Neuregulin-1β induces mature ventricular cardiac differentiation from induced pluripotent stem cells contributing to cardiac tissue repair

Stem Cells and Development

Volumn 24, Issue 4, 2015, Pages 484-496

  Iglesias García, Olalla ^a   Baumgartner, Sven ^b   Macrí Pellizzeri, Laura ^a   Rodriguez Madoz, Juan Roberto ^a   Abizanda, Gloria ^a   Guruceaga, Elizabeth ^a   Albiasu, Edurne ^a   Corbacho, David ^a   Benavides Vallve, Carolina ^a   Soriano Navarro, Mario ^c   González Granero, Susana ^c   Gavira, Juan José ^d   Krausgrill, Benjamin ^b   Rodriguez Mañero, Moises ^d   García Verdugo, Jose Manuel ^c   Ortiz De Solorzano, Carlos ^a   Halbach, Marcel ^b   Hescheler, Juergen ^b   Pelacho, Beatriz ^a   Prósper, Felipe ^a,d  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF VALENCIA   (Spain)

^d UNIVERSITY CLINIC OF NAVARRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DIMETHYL SULFOXIDE; GREEN FLUORESCENT PROTEIN; NEU DIFFERENTIATION FACTOR; NEUREGULIN 1 BETA; UNCLASSIFIED DRUG; NEUREGULIN BETA;

ACUTE HEART INFARCTION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; CORONARY ARTERY LIGATION; ELECTROPHYSIOLOGY; FEMALE; FIBROBLAST; GENE EXPRESSION; HEART FUNCTION; HEART MUSCLE CELL; HEART VENTRICLE; HISTOLOGY; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PATCH CLAMP TECHNIQUE; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TISSUE REGENERATION; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CARDIAC MUSCLE CELL; CELL LINE; CYTOLOGY; DRUG EFFECTS; HEART VENTRICLE FUNCTION; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MYOCARDIAL INFARCTION; PHYSIOLOGY; REGENERATION; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

IPS; MUS;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; DIMETHYL SULFOXIDE; FIBROBLASTS; HEART VENTRICLES; INDUCED PLURIPOTENT STEM CELLS; MICE; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NEUREGULIN-1; REGENERATION; STEM CELL TRANSPLANTATION; VENTRICULAR FUNCTION;

EID: 84923071662     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0211     Document Type: Article

References (55)

1. Passier R, LW van Laake and CL Mummery. (2008). Stemcell- based therapy and lessons from the heart. Nature 453:322-329.
2. Beltrami AP, L Barlucchi, D Torella, M Baker, F Limana, S Chimenti, H Kasahara, M Rota, E Musso, et al. (2003). Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763-776.
3. Winter EM, AA van Oorschot, B Hogers, LM van der Graaf, PA Doevendans, RE Poelmann, DE Atsma, AC Gittenberger-de Groot and MJ Goumans. (2009). A new direction for cardiac regeneration therapy: application of synergistically acting epicardium-derived cells and cardiomyocyte progenitor cells. Circ Heart Fail 2:643-653.
4. van Laake LW, R Passier, J Monshouwer-Kloots, AJ Verkleij, DJ Lips, C Freund, K den Ouden, D Ward-van Oostwaard, J Korving, et al. (2007). Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res 1:9-24.
5. Laflamme MA, KY Chen, AV Naumova, V Muskheli, JA Fugate, SK Dupras, H Reinecke, C Xu, M Hassanipour, 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.
6. Takahashi K and S Yamanaka. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676.
7. Iglesias-Garcia O, B Pelacho and F Prosper. (2013). Induced pluripotent stem cells as a new strategy for cardiac regeneration and disease modeling. J Mol Cell Cardiol 62:43-50.
8. Mauritz C, K Schwanke, M Reppel, S Neef, K Katsirntaki, LS Maier, F Nguemo, S Menke, M Haustein, et al. (2008). Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 118:507-517.
9. Zhang J, GF Wilson, AG Soerens, CH Koonce, J Yu, SP Palecek, JA Thomson and TJ Kamp. (2009). Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104:e30-e41.
10. Nelson TJ, A Martinez-Fernandez, S Yamada, C Perez- Terzic, Y Ikeda and A Terzic. (2009). Repair of acute myocardial infarction by human stemness factors induced pluripotent stem cells. Circulation 120:408-416.
11. Kawamura M, S Miyagawa, K Miki, A Saito, S Fukushima, T Higuchi, T Kawamura, T Kuratani, T Daimon, et al. (2012). Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardiomyopathy model. Circulation 126:S29-S37.
12. Xi J, M Khalil, N Shishechian, T Hannes, K Pfannkuche, H Liang, A Fatima, M Haustein, F Suhr, et al. (2010). Comparison of contractile behavior of native murine ventricular tissue and cardiomyocytes derived from embryonic or induced pluripotent stem cells. FASEB J 24:2739-2751.
13. Odiete O, MF Hill and DB Sawyer. (2012). Neuregulin in cardiovascular development and disease. Circ Res 111:1376-1385.
14. Kuramochi Y, GM Cote, X Guo, NK Lebrasseur, L Cui, R Liao and DB Sawyer. (2004). Cardiac endothelial cells regulate reactive oxygen species-induced cardiomyocyte apoptosis through neuregulin-1beta/erbB4 signaling. J Biol Chem 279:51141-51147.
15. Zhao YY, DR Sawyer, RR Baliga, DJ Opel, X Han, MA Marchionni and RA Kelly. (1998). Neuregulins promote survival and growth of cardiac myocytes. Persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. J Biol Chem 273:10261-10269.
16. Fukazawa R, TA Miller, Y Kuramochi, S Frantz, YD Kim, MA Marchionni, RA Kelly and DB Sawyer. (2003). Neuregulin-1 protects ventricular myocytes from anthracycline- induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J Mol Cell Cardiol 35:1473-1479.
17. Seguchi O, S Takashima, S Yamazaki, M Asakura, Y Asano, Y Shintani, M Wakeno, T Minamino, H Kondo, et al. (2007). A cardiac myosin light chain kinase regulates sarcomere assembly in the vertebrate heart. J Clin Invest 117:2812-2824.
18. Iivanainen E, I Paatero, SM Heikkinen, TT Junttila, R Cao, P Klint, PM Jaakkola, Y Cao and K Elenius. (2007). Intraand extracellular signaling by endothelial neuregulin-1. Exp Cell Res 313:2896-2909.
19. Xu G, T Watanabe, Y Iso, S Koba, T Sakai, M Nagashima, S Arita, S Hongo, H Ota, et al. (2009). Preventive effects of heregulin-beta1 on macrophage foam cell formation and atherosclerosis. Circ Res 105:500-510.
20. Liu X, X Gu, Z Li, X Li, H Li, J Chang, P Chen, J Jin, B Xi, et al. (2006). Neuregulin-1/erbB-activation improves cardiac function and survival in models of ischemic, dilated, and viral cardiomyopathy. J Am Coll Cardiol 48:1438-1447.
21. Gu X, X Liu, D Xu, X Li, M Yan, Y Qi, WYan, WWang, J Pan, et al. (2010). Cardiac functional improvement in rats with myocardial infarction by up-regulating cardiac myosin light chain kinase with neuregulin. Cardiovasc Res 88:334-343.
22. Rentschler S, J Zander, K Meyers, D France, R Levine, G Porter, SA Rivkees, GE Morley and GI Fishman. (2002). Neuregulin-1 promotes formation of the murine cardiac conduction system. Proc Natl Acad Sci U S A 99:10464-10469.
23. Zhu WZ, Y Xie, KW Moyes, JD Gold, B Askari and MA Laflamme. (2010). Neuregulin/ErbB signaling regulates cardiac subtype specification in differentiating human embryonic stem cells. Circ Res 107:776-786.
24. Irizarry RA, BM Bolstad, F Collin, LM Cope, B Hobbs and TP Speed. (2003). Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15.
25. Gentleman R. Carey V. Dudoit S. Irizarry R. Huber W. Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005 Springer, NY
26. Gentleman R, V Carey, S Dudoit, R Irizarry and W Huber. (2005). Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Springer, NY. 26. Gene Ontology Consortium, JA Blake, M Dolan, H Drabkin, DP Hill, N Li, D Sitnikov, S Bridges, S Burgess, et al. (2013). Gene Ontology annotations and resources. Nucleic Acids Res 41:D530-D535.
27. Pelacho B, Y Nakamura, J Zhang, J Ross, Y Heremans, M Nelson-Holte, B Lemke, J Hagenbrock, Y Jiang, et al. (2007). Multipotent adult progenitor cell transplantation increases vascularity and improves left ventricular function after myocardial infarction. J Tissue Eng Regen Med 1:51-59.
28. Benavides-Vallve C, D Corbacho, O Iglesias-Garcia, B Pelacho, E Albiasu, S Castano, A Munoz-Barrutia, F Prosper and C Ortiz-de-Solorzano. (2012). New strategies for echocardiographic evaluation of left ventricular function in a mouse model of long-term myocardial infarction. PLoS One 7:e41691.
29. Behfar A, C Perez-Terzic, RS Faustino, DK Arrell, DM Hodgson, S Yamada, M Puceat, N Niederlander, AE Alekseev, LV Zingman and A Terzic. (2007). Cardiopoietic programming of embryonic stem cells for tumor-free heart repair. J Exp Med 204:405-420.
30. Yamada S, T Nelson, G Kane, A Martinez-Fernandez, RJ Crespo-Diaz, Y Ikeda, C Terzic and A Terzic. (2013). iPS cell intervention rescues wall motion disparity achieving biological cardiac resynchronization post-infarction. J Physiol 591:4335-4349.
31. Zwi L, O Caspi, G Arbel, I Huber, A Gepstein, IH Park and L Gepstein. (2009). Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation 120: 1513-1523.
32. Uosaki H, H Fukushima, A Takeuchi, S Matsuoka, N Nakatsuji, S Yamanaka and JK Yamashita. (2011). Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLoS One 6:e23657.
33. Wang Z, G Xu, Y Wu, Y Guan, L Cui, X Lei, J Zhang, L Mou, B Sun and Q Dai. (2009). Neuregulin-1 enhances differentiation of cardiomyocytes from embryonic stem cells. Med Biol Eng Comput 47:41-48.
34. Sun M, X Yan, Y Bian, AO Caggiano and JP Morgan. (2011). Improving murine embryonic stem cell differentiation into cardiomyocytes with neuregulin-1: differential expression of microRNA. Am J Physiol Cell Physiol 301: C21-C30.
35. Kim HS, JW Cho, K Hidaka and T Morisaki. (2007). Activation of MEK-ERK by heregulin-beta1 promotes the development of cardiomyocytes derived from ES cells. Biochem Biophys Res Commun 361:732-738.
36. Hao J, CL Galindo, TL Tran and DB Sawyer. (2014). Neuregulin-1beta induces embryonic stem cell cardiomyogenesis via ErbB3/ErbB2 receptors. Biochem J 458: 335-341.
37. Zhang YM, C Hartzell, M Narlow and SC Dudley, Jr. (2002). Stem cell-derived cardiomyocytes demonstrate arrhythmic potential. Circulation 106:1294-1299.
38. Chen HS, C Kim and M Mercola. (2009). Electrophysiological challenges of cell-based myocardial repair. Circulation 120:2496-2508.
39. Edwards MK, JF Harris and MW McBurney. (1983). Induced muscle differentiation in an embryonal carcinoma cell line. Mol Cell Biol 3:2280-2286.
40. Halbach M, K Pfannkuche, F Pillekamp, A Ziomka, T Hannes, M Reppel, J Hescheler and J Muller-Ehmsen. (2007). Electrophysiological maturation and integration of murine fetal cardiomyocytes after transplantation. Circ Res 101:484-492.
41. Carpenter L, C Carr, CT Yang, DJ Stuckey, K Clarke and SM Watt. (2011). Efficient differentiation of human induced pluripotent stem cells generates cardiac cells that provide protection following myocardial infarction in the rat. Stem Cells Dev 21:977-986.
42. Reinecke H, M Zhang, T Bartosek and CE Murry. (1999). Survival, integration, and differentiation of cardiomyocyte grafts: a study in normal and injured rat hearts. Circulation 100:193-202.
43. Halbach M, S Baumgartner, RG Sahito, B Krausgrill, M Maass, G Peinkofer, D Ladage, J Hescheler and J Muller- Ehmsen. (2014). Cell persistence and electrical integration of transplanted fetal cardiomyocytes from different developmental stages. Int J Cardiol 171:e122-e124.
44. Mauritz C, A Martens, SV Rojas, T Schnick, C Rathert, N Schecker, S Menke, S Glage, R Zweigerdt, et al. (2011). Induced pluripotent stem cell (iPSC)-derived Flk-1 progenitor cells engraft, differentiate, and improve heart function in a mouse model of acute myocardial infarction. Eur Heart J 32:2634-2641.
45. Halbach M, G Peinkofer, S Baumgartner, M Maass, M Wiedey, K Neef, B Krausgrill, D Ladage, A Fatima, et al. (2013). Electrophysiological integration and action potential properties of transplanted cardiomyocytes derived from induced pluripotent stem cells. Cardiovasc Res 100:432-440.
46. Shiba Y, S Fernandes, WZ Zhu, D Filice, V Muskheli, J Kim, NJ Palpant, J Gantz, KW Moyes, et al. (2012). Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 489:322-325.
47. Mirotsou M, TM Jayawardena, J Schmeckpeper, M Gnecchi and VJ Dzau. (2010). Paracrine mechanisms of stem cell reparative and regenerative actions in the heart. J Mol Cell Cardiol 50:280-289.
48. Sasaki H, PS Ray, L Zhu, N Galang and N Maulik. (2000). Oxidative stress due to hypoxia/reoxygenation induces angiogenic factor VEGF in adult rat myocardium: possible role of NFkappaB. Toxicology 155:27-35.
49. Seko Y, N Takahashi, K Tobe, T Kadowaki and Y Yazaki. (1999). Pulsatile stretch activates mitogen-activated protein kinase (MAPK) family members and focal adhesion kinase (p125(FAK)) in cultured rat cardiac myocytes. Biochem Biophys Res Commun 259:8-14.
50. Zentilin L, U Puligadda, V Lionetti, S Zacchigna, C Collesi, L Pattarini, G Ruozi, S Camporesi, G Sinagra, et al. (2009). Cardiomyocyte VEGFR-1 activation by VEGF-B induces compensatory hypertrophy and preserves cardiac function after myocardial infarction. FASEB J 24:1467-1478.
51. Stevens KR, KL Kreutziger, SK Dupras, FS Korte, M Regnier, V Muskheli, MB Nourse, K Bendixen, H Reinecke and CE Murry. (2009). Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci U S A 106: 16568-16573.
52. Templin C, R Zweigerdt, K Schwanke, R Olmer, JR Ghadri, MY Emmert, E Muller, SM Kuest, S Cohrs, et al. (2012). Transplantation and tracking of human-induced pluripotent stem cells in a pig model of myocardial infarction: assessment of cell survival, engraftment, and distribution by hybrid single photon emission computed tomography/computed tomography of sodium iodide symporter transgene expression. Circulation 126:430-439.
53. Tulloch NL, V Muskheli, MV Razumova, FS Korte, M Regnier, KD Hauch, L Pabon, H Reinecke and CE Murry. (2011). Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 109:47-59.
54. Xiong Q, KL Hill, Q Li, P Suntharalingam, A Mansoor, X Wang, MN Jameel, P Zhang, C Swingen, DS Kaufman and J Zhang. (2011). A fibrin patch-based enhanced delivery of human embryonic stem cell-derived vascular cell transplantation in a porcine model of postinfarction left ventricular remodeling. Stem Cells 29:367-375.
55. Formiga FR, B Pelacho, E Garbayo, I Imbuluzqueta, P Diaz-Herraez, G Abizanda, JJ Gavira, T Simon-Yarza, E Albiasu, et al. (2014). Controlled delivery of fibroblast growth factor-1 and neuregulin-1 from biodegradable microparticles promotes cardiac repair in a rat myocardial infarction model through activation of endogenous regeneration. J Control Release 173:132-139.