Dissecting the genotype in syndromic intellectual disability using whole exome sequencing in addition to genome-wide copy number analysis

Human Genetics

Volumn 132, Issue 7, 2013, Pages 825-841

  Classen, Carl Friedrich ^a   Riehmer, Vera ^b,c   Landwehr, Christina ^c,d   Kosfeld, Anne ^b   Heilmann, Stefanie ^c   Scholz, Caroline ^b   Kabisch, Sarah ^a,e   Engels, Hartmut ^c   Tierling, Sascha ^f   Zivicnjak, Miroslav ^b   Schacherer, Frank ^g   Haffner, Dieter ^a,b   Weber, Ruthild G ^b,c  

^a ROSTOCK UNIVERSITY MEDICAL CENTER   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d Institute for Medical Diagnostics   (Germany)

^e UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^f SAARLAND UNIVERSITY   (Germany)

^g BIOBASE GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANTHROPOMETRY; ARTICLE; BLM1 GENE; CASE REPORT; CDC45L GENE; CHEK2 GENE; CHILD; CHROMOSOME 14Q; CHROMOSOME 22Q; CHROMOSOME DELETION; CHROMOSOME DUPLICATION; CLINICAL FEATURE; DLK1 GENE; EXOME; EYA1 GENE; FBN1 GENE; FEMALE; GENE; GENE DOSAGE; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; GP1BB GENE; HETEROZYGOSITY; HUMAN; HYPERPIGMENTATION; HYPOPIGMENTATION; INTELLECTUAL IMPAIRMENT; KIDNEY MALFORMATION; MALE; MARFAN SYNDROME; MISSENSE MUTATION; PRIORITY JOURNAL; SCHOOL CHILD; SEQUENCE ANALYSIS; TALL STATURE;

CHROMOSOME DELETION; CHROMOSOMES, HUMAN, PAIR 14; CHROMOSOMES, HUMAN, PAIR 22; COGNITION DISORDERS; CYTOSKELETAL PROTEINS; EXOME; FEMALE; GENE DOSAGE; GENETIC DISEASES, INBORN; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; GTPASE-ACTIVATING PROTEINS; HUMANS; MALE; MUTATION, MISSENSE; NUCLEAR PROTEINS;

EID: 84879503677     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-013-1296-1     Document Type: Article

References (49)

1. Abdelhak S, Kalatzis V, Heilig R, Compain S, Samson D, Vincent C, Weil D, Cruaud C, Sahly I, Leibovici M, Bitner-Glindzicz M, Francis M, Lacombe D, Vigneron J, Charachon R, Boven K, Bedbeder P, Van Regemorter N, Weissenbach J, Petit C (1997) A human homologue of the Drosophila eyes absent gene underlies branchio-oto-renal (BOR) syndrome and identifies a novel gene family. Nat Genet 15(2):157-164
2. Bamshad MJ, Ng SB, Bigham AW, Tabor HK, Emond MJ, Nickerson DA, Shendure J (2011) Exome sequencing as a tool for Mendelian disease gene discovery. Nat Rev Genet 12(11):745-755
3. Bell DW, Varley JM, Szydlo TE, Kang DH, Wahrer DC, Shannon KE, Lubratovich M, Verselis SJ, Isselbacher KJ, Fraumeni JF, Birch JM, Li FP, Garber JE, Haber DA (1999) Heterozygous germ line hCHK2 mutations in Li-Fraumeni syndrome. Science 286(5449):2528-2531
4. Bergmann C, Zerres K, Senderek J, Rudnik-Schoneborn S, Eggermann T, Hausler M, Mull M, Ramaekers VT (2003) Oligophrenin 1 (OPHN1) gene mutation causes syndromic X-linked mental retardation with epilepsy, rostral ventricular enlargement and cerebellar hypoplasia. Brain 126:1537-1544
5. Billuart P, Bienvenu T, Ronce N, des Portes V, Vinet MC, Zemni R, Crollius HR, Carrie A, Fauchereau F, Cherry M, Briault S, Hamel B, Fryns J-P, Beldjord C, Kahn A, Moraine C, Chelly J (1998) Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392:923-926
6. Bolar N, Van Laer L, Loeys BL (2012) Marfan syndrome: from gene to therapy. Curr Opin Pediatr 24(4):498-504
7. Chang VY, Quintero-Rivera F, Baldwin EE, Woo K, Martinez-Agosto JA, Fu C, Gomperts BN (2011) B-acute lymphoblastic leukemia and cystinuria in a patient with duplication 22q11.21 detected by chromosomal microarray analysis. Pediatr Blood Cancer 56(3):470-473
8. Cybulski C, Górski B, Huzarski T, Masojć B, Mierzejewski M, Debniak T, Teodorczyk U, Byrski T, Gronwald J, Matyjasik J, Zlowocka E, Lenner M, Grabowska E, Nej K, Castaneda J, Medrek K, Szymańska A, Szymańska J, Kurzawski G, Suchy J, Oszurek O, Witek A, Narod SA, Lubiński J (2004) CHEK2 is a multiorgan cancer susceptibility gene. Am J Hum Genet 75(6):1131-1135
9. de Ligt J, Willemsen MH, van Bon BW, Kleefstra T, Yntema HG, Kroes T, Vulto-van Silfhout AT, Koolen DA, de Vries P, Gilissen C, del Rosario M, Hoischen A, Scheffer H, de Vries BB, Brunner HG, Veltman JA, Vissers LE (2012) Diagnostic exome sequencing in persons with severe intellectual disability. N Engl J Med 367(20):1921-1929
10. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43(5):491-498
11. Desrichard A, Bidet Y, Uhrhammer N, Bignon YJ (2011) CHEK2 contribution to hereditary breast cancer in non-BRCA families. Breast Cancer Res 13(6):R119
12. Dietz HC, Cutting GR, Pyeritz RE, Maslen CL, Sakai LY, Corson GM, Puffenberger EG, Hamosh A, Nanthakumar EJ, Curristin SM, Stetten G, Meyers DA, Francomano CA (1991) Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature 352:337-339
13. El-Maarri O (2004) SIRPH analysis: SNuPE with IP-RP-HPLC for quantitative measurements of DNA methylation at specific CpG sites. Methods Mol Biol 287:195-205
14. Engels H, Brockschmidt A, Hoischen A, Landwehr C, Bosse K, Walldorf C, Toedt G, Radlwimmer B, Propping P, Lichter P, Weber RG (2007) DNA microarray analysis identifies candidate regions and genes in unexplained mental retardation. Neurology 68(10):743-750
15. Ensenauer RE, Adeyinka A, Flynn HC, Michels VV, Lindor NM, Dawson DB, Thorland EC, Lorentz CP, Goldstein JL, McDonald MT, Smith WE, Simon-Fayard E, Alexander AA, Kulharya AS, Ketterling RP, Clark RD, Jalal SM (2003) Microduplication 22q11.2, an emerging syndrome: clinical, cytogenetic, and molecular analysis of thirteen patients. Am J Hum Genet 73(5):1027-1040
16. Faivre L, Masurel-Paulet A, Collod-Béroud G, Callewaert BL, Child AH, Stheneur C, Binquet C, Gautier E, Chevallier B, Huet F, Loeys BL, Arbustini E, Mayer K, Arslan-Kirchner M, Kiotsekoglou A, Comeglio P, Grasso M, Halliday DJ, Béroud C, Bonithon-Kopp C, Claustres M, Robinson PN, Adès L, De Backer J, Coucke P, Francke U, De Paepe A, Boileau C, Jondeau G (2009) Clinical and molecular study of 320 children with Marfan syndrome and related type I fibrillinopathies in a series of 1009 probands with pathogenic FBN1 mutations. Pediatrics 123(1):391-398
17. Fensterer H, Radlwimmer B, Sträter J, Buchholz M, Aust DE, Julié C, Radvanyi F, Nordlinger B, Belluco C, Van Cutsem E, Köhne CH, Kestler HA, Schwaenen C, Nessling M, Lutz MP, Lichter P, Gress TM, EORTC Gastrointestinal (GI) Group (2007) Matrix-comparative genomic hybridization from multicenter formalin-fixed paraffin-embedded colorectal cancer tissue blocks. BMC Cancer 7:58
18. Frisancho AR (2008) Anthropometric standards. An interactive nutritional reference of body size and body composition for children and adults. The University of Michigan Press, Ann Arbor
19. German J (1997) Bloom's syndrome. XX. The first 100 cancers. Cancer Genet Cytogenet 93(1):100-106
20. German J, Sanz MM, Ciocci S, Ye TZ, Ellis NA (2007) Syndrome-causing mutations of the BLM gene in persons in the Bloom's Syndrome Registry. Hum Mutat 28(8):743-753
21. Girirajan S, Rosenfeld JA, Coe BP, Parikh S, Friedman N, Goldstein A, Filipink RA, McConnell JS, Angle B, Meschino WS, Nezarati MM, Asamoah A, Jackson KE, Gowans GC, Martin JA, Carmany EP, Stockton DW, Schnur RE, Penney LS, Martin DM, Raskin S, Leppig K, Thiese H, Smith R, Aberg E, Niyazov DM, Escobar LF, El-Khechen D, Johnson KD, Lebel RR, Siefkas K, Ball S, Shur N, McGuire M, Brasington CK, Spence JE, Martin LS, Clericuzio C, Ballif BC, Shaffer LG, Eichler EE (2012) Phenotypic heterogeneity of genomic disorders and rare copy-number variants. N Engl J Med 367(14):1321-1331
22. Hoffmann K, Heller R (2011) Uniparental disomies 7 and 14. Best Pract Res Clin Endocrinol Metab 25(1):77-100
23. Kagami M, Sekita Y, Nishimura G, Irie M, Kato F, Okada M, Yamamori S, Kishimoto H, Nakayama M, Tanaka Y, Matsuoka K, Takahashi T, Noguchi M, Tanaka Y, Masumoto K, Utsunomiya T, Kouzan H, Komatsu Y, Ohashi H, Kurosawa K, Kosaki K, Ferguson-Smith AC, Ishino F, Ogata T (2008) Deletions and epimutations affecting the human 14q32.2 imprinted region in individuals with paternal and maternal upd(14)-like phenotypes. Nat Genet 40(2):237-242
24. Kaufman AS, Kaufman N (1983) Kaufman assessment battery for children, manual. American Guidance Service, Circle Pines
25. Krug P, Morinière V, Marlin S, Koubi V, Gabriel HD, Colin E, Bonneau D, Salomon R, Antignac C, Heidet L (2011) Mutation screening of the EYA1, SIX1, and SIX5 genes in a large cohort of patients harboring branchio-oto-renal syndrome calls into question the pathogenic role of SIX5 mutations. Hum Mutat 32(2):183-190
26. Le Calvez-Kelm F, Lesueur F, Damiola F, Vallée M, Voegele C, Babikyan D, Durand G, Forey N, McKay-Chopin S, Robinot N, Nguyen-Dumont T, Thomas A, Byrnes GB; Breast Cancer Family Registry, Hopper JL, Southey MC, Andrulis IL, John EM, Tavtigian SV (2011) Rare, evolutionarily unlikely missense substitutions in CHEK2 contribute to breast cancer susceptibility: results from a breast cancer family registry case-control mutation-screening study. Breast Cancer Res 13(1):R6
27. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754-1760
28. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402-408
29. Loeys BL, Dietz HC, Braverman AC, Callewaert BL, De Backer J, Devereux RB, Hilhorst-Hofstee Y, Jondeau G, Faivre L, Milewicz DM, Pyeritz RE, Sponseller PD, Wordsworth P, De Paepe AM (2010) The revised Ghent nosology for the Marfan syndrome. J Med Genet 47(7):476-485
30. Lücke T, Franke D, Clewing JM, Boerkoel CF, Ehrich JH, Das AM, Zivicnjak M (2006) Schimke versus non-Schimke chronic kidney disease: an anthropometric approach. Pediatrics 118(2):e400-e407
31. Mao FJ, Sidorova JM, Lauper JM, Emond MJ, Monnat RJ (2010) The human WRN and BLM RecQ helicases differentially regulate cell proliferation and survival after chemotherapeutic DNA damage. Cancer Res 70(16):6548-6555
32. Marschalek R (2011) Mechanisms of leukemogenesis by MLL fusion proteins. Br J Haematol 152(2):141-154
33. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, Cunningham F (2010) Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics 26(16):2069-2070
34. Ng SB, Turner EH, Robertson PD, Flygare SD, Bigham AW, Lee C, Shaffer T, Wong M, Bhattacharjee A, Eichler EE, Bamshad M, Nickerson DA, Shendure J (2009) Targeted capture and massively parallel sequencing of twelve human exomes. Nature 461(7261):272-276
35. Pacek M, Tutter AV, Kubota Y, Takisawa H, Walter JC (2006) Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol Cell 21(4):581-587
36. Philip N, Chabrol B, Lossi A-M, Cardoso C, Guerrini R, Dobyns WB, Raybaud C, Villard L (2003) Mutations in the oligophrenin-1 gene (OPHN1) cause X linked congenital cerebellar hypoplasia. J Med Genet 40:441-446
37. Pinkel D, Segraves R, Sudar D, Clark S, Poole I, Kowbel D, Collins C, Kuo WL, Chen C, Zhai Y, Dairkee SH, Ljung BM, Gray JW, Albertson DG (1998) High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat Genet 20(2):207-211
38. Portnoï MF (2009) Microduplication 22q11.2: a new chromosomal syndrome. Eur J Med Genet 52(2-3):88-93
39. Rauch A, Wieczorek D, Graf E, Wieland T, Endele S, Schwarzmayr T, Albrecht B, Bartholdi D, Beygo J, Di Donato N, Dufke A, Cremer K, Hempel M, Horn D, Hoyer J, Joset P, Röpke A, Moog U, Riess A, Thiel CT, Tzschach A, Wiesener A, Wohlleber E, Zweier C, Ekici AB, Zink AM, Rump A, Meisinger C, Grallert H, Sticht H, Schenck A, Engels H, Rappold G, Schröck E, Wieacker P, Riess O, Meitinger T, Reis A, Strom TM (2012) Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exome sequencing study. Lancet 380(9854):1674-1682
40. Robinson PN, Booms P, Katzke S, Ladewig M, Neumann L, Palz M, Pregla R, Tiecke F, Rosenberg T (2002) Mutations of FBN1 and genotype-phenotype correlations in Marfan syndrome and related fibrillinopathies. Hum Mutat 20(3):153-161
41. Roeb W, Higgins J, King MC (2012) Response to DNA damage of CHEK2 missense mutations in familial breast cancer. Hum Mol Genet 21(12):2738-2744
42. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
43. Solinas-Toldo S, Lampel S, Stilgenbauer S, Nickolenko J, Benner A, Döhner H, Cremer T, Lichter P (1997) Matrix-based comparative genomic hybridization: biochips to screen for genomic imbalances. Genes Chromosomes Cancer 20(4):399-407
44. Vissers LE, de Vries BB, Veltman JA (2010a) Genomic microarrays in mental retardation: from copy number variation to gene, from research to diagnosis. J Med Genet 47(5):289-297
45. Vissers LE, de Ligt J, Gilissen C, Janssen I, Steehouwer M, de Vries P, van Lier B, Arts P, Wieskamp N, del Rosario M, van Bon BW, Hoischen A, de Vries BB, Brunner HG, Veltman JA (2010b) A de novo paradigm for mental retardation. Nat Genet 42(12):1109-1112
46. Weise A, Mrasek K, Klein E, Mulatinho M, Llerena JC Jr, Hardekopf D, Pekova S, Bhatt S, Kosyakova N, Liehr T (2012) Microdeletion and microduplication syndromes. J Histochem Cytochem 60(5):346-358
47. Zielinski B, Gratias S, Toedt G, Mendrzyk F, Stange DE, Radlwimmer B, Lohmann DR, Lichter P (2005) Detection of chromosomal imbalances in retinoblastoma by matrix-based comparative genomic hybridization. Genes Chromosomes Cancer 43(3):294-301
48. Zivicnjak M, Narancic NS, Szirovicza L, Franke D, Hrenovic J, Bisof V (2003) Gender-specific growth patterns for stature, sitting height and limbs length in Croatian children and youth (3 to 18 years of age). Coll Antropol 27:321-334
49. Zivicnjak M, Franke D, Zenker M, Hoyer J, Lücke T, Pape L, Ehrich JH (2009) SMARCAL1 mutations: a cause of prepubertal idiopathic steroid-resistant nephrotic syndrome. Pediatr Res 65(5):564-568