Genome-wide association study of down syndrome-associated atrioventricular septal defects

G3: Genes, Genomes, Genetics

Volumn 5, Issue 10, 2015, Pages 1961-1971

  Ramachandran, Dhanya ^a   Zeng, Zhen ^b   Locke, Adam E ^c,j   Mulle, Jennifer G ^d   Bean, Lora J H ^a   Rosser, Tracie C ^a   Dooley, Kenneth J ^e   Cua, Clifford L ^f   Capone, George T ^g   Reeves, Roger H ^h   Maslen, Cheryl L ⁱ   Cutler, David J ^a   Feingold, Eleanor ^b   Sherman, Stephanie L ^a   Zwick, Michael E ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^c EMORY UNIVERSITY   (United States)

^d EMORY UNIVERSITY   (United States)

^e SIBLEY HEART CENTER CARDIOLOGY   (United States)

^f NATIONWIDE CHILDREN S HOSPITAL   (United States)

^g KENNEDY KRIEGER INSTITUTE   (United States)

^h JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^j UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

more..

Author keywords

Aneuploidy; Birth defect; Complex trait; Congenital heart defect; Trisomy

Indexed keywords

FRIZZLED PROTEIN; KCNJ6 PROTEIN; LONG UNTRANSLATED RNA; PDXK PROTEIN; PROTEIN; SPACER DNA; TRANSCRIPTION FACTOR GATA; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; ATRIOVENTRICULAR SEPTAL DEFECT; BINDING SITE; CARDIOVASCULAR FUNCTION; CASE CONTROL STUDY; CHROMOSOME 21; CONTROLLED STUDY; DOWN SYNDROME; ENHANCER REGION; EUROPEAN AMERICAN; GENE CONTROL; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HEART DEVELOPMENT; HUMAN; INFANT; MAJOR CLINICAL STUDY; PHENOTYPE; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM; TRISOMY 21; CHROMOSOMAL MAPPING; COMPLICATION; GENETIC ASSOCIATION STUDY; GENETIC VARIATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HEART SEPTAL DEFECTS; PATHOLOGY;

CASE-CONTROL STUDIES; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 21; DOWN SYNDROME; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HEART SEPTAL DEFECTS; HUMANS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84943422903     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.019943     Document Type: Article

References (81)

1. Ackerman, C., A. E. Locke, E. Feingold, B. Reshey, K. Espana et al., 2012 An excess of deleterious variants in VEGF-A pathway genes in Down-syndromeassociated atrioventricular septal defects. Am. J. Hum. Genet. 91: 646-659.
2. Agopian, A. J., L. E. Mitchell, J. Glessner, A. D. Bhalla, A. Sewda et al., 2014 Genome-wide association study of maternal and inherited loci for conotruncal heart defects. PLoS One 9: e96057.
3. Alfieri, C. M., J. Cheek, S. Chakraborty, and K. E. Yutzey, 2010 Wnt signaling in heart valve development and osteogenic gene induction. Dev. Biol. 338: 127-135.
4. Al Turki, S., A. K. Manickaraj, C. L. Mercer, S. S. Gerety, M. P. Hitz et al., 2014 Rare variants in NR2F2 cause congenital heart defects in humans. Am. J. Hum. Genet. 94: 574-585.
5. Bean, L. J., E. G. Allen, S. W. Tinker, N. D. Hollis, A. E. Locke et al., 2011 Lack of maternal folic acid supplementation is associated with heart defects in Down syndrome: a report from the National Down Syndrome Project. Birth Defects Research (Part A). Clin. Mol. Teratol. 91: 885-893.
6. Boneva, R. S., L. D. Botto, C. A. Moore, Q. Yang, A. Correa et al., 2001 Mortality associated with congenital heart defects in the United States: trends and racial disparities, 1979-1997. Circulation 103: 2376-2381.
7. Cleves, M. A., S. Ghaffar, W. Zhao, B. S. Mosley, and C. A. Hobbs, 2003 First-year survival of infants born with congenital heart defects in Arkansas (1993-1998): a survival analysis using registry data. Birth Defects Research (Part A). Clin. Mol. Teratol. 67: 662-668.
8. Cohen, E. D., Y. Tian, and E. E. Morrisey, 2008 Wnt signaling: an essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal. Development 135: 789-798.
9. Cordell, H. J., J. Bentham, A. Topf, D. Zelenika, S. Heath et al., 2013 Genome-wide association study of multiple congenital heart disease phenotypes identifies a susceptibility locus for atrial septal defect at chromosome 4p16. Nat. Genet. 45: 822-824.
10. Cordell, H. J., A. Topf, C. Mamasoula, A. V. Postma, J. Bentham et al., 2013 Genome-wide association study identifies loci on 12q24 and 13q32 associated with tetralogy of Fallot. Hum. Mol. Genet. 22: 1473-1481.
11. Cripe, L., G. Andelfinger, L. J. Martin, K. Shooner, and D. W. Benson, 2004 Bicuspid aortic valve is heritable. J. Am. Coll. Cardiol. 44: 138-143.
12. Dennis, N. R., and J. Warren, 1981 Risks to the offspring of patients with some common congenital heart defects. J. Med. Genet. 18: 8-16.
13. Emanuel, R., J. Somerville, A. Inns, and R. Withers, 1983 Evidence of congenital heart disease in the offspring of parents with atrioventricular defects. Br. Heart J. 49: 144-147.
14. Fahed, A. C., B. D. Gelb, J. G. Seidman, and C. E. Seidman, 2013 Genetics of congenital heart disease: the glass half empty. Circ. Res. 112: 707-720.
15. Ferencz, C., C. A. Neill, J. A. Boughman, J. D. Rubin, J. I. Brenner et al., 1989 Congenital cardiovascular malformations associated with chromosome abnormalities: an epidemiologic study. J. Pediatr. 114: 79-86.
16. Flaquer, A., C. Baumbach, E. Pinero, F. Garcia Algas, M. A. De La Fuente Sanchez et al., 2013 Genome-wide linkage analysis of congenital heart defects using MOD score analysis identifies two novel loci. BMC Genet. 14: 44.
17. Fliegauf, M., T. Benzing, and H. Omran, 2007 When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8: 880-893.
18. Freeman, S. B., L. F. Taft, K. J. Dooley, K. Allran, S. L. Sherman et al., 1998 Population-based study of congenital heart defects in Down syndrome. Am. J. Med. Genet. 80: 213-217.
19. Freeman, S. B., L. H. Bean, E. G. Allen, S. W. Tinker, A. E. Locke et al., 2008 Ethnicity, sex, and the incidence of congenital heart defects: a report from the National Down Syndrome Project. Genet. Med. 10: 173-180.
20. French, V. M., I. M. Van De Laar, M. W. Wessels, C. Rohe, J. W. RoosHesselink et al., 2012 NPHP4 variants are associated with pleiotropic heart malformations. Circ. Res. 110: 1564-1574.
21. Friedland-Little, J. M., A. D. Hoffmann, P. J. Ocbina, M. A. Peterson, J. D. Bosman et al., 2011 A novel murine allele of Intraflagellar Transport Protein 172 causes a syndrome including VACTERL-like features with hydrocephalus. Hum. Mol. Genet. 20: 3725-3737.
22. Fung, A., C. Manlhiot, S. Naik, H. Rosenberg, J. Smythe et al., 2013 Impact of prenatal risk factors on congenital heart disease in the current era. J. Am. Heart Assoc. 2: e000064.
23. Garg, V., I. S. Kathiriya, R. Barnes, M. K. Schluterman, I. N. King et al., 2003 GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424: 443-447.
24. Greenway, S. C., A. C. Pereira, J. C. Lin, S. R. Depalma, S. J. Israel et al., 2009 De novo copy number variants identify new genes and loci in isolated sporadic tetralogy of Fallot. Nat. Genet. 41: 931-935.
25. Gutschner, T., M. Hammerle, M. Eissmann, J. Hsu, Y. Kim et al., 2013 The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 73: 1180-1189.
26. Habbig, S., M. P. Bartram, R. U. Muller, R. Schwarz, N. Andriopoulos et al., 2011 NPHP4, a cilia-associated protein, negatively regulates the Hippo pathway. J. Cell Biol. 193: 633-642.
27. Hartman, R. J., S. A. Rasmussen, L. D. Botto, T. Riehle-Colarusso, C. L. Martin et al., 2011 The contribution of chromosomal abnormalities to congenital heart defects: a population-based study. Pediatr. Cardiol. 32: 1147-1157.
28. Hoffman, J. I., 2013 The global burden of congenital heart disease. Cardiovasc. J. Afr. 24: 141-145.
29. Hoffman, J. I., and S. Kaplan, 2002 The incidence of congenital heart disease. J. Am. Coll. Cardiol. 39: 1890-1900.
30. Hou, X., M. Mrug, B. K. Yoder, E. J. Lefkowitz, G. Kremmidiotis et al., 2002 Cystin, a novel cilia-associated protein, is disrupted in the cpk mouse model of polycystic kidney disease. J. Clin. Invest. 109: 533-540.
31. Hu, Z., Y. Shi, X. Mo, J. Xu, B. Zhao et al., 2013 A genome-wide association study identifies two risk loci for congenital heart malformations in Han Chinese populations. Nat. Genet. 45: 818-821.
32. Hurlstone, A. F., A. P. Haramis, E. Wienholds, H. Begthel, J. Korving et al., 2003 The Wnt/beta-catenin pathway regulates cardiac valve formation. Nature 425: 633-637.
33. Lage, K., S. C. Greenway, J. A. Rosenfeld, H. Wakimoto, J. M. Gorham et al., 2012 Genetic and environmental risk factors in congenital heart disease functionally converge in protein networks driving heart development. Proc. Natl. Acad. Sci. USA 109: 14035-14040.
34. Larson, M. G., L. D. Atwood, E. J. Benjamin, L. A. Cupples, R. B. S. D'agostino et al., 2007 Framingham Heart Study 100K project: genomewide associations for cardiovascular disease outcomes. BMC Med. Genet. 8(Suppl 1): S5.
35. Lewin, M. B., K. L. Mcbride, R. Pignatelli, S. Fernbach, A. Combes et al., 2004 Echocardiographic evaluation of asymptomatic parental and sibling cardiovascular anomalies associated with congenital left ventricular outflow tract lesions. Pediatrics 114: 691-696.
36. Li, C., X. Li, S. Pang, W. Chen, X. Qin et al., 2014 Novel and functional DNA sequence variants within the GATA6 gene promoter in ventricular septal defects. Int. J. Mol. Sci. 15: 12677-12687.
37. Li, H., S. Cherry, D. Klinedinst, V. Deleon, J. Redig et al., 2012 Genetic modifiers predisposing to congenital heart disease in the sensitized Down syndrome population. Circ Cardiovasc Genet 5: 301-308.
38. Li, Y., N. T. Klena, G. C. Gabriel, X. Liu, A. J. Kim et al., 2015 Global genetic analysis in mice unveils central role for cilia in congenital heart disease. Nature 521: 520-524.
39. Lignon, J. M., Z. Bichler, B. Hivert, F. E. Gannier, P. Cosnay et al., 2008 Altered heart rate control in transgenic mice carrying the KCNJ6 gene of the human chromosome 21. Physiol. Genomics 33: 230-239.
40. Lin, X., L. Rinaldo, A. F. Fazly, and X. Xu, 2007 Depletion of Med10 enhances Wnt and suppresses Nodal signaling during zebrafish embryogenesis. Dev. Biol. 303: 536-548.
41. Lin, Y., G. C. Tseng, S. Y. Cheong, L. J. Bean, S. L. Sherman et al., 2008 Smarter clustering methods for SNP genotype calling. Bioinformatics 24: 2665-2671.
42. Liu, C., M. Morishima, T. Yu, S. Matsui, L. Zhang et al., 2011 Genetic analysis of Down syndrome-associated heart defects in mice. Hum. Genet. 130: 623-632.
43. Liu, C., M. Morishima, X. Jiang, T. Yu, K. Meng et al., 2014 Engineered chromosome-based genetic mapping establishes a 3.7 Mb critical genomic region for Down syndrome-associated heart defects in mice. Hum. Genet. 133: 743-753.
44. Locke, A. E., K. J. Dooley, S. W. Tinker, S. Y. Cheong, E. Feingold et al., 2010 Variation in folate pathway genes contributes to risk of congenital heart defects among individuals with Down syndrome. Genet. Epidemiol. 34: 613-623.
45. Ma, H., Y. Hao, X. Dong, Q. Gong, J. Chen et al., 2012 Molecular mechanisms and function prediction of long noncoding RNA. ScientificWorldJournal 2012: 541786.
46. Manning, A. L., N. J. Ganem, S. F. Bakhoum, M. Wagenbach, L. Wordeman et al., 2007 The kinesin-13 proteins Kif2a, Kif2b, and Kif2c/MCAK have distinct roles during mitosis in human cells. Mol. Biol. Cell 18: 2970-2979.
47. Marinou, K., C. Christodoulides, C. Antoniades, and M. Koutsilieris, 2012 Wnt signaling in cardiovascular physiology. Trends Endocrinol. Metab. 23: 628-636.
48. Martinez, S. R., M. S. Gay, and L. Zhang, 2015 Epigenetic mechanisms in heart development and disease. Drug Discov. Today. 20: 799-811.
49. Moller, J. H., H. D. Allen, E. B. Clark, A. S. Dajani, A. Golden et al., 1993 Report of the task force on children and youth. American Heart Association. Circulation 88: 2479-2486.
50. Pierpont, M. E., C. T. Basson, D. W. J. Benson, B. D. Gelb, T. M. Giglia et al., 2007 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 115: 3015-3038.
51. Price, A. L., N. J. Patterson, R. M. Plenge, M. E. Weinblatt, N. A. Shadick et al., 2006 Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38: 904-909.
52. Pruim, R. J., R. P. Welch, S. Sanna, T. M. Teslovich, P. S. Chines et al., 2010 LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26: 2336-2337.
53. Puertollano, R., 2005 Interactions of TOM1L1 with the multivesicular body sorting machinery. J. Biol. Chem. 280: 9258-9264.
54. Purcell, S., B. Neale, K. Todd-Brown, L. Thomas, M. A. Ferreira et al., 2007 PLINK: a tool set for whole-genome association and populationbased linkage analyses. Am. J. Hum. Genet. 81: 559-575.
55. Raid, R., D. Krinka, L. Bakhoff, E. Abdelwahid, E. Jokinen et al., 2009 Lack of Gata3 results in conotruncal heart anomalies in mouse. Mech. Dev. 126: 80-89.
56. Ramachandran, D., J. G. Mulle, A. E. Locke, L. J. Bean, T. C. Rosser et al., 2015 Contribution of copy-number variation to Down syndrome-associated atrioventricular septal defects. Genet. Med. 17: 554-560.
57. Reller, M. D., M. J. Strickland, T. Riehle-Colarusso, W. T. Mahle, and A. Correa, 2008 Prevalence of congenital heart defects in metropolitan Atlanta, 1998-2005. J. Pediatr. 153: 807-813.
58. Ripoll, C., I. Rivals, E. A. Yahya-Graison, L. Dauphinot, E. Paly et al., 2012 Molecular signatures of cardiac defects in down syndrome lymphoblastoid cell lines suggest altered ciliome and hedgehog pathways. PLoS One 7: e41616.
59. Robinson, S. W., C. D. Morris, E. Goldmuntz, M. D. Reller, M. A. Jones et al., 2003 Missense mutations in CRELD1 are associated with cardiac atrioventricular septal defects. Am. J. Hum. Genet. 72: 1047-1052.
60. Rosenbloom, K. R., C. A. Sloan, V. S. Malladi, T. R. Dreszer, K. Learned et al., 2013 ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res. 41: D56-D63.
61. Russo, C. A., and A. Elixhauser, 2007 Healthcare Cost and Utilization Project (HCUP) Statistical Brief #24: Hospitalizations for Birth Defects, 2004. US Agency for Healthcare Research and Quality, Rockville, MD.
62. Sailani, M. R., P. Makrythanasis, A. Valsesia, F. A. Santoni, S. Deutsch et al., 2013 The complex SNP and CNV genetic architecture of the increased risk of congenital heart defects in Down syndrome. Genome Res. 23: 1410-1421.
63. Salemi, M., C. Barone, C. Romano, F. Zolezzi, C. Romano et al., 2012 Gene expression profiling and qRT-PCR expression of RRP1B, PCNT, KIF21A and ADRB2 in leucocytes of Down's syndrome subjects. J. Genet. 91: e18-e23.
64. Sato, S., C. Tomomori-Sato, C. A. Banks, I. Sorokina, T. J. Parmely et al., 2003 Identification of mammalian Mediator subunits with similarities to yeast Mediator subunits Srb5, Srb6, Med11, and Rox3. J. Biol. Chem. 278: 15123-15127.
65. Schott, J. J., D. W. Benson, C. T. Basson, W. Pease, G. M. Silberbach et al., 1998 Congenital heart disease caused by mutations in the transcription factor NKX2-5. Science 281: 108-111.
66. Shan, J. P., X. L. Wang, Y. G. Qiao, H. X. Wan Yan, W. H. Huang et al., 2014 Novel and functional DNA sequence variants within the GATA5 gene promoter in ventricular septal defects. World J. Pediatr. 10: 348-353.
67. Shuler, C. O., G. B. Black, and J. M. Jerrell, 2013 Population-based treated prevalence of congenital heart disease in a pediatric cohort. Pediatr. Cardiol. 34: 606-611.
68. Soemedi, R., I. J. Wilson, J. Bentham, R. Darlay, A. Topf et al., 2012 Contribution of global rare copy-number variants to the risk of sporadic congenital heart disease. Am. J. Hum. Genet. 91: 489-501.
69. St Johnston, D., 2002 The art and design of genetic screens: Drosophila melanogaster. Nat. Rev. Genet. 3: 176-188.
70. Tanner, S. M., J. L. Austin, G. Leone, L. J. Rush, C. Plass et al., 2001 BAALC, the human member of a novel mammalian neuroectoderm gene lineage, is implicated in hematopoiesis and acute leukemia. Proc. Natl. Acad. Sci. USA 98: 13901-13906.
71. Umbhauer, M., A. Djiane, C. Goisset, A. Penzo-Mendez, J. F. Riou et al., 2000 The C-terminal cytoplasmic Lys-thr-X-X-X-Trp motif in frizzled receptors mediates Wnt/beta-catenin signalling. EMBO J. 19: 4944-4954.
72. Vallaster, M., C. D. Vallaster, and S. M. Wu, 2012 Epigenetic mechanisms in cardiac development and disease. Acta Biochim. Biophys. Sin. (Shanghai) 44: 92-102.
73. Van Rijen, E. H. M., E. M. W. J. Utens, J. W. Roos-Hesselink, F. J. Meijboom, R. T. Van Domburg et al., 2005 Longitudinal development of psychopathology in an adult congenital heart disease cohort. Int. J. Cardiol. 99: 315-323.
74. Waitzman, N. J., P. S. Romano, and R. M. Scheffler, 1994 Estimates of the economic costs of birth defects. Inquiry 31: 188-205.
75. Wang, J., X. J. Luo, Y. F. Xin, Y. Liu, Z. M. Liu et al., 2012 Novel GATA6 mutations associated with congenital ventricular septal defect or tetralogy of Fallot. DNA Cell Biol. 31: 1610-1617.
76. Wapinski, O., and H. Y. Chang, 2011 Long noncoding RNAs and human disease. Trends Cell Biol. 21: 354-361.
77. Wilusz, J. E., H. Sunwoo, and D. L. Spector, 2009 Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 23: 1494-1504.
78. Xu, J., Y. Lin, L. Si, G. Jin, J. Dai et al., 2014 Genetic variants at 10p11 confer risk of tetralogy of Fallot in Chinese of Nanjing. PLoS One 9: e89636.
79. Zaidi, S., M. Choi, H. Wakimoto, L. Ma, J. Jiang et al., 2013 De novo mutations in histone-modifying genes in congenital heart disease. Nature 498: 220-223.
80. Zheng, G. F., D. Wei, H. Zhao, N. Zhou, Y. Q. Yang et al., 2012 A novel GATA6 mutation associated with congenital ventricular septal defect. Int. J. Mol. Med. 29: 1065-1071.
81. Zwick, M. E., J. L. Salstrom, and C. H. Langley, 1999 Genetic variation in rates of nondisjunction: association of two naturally occurring polymorphisms in the chromokinesin nod with increased rates of nondisjunction in Drosophila melanogaster. Genetics 152: 1605-1614.