Functional cardiomyocytes derived from isl1 cardiac progenitors via Bmp4 stimulation

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Cagavi, Esra ^a,b   Bartulos, Oscar ^a   Suh, Carol Y ^a   Sun, Baonan ^c   Yue, Zhichao ^c   Jiang, Zhengxin ^a   Yue, Lixia ^c   Qyang, Yibing ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ISTANBUL MEDIPOL UNIVERSITY   (Turkey)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CELL SURFACE MARKER; ISLET 1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX 20; TRANSCRIPTION FACTOR TBX5; TROPONIN T; UNCLASSIFIED DRUG; INSULIN GENE ENHANCER BINDING PROTEIN ISL-1; LIM HOMEODOMAIN PROTEIN; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR 5; TBX20 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CALCIUM SIGNALING; CARDIAC STEM CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; HEART MUSCLE CELL; MOUSE; NONHUMAN; STEM CELL CULTURE; ACTION POTENTIAL; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; LIM-HOMEODOMAIN PROTEINS; MICE; MYOCYTES, CARDIAC; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS;

EID: 84930661525     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110752     Document Type: Article

References (43)

1. Ptaszek LM, Mansour M, Ruskin JN, Chien KR (2012) Series Stem Cells 1 Towards regenerative therapy for cardiac disease. Lancet: 933-942.
2. Cai C-L, Liang X, Shi Y, Chu P-H, Pfaff SL, 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.
3. Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, et al. (2008) Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453: 524-528.
4. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, et al. (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114: 763-776.
5. Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, et al. (2004) Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95: 911-921.
6. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, et al. (2007) Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115: 896-908.
7. Martin CM, Meeson AP, Robertson SM, Hawke TJ, Richardson JA., et al. (2004) Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev Biol 265: 262-275.
8. Cai C-L, Martin JC, Sun Y, Cui L, Wang L, et al. (2008) A myocardial lineage derives from Tbx18 epicardial cells. Nature 454: 104-108.
9. Laugwitz K-L, Moretti A, Lam J, Gruber P, Chen Y, et al. (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433: 647-653.
10. Moretti A, Caron L, Nakano A, Lam JT, Bernshausen A, et al. (2006) Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127: 1151-1165.
11. Ma Q, Zhou B, Pu WT (2008) Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity. Dev Biol 323: 98-104.
12. Moretti A, Bellin M, Jung CB, Thies T-M, Takashima Y, et al. (2010) Mouse and human induced pluripotent stem cells as a source for multipotent Isl1+ cardiovascular progenitors. FASEB J 24: 700- 711.
13. Bu L, Jiang X, Martin-Puig S, Caron L, Zhu S, et al. (2009) Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460: 113-117.
14. Nsair A, Schenke-Layland K, Van Handel B, Evseenko D, Kahn M, et al. (2012) Characterization and therapeutic potential of induced pluripotent stem cell-derived cardiovascular progenitor cells. PLoS One 7: E45603.
15. Ahlgren U, Pfaff SL, Jessell TM, Edlund T, Edlund H (1997) Independent requirement for Isl1 in formation of pancreatic mesenchyme and islet cells. Nature: 257-260.
16. Thor S, Andersson SGE, Tomlinson A, Thomas JB (1999) A LIM-homeodomain combinatorial code for motor- neuron pathway selection system, although expression was also observed in precursors of the. Nature 397: 76-80.
17. Engleka KA, Manderfield LJ, Brust RD, Li L, Cohen A, et al. (2012) Islet1 derivatives in the heart are of both neural crest and second heart field origin. Circ Res 110: 922-926.
18. Qyang Y, Martin-Puig S, Chiravuri M, Chen S, Xu H, 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.
19. Dodou E, Verzi MP, Anderson JP, Xu S-M, Black BL (2004) Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development 131: 3931-3942.
20. Yuasa S, Itabashi Y, Koshimizu U, Tanaka T, Sugimura K, et al. (2005) Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat Biotechnol 23: 607-611.
21. Winnier G, Blessing M, Labosky PA, Hogan BL (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9: 2105-2116.
22. Wang J, Greene SB, Bonilla-Claudio M, Tao Y, Zhang J, et al. (2010) Bmp signaling regulates myocardial differentiation from cardiac progenitors through a MicroRNA-mediated mechanism. Dev Cell 19: 903-912.
23. Yang L, Cai C-L, Lin L, Qyang Y, Chung C, et al. (2006) Isl1Cre reveals a common Bmp pathway in heart and limb development. Development 133: 1575-1585.
24. Naito AT, Shiojima I, Akazawa H, Hidaka K, Morisaki T, et al. (2006) Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci U S A 103: 19812-19817.
25. Lee MY, Cagavi Bozkulak E, Schliffke S, Amos PJ, Ren Y, et al. (2011) High density cultures of embryoid bodies enhanced cardiac differentiation of murine embryonic stem cells. Biochem Biophys Res Commun 416: 51-57.
26. Musunuru K, Domian I, Chien KR (2010) Stem Cell Models of Cardiac Development and Disease. Annu Rev Cell Dev Biol 26: 667-687. doi:10.1146/annurev-cellbio-100109-103948. Stem.
27. He J-Q, Ma Y, Lee Y, Thomson JA, Kamp TJ (2003) Human embryonic stem cells develop into multiple types of cardiac myocytes: Action potential characterization. Circ Res 93: 32-39.
28. Shen T, Aneas I, Sakabe N, Dirschinger RJ, Wang G, et al. (2011) Tbx20 regulates a genetic program essential to adult mouse cardiomyocyte function. J Clin Invest 110. doi:10.1172/JCI59472.4640.
29. Stennard FA, Costa MW, Elliott DA, Rankin S, Haast SJ, et al. (2003) Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart. Dev Biol 262: 206-224.
30. Greulich F, Rudat C, Kispert A (2011) Mechanisms of T-box gene function in the developing heart. Cardiovasc Res 91: 212-222.
31. Clement S, Stouffs M, Bettiol E, Kampf S, Krause K-H, et al. (2007) Expression and function of alphasmooth muscle actin during embryonic-stem-cell-derived cardiomyocyte differentiation. J Cell Sci 120: 229-238.
32. Ruzicka DL, Schwartz RJ (1988) Sequential activation of alpha-actin genes during avian cardiogenesis: vascular smooth muscle alpha-actin gene transcripts mark the onset of cardiomyocyte differentiation. J Cell Biol 107: 2575-2586.
33. Liu W, Selever J, Wang D, Lu M-F, Moses KA, et al. (2004) Bmp4 signaling is required for outflow-tract septation and branchial-arch artery remodeling. Proc Natl Acad Sci U S A 101: 4489-4494.
34. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, 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. Swapna I, Borodinsky LN (2012) Interplay between electrical activity and bone morphogenetic protein signaling regulates spinal neuron differentiation. Proc Natl Acad Sci U S A 109: 16336-16341. doi:10.1073/pnas.1202818109/-/DCSupplemental.
36. Mejia-Luna L, Avila G (2004) Ca2+ channel regulation by transforming growth factor-beta 1 and bone morphogenetic protein-2 in developing mice myotubes. J Physiol 559: 41-54.
37. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, et al. (2009) Evidence for cardiomyocyte renewal in humans. Science 324: 98-102.
38. Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, et al. (2013) Mammalian heart renewal by pre-existing cardiomyocytes. Nature 493: 433-436.
39. Kajstura J, Gurusamy N, Ogorek B, Goichberg P, Clavo-Rondon C, et al. (2010) Myocyte turnover in the aging human heart. Circ Res 107: 1374-1386.
40. Hsieh PCH, Segers VFM, Davis ME, MacGillivray C, Gannon J, et al. (2007) Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 13: 970-974.
41. 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.
42. Ben-David U, Gan Q-F, Golan-Lev T, Arora P, Yanuka O, et al. (2013) Selective elimination of human pluripotent stem cells by an oleate synthesis inhibitor discovered in a high-throughput screen. Cell Stem Cell 12: 167-179.
43. Lee M-O, Moon SH, Jeong H-C, Yi J-Y, Lee T-H, et al. (2013) Inhibition of pluripotent stem cell-derived teratoma formation by small molecules. Proc Natl Acad Sci U S A 110: E3281-90.