Whole-exome sequencing and an iPSC-derived cardiomyocyte model provides a powerful platform for gene discovery in left ventricular hypertrophy

Frontiers in Genetics

Volumn 3, Issue MAY, 2012, Pages

  Zhi, D ^a   lrvin, M R ^a   Gu, C C ^b   Stoddard, A J ^c   Lorier, R ^c   Matter, A ^c   Rao, D C ^b   Srinivasasainagendra, V ^a   Tiwari, H K ^a   Turner, A ^c   Broeckel, U ^c   Arnett, D K ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Cardiomyocyte; Exome; Genomics; Hypertrophy; Left ventricular mass

Indexed keywords

EID: 84870997412     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00092     Document Type: Article

References (51)

1. Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11,R106.
2. Arnett, D. K., Devereux, R. B., Rao, D. C., Li, N., Tang, W., Kraemer, R., Claas, S. A., Leon, J. M., and Broeckel, U. (2009a). Novel genetic variants contributing to left ventricular hypertrophy: the HyperGEN study. J. Hypertens. 27,1585-1593.
3. Arnett, D. K., Li, N., Tang, W., Rao, D. C., Devereux, R. B., Claas, S. A., Kraemer, R., and Broeckel, U. (2009b). Genome-wide association study identifies single-nucleotide polymorphism in KCNB1 associated with left ventricular mass in humans: the HyperGEN Study. BMCMed. Genet. 10,43. doi:10.1186/1471-2350-10-43
4. Arnett, D. K., Hong, Y., Bella, J. N., Oberman, A., Kitzman, D. W., Hopkins, P. N., Rao, D. C., and Devereux, R. B. (2001). Sibling correlation of left ventricular mass and geometry in hypertensive African Americans and whites: the HyperGEN study. Hypertension genetic epidemiology network. Am. J. Hypertens. 14,1226-1230.
5. Arnett, D. K., Meyers, K. J., Devereux, R. B.,Tiwari, H. K., Gu, C. C.,Vaughan, L. K., Perry, R. T., Patki, A., Claas, S. A., Sun, Y. V., Broeckel, U., and Kar-dia, S. L. (2011). Genetic variation in NCAM1 contributes to left ventricular wall thickness in hypertensive families. Circ. Res. 108, 279-283.
6. Benjamin, E. J., and Levy, D. (1999). Why is left ventricular hypertrophy so predictive of morbidity and mortality? Am. J. Med. Sci. 317,168-175.
7. Berry, J. M., Haris Naseem, R., Rother-mel, B. A., and Hill, J. A. (2007). Models of cardiac hypertrophy and transition to heart failure. Drug Dis-cov. Today Dis. Models 4, 197-206.
8. Carvajal-Vergara, X., Sevilla, A., D'Souza, S. L., Ang, Y. S., Schaniel, C., Lee, D. F., Yang, L., Kaplan, A. D., Adler, E. D., Rozov, R., Ge, Y., Cohen, N., Edelmann, L. J., Chang, B., Waghray, A., Su, J., Pardo, S., Lichtenbelt, K. D., Tartaglia, M., Gelb, B. D., and Lemischka, I. R. (2010). Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 465,808-812.
9. Chen, C. C., Hsu, Y J., and Lee, T. M. (2011). Impact of elevated uric acid on ventricular remodeling in infarcted rats with experimental hyperuricemia. Am. J. Physiol. Heart Circ. Physiol. 301, H1107-H1117.
10. Cooper, G. M., Stone, E. A., Asimenos, G., Green, E. D., Batzoglou, S., and Sidow, A. (2005). Distribution and intensity of constraint in mammalian genomic sequence. Genome Res. 15,901-913.
11. Davydov, E. V., Goode, D. L., Sirota, M., Cooper, G. M., Sidow, A., and Batzoglou, S. (2010). Identifying a high fraction of the human genome to be under selective constraint using GERP++. PLoS Comput. Biol. 6, e1001025. doi:10.1371/jour-nal.pcbi. 1001025
12. Devereux, R. B., Lutas, E. M., Casale, P. N., Kligfield, P., Eisenberg, R. R., Hammond, I. W., Miller, D. H., Reis, G., Alderman, M. H., and Laragh, J. H. (1984). Standardization of M-mode echocardiographic left ventricular anatomic measurements. J. Am. Coll. Cardiol. 4, 1222-1230.
13. Devereux, R. B., and Roman, M. J. (1995). "Evaluation of cardiac function and vascular structure and function by echocardiography and other noninvasive techniques," in Hypertension: Pathophysiology, Diagnosis, and Management, eds J. H. Laragh and B. M. Brenner (New York: Raven P), 1969-1985.
14. Fox, E. R., Young, J. H., Li,Y., Dreisbach, A. W., Keating, B. J., Musani, S. K., Liu, K., Morrison, A. C., Ganesh, S., Kutlar, A., Ramachandran, V. S., Polak, J. F., Fabsitz, R. R., Dries, D. L., Farlow, D. N., Redline, S., Adeyemo, A., Hirschorn, J. N., Sun, Y V., Wyatt, S. B., Penman, A. D., Palmas, W., Rotter, J. I., Townsend, R. R., Doumatey, A. P., Tayo, B. O., Mosley, T. H. Jr., Lyon, H. N., Kang, S. J., Rotimi, C. N., Cooper, R. S., Franceschini, N., Curb, J. D., Martin, L. W., Eaton, C. B., Kardia, S. L., Taylor, H. A., Caulfield, M. J., Ehret, G. B., Johnson, T., Chakravarti, A., Zhu, X., and Levy, D. (2011). Association of genetic variation with systolic and diastolic blood pressure among African Americans: the Candidate Gene Association Resource study. Hum. Mol. Genet. 20, 2273-2284.
15. Ganapathy, V., Thangaraju, M., Gopal, E., Martin, P. M., Itagaki, S., Miyauchi, S., and Prasad, P. D. (2008). Sodium-coupled monocar-boxylate transporters in normal tissues and in cancer. AAPS J. 10, 193-199.
16. Germanguz, I., Sedan, O., Zeevi-Levin, N., Shtrichman, R., Barak, E., Ziskind, A., Eliyahu, S., Meiry G., Amit, M., Itskovitz-Eldor, J., and Binah, O. (2011). Molecular characterization and functional properties of cardiomyocytes derived from human inducible pluripotent stem cells. J. Cell. Mol. Med. 15, 38-51.
17. Gu, C. C., Hunt, S. C., Kardia, S., Turner, S. T., Chakravarti, A., Schork, N., Olshen, R., Curb, D., Jaquish, C., Boerwinkle, E., and Rao, D. C. (2007). An investigation of genome-wide associations of hypertension with microsatellite markers in the family blood pressure program (FBPP). Hum. Genet. 121, 577-590.
18. Harshfield, G. A., Grim, C. E., Hwang, C., Savage, D. D., and Anderson, S. J. (1990). Genetic and environmental influences on echocardiographically determined left ventricular mass in black twins. Am. J. Hypertens. 3, 538-543.
19. Isik, T., Ayhan, E., Ergelen, M., and Uyarel, H. (2012). Uric acid: a novel prognostic marker for cardiovascular disease. Int. J. Cardiol. 156, 328-329.
20. Itzhaki, I., Maizels, L., Huber, I., Zwi-Dantsis, L., Caspi, O., Winterstern, A., Feldman, O., Gepstein, A., Arbel, G., Hammerman, H., Boulos, M., and Gepstein, L. (2011). Modelling the long QT syndrome with induced pluripotent stem cells. Nature 471, 225-229.
21. Kim, J. J., Park, Y. M., Baik, K. H., Choi, H. Y., Yang, G. S., Koh, I., Hwang, J. A., Lee, J., Lee, Y S., Rhee, H., Kwon, T. S., Han, B. G., Heath, K. E., Inoue, H., Yoo, H. W., Park, K., and Lee, J. K. (2012). Exome sequencing and subsequent association studies identify five amino acid-altering variants influencing human height. Hum. Genet. 131,471-478.
22. Kong, C. W., Akar, F. G., and Li, R. A. (2010). Translational potential of human embryonic and induced pluripotent stem cells for myocar-dial repair: insights from experimental models. Thromb. Haemost. 104, 30-38.
23. Li, H. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987-2993.
24. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., and Durbin, R. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079.
25. Lijnen, P., and Petrov, V. (1999). Renin-angiotensin system, hypertrophy and gene expression in cardiac myocytes. J. Mol. Cell. Cardiol. 31,949-970.
26. Lourenco, V. M., Pires, A. M., and Kirst, M. (2011). Robust linear regression methods in association studies. Bioinformatics 27, 815-821.
27. Madsen, B. E., and Browning, S. R. (2009). A groupwise association test for rare mutations using a weighted sum statistic. PLoS Genet. 5, e1000384. doi:10.1371/journal.pgen.1000384
28. Majewski, J., Schwartzentruber, J., Lalonde, E., Montpetit, A., and Jabado, N. (2011). What can exome sequencing do for you? J. Med. Genet. 48, 580-589.
29. Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., McCarthy, M. I., Ramos, E. M., Cardon, L. R., Chakravarti, A., Cho, J. H., Guttmacher, A. E., Kong, A., Kruglyak, L., Mardis, E., Rotimi, C. N., Slatkin, M., Valle, D., Whitte-more, A. S., Boehnke, M., Clark, A. G., Eichler, E. E., Gibson, G., Haines, J. L., MacKay, T. F., McCarroll, S. A., and Visscher, P. M. (2009). Finding the missing heritability of complex diseases. Nature 461, 747-753.
30. Moretti, A., Bellin, M., Welling, A., Jung, C. B., Lam, J. T., Bott-Flugel, L., Dorn, T., Goedel, A., Hohnke, C., Hofmann, F., Seyfarth, M., Sinnecker, D., Schomig, A., and Laugwitz, K. L. (2010). Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N. Engl. J. Med. 363, 1397-1409.
31. Ng, S. B., Bigham, A. W., Buckingham, K. J., Hannibal, M. C., McMillin, M. J., Gildersleeve, H. I., Beck, A. E., Tabor, H. K., Cooper, G. M., Mefford, H. C., Lee, C., Turner, E. H., Smith, J. D., Rieder, M. J., Yoshiura, K., Matsumoto, N., Ohta, T., Niikawa, N., Nickerson, D. A., Bamshad, M. J., and Shendure, J. (2010a). Exome sequencing identifies MLL2 mutations as a cause of Kabuki syndrome. Nat. Genet. 42, 790-793.
32. Ng, S. B., Buckingham, K. J., Lee, C., Bigham, A. W., Tabor, H. K., Dent, K. M., Huff, C. D., Shannon, P. T., Jabs, E. W., Nickerson, D. A., Shendure, J., and Bamshad, M. J. (2010b). Exome sequencing identifies the cause of a Mendelian disorder. Nat. Genet. 42, 30-35.
33. Norton, N., Li, D., Rieder, M. J., Siegfried, J. D., Rampersaud, E., Zuchner, S., Mangos, S., Gonzalez-Quintana, J., Wang, L., McGee, S., Reiser, J., Martin, E., Nickerson, D. A., and Hershberger, R. E. (2011). Genome-wide studies of copy number variation and exome sequencing identify rare variants in BAG3 as a cause of dilated cardiomy-opathy. Am. J. Hum. Genet. 88, 273-282.
34. O'Roak, B. J., Deriziotis, P., Lee, C., Vives, L., Schwartz, J. J., Girirajan, S., Karakoc, E., MacKenzie, A. P., Ng, S. B., Baker, C., Rieder, M. J., Nickerson, D. A., Bernier, R., Fisher, S. E., Shendure, J., and Eichler, E. E. (2011). Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat. Genet. 43, 585-589.
35. Ramagopalan, S. V., Dyment, D. A., Cader, M. Z., Morrison, K. M., Disanto, G., Morahan, J. M., Berlanga-Taylor, A. J., Handel, A., De Luca, G. C., Sadovnick, A. D., Lepage, P., Montpetit, A., and Ebers, G. C. (2011). Rare variants in the CYP27B1 gene are associated with multiple sclerosis. Ann. Neurol. 70, 881-886.
36. Ramensky, V., Bork, P., and Sunyaev, S. (2002). Human non-synonymous SNPs: server and survey. Nucleic Acids Res. 30, 3894-3900.
37. Rao, D. C., and Province, M. A. (2000). The future of path analysis, segregation analysis, and combined models for genetic dissection of complex traits. Hum. Hered. 50, 34-42.
38. Rasmussen-Torvik, L. J., North, K. E., Gu, C. C., Lewis, C. E., Wilk, J. B., Chakravarti, A., Chang, Y. P., Miller, M. B., Li, N., Devereux, R. B., and Arnett, D. K. (2005). A population association study of angiotensino-gen polymorphisms and haplotypes with left ventricular phenotypes. Hypertension 46,1294-1299.
39. Robinson, P. N., Krawitz, P., and Mund-los, S. (2011). Strategies for exome and genome sequence data analysis in disease-gene discovery projects. Clin. Genet. 80,127-132.
40. Shi, G., and Rao, D. C. (2011). Optimum designs for next-generation sequencing to discover rare variants for common complex disease. Genet. Epidemiol. 35, 572-579.
41. Su, A. I., Wiltshire, T., Batalov, S., Lapp, H., Ching, K. A., Block, D., Zhang, J., Soden, R., Hayakawa, M., Kreiman, G., Cooke, M. P., Walker, J. R., and Hogenesch, J. B. (2004). A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U.S.A. 101, 6062-6067.
42. Tang, W., Devereux, R. B., Li, N., Oberman, A., Kitzman, D. W., Rao, D. C., Hopkins, P. N., Claas, S. A., and Arnett, D. K. (2009). Identification of a pleiotropic locus on chromosome 7q for a composite left ventricular wall thickness factor and body mass index: the Hyper-GEN Study. BMCMed. Genet. 10,40. doi:10.1186/1471-2350-10-40
43. Thangaraju, M., Ananth, S., Martin, P. M., Roon, P., Smith, S. B., Sterneck, E., Prasad, P. D., and Ganapathy, V. (2006). c/ebpdelta null mouse as a model for the double knock-out of slc5a8 and slc5a12 in kidney. J. Biol. Chem. 281,26769-26773.
44. Trapnell, C., Pachter, L., and Salzberg, S. L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinfor-matics 25, 1105-1111.
45. Vanhoutte, D., and Heymans, S. (2011). Thrombospondin 1: a protective "matri-cellular" signal in the stressed heart. Hypertension 58, 770-771.
46. Wang, K., Li, M., and Hakonarson, H. (2010). ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38,e164.
47. Williams, R. R., Rao, D. C., Ellison, R. C., Arnett, D. K., Heiss, G., Oberman, A., Eckfeldt, J. H., Leppert, M. F., Province, M. A., Mockrin, S. C., and Hunt, S. C. (2000). NHLBI family blood pressure program: methodology and recruitment in the Hyper-GEN network. Hypertension genetic epidemiology network. Ann. Epidemiol. 10,389-400.
48. Wineinger, N. E., Patki, A., Meyers, K. J., Broeckel, U., Gu, C. C., Rao, D. C., Devereux, R. B., Arnett, D. K., and Tiwari, H. K. (2011). Genome-wide joint SNP and CNV analysis of aortic root diameter in African Americans: the HyperGEN study. BMC Med. Genomics 4, 4. doi:10.1186/1755-8794-4-4
49. Xia, Y., Dobaczewski, M., Gonzalez-Quesada, C., Chen,W.,Biernacka,A., Li, N., Lee, D. W., and Frangogian-nis, N. G. (2011). Endogenous thrombospondin 1 protects the pressure-overloaded myocardium by modulating fibroblast phe-notype and matrix metabolism. Hypertension 58, 902-911.
50. Xie, F., Ye, L., Ta, M., Zhang, L., and Jiang, W. G. (2011). MTSS1: a multifunctional protein and its role in cancer invasion and metastasis. Front. Biosci. 3,621-631.
51. Yokoo, N., Baba, S., Kaichi, S., Niwa, A., Mima, T., Doi, H., Yamanaka, S., Nakahata, T., and Heike, T. (2009). The effects of cardioactive drugs on cardiomyocytes derived from human induced pluripotent stem cells. Biochem. Biophys. Res. Com-mun. 387, 482-488.