Pluripotent stem cell-based heart regeneration: From the developmental and immunological perspectives

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 96, Issue 1, 2012, Pages 98-108

  Lui, Kathy O ^a,b   Bu, Lei ^a,b   Li, Ronald A ^b,c   Chan, Camie W ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

ESC; Heart development; Immunogenicity; IPSC; Regenerative medicine; Stem cells; Transplantation

Indexed keywords

ANGIOGENESIS; CARDIOVASCULAR DISEASE; CELL GROWTH; CELL REGENERATION; CELL SURVIVAL; CELL THERAPY; CELL TRANSPLANTATION; EMBRYONIC STEM CELL; ENGRAFTMENT; HEART DEVELOPMENT; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW;

HEART; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; PARACRINE COMMUNICATION; PERICARDIUM; REGENERATION; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING;

MAMMALIA;

EID: 84859149207     PISSN: 1542975X     EISSN: 15429768     Source Type: Journal    
DOI: 10.1002/bdrc.21004     Document Type: Review

References (95)

1. Abu-Issa R, Kirby ML. 2007. Heart field: from mesoderm to heart tube. Annu Rev Cell Dev Biol 23: 45-68.
2. Boheler KR, Czyz J, Tweedie D, et al. 2002. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res 91: 189-201.
3. Bruneau BG, Nemer G, Schmitt JP, et al. 2001. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106: 709-721.
4. Blin G, Nury D, Stefanovic S et al. 2010. A purified population of multipotent cardiovascular progenitors derived from primate pluripotent stem cells engrafts in postmyocardial infarcted nonhuman primates. J Clin Invest. 120: 1125-1139.
5. Bu L, Jiang X, Martin-Puig S, et al. 2009. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460: 113-117.
6. Buckingham M, Meilhac S, Zaffran S. 2005. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet 6: 826-835.
7. Cai CL, Liang X, Shi Y, et al. 2003. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5: 877-889.
8. Deuse T, Seifert M, Phillips N, et al. 2011. Human leukocyte antigen I knockdown human embryonic stem cells induce host ignorance and achieve prolonged xenogeneic survival. Circulation 124: S3-S9.
9. Ding Q, Yeung M, Camirand G, Zeng Q, et al. 2011. Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J Clin Invest 121: 3645-3656.
10. Garg V, Kathiriya IS, Barnes R, et al. 2003. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424: 443-447.
11. Gepstein L, Ding C, Rahmutula D, et al. 2010. In vivo assessment of the electrophysiological integration and arrhythmogenic risk of myocardial cell transplantation strategies. Stem Cells 28: 2151-2161.
12. Giacca M, Baker AH. 2011. Heartening results: the CUPID gene therapy trial for heart failure. Mol Ther 19: 1181-1182.
13. Gore A, Li Z, Fung HL, et al. 2011. Somatic coding mutations in human induced pluripotent stem cells. Nature 471: 63-67.
14. Grinnemo KH, Genead R, Kumagai-Braesch M, et al. 2008. Costimulation blockade induces tolerance to HESC transplanted to the testis and induces regulatory T-cells to HESC transplanted into the heart. Stem Cells 26: 1850-1857.
15. Heidt S, Segundo DS, Chadha R, Wood KJ. 2010. The impact of Th17 cells on transplant rejection and the induction of tolerance. Curr Opin Organ Transplant 15: 456-461.
16. Hochedlinger K, Plath K. 2009. Epigenetic reprogramming and induced pluripotency. Development 136: 509-523.
17. Hoffman JI, Kaplan S. 2002. The incidence of congenital heart disease. JAm Coll Cardiol 39: 1890-1900.
18. Hoffman JI. 1995. Incidence of congenital heart disease. I: Postnatal incidence. Pediatr Cardiol 16: 103-113.
19. Hu K, Yu J, Suknuntha K, et al. 2011. Efficient generation of transgene-free induced pluripotent stem cells from normal and neoplastic bone marrow and cord blood mononuclear cells. Blood 117: e109-e119.
20. Huang M, Nguyen P, Jia F, et al. 2011. Double knockdown of prolyl hydroxylase and factor-inhibiting hypoxia-inducible factor with nonviral minicircle gene therapy enhances stem cell mobilization and angiogenesis after myocardial infarction. Circulation 124: S46-S54.
21. Huangfu D, Osafune K, Maehr R, et al. 2008. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 26: 1269-1275.
22. Ichida JK, Blanchard J, Lam K, Son EY, et al. 2009. A small-molecule inhibitor of TGF-Beta signaling replaces sox2 in reprogramming by inducing nanog. Cell Stem Cell 5: 491-503.
23. Ieda M, Fu JD, Delgado-Olguin P, et al. 2010. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142: 375-386.
24. Itoh M, Kiuru M, Cairo MS, Christiano AM. 2011. Generation of keratinocytes from normal and recessive dystrophic epidermolysis bullosa-induced pluripotent stem cells. Proc Natl Acad Sci USA 108: 8797-8802.
25. James D, Nam HS, Seandel M, et al. 2010. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFbeta inhibition is Id1 dependent. Nat Biotechnol 28: 161-166.
26. Kalogeropoulos AP, Georgiopoulou VV, Butler J. 2012. From risk factors to structural heart disease: the role of inflammation. Heart Fail Clin 8: 113-123.
27. Kim D, Kim CH, Moon JI, et al. 2009a. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4: 472-476.
28. Kim JB, Greber B, Arauzo-Bravo MJ, et al. 2009b. Direct reprogramming of human neural stem cells by OCT4. Nature 461: 649-643.
29. Kim JB, Zaehres H, Wu G, et al. 2008. Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454: 646-650.
30. Kim J, Efe JA, Zhu S et al. 2011. Direct reprogramming of mouse fibroblasts to neural progenitors. Proc Natl Acad Sci U S A. 108: 7838-7843.
31. Kong CW, Akar FG, Li RA. 2010. Translational potential of human embryonic and induced pluripotent stem cells for myocardial repair: insights from experimental models. Thromb Haemostat 104: 30-38.
32. Kormann MS, Hasenpusch G, Aneja MK, et al. 2011. Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nat Biotechnol 29: 154-157.
33. Kurpinski K, Lam H, Chu J, et al. 2010. Transforming growth factor-beta and notch signaling mediate stem cell differentiation into smooth muscle cells. Stem Cells 28: 734-742.
34. Laflamme MA, Chen KY, Naumova AV, et al. 2007. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25: 1015-1024.
35. Laugwitz KL, Moretti A, Caron L, et al. 2008. Islet1 cardiovascular progenitors: a single source for heart lineages? Development 135: 193-205.
36. Laugwitz KL, Moretti A, Lam J, et al. 2005. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433: 647-653.
37. Li F, He Z, Shen J, et al. 2010. Apoptotic caspases regulate induction of iPSCs from human fibroblasts. Cell Stem Cell 7: 508-520.
38. Li W, Zhou H, Abujarour R, et al. 2009. Generation of human-induced pluripotent stem cells in the absence of exogenous Sox2. Stem Cells 27: 2992-3000.
39. Lin Q, Schwarz J, Bucana C, Olson EN. 1997. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276: 1404-1407.
40. Lin SL, Chang DC, Lin CH, et al. 2011. Regulation of somatic cell reprogramming through inducible mir-302 expression. Nucleic Acids Res 39: 1054-1065.
41. Lin T, Ambasudhan R, Yuan X, et al. 2009. A chemical platform for improved induction of human iPSCs. Nat Methods 6: 805-808.
42. Liu J, Fu JD, Siu CW, Li RA. 2007. Functional sarcoplasmic reticulum for calcium handling of human embryonic stem cell-derived cardiomyocytes: insights for driven maturation. Stem Cells 25: 3038-3044.
43. Loffredo FS, Steinhauser ML, Gannon J, Lee RT. 2011. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell 8: 389-398.
44. Lui KO, Boyd AS, Cobbold SP, et al. 2010. A role for regulatory T cells in acceptance of ESC-derived tissues transplanted across an major histocompatibility complex barrier. Stem Cells 28: 1905-1914.
45. Lui KO, Waldmann H, Fairchild PJ. 2009. Embryonic stem cells: overcoming the immunological barriers to cell replacement therapy. Curr Stem Cell Res Ther 4: 70-80.
46. Ma F, Ebihara Y, Umeda K, et al. 2008. Generation of functional erythrocytes from human embryonic stem cell-derived definitive hematopoiesis. Proc Natl Acad Sci USA 105: 13087-13092.
47. Marro S, Pang ZP, Yang N et al. 2011. Direct lineage conversion of terminally differentiated hepatocytes to functional neurons. Cell Stem Cell. 9: 374-382.
48. Manner J. 1999. Does the subepicardial mesenchyme contribute myocardioblasts to the myocardium of the chick embryo heart? A quail-chick chimera study tracing the fate of the epicardial primordium. Anat Rec 255: 212-226.
49. Marson A, Foreman R, Chevalier B, et al. 2008. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 3: 132-135.
50. 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: 1189-1200.
51. Milgrom-Hoffman M, Harrelson Z, Ferrara N, et al. 2011. The heart endocardium is derived from vascular endothelial progenitors. Development 138: 4777-4787.
52. Moretti A, Caron L, Nakano A, et al. 2006. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127: 1151-1165.
53. Martins, pang ZI, Yang N, et al. 2011. Direct lineage conversion of terminally differntiated hepatocytes to functional neunivs. Cell Stream Cell 9: 374-382.
54. Murry CE, Keller G. 2008. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132: 661-680.
55. Nakagawa M, Koyanagi M, Tanabe K, et al. 2008. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26: 101-106.
56. Olivey HE, Svensson EC. 2010. Epicardial-myocardial signaling directing coronary vasculogenesis. Circ Res 106: 818-832.
57. Pearl JI, Lee AS, Leveson-Gower DB, et al. 2011. Short-term immunosuppression promotes engraftment of embryonic and induced pluripotent stem cells. Cell Stem Cell 8: 309-317.
58. Poon E, Kong CW, Li RA. 2011. Human pluripotent stem cell-based approaches for myocardial repair: from the electrophysiological perspective. Mol Pharm 8: 1495-1504.
59. Porrello ER, Mahmoud AI, Simpson E, et al. 2011. Transient regenerative potential of the neonatal mouse heart. Science 331: 1078-1080.
60. Qyang Y, Martin-Puig S, Chiravuri M, et al. 2007. The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell 1: 165-179.
61. Raya A, Rodriguez-Piza I, Guenechea G, et al. 2009. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 460: 53-59.
62. Riley P, Anson-Cartwright L, Cross JC. 1998. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat Genet 18: 271-275.
63. Robertson NJ, Brook FA, Gardner RL, et al. 2007. Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance. Proc Natl Acad Sci USA 104: 20920-20925.
64. Sachinidis A, Fleischmann BK, Kolossov E, et al. 2003. Cardiac specific differentiation of mouse embryonic stem cells. Cardiovasc Res 58: 278-291.
65. Schachinger V, Erbs S, Elsasser A, et al. 2006. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 355: 1210-1221.
66. Schott JJ, Benson DW, Basson CT, et al. 1998. Congenital heart disease caused by mutations in the transcription factor NKX2-5. Science 281: 108-111.
67. Segers VF, Lee RT. 2008. Stem-cell therapy for cardiac disease. Nature 451: 937-942.
68. Segers VF, Tokunou T, Higgins LJ, et al. 2007. Local delivery of protease-resistant stromal cell derived factor-1 for stem cell recruitment after myocardial infarction. Circulation 116: 1683-1692.
69. Sharma R, Davidoff MN. 2002. Oxidative stress and endothelial dysfunction in heart failure. Congest Heart Fail 8: 165-172.
70. Shi Y, Do JT, Desponts C, et al. 2008. A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell 2: 525-528.
71. Smart N, Bollini S, Dube KN, et al. 2011. De novo cardiomyocytes from within the activated adult heart after injury. Nature 474: 640-644.
72. Smart N, Risebro CA, Melville AA, et al. 2007. Thymosin beta-4 is essential for coronary vessel development and promotes neovascularization via adult epicardium. Ann N Y Acad Sci 1112: 171-188.
73. Srivastava D, Thomas T, Lin Q, et al. 1997. Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nat Genet 16: 154-160.
74. Stadtfeld M, Apostolou E, Akutsu H, et al. 2010. Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 465: 175-181.
75. Stadtfeld M, Brennand K, Hochedlinger K. 2008. Reprogramming of pancreatic beta cells into induced pluripotent stem cells. Curr Biol 18: 890-894.
76. Strauss S. 2010. Geron trial resumes, but standards for stem cell trials remain elusive. Nat Biotechnol 28: 989-990.
77. Sun Y, Liang X, Najafi N, et al. 2007. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev Biol 304: 286-296.
78. Tomescot A, Leschik J, Bellamy V, et al. 2007. Differentiation in vivo of cardiac committed human embryonic stem cells in postmyocardial infarcted rats. Stem Cells 25: 2200-2205.
79. Tse HF, Xue T, Lau CP, et al. 2006. Bioartificial sinus node constructed via in vivo gene transfer of an engineered pacemaker HCN Channel reduces the dependence on electronic pacemaker in a sick-sinus syndrome model. Circulation 114: 1000-1011.
80. van Laake LW, van Donselaar EG, Monshouwer-Kloots J, et al. 2010. Extracellular matrix formation after transplantation of human embryonic stem cell-derived cardiomyocytes. Cell Mol Life Sci 67: 277-290.
81. van Ramshorst J, Bax JJ, Beeres SL, et al. 2009. Intramyocardial bone marrow cell injection for chronic myocardial ischemia: a randomized controlled trial. JAMA 301: 1997-2004.
82. Verbinnen B, Billiau AD, Vermeiren J, et al. 2008. Contribution of regulatory T cells and effector T cell deletion in tolerance induction by costimulation blockade. J Immunol 181: 1034-1042.
83. Vunjak-Novakovic G, Lui KO, Tandon N, Chien KR. 2011. Bioengineering heart muscle: a paradigm for regenerative medicine. Annu Rev Biomed Eng 13: 245-267.
84. Waldmann H. 2010. Tolerance: an overview and perspectives. Nat Rev Nephrol 6: 569-576.
85. Warren L, Manos PD, Ahfeldt T, et al. 2010. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7: 618-630.
86. Wekerle T, Kurtz J, Bigenzahn S, et al. 2002. Mechanisms of transplant tolerance induction using costimulatory blockade. Curr Opin Immunol 14: 592-600.
87. Wollert KC, Drexler H. 2010. Cell therapy for the treatment of coronary heart disease: a critical appraisal. Nat Rev Cardiol 7: 204-215.
88. Wu SM, Hochedlinger K. 2011. Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat Cell Biol 13: 497-505.
89. Yamanaka S. 2009. A fresh look at iPS cells. Cell 137: 13-17.
90. Yoder MC. 2010. Is endothelium the origin of endothelial progenitor cells? Arterioscler Thromb Vasc Biol 30: 1094-1103.
91. Yu J, Hu K, Smuga-Otto K, et al. 2009. Human induced pluripotent stem cells free of vector and transgene sequences. Science 324: 797-801.
92. Zhao T, Zhang ZN, Rong Z, Xu Y. 2011. Immunogenicity of induced pluripotent stem cells. Nature 474: 212-215.
93. Zhou B, Honor LB, He H, et al. 2011. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J Clin Invest 121: 1894-1904.
94. Zhou B, Ma Q, Rajagopal S, et al. 2008. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454: 109-113.
95. Zhou H, Wu S, Joo JY, et al. 2009. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4:381-384.