FGF10 promotes regional foetal cardiomyocyte proliferation and adult cardiomyocyte cell-cycle re-entry

Cardiovascular Research

Volumn 104, Issue 3, 2014, Pages 432-442

  Rochais, Francesca ^a   Sturny, Rachel ^a   Chao, Cho Ming ^b   Mesbah, Karim ^a   Bennett, Michael ^c   Mohun, Tim J ^c   Bellusci, Saverio ^b,d   Kelly, Robert G ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d KAZAN FEDERAL UNIVERSITY   (Russian Federation)

Author keywords

Cardiac repair; Cardiomyocyte proliferation; Fibroblast growth factor 10; Heart development

Indexed keywords

ALPHA ACTININ; CYCLIN DEPENDENT KINASE INHIBITOR 1B; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 2B; MEMBRANE ANTIGEN; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; VIMENTIN; FGF10 PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANTIBODY LABELING; ARTICLE; CARDIAC STEM CELL; CELL CULTURE; CELL CYCLE RE ENTRY; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FETUS; FETUS HEART; FIBROBLAST; GENE OVEREXPRESSION; HEART DEVELOPMENT; HEART FUNCTION; HEART MUSCLE CELL; HEART RIGHT VENTRICLE; HEART RIGHT VENTRICLE HYPERTROPHY; HEART VENTRICLE WALL; IMMUNODETECTION; IN VIVO STUDY; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA SPLICING; UPREGULATION; WESTERN BLOTTING; ANIMAL; CARDIAC MUSCLE CELL; CELL CYCLE; EMBRYOLOGY; HEART; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FIBROBLAST GROWTH FACTOR 10; FORKHEAD TRANSCRIPTION FACTORS; HEART; MICE; MYOCYTES, CARDIAC;

EID: 84924857741     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu232     Document Type: Article

References (49)

1. Rochais F, Mesbah K, Kelly RG. Signaling pathways controlling second heart field development. Circ Res 2009;104:933-942.
2. Ahuja P, Sdek P, MacLellan WR. Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol Rev 2007;87:521-544.
3. Pasumarthi KB, Field LJ. Cardiomyocyte cell cycle regulation. Circ Res 2002;90: 1044-1054.
4. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisen J. Evidence for cardiomyocyte renewal in humans. Science 2009;324:98-102.
5. Kajstura J, Urbanek K, Perl S, Hosoda T, Zheng H, Ogorek B, Ferreira-Martins J, Goichberg P, Rondon-Clavo C, Sanada F, D'Amario D, Rota M, Del Monte F, Orlic D, Tisdale J, Leri A, Anversa P. Cardiomyogenesis in the adult human heart. Circ Res 2010; 107:305-315.
6. Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, Sadek HA. Transient regenerative potential of the neonatal mouse heart. Science 2011;331:1078-1080.
7. Walsh S, Ponten A, Fleischmann BK, Jovinge S. Cardiomyocyte cell cycle control and growth estimation in vivo-an analysis based on cardiomyocyte nuclei. Cardiovasc Res 2010;86:365-373.
8. Xin M, Olson EN, Bassel-Duby R. Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat Rev Mol Cell Biol 2013;14:529-541.
9. Smith TK, Bader DM. Signals from both sides: control of cardiac development by the endocardium and epicardium. Semin Cell Dev Biol 2007;18:84-89.
10. Thisse B, Thisse C. Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 2005;287:390-402.
11. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. Receptor specificity of the fibroblast growth factor family. The complete mammalian Fgf family. J Biol Chem 2006;281:15694-15700.
12. Lu SY, Sheikh F, Sheppard PC, Fresnoza A, Duckworth ML, Detillieux KA, Cattini PA. Fgf-16 is required for embryonic heart development. Biochem Biophys Res Commun 2008;373:270-274.
13. Hotta Y, Sasaki S, Konishi M, Kinoshita H, Kuwahara K, Nakao K, Itoh N. Fgf16 is required for cardiomyocyte proliferation in the mouse embryonic heart. Dev Dyn 2008;237: 2947-2954.
14. Lavine KJ, Yu K, White AC, Zhang X, Smith C, Partanen J, Ornitz DM. Endocardial and epicardial derived fgf signals regulate myocardial proliferation and differentiation in vivo. Dev Cell 2005;8:85-95.
15. Kelly RG, Brown NA, Buckingham ME. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 2001;1:435-440.
16. Chan SS, Li HJ, Hsueh YC, Lee DS, ChenJH, HwangSM, ChenCY, Shih E, Hsieh PC. Fibroblast growth factor-10 promotes cardiomyocyte differentiation from embryonic and induced pluripotent stem cells. PLoS ONE 2010;5:e14414.
17. Watanabe Y, Miyagawa-Tomita S, Vincent SD, Kelly RG, Moon AM, Buckingham ME. Role of mesodermal Fgf8 and Fgf10 overlaps in the development of the arterial pole of the heart and pharyngeal arch arteries. Circ Res 2010;106:495-503.
18. Urness LD, Bleyl SB, Wright TJ, Moon AM, Mansour SL. Redundant and dosage sensitive requirements for Fgf3 and Fgf10 in cardiovascular development. Dev Biol 2011;356: 383-397.
19. Marguerie A, Bajolle F, Zaffran S, BrownNA, Dickson C, Buckingham ME, Kelly RG. Congenital heart defects in Fgfr2-IIIb and Fgf10 mutant mice. Cardiovasc Res 2006;71:50-60.
20. Vega-Hernandez M, Kovacs A, De Langhe S, Ornitz DM. Fgf10/Fgfr2b signaling is essential for cardiac fibroblast development and growth of the myocardium. Development 2011;138:3331-3340.
21. Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, Yagishita N, Matsui D, Koga Y, Itoh N, Kato S. Fgf10 is essential for limb and lung formation. Nat Genet 1999;21: 138-141.
22. Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simonet WS. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to drosophila branchless. Genes Dev 1998;12:3156-3161.
23. Huang H, Tindall DJ. Dynamic foxo transcription factors. J Cell Sci 2007;120:2479-2487.
24. Evans-Anderson HJ, Alfieri CM, Yutzey KE. Regulation of cardiomyocyte proliferation and myocardial growth during development by foxo transcription factors. Circ Res 2008;102:686-694.
25. Ni YG, Berenji K, Wang N, Oh M, Sachan N, Dey A, Cheng J, Lu G, Morris DJ, Castrillon DH, Gerard RD, Rothermel BA, Hill JA. Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling. Circulation 2006;114:1159-1168.
26. Tagashira S, Harada H, Katsumata T, Itoh N, Nakatsuka M. Cloning of mouse Fgf10 and up-regulation of its gene expression during wound healing. Gene 1997;197:399-404.
27. Beer HD, Florence C, Dammeier J, McGuire L, Werner S, Duan DR. Mouse fibroblast growth factor 10: cDNA cloning, protein characterization, and regulation of mRNA expression. Oncogene 1997;15:2211-2218.
28. Ieda M, Tsuchihashi T, Ivey KN, Ross RS, Hong TT, Shaw RM, Srivastava D. Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev Cell 2009; 16:233-244.
29. Clark JC, Tichelaar JW, Wert SE, Itoh N, Perl AK, Stahlman MT, Whitsett JA. Fgf-10 disrupts lung morphogenesis and causes pulmonary adenomas in vivo. Am J Physiol Lung Cell Mol Physiol 2001;280:L705-L715.
30. Naqvi N, Li M, Calvert JW, Tejada T, Lambert JP, Wu J, Kesteven SH, Holman SR, Matsuda T, Lovelock JD, Howard WW, Iismaa SE, Chan AY, Crawford BH, Wagner MB, Martin DI, Lefer DJ, Graham RM, Husain A.Aproliferative burst during preadolescence establishes the final cardiomyocyte number. Cell 2014;157:795-807.
31. Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, Woodard S, Lin LZ, Cai CL, Lu MM, Reth M, Platoshyn O, Yuan JX, Evans S, Chien KR. Postnatal Isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005;433:647-653.
32. de Boer BA, van den Berg G, de Boer PA, Moorman AF, Ruijter JM. Growth of the developing mouse heart: an interactive qualitative and quantitative3Datlas. Dev Biol 2012;368: 203-213.
33. Meilhac SM, Esner M, Kerszberg M, Moss JE, Buckingham ME. Oriented clonal cell growth in the developing mouse myocardium underlies cardiac morphogenesis. J Cell Biol 2004; 164:97-109.
34. Rudat C, Norden J, Taketo MM, Kispert A. Epicardial function of canonical wnt-, hedgehog-, Fgfr1/2-and Pdgfra-signaling. Cardiovasc Res 2013;100:411-421.
35. Rudat C, Kispert A. Wt1 and epicardial fate mapping. Circ Res 2012;111:165-169.
36. Mansour SL, Goddard JM, Capecchi MR. Mice homozygous for a targeted disruption of the proto-oncogene Int-2 have developmental defects in the tail and inner ear. Development 1993;117:13-28.
37. Mason IJ, Fuller-Pace F, Smith R, Dickson C. Fgf-7 (keratinocyte growth factor) expression during mouse development suggests roles in myogenesis, forebrain regionalisation and epithelial-mesenchymal interactions. Mech Dev 1994;45:15-30.
38. Accili D, Arden KC.FOXOsat the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004;117:421-426.
39. Poolman RA, Gilchrist R, Brooks G. Cell cycle profiles and expressions of p21cip1 and p27kip1 during myocyte development. Int J Cardiol 1998;67:133-142.
40. Lavine KJ, Schmid GJ, Smith CS, Ornitz DM. Novel tool to suppress cell proliferation in vivo demonstrates that myocardial and coronary vascular growth represent distinct developmental programs. Dev Dyn 2008;237:713-724.
41. Heallen T, Zhang M, Wang J, Bonilla-Claudio M, Klysik E, Johnson RL, Martin JF. Hippo pathway inhibits wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 2011;332:458-461.
42. Engel FB, Hsieh PC, Lee RT, Keating MT. Fgf1/p38 map kinase inhibitor therapy induces cardiomyocyte mitosis, reduces scarring, and rescues function after myocardial infarction. Proc Natl Acad Sci USA 2006;103:15546-15551.
43. Pasumarthi KB, Kardami E, Cattini PA. High and low molecular weight fibroblast growth factor-2 increase proliferation of neonatal rat cardiac myocytes but have differential effects on binucleation and nuclear morphology. Evidence for both paracrine and intracrine actions of fibroblast growth factor-2. Circ Res 1996;78:126-136.
44. Beenken A, Mohammadi M. The fgf family: biology, pathophysiology and therapy. Nat Rev Drug Discov 2009;8:235-253.
45. Virag JA, Rolle ML, Reece J, Hardouin S, Feigl EO, Murry CE. Fibroblast growth factor-2 regulates myocardial infarct repair: effects on cell proliferation, scar contraction, and ventricular function. Am J Pathol 2007;171:1431-1440.
46. Itoh N, Ohta H. Pathophysiological roles of fgf signaling in the heart. Front Physiol 2013;4: 247.
47. Matsumoto E, Sasaki S, Kinoshita H, Kito T, Ohta H, Konishi M, Kuwahara K, Nakao K, Itoh N. Angiotensin II-induced cardiac hypertrophy and fibrosis are promoted in mice lacking Fgf16. Genes Cells 2013;18:544-553.
48. Planavila A, Redondo I, Hondares E, Vinciguerra M, Munts C, Iglesias R, Gabrielli LA, Sitges M, Giralt M, van Bilsen M, Villarroya F. Fibroblast growth factor 21 protects against cardiac hypertrophy in mice. Nat Commun 2013;4:2019.
49. Korf-Klingebiel M, Kempf T, Schluter KD, Willenbockel C, Brod T, Heineke J, Schmidt VJ, Jantzen F, Brandes RP, Sugden PH, Drexler H, Molkentin JD, Wollert KC. Conditional transgenic expression of fibroblast growth factor 9 in the adult mouse heart reduces heart failure mortality after myocardial infarction. Circulation 2011;123:504-514.