The zebrafish as a tool to identify novel therapies for human cardiovascular disease

DMM Disease Models and Mechanisms

Volumn 7, Issue 7, 2014, Pages 763-767

  Asnani, Aarti ^a   Peterson, Randall T ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Cardiovascular; Drug discovery; Zebrafish

Indexed keywords

ANGIOGENESIS; CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL REGENERATION; HEART DEVELOPMENT; HEART MUSCLE CELL; HIGH THROUGHPUT SCREENING; NONHUMAN; PRIORITY JOURNAL; REVIEW; ZEBRA FISH; ANIMAL; BLOOD VESSEL; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; DISEASE MODEL; EMBRYOLOGY; HEART; HUMAN; METABOLISM; PATHOLOGY;

ANIMALS; BLOOD VESSELS; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; DISEASE MODELS, ANIMAL; HEART; HUMANS; ZEBRAFISH;

EID: 84904002179     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.016170     Document Type: Review

References (61)

1. Banjo, T., Grajcarek, J., Yoshino, D., Osada, H., Miyasaka, K. Y., Kida, Y. S., Ueki, Y., Nagayama, K., Kawakami, K., Matsumoto, T. et al. (2013). Haemodynamically dependent valvulogenesis of zebrafish heart is mediated by flow-dependent expression of miR-21. Nat. Commun. 4, 1978.
2. Bartman, T., Walsh, E. C., Wen, K. K., McKane, M., Ren, J., Alexander, J., Rubenstein, P. A. and Stainier, D. Y. (2004). Early myocardial function affects endocardial cushion development in zebrafish. PLoS Biol. 2, e129.
3. Bedell, V. M., Wang, Y., Campbell, J. M., Poshusta, T. L., Starker, C. G., Krug, R. G., II, Tan, W., Penheiter, S. G., Ma, A. C., Leung, A. Y. et al. (2012). In vivo genome editing using a high-efficiency TALEN system. Nature 491, 114-118.
4. 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. (Pubitemid 41488867)
5. Benson, D. W., Silberbach, G. M., Kavanaugh-McHugh, A., Cottrill, C., Zhang, Y., Riggs, S., Smalls, O., Johnson, M. C., Watson, M. S., Seidman, J. G. et al. (1999). Mutations in the cardiac transcription factor NKX2.5 affect diverse cardiac developmental pathways. J. Clin. Invest. 104, 1567-1573. (Pubitemid 30002368)
6. Biben, C., Weber, R., Kesteven, S., Stanley, E., McDonald, L., Elliott, D. A., Barnett, L., Köentgen, F., Robb, L., Feneley, M. et al. (2000). Cardiac septal and valvular dysmorphogenesis in mice heterozygous for mutations in the homeobox gene Nkx2-5. Circ. Res. 87, 888-895.
7. Buckingham, M., Meilhac, S. and Zaffran, S. (2005). Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 6, 826-837.
8. Chen, J. N., Haffter, P., Odenthal, J., Vogelsang, E., Brand, M., van Eeden, F. J., Furutani-Seiki, M., Granato, M., Hammerschmidt, M., Heisenberg, C. P. et al. (1996). Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development 123, 293-302. (Pubitemid 27056756)
9. Chen, M. H., Kerkelä, R. and Force, T. (2008). Mechanisms of cardiac dysfunction associated with tyrosine kinase inhibitor cancer therapeutics. Circulation 118, 84-95.
10. Cheng, H., Kari, G., Dicker, A. P., Rodeck, U., Koch, W. J. and Force, T. (2011). A novel preclinical strategy for identifying cardiotoxic kinase inhibitors and mechanisms of cardiotoxicity. Circ. Res. 109, 1401-1409.
11. Chi, N. C., Shaw, R. M., Jungblut, B., Huisken, J., Ferrer, T., Arnaout, R., Scott, I., Beis, D., Xiao, T., Baier, H. et al. (2008). Genetic and physiologic dissection of the vertebrate cardiac conduction system. PLoS Biol. 6, e109.
12. Choi, W. Y., Gemberling, M., Wang, J., Holdway, J. E., Shen, M. C., Karlstrom, R. O. and Poss, K. D. (2013). In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development 140, 660-666.
13. Combs, M. D. and Yutzey, K. E. (2009). Heart valve development: regulatory networks in development and disease. Circ. Res. 105, 408-421.
14. Corti, P., Young, S., Chen, C. Y., Patrick, M. J., Rochon, E. R., Pekkan, K. and Roman, B. L. (2011). Interaction between alk1 and blood flow in the development of arteriovenous malformations. Development 138, 1573-1582.
15. Cuny, G. D., Yu, P. B., Laha, J. K., Xing, X., Liu, J. F., Lai, C. S., Deng, D. Y., Sachidanandan, C., Bloch, K. D. and Peterson, R. T. (2008). Structure-activity relationship study of bone morphogenetic protein (BMP) signaling inhibitors. Bioorg. Med. Chem. Lett. 18, 4388-4392.
16. de Pater, E., Clijsters, L., Marques, S. R., Lin, Y. F., Garavito-Aguilar, Z. V., Yelon, D. and Bakkers, J. (2009). Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. Development 136, 1633-1641.
17. Derwall, M., Malhotra, R., Lai, C. S., Beppu, Y., Aikawa, E., Seehra, J. S., Zapol, W. M., Bloch, K. D. and Yu, P. B. (2012). Inhibition of bone morphogenetic protein signaling reduces vascular calcification and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 32, 613-622.
18. Driever, W., Solnica-Krezel, L., Schier, A. F., Neuhauss, S. C., Malicki, J., Stemple, D. L., Stainier, D. Y., Zwartkruis, F., Abdelilah, S., Rangini, Z. et al. (1996). A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123, 37-46. (Pubitemid 27056734)
19. Elliott, D. A., Kirk, E. P., Yeoh, T., Chandar, S., McKenzie, F., Taylor, P., Grossfeld, P., Fatkin, D., Jones, O., Hayes, P. et al. (2003). Cardiac homeobox gene NKX2-5 mutations and congenital heart disease: associations with atrial septal defect and hypoplastic left heart syndrome. J. Am. Coll. Cardiol. 41, 2072-2076. (Pubitemid 36677134)
20. Hami, D., Grimes, A. C., Tsai, H. J. and Kirby, M. L. (2011). Zebrafish cardiac development requires a conserved secondary heart field. Development 138, 2389-2398.
21. Heinke, J., Juschkat, M., Charlet, A., Mnich, L., Helbing, T., Bode, C., Patterson, C. and Moser, M. (2013). Antagonism and synergy between extracellular BMP modulators Tsg and BMPER balance blood vessel formation. J. Cell Sci. 126, 3082-3094.
22. Herman, D. S., Lam, L., Taylor, M. R., Wang, L., Teekakirikul, P., Christodoulou, D., Conner, L., DePalma, S. R., McDonough, B., Sparks, E. et al. (2012). Truncations of titin causing dilated cardiomyopathy. N. Engl. J. Med. 366, 619-628.
23. Hershman, D. L., McBride, R. B., Eisenberger, A., Tsai, W. Y., Grann, V. R. and Jacobson, J. S. (2008). Doxorubicin, cardiac risk factors, and cardiac toxicity in elderly patients with diffuse B-cell non-Hodgkin's lymphoma. J. Clin. Oncol. 26, 3159-3165.
24. Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., Collins, J. E., Humphray, S., McLaren, K., Matthews, L. et al. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498-503.
25. Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., Peterson, R. T., Yeh, J. R. and Joung, J. K. (2013). Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol. 31, 227-229.
26. Jensen, B., Boukens, B. J., Postma, A. V., Gunst, Q. D., van den Hoff, M. J., Moorman, A. F., Wang, T. and Christoffels, V. M. (2012). Identifying the evolutionary building blocks of the cardiac conduction system. PLoS ONE 7, e44231.
27. Johnson, D. W., Berg, J. N., Baldwin, M. A., Gallione, C. J., Marondel, I., Yoon, S. J., Stenzel, T. T., Speer, M., Pericak-Vance, M. A., Diamond, A. et al. (1996). Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat. Genet. 13, 189-195.
28. Jopling, C., Sleep, E., Raya, M., Martí, M., Raya, A. and Izpisúa Belmonte, J. C. (2010). Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464, 606-609.
29. Kettleborough, R. N., Busch-Nentwich, E. M., Harvey, S. A., Dooley, C. M., de Bruijn, E., van Eeden, F., Sealy, I., White, R. J., Herd, C., Nijman, I. J. et al. (2013). A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature 496, 494-497.
30. Kikuchi, K., Holdway, J. E., Werdich, A. A., Anderson, R. M., Fang, Y., Egnaczyk, G. F., Evans, T., MacRae, C. A., Stainier, D. Y. and Poss, K. D. (2010). Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464, 601-605.
31. Kolpa, H. J., Peal, D. S., Lynch, S. N., Giokas, A. C., Ghatak, S., Misra, S., Norris, R. A., MacRae, C. A., Markwald, R. R., Ellinor, P. et al. (2013). miR-21 represses Pdcd4 during cardiac valvulogenesis. Development 140, 2172-2180.
32. Lagendijk, A. K., Goumans, M. J., Burkhard, S. B. and Bakkers, J. (2011). MicroRNA-23 restricts cardiac valve formation by inhibiting Has2 and extracellular hyaluronic acid production. Circ. Res. 109, 649-657.
33. Lane, K. B., Machado, R. D., Pauciulo, M. W., Thomson, J. R., Phillips, J. A., III, Loyd, J. E., Nichols, W. C., Trembath, R. C., Trembath, R. C.; International PPH Consortium (2000). Heterozygous germline mutations in BMPR2, encoding a TGFbeta receptor, cause familial primary pulmonary hypertension. Nat. Genet. 26, 81-84.
34. Langheinrich, U., Vacun, G. and Wagner, T. (2003). Zebrafish embryos express an orthologue of HERG and are sensitive toward a range of QT-prolonging drugs inducing severe arrhythmia. Toxicol. Appl. Pharmacol. 193, 370-382. (Pubitemid 37543544)
35. Lazic, S. and Scott, I. C. (2011). Mef2cb regulates late myocardial cell addition from a second heart field-like population of progenitors in zebrafish. Dev. Biol. 354, 123-133.
36. Lipshultz, S. E., Colan, S. D., Gelber, R. D., Perez-Atayde, A. R., Sallan, S. E. and Sanders, S. P. (1991). Late cardiac effects of doxorubicin therapy for acute lymphoblastic leukemia in childhood. N. Engl. J. Med. 324, 808-815.
37. Lyons, I., Parsons, L. M., Hartley, L., Li, R., Andrews, J. E., Robb, L. and Harvey, R. P. (1995). Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9, 1654-1666.
38. Martin, R. T. and Bartman, T. (2009). Analysis of heart valve development in larval zebrafish. Dev. Dyn. 238, 1796-1802.
39. McElhinney, D. B., Geiger, E., Blinder, J., Benson, D. W. and Goldmuntz, E. (2003). NKX2.5 mutations in patients with congenital heart disease. J. Am. Coll. Cardiol. 42, 1650-1655. (Pubitemid 37378448)
40. 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.
41. Mishra, S., Guan, J., Plovie, E., Seldin, D. C., Connors, L. H., Merlini, G., Falk, R. H., MacRae, C. A. and Liao, R. (2013). Human amyloidogenic light chain proteins result in cardiac dysfunction, cell death, and early mortality in zebrafish. Am. J. Physiol. 305, H95-H103.
42. Nevis, K., Obregon, P., Walsh, C., Guner-Ataman, B., Burns, C. G. and Burns, C. E. (2013). Tbx1 is required for second heart field proliferation in zebrafish. Dev. Dyn. 242, 550-559.
43. Nicoli, S. and Presta, M. (2007). The zebrafish/tumor xenograft angiogenesis assay. Nat. Protoc. 2, 2918-2923.
44. Peal, D. S., Mills, R. W., Lynch, S. N., Mosley, J. M., Lim, E., Ellinor, P. T., January, C. T., Peterson, R. T. and Milan, D. J. (2011). Novel chemical suppressors of long QT syndrome identified by an in vivo functional screen. Circulation 123, 23-30.
45. Peterson, R. T., Shaw, S. Y., Peterson, T. A., Milan, D. J., Zhong, T. P., Schreiber, S. L., MacRae, C. A. and Fishman, M. C. (2004). Chemical suppression of a genetic mutation in a zebrafish model of aortic coarctation. Nat. Biotechnol. 22, 595-599. (Pubitemid 38585912)
46. Piotrowski, T., Ahn, D. G., Schilling, T. F., Nair, S., Ruvinsky, I., Geisler, R., Rauch, G. J., Haffter, P., Zon, L. I., Zhou, Y. et al. (2003). The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 130, 5043-5052. (Pubitemid 37321885)
47. Poss, K. D., Wilson, L. G. and Keating, M. T. (2002). Heart regeneration in zebrafish. Science 298, 2188-2190. (Pubitemid 35471243)
48. Sander, J. D., Cade, L., Khayter, C., Reyon, D., Peterson, R. T., Joung, J. K. and Yeh, J. R. (2011). Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat. Biotechnol. 29, 697-698.
49. Sanvitale, C. E., Kerr, G., Chaikuad, A., Ramel, M. C., Mohedas, A. H., Reichert, S., Wang, Y., Triffitt, J. T., Cuny, G. D., Yu, P. B. et al. (2013). A new class of small molecule inhibitor of BMP signaling. PLoS ONE 8, e62721.
50. Schott, J. J., Benson, D. W., Basson, C. T., Pease, W., Silberbach, G. M., Moak, J. P., Maron, B. J., Seidman, C. E. and Seidman, J. G. (1998). Congenital heart disease caused by mutations in the transcription factor NKX2-5. Science 281, 108-111. (Pubitemid 28354055)
51. Sehnert, A. J., Huq, A., Weinstein, B. M., Walker, C., Fishman, M. and Stainier, D. Y. (2002). Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 31, 106-110.
52. Shi, J., Guan, J., Jiang, B., Brenner, D. A., Del Monte, F., Ward, J. E., Connors, L. H., Sawyer, D. B., Semigran, M. J., Macgillivray, T. E. et al. (2010). Amyloidogenic light chains induce cardiomyocyte contractile dysfunction and apoptosis via a noncanonical p38alpha MAPK pathway. Proc. Natl. Acad. Sci. USA 107, 4188-4193.
53. Stainier, D. Y., Fouquet, B., Chen, J. N., Warren, K. S., Weinstein, B. M., Meiler, S. E., Mohideen, M. A., Neuhauss, S. C., Solnica-Krezel, L., Schier, A. F. et al. (1996). Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development 123, 285-292. (Pubitemid 27056755)
54. Targoff, K. L., Colombo, S., George, V., Schell, T., Kim, S. H., Solnica-Krezel, L. and Yelon, D. (2013). Nkx genes are essential for maintenance of ventricular identity. Development 140, 4203-4213.
55. Venkatesha, S., Toporsian, M., Lam, C., Hanai, J., Mammoto, T., Kim, Y. M., Bdolah, Y., Lim, K. H., Yuan, H. T., Libermann, T. A. et al. (2006). Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat. Med. 12, 642-649. (Pubitemid 43865232)
56. Weinstein, B. M., Stemple, D. L., Driever, W. and Fishman, M. C. (1995). Gridlock, a localized heritable vascular patterning defect in the zebrafish. Nat. Med. 1, 1143-1147.
57. Wiley, D. M., Kim, J. D., Hao, J., Hong, C. C., Bautch, V. L. and Jin, S. W. (2011). Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nat. Cell Biol. 13, 686-692.
58. Xu, X., Meiler, S. E., Zhong, T. P., Mohideen, M., Crossley, D. A., Burggren, W. W. and Fishman, M. C. (2002). Cardiomyopathy in zebrafish due to mutation in an alternatively spliced exon of titin. Nat. Genet. 30, 205-209.
59. Yamagishi, H., Yamagishi, C., Nakagawa, O., Harvey, R. P., Olson, E. N. and Srivastava, D. (2001). The combinatorial activities of Nkx2.5 and dHAND are essential for cardiac ventricle formation. Dev. Biol. 239, 190-203. (Pubitemid 33108833)
60. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin, H. Y., Bloch, K. D. and Peterson, R. T. (2008). Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41. (Pubitemid 350273653)
61. Zhao, L., Borikova, A. L., Ben-Yair, R., Guner-Ataman, B., MacRae, C. A., Lee, R. T., Burns, C. G. and Burns, C. E. (2014). Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc. Natl. Acad. Sci. USA 111, 1403-1408