Novel cardiovascular gene functions revealed via systematic phenotype prediction in zebrafish

Development (Cambridge)

Volumn 141, Issue 1, 2014, Pages 224-235

  Musso, Gabriel ^a,b   Tasan, Murat ^a,c   Mosimann, Christian ^d,e   Beaver, John E ^a   Plovie, Eva ^b   Carr, Logan A ^d,e   Chua, Hon Nian ^c   Dunham, Julie ^c   Zuberi, Khalid ^c   Rodriguez, Harold ^c   Morris, Quaid ^c   Zon, Leonard ^d,e   Roth, Frederick P ^a,c,f,g   MacRae, Calum A ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f MOUNT SINAI HOSPITAL   (Canada)

^g DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

Cardiovascular; Systems biology; Tmem88a; Zebrafish

Indexed keywords

WNT11 PROTEIN;

ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL GENE; DNA BASE COMPOSITION; EMBRYO; FEMALE; GENE FUNCTION; GENE SILENCING; GENETIC ASSOCIATION; HEART ATRIUM CONTRACTION; HEART FUNCTION; HEART OUTPUT; HEART VENTRICLE CONTRACTION; LOSS OF FUNCTION MUTATION; MACHINE LEARNING; MALE; NONHUMAN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; TRANSCRIPTION INITIATION SITE; WNT SIGNALING PATHWAY; ZEBRA FISH;

CARDIOVASCULAR; SYSTEMS BIOLOGY; TMEM88A; ZEBRAFISH;

ANIMALS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HEART; MEMBRANE PROTEINS; MORPHOLINOS; MYOCARDIUM; PHENOTYPE; WNT SIGNALING PATHWAY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84890453567     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.099796     Document Type: Article

References (76)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Amsterdam, A., Burgess, S., Golling, G., Chen, W., Sun, Z., Townsend, K., Farrington, S., Haldi, M. and Hopkins, N. (1999). A large-scale insertional mutagenesis screen in zebrafish. Genes Dev. 13, 2713-2724.
3. Amsterdam, A., Nissen, R. M., Sun, Z., Swindell, E. C., Farrington, S. and Hopkins, N. (2004). Identification of 315 genes essential for early zebrafish development. Proc. Natl. Acad. Sci. USA 101, 12792-12797.
4. Arnaout, R., Ferrer, T., Huisken, J., Spitzer, K., Stainier, D. Y., Tristani-Firouzi, M. and Chi, N. C. (2007). Zebrafish model for human long QT syndrome. Proc. Natl. Acad. Sci. USA 104, 11316-11321.
5. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T. et al.; The Gene Ontology Consortium (2000). Gene ontology: tool for the unification of biology. Nat. Genet. 25, 25-29.
6. Auman, H. J., Coleman, H., Riley, H. E., Olale, F., Tsai, H. J. and Yelon, D. (2007). Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol. 5, e53.
7. Barrett, T. and Edgar, R. (2006). Gene expression omnibus: microarray data storage, submission, retrieval, and analysis. Methods Enzymol. 411, 352-369.
8. Beaver, J. E., Tasan, M., Gibbons, F. D., Tian, W., Hughes, T. R. and Roth, F. P. (2010). FuncBase: a resource for quantitative gene function annotation. Bioinformatics 26, 1806-1807.
9. Boutros, M., Kiger, A. A., Armknecht, S., Kerr, K., Hild, M., Koch, B., Haas, S. A., Paro, R., Perrimon, N.; Heidelberg Fly Array Consortium (2004). Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303, 832-835.
10. Bradford, Y., Conlin, T., Dunn, N., Fashena, D., Frazer, K., Howe, D. G., Knight, J., Mani, P., Martin, R., Moxon, S. A. et al. (2011). ZFIN: enhancements and updates to the Zebrafish Model Organism Database. Nucleic Acids Res. 39, D822-D829.
11. Burns, C. G., Milan, D. J., Grande, E. J., Rottbauer, W., MacRae, C. A. and Fishman, M. C. (2005). High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nat. Chem. Biol. 1, 263-264.
12. Camarata, T., Krcmery, J., Snyder, D., Park, S., Topczewski, J. and Simon, H. G. (2010). Pdlim7 (LMP4) regulation of Tbx5 specifies zebrafish heart atrio-ventricular boundary and valve formation. Dev. Biol. 337, 233-245.
13. Cannon, J. E., Place, E. S., Eve, A. M., Bradshaw, C. R., Sesay, A., Morrell, N. W. and Smith, J. C. (2013). Global analysis of the haematopoietic and endothelial transcriptome during zebrafish development. Mech. Dev. 130, 122-131.
14. Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E. D., Sevier, C. S., Ding, H., Koh, J. L., Toufighi, K., Mostafavi, S. et al. (2010). The genetic landscape of a cell. Science 327, 425-431.
15. Deng, M., Chen, T. and Sun, F. (2004). An integrated probabilistic model for functional prediction of proteins. J. Comput. Biol. 11, 463-475.
16. 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.
17. Ekker, S. C. and Larson, J. D. (2001). Morphant technology in model developmental systems. Genesis 30, 89-93.
18. Etard, C., Roostalu, U. and Strähle, U. (2010). Lack of Apobec2-related proteins causes a dystrophic muscle phenotype in zebrafish embryos. J. Cell Biol. 189, 527-539.
19. Fu, C. Y., Lee, H. C. and Tsai, H. J. (2009). The molecular structures and expression patterns of zebrafish troponin I genes. Gene Expr. Patterns 9, 348-356.
20. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
21. Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Véronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., André, B. et al. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
22. Golling, G., Amsterdam, A., Sun, Z., Antonelli, M., Maldonado, E., Chen, W., Burgess, S., Haldi, M., Artzt, K., Farrington, S. et al. (2002). Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat. Genet. 31, 135-140.
23. Guan, Y., Myers, C. L., Lu, R., Lemischka, I. R., Bult, C. J. and Troyanskaya, O. G. (2008). A genomewide functional network for the laboratory mouse. PLoS Comput. Biol. 4, e1000165.
24. Haffter, P., Granato, M., Brand, M., Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., van Eeden, F. J., Jiang, Y. J., Heisenberg, C. P. et al. (1996). The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1-36.
25. Hasdemir, C., Aydin, H. H., Celik, H. A., Simsek, E., Payzin, S., Kayikcioglu, M., Aydin, M., Kultursay, H. and Can, L. H. (2010). Transcriptional profiling of septal wall of the right ventricular outflow tract in patients with idiopathic ventricular arrhythmias. Pacing Clin. Electrophysiol. 33, 159-167.
26. Heasman, J. (2002). Morpholino oligos: making sense of antisense? Dev. Biol. 243, 209-214.
27. 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.
28. Huang, P., Xiao, A., Zhou, M., Zhu, Z., Lin, S. and Zhang, B. (2011). Heritable gene targeting in zebrafish using customized TALENs. Nat. Biotechnol. 29, 699-700.
29. Huttenhower, C., Haley, E. M., Hibbs, M. A., Dumeaux, V., Barrett, D. R., Coller, H. A. and Troyanskaya, O. G. (2009). Exploring the human genome with functional maps. Genome Res. 19, 1093-1106.
30. 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.
31. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
32. Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S., Tokimatsu, T. et al. (2008). KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36, D480-D484.
33. Karaoz, U., Murali, T. M., Letovsky, S., Zheng, Y., Ding, C., Cantor, C. R. and Kasif, S. (2004). Whole-genome annotation by using evidence integration in functionallinkage networks. Proc. Natl. Acad. Sci. USA 101, 2888-2893.
34. 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.
35. King, O. D., Lee, J. C., Dudley, A. M., Janse, D. M., Church, G. M. and Roth, F. P. (2003). Predicting phenotype from patterns of annotation. Bioinformatics 19 Suppl. 1, i183-i189.
36. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C. B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
37. Langenbacher, A. D., Dong, Y., Shu, X., Choi, J., Nicoll, D. A., Goldhaber, J. I., Philipson, K. D. and Chen, J. N. (2005). Mutation in sodium-calcium exchanger 1 (NCX1) causes cardiac fibrillation in zebrafish. Proc. Natl. Acad. Sci. USA 102, 17699-17704.
38. 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.
39. Lee, I., Date, S. V., Adai, A. T. and Marcotte, E. M. (2004). A probabilistic functional network of yeast genes. Science 306, 1555-1558.
40. Lee, I., Lehner, B., Crombie, C., Wong, W., Fraser, A. G. and Marcotte, E. M. (2008). A single gene network accurately predicts phenotypic effects of gene perturbation in Caenorhabditis elegans. Nat. Genet. 40, 181-188.
41. Lee, H. J., Finkelstein, D., Li, X., Wu, D., Shi, D. L. and Zheng, J. J. (2010). Identification of transmembrane protein 88 (TMEM88) as a dishevelled-binding protein. J. Biol. Chem. 285, 41549-41556.
42. Levesque, M., Shasha, D., Kim, W., Surette, M. G. and Benfey, P. N. (2003). Trait-togene: a computational method for predicting the function of uncharacterized genes. Curr. Biol. 13, 129-133.
43. Linghu, B., Snitkin, E. S., Hu, Z., Xia, Y. and Delisi, C. (2009). Genomewide prioritization of disease genes and identification of disease-disease associations from an integrated human functional linkage network. Genome Biol. 10, R91.
44. Manning, C. D., Raghavan, P. and Schutze, H. (2008). Introduction to Information Retrieval. Cambridge: Cambridge University Press.
45. Maranto, A. R. (1994). Primary structure, ligand binding, and localization of the human type 3 inositol 1,4,5-trisphosphate receptor expressed in intestinal epithelium. J. Biol. Chem. 269, 1222-1230.
46. Marlow, F., Zwartkruis, F., Malicki, J., Neuhauss, S. C., Abbas, L., Weaver, M., Driever, W. and Solnica-Krezel, L. (1998). Functional interactions of genes mediating convergent extension, knypek and trilobite, during the partitioning of the eye primordium in zebrafish. Dev. Biol. 203, 382-399.
47. Meng, X., Noyes, M. B., Zhu, L. J., Lawson, N. D. and Wolfe, S. A. (2008). Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat. Biotechnol. 26, 695-701.
48. Mosimann, C., Kaufman, C. K., Li, P., Pugach, E. K., Tamplin, O. J. and Zon, L. I. (2011). Ubiquitous transgene expression and Cre-based recombination driven by the ubiquitin promoter in zebrafish. Development 138, 169-177.
49. Mostafavi, S., Ray, D., Warde-Farley, D., Grouios, C. and Morris, Q. (2008). GeneMANIA: a real-time multiple association network integration algorithm for predicting gene function. Genome Biol. 9 Suppl. 1, S4.
50. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
51. Novikov, N. and Evans, T. (2013). Tmem88a mediates GATA-dependent specification of cardiomyocyte progenitors by restricting WNT signaling. Development 140, 3787-3798.
52. Palpant, N. J., Pabon, L., Rabinowitz, J. S., Hadland, B. K., Stoick-Cooper, C. L., Paige, S. L., Bernstein, I. D., Moon, R. T. and Murry, C. E. (2013). Transmembrane protein 88: a Wnt regulatory protein that specifies cardiomyocyte development. Development 140, 3799-3808.
53. Panáková, D., Werdich, A. A. and Macrae, C. A. (2010). Wnt11 patterns a myocardial electrical gradient through regulation of the L-type Ca(2+) channel. Nature 466, 874-878.
54. Pellegrini, M., Marcotte, E. M., Thompson, M. J., Eisenberg, D. and Yeates, T. O. (1999). Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc. Natl. Acad. Sci. USA 96, 4285-4288.
55. Peña-Castillo, L., Tasan, M., Myers, C. L., Lee, H., Joshi, T., Zhang, C., Guan, Y., Leone, M., Pagnani, A., Kim, W. K. et al. (2008). A critical assessment of Mus musculus gene function prediction using integrated genomic evidence. Genome Biol. 9 Suppl. 1, S2.
56. Peterson, S. M. and Freeman, J. L. (2009). RNA isolation from embryonic zebrafish and cDNA synthesis for gene expression analysis. J. Vis. Exp. 30, 1470.
57. Peterson, R. T., Link, B. A., Dowling, J. E. and Schreiber, S. L. (2000). Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc. Natl. Acad. Sci. USA 97, 12965-12969.
58. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A. and Ekker, S. C. (2007). p53 activation by knockdown technologies. PLoS Genet. 3, e78.
59. Saha, S. and Heber, S. (2006). In silico prediction of yeast deletion phenotypes. Genet. Mol. Res. 5, 224-232.
60. 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.
61. Shin, J. T., Pomerantsev, E. V., Mably, J. D. and MacRae, C. A. (2010). Highresolution cardiovascular function confirms functional orthology of myocardial contractility pathways in zebrafish. Physiol. Genomics 42, 300-309.
62. Sing, T., Sander, O., Beerenwinkel, N. and Lengauer, T. (2005). ROCR: visualizing classifier performance in R. Bioinformatics 21, 3940-3941.
63. 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.
64. Stark, K., Esslinger, U. B., Reinhard, W., Petrov, G., Winkler, T., Komajda, M., Isnard, R., Charron, P., Villard, E., Cambien, F. et al. (2010). Genetic association study identifies HSPB7 as a risk gene for idiopathic dilated cardiomyopathy. PLoS Genet. 6, e1001167.
65. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S. et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545-15550.
66. Taşan, M., Tian, W., Hill, D. P., Gibbons, F. D., Blake, J. A. and Roth, F. P. (2008). An en masse phenotype and function prediction system for Mus musculus. Genome Biol. 9 Suppl. 1, S8.
67. Tasan, M., Drabkin, H. J., Beaver, J. E., Chua, H. N., Dunham, J., Tian, W., Blake, J. A. and Roth, F. P. (2012). A resource of quantitative functional annotation for homo sapiens genes. G3 (Bethesda) 2, 223-233.
68. Thisse, C. and Thisse, B. (2008). High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3, 59-69.
69. Tian, W., Zhang, L. V., Taşan, M., Gibbons, F. D., King, O. D., Park, J., Wunderlich, Z., Cherry, J. M. and Roth, F. P. (2008). Combining guilt-by-association and guilt-byprofiling to predict Saccharomyces cerevisiae gene function. Genome Biol. 9 Suppl. 1, S7.
70. Troyanskaya, O. G., Dolinski, K., Owen, A. B., Altman, R. B. and Botstein, D. (2003). A Bayesian framework for combining heterogeneous data sources for gene function prediction (in Saccharomyces cerevisiae). Proc. Natl. Acad. Sci. USA 100, 8348-8353.
71. Villard, E., Perret, C., Gary, F., Proust, C., Dilanian, G., Hengstenberg, C., Ruppert, V., Arbustini, E., Wichter, T., Germain, M. et al.; Cardiogenics Consortium (2011). A genome-wide association study identifies two loci associated with heart failure due to dilated cardiomyopathy. Eur. Heart J. 32, 1065-1076.
72. Vogel, B., Meder, B., Just, S., Laufer, C., Berger, I., Weber, S., Katus, H. A. and Rottbauer, W. (2009). In-vivo characterization of human dilated cardiomyopathy genes in zebrafish. Biochem. Biophys. Res. Commun. 390, 516-522.
73. Westerfield, M. (2000). The Zebrafish Book: A Guide for the Laboratory use of Zebrafish (Danio rerio), 4th edn. Eugene, OR: University of Oregon Press.
74. Woods, J. O., Singh-Blom, U. M., Laurent, J. M., McGary, K. L. and Marcotte, E. M. (2013). Prediction of gene-phenotype associations in humans, mice, and plants using phenologs. BMC Bioinformatics 14, 203.
75. Wu, Z., Irizarry, R. A., Gentleman, R., Martinez-Murillo, F. and Spencer, F. (2004). A model-based background adjustment for oligonucleotide expression arrays. J. Am. Stat. Assoc. 99, 909-917.
76. Zhou, Y., Cashman, T. J., Nevis, K. R., Obregon, P., Carney, S. A., Liu, Y., Gu, A., Mosimann, C., Sondalle, S., Peterson, R. E. et al. (2011). Latent TGF-β binding protein 3 identifies a second heart field in zebrafish. Nature 474, 645-648.