TGFβ-dependent epithelial-to-mesenchymal transition is required to generate cardiospheres from human adult heart biopsies

Stem Cells and Development

Volumn 21, Issue 17, 2012, Pages 3081-3090

  Forte, Elvira ^a   Miraldi, Fabio ^b   Chimenti, Isotta ^b   Angelini, Francesco ^b   Zeuner, Ann ^c   Giacomello, Alessandro ^a   Mercola, Mark ^d   Messina, Elisa ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN INHIBITOR; SB 431452; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; CARDIOSPHERE; CELL DIFFERENTIATION; CELL GROWTH; CELL STRUCTURE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EXPLANT; HEART MUSCLE BIOPSY; HEART MUSCLE INJURY; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; REGENERATIVE ABILITY; STEM CELL; STEM CELL NICHE;

ADULT; BENZAMIDES; BIOLOGICAL MARKERS; BIOPSY; CELL DIFFERENTIATION; CELLS, CULTURED; DIOXOLES; EPITHELIAL-MESENCHYMAL TRANSITION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MYOCARDIAL ISCHEMIA; MYOCARDIUM; MYOCYTES, CARDIAC; RECEPTOR, NOTCH1; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; REGENERATION; STEM CELLS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84869061537     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0277     Document Type: Article

References (59)

1. Dobaczewski M, C Gonzalez-Quesada and NG Frangogiannis. (2010). The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol 48:504-511.
2. Pfeffer MA and E Braunwald. (1990). Ventricular remodeling after myocardial infarction. Experimental observations and clinical implications. Circulation 81:1161-1172. (Pubitemid 20119612)
3. Gaetani R, L Barile, E Forte, I Chimenti, V Ionta, A Di Consiglio, F Miraldi, G Frati, E Messina and A Giacomello. (2009). New perspectives to repair a broken heart. Cardiovasc Hematol Agents Med Chem 7:91-107.
4. Forte E, I Chimenti, L Barile, R Gaetani, F Angelini, V Ionta, E Messina and A Giacomello. (2011). Cardiac cell therapy: the next (re)generation. Stem Cell Rev 7:1018-1030.
5. Messina E, L De Angelis, G Frati, S Morrone, S Chimenti, F Fiordaliso, M Salio, M Battaglia, MV Latronico, et al. (2004). Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95:911-921. (Pubitemid 39435006)
6. Smith RR, L Barile, HC Cho, MK Leppo, JM Hare, E Messina, A Giacomello, MR Abraham and E Marban. (2007). Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115:896-908. (Pubitemid 46294730)
7. Davis DR, R Ruckdeschel Smith and E Marban. (2010). Human cardiospheres are a source of stem cells with cardiomyogenic potential. Stem Cells 28:903-904.
8. Makkar RR, RR Smith, K Cheng, K Malliaras, LE Thomson, D Berman, LS Czer, L Marban, A Mendizabal, et al. (2012). Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379:895-904.
9. Li TS, K Cheng, K Malliaras, RR Smith, Y Zhang, B Sun, N Matsushita, A Blusztajn, J Terrovitis, 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 59:942-953.
10. Li TS, K Cheng, ST Lee, S Matsushita, D Davis, K Malliaras, Y Zhang, N Matsushita, et al. (2010). Cardiospheres recapitulate a niche-like microenvironment rich in stemness and cell-matrix interactions, rationalizing their enhanced functional potency for myocardial repair. Stem Cells 28: 2088-2098.
11. Lee ST, AJ White, S Matsushita, K Malliaras, C Steenbergen, Y Zhang, TS Li, J Terrovitis, et al. (2011). Intramyocardial injection of autologous cardiospheres or cardiosphere-derived cells preserves function and minimizes adverse ventricular remodeling in pigs with heart failure post-myocardial infarction. J Am Coll Cardiol 57:455-465.
12. Shen D, K Cheng and E Marban. (2012). Dose-dependent functional benefit of human cardiosphere transplantation in mice with acute myocardial infarction. J Cell Mol Med [Epub ahead of print]; DOI: 10. 111/j.1582-4934. 011.01512.x.
13. Chimenti I, RR Smith, TS Li, G Gerstenblith, E Messina, A Giacomello and E Marban. (2010). Relative roles of direct regeneration versus paracrine effects of human cardiospherederived cells transplanted into infarcted mice. Circ Res 106: 971-980.
14. Boudoulas KD and AK Hatzopoulos. (2009). Cardiac repair and regeneration: the Rubik's cube of cell therapy for heart disease. Dis Model Mech. 2:344-358.
15. Zavadil J and EP Bottinger. (2005). TGF-beta and epithelialto-mesenchymal transitions. Oncogene 24:5764-5774.
16. Thiery JP and JP Sleeman. (2006). Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7:131-142. (Pubitemid 43278296)
17. Laping NJ, E Grygielko, A Mathur, S Butter, J Bomberger, C Tweed,WMartin, J Fornwald, R Lehr, et al. (2002). Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol Pharmacol 62:58-64. (Pubitemid 34680516)
18. Kalluri R and RA Weinberg. (2009). The basics of epithelialmesenchymal transition. J Clin Invest 119:1420-1428.
19. Chua KN, KL Poon, J Lim, WJ Sim, RY Huang and JP Thiery. (2011). Target cell movement in tumor and cardiovascular diseases based on the epithelial-mesenchymal transition concept. Adv Drug Deliv Rev 63:558-567.
20. Mani SA, W Guo, MJ Liao, EN Eaton, A Ayyanan, AY Zhou, M Brooks, F Reinhard, CC Zhang, et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133:704-715. (Pubitemid 351636299)
21. Caja L, E Bertran, J Campbell, N Fausto and I Fabregat. (2011). The transforming growth factor-beta (TGF-beta) mediates acquisition of a mesenchymal stem cell-like phenotype in human liver cells. J Cell Physiol 226:1214-1223.
22. Chimenti I, R Gaetani, L Barile, E Forte, V Ionta, F Angelini, G Frati, E Messina and A Giacomello. (2012). Isolation and expansion of adult cardiac stem/progenitor cells in the form of cardiospheres from human cardiac biopsies and murine hearts. Methods Mol Biol 879:327-338.
23. Takahashi K, K Tanabe, M Ohnuki, M Narita, T Ichisaka, K Tomoda and S Yamanaka. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872. (Pubitemid 350138099)
24. Yu J, MA Vodyanik, K Smuga-Otto, J Antosiewicz-Bourget, JL Frane, S Tian, J Nie, GA Jonsdottir, V Ruotti, et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917-1920.
25. Ieda M, JD Fu, P Delgado-Olguin, V Vedantham, Y Hayashi, BG Bruneau and D Srivastava. (2010). Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142:375-386.
26. Qian L, Y Huang, CI Spencer, A Foley, V Vedantham, L Liu, SJ Conway, JD Fu and D Srivastava. (2012). In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485:593-598.
27. Gustafsson MV, X Zheng, T Pereira, K Gradin, S Jin, J Lundkvist, JL Ruas, L Poellinger, U Lendahl and M Bondesson. (2005). Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9:617-628. (Pubitemid 41555144)
28. Jordan NV, GL Johnson and AN Abell. (2011). Tracking the intermediate stages of epithelial-mesenchymal transition in epithelial stem cells and cancer. Cell Cycle 10: 2865-2873.
29. Kluppel M and JL Wrana. (2005). Turning it up a Notch: cross-talk between TGF beta and Notch signaling. Bioessays 27:115-118. (Pubitemid 40292381)
30. Nemir M and T Pedrazzini. (2008). Functional role of Notch signaling in the developing and postnatal heart. J Mol Cell Cardiol 45:495-504.
31. Sansone P, G Storci, C Giovannini, S Pandolfi, S Pianetti, M Taffurelli, D Santini, C Ceccarelli, P Chieco and M Bonafe. (2007). p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres. Stem Cells 25:807-815. (Pubitemid 46354241)
32. Li R, J Liang, S Ni, T Zhou, X Qing, H Li, W He, J Chen, F Li, et al. (2010). A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 7:51-63.
33. Zhang R, M Han, B Zheng, YJ Li, YN Shu and JK Wen. (2010). Kruppel-like factor 4 interacts with p300 to activate mitofusin 2 gene expression induced by all-trans retinoic acid in VSMCs. Acta Pharmacol Sin 31:1293-1302.
34. Zeisberg M, AA Shah and R Kalluri. (2005). Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney. J Biol Chem 280:8094-8100. (Pubitemid 40349708)
35. Asazuma-Nakamura Y, P Dai, Y Harada, Y Jiang, K Hamaoka and T Takamatsu. (2009). Cx43 contributes to TGF-beta signaling to regulate differentiation of cardiac fibroblasts into myofibroblasts. Exp Cell Res 315: 1190-1199.
36. Saga Y, S Kitajima and S Miyagawa-Tomita. (2000). Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc Med 10:345-352. (Pubitemid 32448044)
37. Willems E, M Lanier, E Forte, F Lo, J Cashman and M Mercola. (2011). A chemical biology approach to myocardial regeneration. J Cardiovasc Transl Res 4:340-350.
38. Lickert H, JK Takeuchi, I Von Both, JR Walls, F McAuliffe, SL Adamson, RM Henkelman, JL Wrana, J Rossant and BG Bruneau. (2004). Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432:107-112. (Pubitemid 39490836)
39. Mercola M, P Ruiz-Lozano and MD Schneider. (2011). Cardiac muscle regeneration: lessons from development. Genes Dev 25:299-309.
40. Medici D, EM Shore, VY Lounev, FS Kaplan, R Kalluri and BR Olsen. (2010). Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 16:1400-1406.
41. Kelm JM, E Ehler, LK Nielsen, S Schlatter, JC Perriard and M Fussenegger. (2004). Design of artificial myocardial microtissues. Tissue Eng 10:201-214. (Pubitemid 38199376)
42. Limana F, MC Capogrossi and A Germani. (2011). The epicardium in cardiac repair: from the stem cell view. Pharmacol Ther 129:82-96.
43. Wagner KD, N Wagner, A Bondke, B Nafz, B Flemming, H Theres and H Scholz. (2002). The Wilms' tumor suppressor Wt1 is expressed in the coronary vasculature after myocardial infarction. FASEB J 16:1117-1119.
44. Wagner KD, N Wagner, S Wellmann, G Schley, A Bondke, H Theres and H Scholz. (2003). Oxygen-regulated expression of the Wilms' tumor suppressor Wt1 involves hypoxiainducible factor-1 (HIF-1). FASEB J 17:1364-1366.
45. Kanemura Y, H Mori, S Kobayashi, O Islam, E Kodama, A Yamamoto, Y Nakanishi, N Arita, M Yamasaki, et al. (2002). Evaluation of in vitro proliferative activity of human fetal neural stem/progenitor cells using indirect measurements of viable cells based on cellular metabolic activity. J Neurosci Res 69:869-879. (Pubitemid 34984704)
46. Inman GJ, FJ Nicolas, JF Callahan, JD Harling, LM Gaster, AD Reith, NJ Laping and CS Hill. (2002). SB-431542 is a potent and specific inhibitor of transforming growth factorbeta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 62: 65-74. (Pubitemid 34680517)
47. Bax NA, AA van Oorschot, S Maas, J Braun, J van Tuyn, AA de Vries, AC Groot and MJ Goumans. (2011). In vitro epithelial-to-mesenchymal transformation in human adult epicardial cells is regulated by TGFbeta-signaling and WT1. Basic Res Cardiol 106:829-847.
48. Willis BC and Z Borok. (2007). TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 293:L525-L534. (Pubitemid 47358808)
49. Halder SK, RD Beauchamp and PK Datta. (2005). A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 7:509-521. (Pubitemid 40791869)
50. Altomare C, L Barile, S Marangoni, M Rocchetti, M Alemanni, G Mostacciuolo, A Giacomello, E Messina and A Zaza. (2010). Caffeine-induced Ca(2 +) signaling as an index of cardiac progenitor cells differentiation. Basic Res Cardiol 105:737-749.
51. Cai CL, JC Martin, Y Sun, L Cui, L Wang, K Ouyang, L Yang, L Bu, X Liang, et al. (2008). A myocardial lineage derives from Tbx18 epicardial cells. Nature 454:104-108. (Pubitemid 351931969)
52. Zhou B, Q Ma, S Rajagopal, SM Wu, I Domian, J Rivera-Feliciano, D Jiang, A von Gise, S Ikeda, et al. (2008). Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454:109-113. (Pubitemid 351931979)
53. Limana F, C Bertolami, A Mangoni, A Di Carlo, D Avitabile, D Mocini, P Iannelli, R De Mori, C Marchetti, et al. (2010). Myocardial infarction induces embryonic reprogramming of epicardial c-kit (+) cells: role of the pericardial fluid. J Mol Cell Cardiol 48:609-618.
54. Martinez-Estrada OM, LA Lettice, A Essafi, JA Guadix, J Slight, V Velecela, E Hall, J Reichmann, PS Devenney, et al. (2010). Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat Genet 42:89-93.
55. Limana F, A Zacheo, D Mocini, A Mangoni, G Borsellino, A Diamantini, R De Mori, L Battistini, E Vigna, et al. (2007). Identification of myocardial and vascular precursor cells in human and mouse epicardium. Circ Res 101:1255-1265. (Pubitemid 350294642)
56. Russell JL, SC Goetsch, NR Gaiano, JA Hill, EN Olson and JW Schneider. (2011). A dynamic notch injury response activates epicardium and contributes to fibrosis repair. Circ Res 108:51-59.
57. Di Meglio F, C Castaldo, D Nurzynska, V Romano, R Miraglia, C Bancone, G Langella, C Vosa and S Montagnani. (2010). Epithelial-mesenchymal transition of epicardial mesothelium is a source of cardiac CD117-positive stem cells in adult human heart. J Mol Cell Cardiol 49:719-727.
58. Blokzijl A, C Dahlqvist, E Reissmann, A Falk, A Moliner, U Lendahl and CF Ibanez. (2003). Cross-talk between the Notch and TGF-beta signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J Cell Biol 163:723-728. (Pubitemid 37517880)
59. Zavadil J, L Cermak, N Soto-Nieves and EP Bottinger. (2004). Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J 23:1155-1165. (Pubitemid 38436879)