Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Zebrafish Crip2 Plays a Critical Role in Atrioventricular Valve Development by Downregulating the Expression of ECM Genes in the Endocardial Cushion

  • Kim, Jun-Dae (School of Life Science and Biotechnology (Brain Korea 21 plus program), Kyungpook National University) ;
  • Kim, Hey-Jin (School of Life Science and Biotechnology (Brain Korea 21 plus program), Kyungpook National University) ;
  • Koun, Soonil (School of Life Science and Biotechnology (Brain Korea 21 plus program), Kyungpook National University) ;
  • Ham, Hyung-Jin (School of Life Science and Biotechnology (Brain Korea 21 plus program), Kyungpook National University) ;
  • Kim, Myoung-Jin (School of Life Science and Biotechnology (Brain Korea 21 plus program), Kyungpook National University) ;
  • Rhee, Myungchull (Department of Biological Sciences, College of Bioscience and Biotechnology, Chungnam National University) ;
  • Huh, Tae-Lin (School of Life Science and Biotechnology (Brain Korea 21 plus program), Kyungpook National University)
  • Received : 2014.03.27
  • Accepted : 2014.04.28
  • Published : 2014.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

The initial step of atrioventricular (AV) valve development involves the deposition of extracellular matrix (ECM) components of the endocardial cushion and the endocardialmesenchymal transition. While the appropriately regulated expression of the major ECM components, Versican and Hyaluronan, that form the endocardial cushion is important for heart valve development, the underlying mechanism that regulates ECM gene expression remains unclear. We found that zebrafish crip2 expression is restricted to a subset of cells in the AV canal (AVC) endocardium at 55 hours post-fertilization (hpf). Knockdown of crip2 induced a heart-looping defect in zebrafish embryos, although the development of cardiac chambers appeared to be normal. In the AVC of Crip2-deficient embryos, the expression of both versican a and hyaluronan synthase 2 (has2) was highly upregulated, but the expression of bone morphogenetic protein 4 (bmp4) and T-box 2b (tbx2b) in the myocardium and of notch1b in the endocardium in the AVC did not change. Taken together, these results indicate that crip2 plays an important role in AV valve development by downregulating the expression of ECM components in the endocardial cushion.

Keywords

References

  1. Armstrong, E.J., and Bischoff, J. (2004). Heart valve development: endothelial cell signaling and differentiation. Circ. Res. 95, 459-470. https://doi.org/10.1161/01.RES.0000141146.95728.da
  2. Beis, D., Bartman, T., Jin, S.W., Scott, I.C., D'Amico, 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. https://doi.org/10.1242/dev.01970
  3. Camenisch, T.D., Spicer, A.P., Brehm-Gibson, T., Biesterfeldt, J., Augustine, M.L., Calabro, A., Kubalak, S., Klewer, S.E., and McDonald, J.A. (2000). Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronanmediated transformation of epithelium to mesenchyme. J. Clin. Invest. 106, 349-360. https://doi.org/10.1172/JCI10272
  4. Combs, M.D., and Yutzey, K.E. (2009). Heart valve development: regulatory networks in development and disease. Circ. Res. 105, 408-421. https://doi.org/10.1161/CIRCRESAHA.109.201566
  5. Delot, E.C. (2003). Control of endocardial cushion and cardiac valve maturation by BMP signaling pathways. Mol. Genet. Metab. 80, 27-35. https://doi.org/10.1016/j.ymgme.2003.07.004
  6. Hu, N., Sedmera, D., Yost, H.J., and Clark, E.B. (2000). Structure and function of the developing zebrafish heart. Anat. Rec. 260, 148-157. https://doi.org/10.1002/1097-0185(20001001)260:2<148::AID-AR50>3.0.CO;2-X
  7. 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. https://doi.org/10.1002/dvdy.10356
  8. Hurlstone, A.F., Haramis, A.P., Wienholds, E., Begthel, H., Korving, J., Van Eeden, F., Cuppen, E., Zivkovic, D., Plasterk, R.H., and Clevers, H. (2003). The Wnt/beta-catenin pathway regulates cardiac valve formation. Nature 425, 633-637. https://doi.org/10.1038/nature02028
  9. Jiao, K., Kulessa, H., Tompkins, K., Zhou, Y., Batts, L., Baldwin, H.S., and Hogan, B.L. (2003) An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev. 17, 2362-2367. https://doi.org/10.1101/gad.1124803
  10. Jin, S.W., Beis, D., Mitchell, T., Chen, J.N., and Stainier, D.Y. (2005). Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132, 5199-5209. https://doi.org/10.1242/dev.02087
  11. Jowett, T., and Lettice, L. (1994). Whole-mount in situ hybridizations on zebrafish embryos using a mixture of digoxigenin- and fluorescein-labelled probes. Trends Genet. 10, 73-74. https://doi.org/10.1016/0168-9525(94)90220-8
  12. Karim, M.A., Ohta, K., Egashira, M., Jinno, Y., Niikawa, N., Matsuda, I., and Indo, Y. (1996). Human ESP1/CRP2, a member of the LIM domain protein family: characterization of the cDNA and assignment of the gene locus to chromosome 14q32.3. Genomics 31, 167-176. https://doi.org/10.1006/geno.1996.0028
  13. Kihara, T., Shinohara, S., Fujikawa, R., Sugimoto, Y., Murata, M., and Miyake, J. (2011). Regulation of cysteine-rich protein 2 localization by the development of actin fibers during smooth muscle cell differentiation. Biochem. Biophys. Res. Commun. 411, 96-101. https://doi.org/10.1016/j.bbrc.2011.06.100
  14. Kim, J.D., and Kim, J. (2014). Alk3/Alk3b and Smad5 Mediate BMP signaling during lymphatic development in zebrafish. Mol. Cells 37, 270-274. https://doi.org/10.14348/molcells.2014.0005
  15. Kim, J.D., Kang, H., Larrivee, B., Lee, M.Y., Mettlen, M., Schmid, S.L., Roman, B.L., Qyang, Y., Eichmann, A., and Jin, S.W. (2012a). Context-dependent proangiogenic function of bone morphogenetic protein signaling is mediated by disabled homolog 2. Dev. Cell 23, 441-448. https://doi.org/10.1016/j.devcel.2012.07.007
  16. Kim, Y.S., Kim, M.J., Koo, T.H., Kim, J.D., Koun, S., Ham, H.J., Lee, Y.M., Rhee, M., Yeo, S.Y., and Huh, T.L. (2012b). Histone deacetylase is required for the activation of Wnt/$\beta$-catenin signaling crucial for heart valve formation in zebrafish embryos. Biochem. Biophys. Res. Commun. 423, 140-146. https://doi.org/10.1016/j.bbrc.2012.05.098
  17. Kim, J.D., Kang, Y., Kim, J., Papangeli, I., Kang, H., Wu, J., Park, H., Nadelmann, E., Rockson, S.G., Chun, H.J., et al. (2013a). Essential role of Apelin signaling during lymphatic development in zebrafish. Arterioscler. Thromb. Vasc. Biol. 34, 338-345.
  18. Kim, S.H., Schmitt, C.E., Woolls, M.J., Holland, M.B., Kim, J.D., and Jin, S.W. (2013b). Vascular endothelial growth factor signaling regulates the segregation of artery and vein via ERK activity during vascular development. Biochem. Biophys. Res. Commun. 430, 1212-1216. https://doi.org/10.1016/j.bbrc.2012.12.076
  19. Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., and Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310. https://doi.org/10.1002/aja.1002030302
  20. Krug, E.L., Runyan, R.B., and Markwald, R.R. (1985). Protein extracts from early embryonic hearts initiate cardiac endothelial cytodifferentiation. Dev. Biol. 112, 414-426. https://doi.org/10.1016/0012-1606(85)90414-2
  21. Larson, J.D., Wadman, S.A., Chen, E., Kerley, L., Clark, K.J., Eide, M., Lippert, S., Nasevicius, A., Ekker, S.C., Hackett, P.B., et al. (2004). Expression of VE-cadherin in zebrafish embryos: a new tool to evaluate vascular development. Dev. Dyn. 231, 204-213. https://doi.org/10.1002/dvdy.20102
  22. Ma, L., Lu, M.F., Schwartz, R.J., and Martin, J.F. (2005). Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132, 5601-5611. https://doi.org/10.1242/dev.02156
  23. Mjaatvedt, C.H., Yamamura, H., Capehart, A.A., Turner, D., and Markwald, R.R. (1998). The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev. Biol. 202, 56-66. https://doi.org/10.1006/dbio.1998.9001
  24. Nakajima, Y., Yamagishi, T., Hokari, S., and Nakamura, H. (2000) Mechanisms involved in valvuloseptal endocardial cushion formation in early cardiogenesis: roles of transforming growth factor (TGF)-beta and bone morphogenetic protein (BMP). Anat. Rec. 258, 119-127. https://doi.org/10.1002/(SICI)1097-0185(20000201)258:2<119::AID-AR1>3.0.CO;2-U
  25. Schroeder, J.A., Jackson, L.F., Lee, D.C., and Camenisch, T.D. (2003). Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling. J. Mol. Med. 81, 392-403. https://doi.org/10.1007/s00109-003-0456-5
  26. 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. https://doi.org/10.1101/sqb.2002.67.49
  27. Sun, X., Zhang, R., Lin, X., and Xu, X. (2008) Wnt3a regulates the development of cardiac neural crest cells by modulating expression of cysteine-rich intestinal protein 2 in rhombomere 6. Circ. Res. 102, 831-839. https://doi.org/10.1161/CIRCRESAHA.107.166488
  28. Timmerman, L.A., Grego-Bessa, J., Raya, A., Bertran, E., Perez-Pomares, J.M., Diez, J., Aranda, S., Palomo, S., McCormick, F., Izpisua-Belmonte, J.C., et al. (2004) Notch promotes epithelialmesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 18, 99-115. https://doi.org/10.1101/gad.276304
  29. Tsui, S.K., Chan, P.P., Cheuk, C.W., Liew, C.C., Waye, M.M., Fung, K.P., and Lee, C.Y. (1996) A novel cDNA encoding for a LIM domain protein located at human chromosome 14q32 as a candidate for leukemic translocation. Biochem. Mol. Biol. Int. 39, 747-754.
  30. van Ham, M., Croes, H., Schepens, J., Fransen, J., Wieringa, B., and Hendriks, W. (2003) Cloning and characterization of mCRIP2, a mouse LIM-only protein that interacts with PDZ domain IV of PTP-BL. Genes Cells 8, 631-644. https://doi.org/10.1046/j.1365-2443.2003.00660.x
  31. Walsh, E.C., and Stainier, D.Y. (2001) UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 293, 1670-1673. https://doi.org/10.1126/science.293.5535.1670
  32. 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. https://doi.org/10.1006/dbio.1999.9406

Cited by

  1. Proper Activity of Histone H3 Lysine 4 (H3K4) Methyltransferase Is Required for Morphogenesis during Zebrafish Cardiogenesis vol.38, pp.6, 2015, https://doi.org/10.14348/molcells.2015.0053
  2. Amplified pathogenic actions of angiotensin II in cysteine-rich LIM-only protein 4–negative mouse hearts vol.31, pp.4, 2017, https://doi.org/10.1096/fj.201601186
  3. Knockout of hyaluronan synthase 1, but not 3, impairs formation of the retrocalcaneal bursa pp.07360266, 2018, https://doi.org/10.1002/jor.24027
  4. A Transcriptome Study of Progeroid Neurocutaneous Syndrome Reveals POSTN As a New Element in Proline Metabolic Disorder vol.9, pp.6, 2014, https://doi.org/10.14336/ad.2018.0222
  5. Knockout of tnni1b in zebrafish causes defects in atrioventricular valve development via the inhibition of the myocardial wnt signaling pathway vol.33, pp.1, 2019, https://doi.org/10.1096/fj.201800481rr
  6. Aging-regulated anti-apoptotic long non-coding RNA Sarrah augments recovery from acute myocardial infarction vol.11, pp.1, 2014, https://doi.org/10.1038/s41467-020-15995-2
  7. Protective effect of Ganoderma lucidum spore extract in trimethylamine‐ N ‐oxide‐induced cardiac dysfunction in rats vol.86, pp.2, 2014, https://doi.org/10.1111/1750-3841.15575