Identification of novel candidate gene loci and increased sex chromosome aneuploidy among infants with conotruncal heart defects

American Journal of Medical Genetics, Part A

Volumn 164, Issue 2, 2014, Pages 397-406

  Osoegawa, Kazutoyo ^a   Iovannisci, David M ^a   Lin, Bin ^a   Parodi, Christina ^a   Schultz, Kathleen ^a   Shaw, Gary M ^b   Lammer, Edward J ^a  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Array comparative genomic hybridization (array CGH); Candidate genes; Conotruncal heart defects; Microdeletions duplications; Sex chromosome aneuploidy

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; CRK LIKE PROTEIN; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR SLUG;

ARTICLE; BMPR1A GENE; COMPARATIVE GENOMIC HYBRIDIZATION; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; CRKL GENE; DISEASE ACTIVITY; DISEASE ASSOCIATION; FEMALE; GATA4 GENE; GENE; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENETIC VARIABILITY; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RISK ASSESSMENT; RISK FACTOR; SENSITIVITY ANALYSIS; SEX CHROMOSOME ABERRATION; SNAI2 GENE; ZFHX4 GENE;

ARRAY COMPARATIVE GENOMIC HYBRIDIZATION (ARRAY-CGH); CANDIDATE GENES; CONOTRUNCAL HEART DEFECTS; MICRODELETIONS/DUPLICATIONS; SEX CHROMOSOME ANEUPLOIDY;

ANEUPLOIDY; CALIFORNIA; CHROMOSOME ABERRATIONS; CHROMOSOME DELETION; CHROMOSOME DUPLICATION; CHROMOSOMES, HUMAN, PAIR 22; COMPARATIVE GENOMIC HYBRIDIZATION; DNA COPY NUMBER VARIATIONS; FEMALE; GENE ORDER; GENETIC LOCI; HEART DEFECTS, CONGENITAL; HUMANS; INFANT; INFANT, NEWBORN; KARYOTYPE; MALE; REGISTRIES; SEX CHROMOSOMES;

EID: 84892865401     PISSN: 15524825     EISSN: 15524833     Source Type: Journal    
DOI: 10.1002/ajmg.a.36291     Document Type: Article

References (57)

1. Aerts S, Lambrechts D, Maity S, Van Loo P, Coessens B, De Smet F, Tranchevent LC, De Moor B, Marynen P, Hassan B, Carmeliet P, Moreau Y. 2006. Gene prioritization through genomic data fusion. Nat Biotechnol 24:537-544.
2. Alliman S, Coppinger J, Marcadier J, Thiese H, Brock P, Shafer S, Weaver C, Asamoah A, Leppig K, Dyack S, Morash B, Schultz R, Torchia BS, Lamb AN, Bejjani BA. 2010. Clinical and molecular characterization of individuals with recurrent genomic disorder at 10q22.3q23.2. Clin Genet 78:162-168.
3. Balciuniene J, Feng N, Iyadurai K, Hirsch B, Charnas L, Bill BR, Easterday MC, Staaf J, Oseth L, Czapansky-Beilman D, Avramopoulos D, Thomas GH, Borg A, Valle D, Schimmenti LA, Selleck SB. 2007. Recurrent 10q22-q23 deletions: A genomic disorder on 10q associated with cognitive and behavioral abnormalities. Am J Hum Genet 80:938-947.
4. Barber JC, Maloney VK, Huang S, Bunyan DJ, Cresswell L, Kinning E, Benson A, Cheetham T, Wyllie J, Lynch SA, Zwolinski S, Prescott L, Crow Y, Morgan R, Hobson E. 2008. 8p23.1 duplication syndrome; a novel genomic condition with unexpected complexity revealed by array CGH. Eur J Hum Genet 16:18-27.
5. Barber JC, Bunyan D, Curtis M, Robinson D, Morlot S, Dermitzel A, Liehr T, Alves C, Trindade J, Paramos AI, Cooper C, Ocraft K, Taylor EJ, Maloney VK. 2010. 8p23.1 duplication syndrome differentiated from copy number variation of the defensin cluster at prenatal diagnosis in four new families. Mol Cytogenet 3:3.
6. Barriot R, Breckpot J, Thienpont B, Brohee S, Van Vooren S, Coessens B, Tranchevent LC, Van Loo P, Gewillig M, Devriendt K, Moreau Y. 2010. Collaboratively charting the gene-to-phenotype network of human congenital heart defects. Genome Med 2:16.
7. Breckpot J, Thienpont B, Bauters M, Tranchevent LC, Gewillig M, Allegaert K, Vermeesch JR, Moreau Y, Devriendt K. 2012a. Congenital heart defects in a novel recurrent 22q11.2 deletion harboring the genes CRKL and MAPK1. Am J Med Genet Part A 158A:574-580.
8. Breckpot J, Tranchevent LC, Thienpont B, Bauters M, Troost E, Gewillig M, Vermeesch JR, Moreau Y, Devriendt K, Van Esch H. 2012b. BMPR1A is a candidate gene for congenital heart defects associated with the recurrent 10q22q23 deletion syndrome. Eur J Med Genet 55:12-16.
9. Chen J, Bardes EE, Aronow BJ, Jegga AG. 2009. ToppGene suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res 37:305-311.
10. Clark EB. 1996. Pathogenetic mechanisms of congenital cardiovascular malformations revisited. Semin Perinatol 20:465-472.
11. Ferencz C, Rubin JD, McCarter RJ, Brenner JI, Neill CA, Perry LW, Hepner SI, Downing JW. 1985. Congenital heart disease: Prevalence at livebirth. The Baltimore-Washington Infant Study. Am J Epidemiol 121:31-36.
12. Garg V, Kathiriya IS, Barnes R, Schluterman MK, King IN, Butler CA, Rothrock CR, Eapen RS, Hirayama-Yamada K, Joo K, Matsuoka R, Cohen JC, Srivastava D. 2003. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424:443-447.
13. Greenway SC, Pereira AC, Lin JC, DePalma SR, Israel SJ, Mesquita SM, Ergul E, Conta JH, Korn JM, McCarroll SA, Gorham JM, Gabriel S, Altshuler DM, Quintanilla-Dieck Mde L, Artunduaga MA, Eavey RD, Plenge RM, Shadick NA, Weinblatt ME, De Jager PL, Hafler DA, Breitbart RE, Seidman JG, Seidman CE. 2009. De novo copy number variants identify new genes and loci in isolated sporadic tetralogy of Fallot. Nat Genet 41:931-935.
14. Hemmi K, Ma D, Miura Y, Kawaguchi M, Sasahara M, Hashimoto-Tamaoki T, Tamaoki T, Sakata N, Tsuchiya K. 2006. A homeodomain-zinc finger protein, ZFHX4, is expressed in neuronal differentiation manner and suppressed in muscle differentiation manner. Biol Pharm Bull 29:1830-1835.
15. Hollox EJ, Armour JA, Barber JC. 2003. Extensive normal copy number variation of a beta-defensin antimicrobial-gene cluster. Am J Hum Genet 73:591-600.
16. Jenkins KJ, Correa A, Feinstein JA, Botto L, Britt AE, Daniels SR, Elixson M, Warnes CA, Webb CL. 2007. Noninherited risk factors and congenital cardiovascular defects: Current knowledge: A scientific statement from the American Heart Association Council on Cardiovascular Disease in the Young: Endorsed by the American Academy of Pediatrics. Circulation 115:2995-3014.
17. Jiang R, Lan Y, Norton CR, Sundberg JP, Gridley T. 1998. The Slug gene is not essential for mesoderm or neural crest development in mice. Dev Biol 198:277-285.
18. Jonsson G, Staaf J, Olsson E, Heidenblad M, Vallon-Christersson J, Osoegawa K, de Jong P, Oredsson S, Ringner M, Hoglund M, Borg A. 2007. High-resolution genomic profiles of breast cancer cell lines assessed by tiling BAC array comparative genomic hybridization. Genes Chromosomes Cancer 46:543-558.
19. Karsh RB. 1975. Congenital heart disease in 49, XXXXY syndrome. Pediatrics 56:462-464.
20. Kirby ML. 2002. Molecular embryogenesis of the heart. Pediatr Dev Pathol 5:516-543.
21. Krzywinski M, Bosdet I, Smailus D, Chiu R, Mathewson C, Wye N, Barber S, Brown-John M, Chan S, Chand S, Cloutier A, Girn N, Lee D, Masson A, Mayo M, Olson T, Pandoh P, Prabhu AL, Schoenmakers E, Tsai M, Albertson D, Lam W, Choy CO, Osoegawa K, Zhao S, de Jong PJ, Schein J, Jones S, Marra MA. 2004. A set of BAC clones spanning the human genome. Nucleic Acids Res 32:3651-3660.
22. Kurahashi H, Tsuda E, Kohama R, Nakayama T, Masuno M, Imaizumi K, Kamiya T, Sano T, Okada S, Nishisho I. 1997. Another critical region for deletion of 22q11: A study of 100 patients. Am J Med Genet 72:180-185.
23. Lammer EJ, Chak JS, Iovannisci DM, Schultz K, Osoegawa K, Yang W, Carmichael SL, Shaw GM. 2009. Chromosomal abnormalities among children born with conotruncal cardiac defects. Birth Defects Res A Clin Mol Teratol 85:30-35.
24. Lary JM, Paulozzi LJ. 2001. Sex differences in the prevalence of human birth defects: A population-based study. Teratology 64:237-251.
25. Lindsay EA, Vitelli F, Su H, Morishima M, Huynh T, Pramparo T, Jurecic V, Ogunrinu G, Sutherland HF, Scambler PJ, Bradley A, Baldini A. 2001. Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410:97-101.
26. Ma C, Quesnelle KM, Sparano A, Rao S, Park MS, Cohen MA, Wang Y, Samanta M, Kumar MS, Aziz MU, Naylor TL, Weber BL, Fakharzadeh SS, Weinstein GS, Vachani A, Feldman MD, Brose MS. 2009. Characterization CSMD1 in a large set of primary lung, head and neck, breast and skin cancer tissues. Cancer Biol Ther 8:907-916.
27. Merscher S, Funke B, Epstein JA, Heyer J, Puech A, Lu MM, Xavier RJ, Demay MB, Russell RG, Factor S, Tokooya K, Jore BS, Lopez M, Pandita RK, Lia M, Carrion D, Xu H, Schorle H, Kobler JB, Scambler P, Wynshaw-Boris A, Skoultchi AI, Morrow BE, Kucherlapati R. 2001. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104:619-629.
28. Meschede D, Nekarda T, Kececioglu D, Loser H, Vogt J, Miny P, Horst J. 1995. Congenital heart disease in the 48, XXYY syndrome. Clin Genet 48:100-102.
29. Moon AM, Guris DL, Seo JH, Li L, Hammond J, Talbot A, Imamoto A. 2006. Crkl deficiency disrupts Fgf8 signaling in a mouse model of 22q11 deletion syndromes. Dev Cell 10:71-80.
30. Morris JK, Alberman E, Scott C, Jacobs P. 2008. Is the prevalence of Klinefelter syndrome increasing? Eur J Hum Genet 16:163-170.
31. Nemer G, Fadlalah F, Usta J, Nemer M, Dbaibo G, Obeid M, Bitar F. 2006. A novel mutation in the GATA4 gene in patients with Tetralogy of Fallot. Hum Mutat 27:293-294.
32. O'Malley CD, Shaw GM, Wasserman CR, Lammer EJ. 1996. Epidemiologic characteristics of conotruncal heart defects in California, 1987-1988. Teratology 53:374-377.
33. Oram KF, Carver EA, Gridley T. 2003. Slug expression during organogenesis in mice. Anat Rec A Discov Mol Cell Evol Biol 271:189-191.
34. Osoegawa K, Vessere GM, Utami KH, Mansilla MA, Johnson MK, Riley BM, L'Heureux J, Pfundt R, Staaf J, van der Vliet WA, Lidral AC, Schoenmakers EF, Borg A, Schutte BC, Lammer EJ, Murray JC, de Jong PJ. 2008. Identification of novel candidate genes associated with cleft lip and palate using array comparative genomic hybridisation. J Med Genet 45:81-86.
35. Pehlivan T, Pober BR, Brueckner M, Garrett S, Slaugh R, Van Rheeden R, Wilson DB, Watson MS, Hing AV. 1999. GATA4 haploinsufficiency in patients with interstitial deletion of chromosome region 8p23.1 and congenital heart disease. Am J Med Genet 83:201-206.
36. Perez-Mancera PA, Gonzalez-Herrero I, Maclean K, Turner AM, Yip MY, Sanchez-Martin M, Garcia JL, Robledo C, Flores T, Gutierrez-Adan A, Pintado B, Sanchez-Garcia I. 2006. SLUG (SNAI2) overexpression in embryonic development. Cytogenet Genome Res 114:24-29.
37. Rauch A, Zink S, Zweier C, Thiel CT, Koch A, Rauch R, Lascorz J, Huffmeier U, Weyand M, Singer H, Hofbeck M. 2005. Systematic assessment of atypical deletions reveals genotype-phenotype correlation in 22q11.2. J Med Genet 42:871-876.
38. Rauch R, Hofbeck M, Zweier C, Koch A, Zink S, Trautmann U, Hoyer J, Kaulitz R, Singer H, Rauch A. 2010. Comprehensive genotype-phenotype analysis in 230 patients with tetralogy of Fallot. J Med Genet 47:321-331.
39. Reller MD, Strickland MJ, Riehle-Colarusso T, Mahle WT, Correa A. 2008. Prevalence of congenital heart defects in metropolitan Atlanta, 1998-2005. J Pediatr 153:807-813.
40. Sanchez-Martin M, Rodriguez-Garcia A, Perez-Losada J, Sagrera A, Read AP, Sanchez-Garcia I. 2002. SLUG (SNAI2) deletions in patients with Waardenburg disease. Hum Mol Genet 11:3231-3236.
41. Sanchez-Martin M, Perez-Losada J, Rodriguez-Garcia A, Gonzalez-Sanchez B, Korf BR, Kuster W, Moss C, Spritz RA, Sanchez-Garcia I. 2003. Deletion of the SLUG (SNAI2) gene results in human piebaldism. Am J Med Genet Part A 122A:125-132.
42. Shaikh TH, Kurahashi H, Saitta SC, O'Hare AM, Hu P, Roe BA, Driscoll DA, McDonald-McGinn DM, Zackai EH, Budarf ML, Emanuel BS. 2000. Chromosome 22-specific low copy repeats and the 22q11.2 deletion syndrome: Genomic organization and deletion endpoint analysis. Hum Mol Genet 9:489-501.
43. Shaikh TH, O'Connor RJ, Pierpont ME, McGrath J, Hacker AM, Nimmakayalu M, Geiger E, Emanuel BS, Saitta SC. 2007. Low copy repeats mediate distal chromosome 22q11.2 deletions: Sequence analysis predicts breakpoint mechanisms. Genome Res 17:482-491.
44. Shaw GM, Carmichael SL, Yang W, Lammer EJ. 2010. Periconceptional nutrient intakes and risks of conotruncal heart defects. Birth Defects Res A Clin Mol Teratol 88:144-151.
45. Soemedi R, Wilson IJ, Bentham J, Darlay R, Topf A, Zelenika D, Cosgrove C, Setchfield K, Thornborough C, Granados-Riveron J, Blue GM, Breckpot J, Hellens S, Zwolinkski S, Glen E, Mamasoula C, Rahman TJ, Hall D, Rauch A, Devriendt K, Gewillig M, J Os, Winlaw DS, Bu'Lock F, Brook JD, Bhattacharya S, Lathrop M, Santibanez-Koref M, Cordell HJ, Goodship JA, Keavney BD. 2012. Contribution of global rare copy-number variants to the risk of sporadic congenital heart disease. Am J Hum Genet 91:489-501.
46. Takash W, Canizares J, Bonneaud N, Poulat F, Mattei MG, Jay P, Berta P. 2001. SOX7 transcription factor: Sequence, chromosomal localisation, expression, transactivation and interference with Wnt signalling. Nucleic Acids Res 29:4274-4283.
47. Tartaglia N, Ayari N, Howell S, D'Epagnier C, Zeitler P. 2011. 48, XXYY, 48, XXXY and 49, XXXXY syndromes: Not just variants of Klinefelter syndrome. Acta Paediatr 100:851-860.
48. Tennant PW, Samarasekera SD, Pless-Mulloli T, Rankin J. 2011. Sex differences in the prevalence of congenital anomalies: A population-based study. Birth Defects Res A Clin Mol Teratol 91:894-901.
49. Tomita-Mitchell A, Maslen CL, Morris CD, Garg V, Goldmuntz E. 2007. GATA4 sequence variants in patients with congenital heart disease. J Med Genet 44:779-783.
50. Vallejo-Illarramendi A, Zang K, Reichardt LF. 2009. Focal adhesion kinase is required for neural crest cell morphogenesis during mouse cardiovascular development. J Clin Invest 119:2218-2230.
51. van Bon BW, Balciuniene J, Fruhman G, Nagamani SC, Broome DL, Cameron E, Martinet D, Roulet E, Jacquemont S, Beckmann JS, Irons M, Potocki L, Lee B, Cheung SW, Patel A, Bellini M, Selicorni A, Ciccone R, Silengo M, Vetro A, Knoers NV, de Leeuw N, Pfundt R, Wolf B, Jira P, Aradhya S, Stankiewicz P, Brunner HG, Zuffardi O, Selleck SB, Lupski JR, de Vries BB. 2011. The phenotype of recurrent 10q22q23 deletions and duplications. Eur J Hum Genet 19:400-408.
52. van Engelen K, Topf A, Keavney BD, Goodship JA, van der Velde ET, Baars MJ, Snijder S, Moorman AF, Postma AV, Mulder BJ. 2010. 22q11.2 deletion syndrome is under-recognised in adult patients with tetralogy of Fallot and pulmonary atresia. Heart 96:621-624.
53. Vissers LE, van Ravenswaaij CM, Admiraal R, Hurst JA, de Vries BB, Janssen IM, van der Vliet WA, Huys EH, de Jong PJ, Hamel BC, Schoenmakers EF, Brunner HG, Veltman JA, van Kessel AG. 2004. Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet 36:955-957.
54. Wat MJ, Shchelochkov OA, Holder AM, Breman AM, Dagli A, Bacino C, Scaglia F, Zori RT, Cheung SW, Scott DA, Kang SH. 2009. Chromosome 8p23.1 deletions as a cause of complex congenital heart defects and diaphragmatic hernia. Am J Med Genet Part A 149A:1661-1677.
55. Xu H, Morishima M, Wylie JN, Schwartz RJ, Bruneau BG, Lindsay EA, Baldini A. 2004. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 131:3217-3227.
56. Yagi H, Furutani Y, Hamada H, Sasaki T, Asakawa S, Minoshima S, Ichida F, Joo K, Kimura M, Imamura S, Kamatani N, Momma K, Takao A, Nakazawa M, Shimizu N, Matsuoka R. 2003. Role of TBX1 in human del22q11.2 syndrome. Lancet 362:1366-1373.
57. Zhang C, Basta T, Klymkowsky MW. 2005. SOX7 and SOX18 are essential for cardiogenesis in Xenopus. Dev Dyn 234:878-891.