Thymosin beta4 regulates cardiac valve formation via endothelial- mesenchymal transformation in zebrafish embryos

Molecules and Cells

Volumn 37, Issue 4, 2014, Pages 330-336

  Shin, Sun Hye ^a   Lee, Sangkyu ^a   Bae, Jong Sup ^a   Jee, Jun Goo ^a   Cha, Hee Jae ^b   Lee, You Mie ^a  

^a Kyungpook National University   (South Korea)

^b Kosin University College of Medicine   (South Korea)

Author keywords

Endothelial mesenchymal transformation; Heart valve formation; Thymosin beta4; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; HYALURONAN SYNTHASE 2; HYALURONIC ACID BINDING PROTEIN; NOTCH1 RECEPTOR; NOTCH1B PROTEIN; SMALL INTERFERING RNA; THYMOSIN BETA4; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ANTISENSE OLIGONUCLEOTIDE; THYMOSIN; THYMOSIN BETA(4);

ANIMAL CELL; ARTICLE; ATRIOVENTRICULAR CANAL; CARDIAC VALVE FORMATION; CELL TRANSFORMATION; CONTROLLED STUDY; EMBRYO; ENDOCARDIAL CUSHION; ENDOCARDIUM; ENDOTHELIAL MESENCHYMAL TRANSFORMATION; ENDOTHELIUM CELL; HEART DEVELOPMENT; HEART VALVE; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; LATERAL PLATE MESODERM; MARKER GENE; MESODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEEP; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; BOVINAE; CELL DIFFERENTIATION; CELL LINE; EMBRYO DEVELOPMENT; EMBRYOLOGY; ENDOTHELIUM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; ORGANOGENESIS; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CATTLE; CELL DIFFERENTIATION; CELL LINE; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOTHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART VALVES; HUMANS; MESODERM; OLIGONUCLEOTIDES, ANTISENSE; ORGANOGENESIS; RNA, SMALL INTERFERING; SHEEP; THYMOSIN; TRANSFORMING GROWTH FACTOR BETA; ZEBRAFISH;

EID: 84901453347     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2014.0003     Document Type: Article

References (36)

1. Armstrong, E.J., and Bischoff, J. (2004). Heart valve development: endothelial cell signaling and differentiation. Circ. Res. 95, 459-470. (Pubitemid 39180926)
2. Bakkers, J. (2011). Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc. Res. 91, 279-288.
3. Bakkers, J., Verhoeven, M.C., and Abdelilah-Seyfried, S. (2009). Shaping the zebrafish heart: from left-right axis specification to epithelial tissue morphogenesis. Dev. Biol. 330, 213-220.
4. Beis, D., Bartman, T., Jin, S.W., Scott, I.C., D'mico, L.A., Ober, E.A., Verkade, H., Frantsve, J., Field, H.A., Wehman, A., et al. (2005). Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development 132, 4193-4204. (Pubitemid 41488867)
5. Bock-Marquette, I., Saxena, A., White, M.D., DiMaio, J.M., and Srivastava, D. (2004). Thymosin β4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432, 466-472. (Pubitemid 39576522)
6. Bock-Marquette, I., Shrivastava, S., Pipes, G., Thatcher, J.E., Blystone, A., Shelton, J.M., Galindo, C.L., Melegh, B., Srivastava, D., and Olson, E.N. (2009). Thymosin β4 mediated PKC activation is essential to initiate the embryonic coronary developmental program and epicardial progenitor cell activation in adult mice in vivo. J. Mol. Cell. Cardiol. 46, 728-738.
7. Derynck, R., and Zhang, Y.E. (2003). Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425, 577-584. (Pubitemid 37280136)
8. Dube, K.N., Bollini, S., Smart, N., and Riley, P.R. (2012). Thymosin beta4 protein therapy for cardiac repair. Curr. Pharm. Des. 18, 799-806.
9. Goldstein, A.L., Hannappel, E., Sosne, G., and Kleinman, H.K. (2012). Thymosin β4: a multi-functional regenerative peptide. Basic properties and clinical applications. Exp. Opin. Biol. Ther. 12, 37-51.
10. Gomez-Marquez, J., Franco del Amo, F., Carpintero, P., and Anadon, R. (1996). High levels of mouse thymosin β4 mRNA in differentiating P19 embryonic cells and during evelopment of cardiovascular tissues. Biochim. Biophys. Acta 1306, 187-193. (Pubitemid 26155067)
11. Huang, C.J., Tu, C.T., Hsiao, C.D., Hsieh, F.J., and Tsai, H.J. (2003). Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev. Dyn. 228, 30-40.
12. Huff, T., Müller, C.S., Otto, A.M., Netzker, R., and Hannappel, E. (2001). β-Thymosins, small acidic peptides with multiple functions. Int. J. Biochem. Cell Biol. 33, 205-220. (Pubitemid 32304390)
13. Jang, G.H., Park, I.S., Yang, J.H., Bischoff, J., and Lee, Y.M. (2010). Differential functions of genes regulated by VEGF-NFATc1 signaling pathway in the migration of pulmonary valve endothelial cells. FEBS Lett. 584, 141-146.
14. Ji, Y.I., Lee, B.Y., Kang, Y.J., Jo, J.O., Lee, S.H., Kim, H.Y., Kim, Y.O., Lee, C., Koh, S.B., Kim, A., et al. (2013). Expression patterns of Thymosin β4 and cancer stem cell marker CD133 in ovarian cancers. Pathol. Oncol. Res. 19, 237-245.
15. Jin, S.W., Beis, D., Mitchell, T., Chen, J.N., and Stainier, D.Y.R. (2005). Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132, 5199-5209. (Pubitemid 43020175)
16. Johnson, E.N., Lee, Y.M., Sander, T.L., Rabkin, E., Schoen, F.J., Kaushal, S., and Bischoff, J. (2003). NFATc1 mediates vascular endothelial growth factor-induced proliferation of human pulmonary valve endothelial cells. J. Biol. Chem. 278, 1686-1692. (Pubitemid 36801401)
17. Kim, S.H., Shin, J., Park, H.C., Yeo, S.Y., Hong, S.K., Han, S., Rhee, M., Kim, C.H., Chitnis, A.B., and Huh, T.L. (2002). Specification of an anterior neuroectoderm patterning by Frizzled8a-mediated Wnt8b signalling during late gastrulation in zebrafish. Development 129, 4443-4455. (Pubitemid 35203728)
18. Lee, Y.M., Cope, J.J., Ackermann, G.E., Goishi, K., Armstrong, E.J., Paw, B.H., and Bischoff, J. (2006). Vascular endothelial growth factor receptor signaling is required for cardiac valve formation in zebrafish. Dev. Dyn. 235, 29-37. (Pubitemid 46939700)
19. Lee, S.I., Kim, D.S., Lee, H.J., Cha, H.J., and Kim, E.C. (2013). The role of thymosin beta 4 on odontogenic differentiation in human dental pulp cells. PLoS One 8, e61960.
20. Li, Q., Jones, P., Lafferty, R., Safer, D., and Levy, R. (2002). Thymosin beta4 regulation, expression and function in aortic valve interstitial cells. J. Heart Valve Dis. 11, 726-735.
21. Malinda, K., Goldstein, A., and Kleinman, H. (1997). Thymosin beta 4 stimulates directional migration of human umbilical vein endothelial cells. FASEB J. 11, 474-481. (Pubitemid 27259989)
22. Malinda, K.M., Sidhu, G.S., Mani, H., Banaudha, K., Maheshwari, R.K., Goldstein, A.L., and Kleinman, H.K. (1999). Thymosin β4 accelerates wound healing. J. Invest. Dermatol. 113, 364-368.
23. Markwald, R.R., Fitzharris, T.P., and Manasek, F.J. (1977). Structural development of endocardial cushions. Am. J. Anat. 148, 85-119. (Pubitemid 8034351)
24. Milan, D.J., Giokas, A.C., Serluca, F.C., Peterson, R.T., and MacRae, C.A. (2006). Notch1b and neuregulin are required for specification of central cardiac conduction tissue. Development 133, 1125-1132.
25. Paranya, G., Vineberg, S., Dvorin, E., Kaushal, S., Roth, S.J., Rabkin,E., Schoen, F.J., and Bischoff, J. (2001). Aortic valve endothelial cells undergo transforming growth factor-beta-mediated and non-transforming growth factor-beta-mediated transdifferentiation in vitro. Am. J. Pathol. 159, 1335-1343. (Pubitemid 32947963)
26. Smart, N., Risebro, C.A., Melville, A.A., Moses, K., Schwartz, R.J., Chien, K.R., and Riley, P.R. (2006). Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 445, 177-182. (Pubitemid 46095717)
27. Smart, N., Bollini, S., Dubé, K.N., Vieira, J.M., Zhou, B., Davidson, S., Yellon, D., Riegler, J., Price, A.N., and Lythgoe, M.F. (2011). De novo cardiomyocytes from within the activated adult heart after injury. Nature 474, 640-644.
28. Sosne, G., Szliter, E.A., Barrett, R., Kernacki, K.A., Kleinman, H., and Hazlett, L.D. (2002). Thymosin beta 4 promotes corneal wound healing and decreases inflammation in vivo following alkali injury. Exp. Eye Res. 74, 293-299. (Pubitemid 34948404)
29. Sosne, G., Xu, L., Prach, L., Mrock, L.K., Kleinman, H.K., Letterio, J.J., Hazlett, L.D., and Kurpakus-Wheater, M. (2004). Thymosin beta 4 stimulates laminin-5 production independent of TGF-beta. Exp. Cell Res. 293, 175-183. (Pubitemid 38064424)
30. Sribenja, S., Wongkham, S., Wongkham, C., Yao, Q., and Chen, C. (2013). Roles and mechanisms of β-thymosins in cell migration and cancer metastasis: an update. Cancer Invest. 31, 103-110.
31. Stainier, D.Y., Beis, D., Jungblut, B., and Bartman, T. (2002). Endocardial cushion formation in zebrafish. Cold Spring Harb. Symp. Quant. Biol. 67, 49-56. (Pubitemid 36775494)
32. Stankunas, K., Ma, G.K., Kuhnert, F.J., Kuo, C.J., and Chang, C.P. (2010). VEGF signaling has distinct spatiotemporal roles during heart valve development. Dev. Biol. 347, 325-336.
33. Thatcher, J.E., Welch, T., Eberhart, R.C., Schelly, Z.A., and Michael DiMaio, J. (2012). Thymosin β4 sustained release from poly (lactide-co-glycolide) microspheres: synthesis and implications for treatment of myocardial ischemia. Ann. N Y Acad. Sci. 1270, 112-119.
34. Westerfield, M. (1993). The zebrafish book: a guide for the laboratory use of zebrafish (Brachydanio rerio), (University of Oregon Press, USA).
35. Yang, J.H., Wylie-Sears, J., and Bischoff, J. (2008). Opposing actions of Notch1 and VEGF in post-natal cardiac valve endothelial cells. Biochem. Biophys. Res. Commun. 374, 512-516.
36. Yelon, D., Horne, S.A., and Stainier, D.Y. (1999). Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 214, 23-37. (Pubitemid 29463353)