Snai1 is important for avian epicardial cell transformation and motility

Developmental Dynamics

Volumn 242, Issue 6, 2013, Pages 699-708

  Tao, Ge ^a,b   Miller, Lindsey J ^b,c   Lincoln, Joy ^b,c  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b NATIONWIDE CHILDREN S HOSPITAL   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Chicken embryo; Epicardium; Snai1

Indexed keywords

CELL PROTEIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 15; PROTEIN SNAI1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRD; CELL INVASION; CELL MIGRATION; CHICK; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; EPICARDIUM; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; MATRIX METALLOPROTEINASE 15; MATRIX METALLOPROTEINASES; MICE; MYOCARDIUM; PERICARDIUM; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS;

AVES;

EID: 84878156641     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23967     Document Type: Article

References (58)

1. Acharya A, Baek ST, Huang G, Eskiocak B, Goetsch S, Sung CY, Banfi S, Sauer MF, Olsen GS, Duffield JS, Olson EN, Tallquist MD. 2012. The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors. Development 139:2139-2149.
2. Austin AF, Compton LA, Love JD, Brown CB, Barnett JV. 2008. Primary and immortalized mouse epicardial cells undergo differentiation in response to TGFbeta. Dev Dyn 237:366-376.
3. Baek ST, Tallquist MD. 2012. Nf1 limits epicardial derivative expansion by regulating epithelial to mesenchymal transition and proliferation. Development 139:2040-2049.
4. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A. 2000. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2:84-89.
5. Bax NA, van Oorschot AA, Maas S, Braun J, van Tuyn J, de Vries AA, Groot AC, Goumans MJ. 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.
6. Braitsch CM, Combs MD, Quaggin SE, Yutzey KE. 2012. Pod1/Tcf21 is regulated by retinoic acid signaling and inhibits differentiation of epicardium-derived cells into smooth muscle in the developing heart. Dev Biol 368:345-357.
7. Cai CL, Martin JC, Sun Y, Cui L, Wang L, Ouyang K, Yang L, Bu L, Liang X, Zhang X, Stallcup WB, Denton CP, McCulloch A, Chen J, Evans SM. 2008. A myocardial lineage derives from Tbx18 epicardial cells. Nature 454:104-108.
8. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. 2000. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76-83.
9. Carver EA, Jiang R, Lan Y, Oram KF, Gridley T. 2001. The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 21:8184-8188.
10. Casanova JC, Travisano S, de la Pompa JL. 2012. Epithelial-to-mesenchymal transition in epicardium is independent of Snail1. Genesis 22:639-650.
11. Chen IH, Wang HH, Hsieh YS, Huang WC, Yeh HI, Chuang YJ. 2011. PRSS23 is essential for the Snail-dependent endothelial to mesenchymal transition during valvulogenesis in zebrafish. Cardiovasc Res 97:443-453.
12. Combs MD, Braitsch CM, Lange AW, James JF, Yutzey KE. 2011. NFATC1 promotes epicardium-derived cell invasion into myocardium. Development 138:1747-1757.
13. Compton LA, Potash DA, Brown CB, Barnett JV. 2007. Coronary vessel development is dependent on the type III transforming growth factor beta receptor. Circ Res 101:784-791.
14. Dettman RW, Denetclaw W, Jr., Ordahl CP, Bristow J. 1998. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev Biol 193:169-181.
15. Dokic D, Dettman RW. 2006. VCAM-1 inhibits TGFbeta stimulated epithelial-mesenchymal transformation by modulating Rho activity and stabilizing intercellular adhesion in epicardial mesothelial cells. Dev Biol 299:489-504.
16. Gittenberger-de Groot AC, Vrancken Peeters MP, Mentink MM, Gourdie RG, Poelmann RE. 1998. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 82:1043-1052.
17. Gittenberger-de Groot AC, Vrancken Peeters MP, Bergwerff M, Mentink MM, Poelmann RE. 2000. Epicardial outgrowth inhibition leads to compensatory mesothelial outflow tract collar and abnormal cardiac septation and coronary formation. Circ Res 87:969-971.
18. Horvay K, Casagranda F, Gany A, Hime GR, Abud HE. 2011. Wnt signaling regulates Snai1 expression and cellular localization in the mouse intestinal epithelial stem cell niche. Stem Cells Dev 20:737-745.
19. Hotary K, Allen E, Punturieri A, Yana I, Weiss SJ. 2000. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J Cell Biol 149:1309-1323.
20. Huang GN, Thatcher JE, McAnally J, Kong Y, Qi X, Tan W, Dimaio JM, Amatruda JF, Gerard RD, Hill JA, Bassel-Duby R, Olson EN. 2012. C/EBP transcription factors mediate epicardial activation during heart development and injury. Science 338:1599-1603.
21. Ishii Y, Garriock RJ, Navetta AM, Coughlin LE, Mikawa T. 2010. BMP signals promote proepicardial protrusion necessary for recruitment of coronary vessel and epicardial progenitors to the heart. Dev Cell 19:307-316.
22. Jopling C, Sleep E, Raya M, Marti M, Raya A, Izpisua Belmonte JC. 2010. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464:606-609.
23. Katz TC, Singh MK, Degenhardt K, Rivera-Feliciano J, Johnson RL, Epstein JA, Tabin CJ. 2012. Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. Dev Cell 22:639-650.
24. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, Evans T, Macrae CA, Stainier DY, Poss KD. 2010. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464:601-605.
25. Kikuchi K, Holdway JE, Major RJ, Blum N, Dahn RD, Begemann G, Poss KD. 2011. Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev Cell 20:397-404.
26. Kwee L, Baldwin HS, Shen HM, Stewart CL, Buck C, Buck CA, Labow MA. 1995. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121:489-503.
27. Lavine KJ, White AC, Park C, Smith CS, Choi K, Long F, Hui CC, Ornitz DM. 2006. Fibroblast growth factor signals regulate a wave of Hedgehog activation that is essential for coronary vascular development. Genes Dev 20:1651-1666.
28. Lepilina A, Coon AN, Kikuchi K, Holdway JE, Roberts RW, Burns CG, Poss KD. 2006. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127:607-619.
29. Li P, Cavallero S, Gu Y, Chen TH, Hughes J, Hassan AB, Bruning JC, Pashmforoush M, Sucov HM. 2011. IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 138:1795-1805.
30. Limana F, Bertolami C, Mangoni A, Di Carlo A, Avitabile D, Mocini D, Iannelli P, De Mori R, Marchetti C, Pozzoli O, Gentili C, Zacheo A, Germani A, Capogrossi MC. 2010. Myocardial infarction induces embryonic reprogramming of epicardial c-kit(+) cells: role of the pericardial fluid. J Mol Cell Cardiol 48:609-618.
31. Lin SC, Dolle P, Ryckebusch L, Noseda M, Zaffran S, Schneider MD, Niederreither K. 2010. Endogenous retinoic acid regulates cardiac progenitor differentiation. Proc Natl Acad Sci USA 107:9234-9239.
32. Lomeli H, Starling C, Gridley T. 2009. Epiblast-specific Snai1 deletion results in embryonic lethality due to multiple vascular defects. BMC Res Notes 2:22.
33. Martinez-Estrada OM, Lettice LA, Essafi A, Guadix JA, Slight J, Velecela V, Hall E, Reichmann J, Devenney PS, Hohenstein P, Hosen N, Hill RE, Munoz-Chapuli R, Hastie ND. 2010. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat Genet 42:89-93.
34. Nesbitt TL, Roberts A, Tan H, Junor L, Yost MJ, Potts JD, Dettman RW, Goodwin RL. 2009. Coronary endothelial proliferation and morphogenesis are regulated by a VEGF-mediated pathway. Dev Dyn 238:423-430.
35. Ota I, Li XY, Hu Y, Weiss SJ. 2009. Induction of a MT1-MMP and MT2-MMP-dependent basement membrane transmigration program in cancer cells by Snail1. Proc Natl Acad Sci USA 106:20318-20323.
36. Pae SH, Dokic D, Dettman RW. 2008. Communication between integrin receptors facilitates epicardial cell adhesion and matrix organization. Dev Dyn 237:962-978.
37. Peacock JD, Levay AK, Gillaspie DB, Tao G, Lincoln J. 2010. Reduced sox9 function promotes heart valve calcification phenotypes in vivo. Circ Res 106:712-719.
38. Rebustini IT, Myers C, Lassiter KS, Surmak A, Szabova L, Holmbeck K, Pedchenko V, Hudson BG, Hoffman MP. 2009. MT2-MMP-dependent release of collagen IV NC1 domains regulates submandibular gland branching morphogenesis. Dev Cell 17:482-493.
39. Rodgers LS, Lalani S, Runyan RB, Camenisch TD. 2008. Differential growth and multicellular villi direct proepicardial translocation to the developing mouse heart. Dev Dyn 237:145-152.
40. Sanchez NS, Barnett JV. 2012. TGFbeta and BMP-2 regulate epicardial cell invasion via TGFbetaR3 activation of the Par6/Smurf1/RhoA pathway. Cell Signal 24:539-548.
41. Schlueter J, Brand T. 2009. A right-sided pathway involving FGF8/Snai1 controls asymmetric development of the proepicardium in the chick embryo. Proc Natl Acad Sci USA 106:7485-7490.
42. Schlueter J, Brand T. 2012. Epicardial progenitor cells in cardiac development and regeneration. J Cardiovasc Transl Res 5:641-653.
43. Smart N, Bollini S, Dube KN, Vieira JM, Zhou B, Davidson S, Yellon D, Riegler J, Price AN, Lythgoe MF, Pu WT, Riley PR. 2011. De novo cardiomyocytes from within the activated adult heart after injury. Nature 474:640-644.
44. Smart N, Dube KN, Riley PR. 2013. Epicardial progenitor cells in cardiac regeneration and neovascularisation. Vascul Pharmacol 58:164--173.
45. Smith CL, Baek ST, Sung CY, Tallquist MD. 2011. Epicardial-derived cell epithelial-to-mesenchymal transition and fate specification require PDGF receptor signaling. Circ Res 108:e15-26.
46. Tao G, Levay AK, Gridley T, Lincoln J. 2011. Mmp15 is a direct target of Snai1 during endothelial to mesenchymal transformation and endocardial cushion development. Dev Biol 359:209-221.
47. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7:131-142.
48. Thiery JP, Acloque H, Huang RY, Nieto MA. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139:871-890.
49. Timmerman LA, Grego-Bessa J, Raya A, Bertran E, Perez-Pomares JM, Diez J, Aranda S, Palomo S, McCormick F, Izpisua-Belmonte JC, de la Pompa JL. 2004. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 18:99-115.
50. von Gise A, Zhou B, Honor LB, Ma Q, Petryk A, Pu WT. 2011. WT1 regulates epicardial epithelial to mesenchymal transition through beta-catenin and retinoic acid signaling pathways. Dev Biol 356:421-431.
51. Wagner KD, Wagner N, Bondke A, Nafz B, Flemming B, Theres H, Scholz H. 2002. The Wilms' tumor suppressor Wt1 is expressed in the coronary vasculature after myocardial infarction. FASEB J 16:1117-1119.
52. Wu M, Smith CL, Hall JA, Lee I, Luby-Phelps K, Tallquist MD. 2010. Epicardial spindle orientation controls cell entry into the myocardium. Dev Cell 19:114-125.
53. Wu Y, Zhou BP. 2010. Snail: More than EMT. Cell Adh Migr 4:199-203.
54. Yang JT, Rayburn H, Hynes RO. 1995. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 121:549-560.
55. Zamora M, Manner J, Ruiz-Lozano P. 2007. Epicardium-derived progenitor cells require beta-catenin for coronary artery formation. Proc Natl Acad Sci USA 104:18109-18114.
56. Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien KR, Pu WT. 2008. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454:109-113.
57. Zhou B, von Gise A, Ma Q, Hu YW, Pu WT. 2010. Genetic fate mapping demonstrates contribution of epicardium-derived cells to the annulus fibrosis of the mammalian heart. Dev Biol 338:251-261.
58. Zhou B, Honor LB, He H, Ma Q, Oh JH, Butterfield C, Lin RZ, Melero-Martin JM, Dolmatova E, Duffy HS, Gise A, Zhou P, Hu YW, Wang G, Zhang B, Wang L, Hall JL, Moses MA, McGowan FX, Pu WT. 2011. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J Clin Invest 121:1894-1904.