PRSS23 is essential for the Snail-dependent endothelial-to-mesenchymal transition during valvulogenesis in zebrafish

Cardiovascular Research

Volumn 97, Issue 3, 2013, Pages 443-453

  Chen, I Hui ^a   Wang, Hsueh Hsiao ^b   Hsieh, Yi Shan ^a   Huang, Wei Chang ^a   Yeh, Hung I ^b   Chuang, Yung Jen ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b MACKAY MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Cardiac valve formation; EndoMT; PRSS23; Snail; Zebrafish

Indexed keywords

FLUORESCENT DYE; MORPHOLINO OLIGONUCLEOTIDE; SERINE PROTEINASE; SERINE PROTEINASE PRSS23; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; ARTERY ENDOTHELIUM; ARTICLE; ATRIOVENTRICULAR CANAL; CELL ASSAY; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOCARDIAL CUSHION DEFECT; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE SEQUENCE; GENE SILENCING; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; HEART ATRIUM; HEART DEVELOPMENT; HEART VALVE; HEART VENTRICLE; HUMAN; HUMAN CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL; VASCULARIZATION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HEART VALVES; HUMANS; MODELS, ANIMAL; MORPHOLINOS; RNA, SMALL INTERFERING; SERINE PROTEASES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA2; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84874251061     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs355     Document Type: Article

References (38)

1. Loffredo CA. Epidemiology of cardiovascular malformations: prevalence and risk factors. Am J Med Genet 2000;97:319-325.
2. Pierpont ME, Basson CT, Benson DW Jr, Gelb BD, Giglia TM, Goldmuntz E et al. Genetic basis for congenital heart defects: current knowledge: a scientific statement from the American Heart Association Congenital Cardiac Defects Committee, Council on Cardiovascular Disease in the Young: endorsed by the American Academy of Pediatrics. Circulation 2007;115:3015-3038.
3. Stainier DY. Zebrafish genetics and vertebrate heart formation. Nat Rev Genet 2001; 2:39-48.
4. Armstrong EJ, Bischoff J. Heart valve development: endothelial cell signaling and differentiation. Circ Res 2004;95:459-470.
5. Combs MD, Yutzey KE. Heart valve development: regulatory networks in development and disease. Circ Res 2009;105:408-421.
6. Wagner M, Siddiqui MA. Signal transduction in early heart development (II): ventricular chamber specification, trabeculation, and heart valve formation. Exp Biol Med (Maywood) 2007;232:866-880.
7. Romano LA, Runyan RB. Slug is an essential target of TGFbeta2 signaling in the developing chicken heart. Dev Biol 2000;223:91-102.
8. Wang J, Sridurongrit S, Dudas M, Thomas P, Nagy A, Schneider MD et al. Atrioventricular cushion transformation is mediated by ALK2 in the developing mouse heart. Dev Biol 2005;286:299-310.
9. Timmerman LA, Grego-Bessa J, Raya A, Bertran E, Perez-Pomares JM, Diez J et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 2004;18:99-115.
10. Niessen K, Fu Y, Chang L, Hoodless PA, McFadden D, Karsan A. Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J Cell Biol 2008; 182:315-325.
11. Bakkers J. Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res 2011;91:279-288.
12. Stainier DY, Fishman MC. The zebrafish as a model system to study cardiovascular development. Trends Cardiovasc Med 1994;4:207-212.
13. Beis D, Bartman T, Jin SW, Scott IC, D'Amico LA, Ober EA et al. Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development 2005;132:4193-4204.
14. Wahlberg P, Nylander A, Ahlskog N, Liu K, Ny T. Expression and localization of the serine proteases high-temperature requirement factor A1, serine protease 23, and serine protease 35 in the mouse ovary. Endocrinology 2008;149:5070-5077.
15. Chan HS, Chang SJ, Wang TY, Ko HJ, Lin YC, Lin KT et al. Serine protease PRSS23 is upregulated by estrogen receptor alpha and associated with proliferation of breast cancer cells. PLoS One 2012;7:e30397.
16. AG BH. PRSS23 as a biomaker, therapeutic an diagnostc target. Patent Cooperation Treaty (PCT). EUROPE, 2007.
17. Wang CH, Chen IH, Kuo MW, Su PT, Lai ZY, Huang WC et al. Zebrafish Thsd7a is a neural protein required for angiogenic patterning during development. Dev Dyn 2011; 240:1412-1421.
18. Huang WC, Hsieh YS, Chen IH,Wang CH, Chang HW, Yang CC et al. Combined use of MS-222 (tricaine) and isoflurane extends anesthesia time and minimizes cardiac rhythm side effects in adult zebrafish. Zebrafish 2010;7:297-304.
19. Kokudo T, Suzuki Y, Yoshimatsu Y, Yamazaki T, Watabe T, Miyazono K. Snail is required for TGFbeta-induced endothelial-mesenchymal transition of embryonic stem cell-derived endothelial cells. J Cell Sci 2008;121:3317-3324.
20. Wang CH, Su PT, Du XY, Kuo MW, Lin CY, Yang CC et al. Thrombospondin type I domain containing 7A (THSD7A) mediates endothelial cell migration and tube formation. J Cell Physiol 2010;222:685-694.
21. Ribeiro I, Kawakami Y, Buscher D, Raya A, Rodriguez-Leon J, Morita M et al. Tbx2 and Tbx3 regulate the dynamics of cell proliferation during heart remodeling. PLoS One 2007;2:e398.
22. Walsh EC, Stainier DY. UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 2001;293:1670-1673.
23. Hurlstone AF, Haramis AP, Wienholds E, Begthel H, Korving J, Van Eeden F et al. The Wnt/beta-catenin pathway regulates cardiac valve formation. Nature 2003; 425:633-637.
24. Butcher JT, Markwald RR. Valvulogenesis: the moving target. Philos Trans R Soc Lond B Biol Sci 2007;362:1489-1503.
25. Zeisberg EM, Tarnavski O, Zeisberg M, Dorfman AL, McMullen JR, Gustafsson E et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007; 13:952-961.
26. Paruchuri S, Yang JH, Aikawa E, Melero-Martin JM, Khan ZA, Loukogeorgakis S et al. Human pulmonary valve progenitor cells exhibit endothelial/mesenchymal plasticity in response to vascular endothelial growth factor-A and transforming growth factorbeta2. Circ Res 2006;99:861-869.
27. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H et al. A human protein-protein interaction network: a resource for annotating the proteome. Cell 2005;122:957-968.
28. Lee CC, Chen WS, Chen CC, Chen LL, Lin YS, Fan CS et al. TCF12 protein functions as transcriptional repressor of E-cadherin, and its overexpression is correlated with metastasis of colorectal cancer. J Biol Chem 2012;287: 2798-2809.
29. Jiao K, Kulessa H, Tompkins K, Zhou Y, Batts L, Baldwin HS et al. An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev 2003; 17:2362-2367.
30. Ma L, Lu MF, Schwartz RJ, Martin JF. Bmp2 is essential for cardiac cushion epithelialmesenchymal transition and myocardial patterning. Development 2005;132: 5601-5611.
31. Noseda M, McLean G, Niessen K, Chang L, Pollet I, Montpetit R et al. Notch activation results in phenotypic and functional changes consistent with endothelial-to-mesenchymal transformation. Circ Res 2004;94:910-917.
32. MacGrogan D, Luna-Zurita L, de la Pompa JL. Notch signaling in cardiac valve development and disease. Birth Defects Res A Clin Mol Teratol 2011;91:449-459.
33. Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 2005;21:659-693.
34. Goumans MJ, van Zonneveld AJ, ten Dijke P. Transforming growth factor beta-induced endothelial-to-mesenchymal transition: a switch to cardiac fibrosis? Trends Cardiovasc Med 2008;18:293-298.
35. Rivera-Feliciano J, Lee KH, Kong SW, Rajagopal S, Ma Q, Springer Z et al. Development of heart valves requires Gata4 expression in endothelial-derived cells. Development 2006;133:3607-3618.
36. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007;7:415-428.
37. Cano A, Portillo F. An emerging role for class I bHLH E2-2 proteins in EMT regulation and tumor progression. Cell Adhes Migr 2010;4:56-60.
38. Sobrado VR, Moreno-Bueno G, Cubillo E, Holt LJ, Nieto MA, Portillo F et al. The class I bHLH factors E2-2A and E2-2B regulate EMT. J Cell Sci 2009;122:1014-1024.