mech Ageing Dev 2001; 122:713-734.
69. Fehrer C, Lepperdinger G. Mesenchymal stem cell aging. Exp Gerontol 2005; 40:926-930.
70. Madonna R, Cellini C, Renna F, Cotellese R, Picardi N, De Caterina R. Agedependent impairment of number and angiogenic potential of adipose tissue-derived progenitor cells. Eur Heart J 2008; 29:4301.
71. Zhu M, Kohan E, Bradley J, Hedrick M, Benhaim P, Zuk P. The effect of age on osteogenic, adipogenic and proliferative potential of female adiposederived stem cells. J Tissue Eng Regen Med 2009 [Epub ahead of print].
72. Mendez-Ferrer S, Ellison GM, Torella D, Nadal-Ginard B. Resident progenitors and bone marrow stem cells in myocardial renewal and repair. Nat Clin Pract Cardiovasc Med 2006; 3 (Suppl 1):S83-S89.
73. Chien KR. Lost and found: cardiac stem cell therapy revisited. J Clin Invest 2006; 116:1838-1840.
74. Cleland JG, Freemantle N, Coletta AP, Clark AL. Clinical trials update from the American Heart Association: REPAIR-AMI, ASTAMI, JELIS, MEGA, REVIVE-II, SURVIVE, and PROACTIVE. Eur J Heart Fail 2006; 8:105-110.
75. Bartunek J, Vanderheyden M, Wijns W, Timmermans F, Vandekerkhove B, Villa A, et al. Bone-marrow-derived cells for cardiac stem cell therapy: safe or still under scrutiny? Nat Clin Pract Cardiovasc Med 2007; 4 (Suppl 1): S100-S105. (Pubitemid 46151912)
76. Nakagami H, Maeda K, Morishita R, Iguchi S, Nishikawa T, Takami Y, et al. Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol 2005; 25:2542-2547.
77. Moon MH, Kim SY, Kim YJ, Kim SJ, Lee JB, Bae YC, et al. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem 2006; 17:279-290.
78. Cao Y, Sun Z, Laio L, Meng Y, Han Q, Zhao RC. Human adipose tissuederived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun 2005; 332:370-379.
79. Sumi M, Sata M, Toya N, Yanaga K, Ohki T, Nagai R. Transplantation of adipose stromal cells, but not mature adipocytes, augments ischemiainduced angiogenesis. Life Sci 2006.
80. Yamada Y, Wang X, Yokoyama S, Fukuda N, Takakura N. Cardiac progenitor cells in brown adipose tissue repaired damaged myocardium. Biochem Biophys Res Commun 2006; 342:662-670.
81. Li B, Zeng Q, Wang H, Shao S, Mao X, Zhang F, et al. Adipose tissue stromal cells transplantation in rats of acute myocardial infarction. Coron Artery Dis 2007; 18:221-227.
82. Zhang D-Z, Gai L-Y, Liu H-W, Jin Q-H, Huang J-H, Zhu X-Y. Transplantation of autologous adipose-derived stem cells ameliorates cardiac function in rabbits with myocardial infarction. Chin Med J 2007; 120:300-307.
83. Bartunek J, Dimmeler S, Drexler H, Fernasndez-Avile F, Galinanes M, Janssens S, et al. The consensus of the task force of the European Society of Cardiology concerning the clinical investigation of the use of autologous adult stem cells for repair of the heart. Eur Heart J 2006; 27:1338-1340.
84. Pompilio G, Ambrosio G, Briguori C, Canepa M, Marra S, Capogrossi MC, Cardiologia GdSdTCCdFId. Clinical studies of cardiac cell therapy in Italy. G Ital Cardiol 2007; 8:586-591.