A cohort of balanced reciprocal translocations associated with dyslexia: Identification of two putative candidate genes at DYX1

Behavior Genetics

Volumn 41, Issue 1, 2011, Pages 125-133

  Buonincontri, Roberta ^a   Bache, Iben ^a,b   Silahtaroglu, Asli ^a   Elbro, Carsten ^a   Nielsen, Anne Mette Veber ^a   Ullmann, Reinhard ^c   Arkesteijn, Ger ^d   Tommerup, Niels ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Rigshospitalet   (Denmark)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Brain comorbidity; Dyslexia; DYX1; PDE7B; Reciprocal translocations; TCF12; ZNF280D

Indexed keywords

ADULT; ARTICLE; CHROMOSOME 15Q; CHROMOSOME 19Q; CHROMOSOME 1P; CHROMOSOME 2P; CHROMOSOME 6Q; CHROMOSOME BREAKAGE; CLINICAL ARTICLE; COHORT ANALYSIS; DISEASE ASSOCIATION; DYSLEXIA; DYX1 GENE; GENE; GENE LOCATION; GENE MAPPING; GENETIC LINKAGE; HUMAN; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PDE7B GENE; RECIPROCAL CHROMOSOME TRANSLOCATION; RISK FACTOR; TCF12 GENE; ZNF280D GENE;

ADULT; AMNIOCENTESIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CHILD; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 15; CHROMOSOMES, HUMAN, PAIR 6; COHORT STUDIES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 7; DENMARK; DYSLEXIA; FEMALE; GENETIC ASSOCIATION STUDIES; HETEROZYGOTE DETECTION; HUMANS; KARYOTYPING; MALE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEDIGREE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; PREGNANCY; TRANSLOCATION, GENETIC; ZINC FINGERS;

EID: 79952450048     PISSN: 00018244     EISSN: 15733297     Source Type: Journal    
DOI: 10.1007/s10519-010-9389-2     Document Type: Article

References (58)

1. H Anthoni M Zucchelli H Matsson B Muller-Myhsok I Fransson J Schumacher S Massinen P Onkamo A Warnke H Griesemann P Hoffmann J Nopola-Hemmi H Lyytinen G Schulte-Korne J Kere MM Nothen M Peyrard-Janvid 2007 A locus on 2p12 containing the co-regulated MRPL19 and C2ORF3 genes is associated to dyslexia Hum Mol Genet 16 6 667 677 10.1093/hmg/ddm009 17309879 (Pubitemid 46585666)
2. I Bache M Hjorth M Bugge S Holstebroe J Hilden L Schmidt K Brondum-Nielsen G Bruun-Petersen PK Jensen C Lundsteen E Niebuhr K Rasmussen N Tommerup 2006 Systematic re-examination of carriers of balanced reciprocal translocations: a strategy to search for candidate regions for common and complex diseases Eur J Hum Genet 14 4 410 417 10.1038/sj.ejhg.5201592 16493440
3. TC Bates M Luciano A Castles M Coltheart MJ Wright NG Martin 2007 Replication of reported linkages for dyslexia and spelling and suggestive evidence for novel regions on chromosomes 4 and 17 Eur J Hum Genet 15 2 194 203 10.1038/sj.ejhg.5201739 17119535 (Pubitemid 46111858)
4. Bates TC, Lind PA, Luciano M, Montgomery GW, Martin NG, Wright MJ (2009) Dyslexia and DYX1C1: deficits in reading and spelling associated with a missense mutation. Mol Psychiatry Nov 10, 2009 [Epub ahead of print]
5. M Bugge G Bruun-Petersen K Brondum-Nielsen U Friedrich J Hansen G Jensen PK Jensen U Kristoffersson C Lundsteen E Niebuhr KR Rasmussen K Rasmussen N Tommerup 2000 Disease associated balanced chromosome rearrangements: a resource for large scale genotype-phenotype delineation in man J Med Genet 37 11 858 865 10.1136/jmg.37.11.858 11073540
6. NH Chapman RP Igo JB Thomson M Matsushita Z Brkanac T Holzman VW Berninger EM Wijsman WH Raskind 2004 Linkage analyses of four regions previously implicated in dyslexia: confirmation of a locus on chromosome 15q Am J Med Genet B Neuropsychiatr Genet 131B 1 67 75 10.1002/ajmg.b.30018 15389770 (Pubitemid 39458440)
7. N Cope D Harold G Hill V Moskvina J Stevenson P Holmans MJ Owen MC O'Donovan J Williams 2005 Strong evidence that KIAA0319 on chromosome 6p is a susceptibility gene for developmental dyslexia Am J Hum Genet 76 4 581 591 10.1086/429131 15717286 (Pubitemid 40432166)
8. NA Cope G Hill M van den Bree D Harold V Moskvina EK Green MJ Owen J Williams MC O'Donovan 2005 No support for association between dyslexia susceptibility 1 candidate 1 and developmental dyslexia Mol Psychiatry 10 3 237 238 10.1038/sj.mp.4001596 15477871 (Pubitemid 40432677)
9. F Dahdouh H Anthoni I Tapia-Paez M Peyrard-Janvid G Schulte-Korne A Warnke H Remschmidt A Ziegler J Kere B Muller-Myhsok MM Nothen J Schumacher M Zucchelli 2009 Further evidence for DYX1C1 as a susceptibility factor for dyslexia Psychiatr Genet 19 2 59 63 10.1097/YPG.0b013e32832080e1 19240663
10. CG de Kovel FA Hol JG Heister JJ Willemen LA Sandkuijl B Franke GW Padberg 2004 Genomewide scan identifies susceptibility locus for dyslexia on Xq27 in an extended Dutch family J Med Genet 41 9 652 657 10.1136/jmg.2003. 012294 15342694 (Pubitemid 39208604)
11. CG de Kovel B Franke FA Hol JJ Lebrec B Maassen H Brunner GW Padberg J Platko D Pauls 2008 Confirmation of dyslexia susceptibility loci on chromosomes 1p and 2p, but not 6p in a Dutch sib-pair collection Am J Med Genet B Neuropsychiatr Genet 147 3 294 300 17886254 (Pubitemid 351536791)
12. KE Deffenbacher JB Kenyon DM Hoover RK Olson BF Pennington JC DeFries SD Smith 2004 Refinement of the 6p21.3 quantitative trait locus influencing dyslexia: linkage and association analyses Hum Genet 115 2 128 138 10.1007/s00439-004-1126-6 15138886 (Pubitemid 39010927)
13. JC DeFries DW Fulker MC LaBuda 1987 Evidence for a genetic aetiology in reading disability of twins Nature 329 6139 537 539 10.1038/329537a0 3657975 (Pubitemid 17124772)
14. T Fagerheim P Raeymaekers FE Tonnessen M Pedersen L Tranebjaerg HA Lubs 1999 A new gene (DYX3) for dyslexia is located on chromosome 2 J Med Genet 36 9 664 669 10507721 (Pubitemid 29433723)
15. H Fiegler SM Gribble DC Burford P Carr E Prigmore KM Porter S Clegg JA Crolla NR Dennis P Jacobs NP Carter 2003 Array painting: a method for the rapid analysis of aberrant chromosomes using DNA microarrays J Med Genet 40 9 664 670 10.1136/jmg.40.9.664 12960211 (Pubitemid 37100698)
16. SE Fisher JC DeFries 2002 Developmental dyslexia: genetic dissection of a complex cognitive trait Nat Rev Neurosci 3 10 767 780 10.1038/nrn936 12360321 (Pubitemid 135706688)
17. SE Fisher C Francks AJ Marlow IL MacPhie DF Newbury LR Cardon Y Ishikawa-Brush AJ Richardson JB Talcott J Gayan RK Olson BF Pennington SD Smith JC DeFries JF Stein AP Monaco 2002 Independent genome-wide scans identify a chromosome 18 quantitative-trait locus influencing dyslexia Nat Genet 30 1 86 91 10.1038/ng792 11743577
18. C Francks SE Fisher RK Olson BF Pennington SD Smith JC DeFries AP Monaco 2002 Fine mapping of the chromosome 2p12-16 dyslexia susceptibility locus: quantitative association analysis and positional candidate genes SEMA4F and OTX1 Psychiatr Genet 12 1 35 41 10.1097/00041444-200203000-00005 11901358 (Pubitemid 34274492)
19. C Gardner N Robas D Cawkill M Fidock 2000 Cloning and characterization of the human and mouse PDE7B, a novel cAMP-specific cyclic nucleotide phosphodiesterase Biochem Biophys Res Commun 272 1 186 192 10.1006/bbrc.2000. 2743 10872825 (Pubitemid 30444920)
20. J Gayan EG Willcutt SE Fisher C Francks LR Cardon RK Olson BF Pennington SD Smith AP Monaco JC DeFries 2005 Bivariate linkage scan for reading disability and attention-deficit/hyperactivity disorder localizes pleiotropic loci J Child Psychol Psychiatry 46 10 1045 1056 10.1111/j.1469-7610.2005.01447.x 16178928 (Pubitemid 44201555)
21. EL Grigorenko FB Wood MS Meyer LA Hart WC Speed A Shuster DL Pauls 1997 Susceptibility loci for distinct components of developmental dyslexia on chromosomes 6 and 15 Am J Hum Genet 60 1 27 39 8981944 (Pubitemid 26427775)
22. EL Grigorenko FB Wood MS Meyer JE Pauls LA Hart DL Pauls 2001 Linkage studies suggest a possible locus for developmental dyslexia on chromosome 1p Am J Med Genet 105 1 120 129 10.1002/1096-8628(20010108)105:1<120::AID- AJMG1075>3.0.CO;2-T 11424982 (Pubitemid 32105214)
23. K Hannula-Jouppi N Kaminen-Ahola M Taipale R Eklund J Nopola-Hemmi H Kaariainen J Kere 2005 The axon guidance receptor gene ROBO1 is a candidate gene for developmental dyslexia PLoS Genet 1 4 e50 10.1371/journal.pgen.0010050 16254601
24. GY Hsiung BJ Kaplan TL Petryshen S Lu LL Field 2004 A dyslexia susceptibility locus (DYX7) linked to dopamine D4 receptor (DRD4) region on chromosome 11p15.5 Am J Med Genet B Neuropsychiatr Genet 125B 1 112 119 10.1002/ajmg.b.20082 14755455 (Pubitemid 38141414)
25. A Ingason I Giegling T Hansen HB Rasmussen J Nielsen G Jurgens P Muglia AM Hartmann E Strengman C Vasilescu TW Muhleisen S Djurovic I Melle B Lerer HJ Moller C Francks OP Pietilainen J Suvisaari A Tuulio-Henriksson M Walshe E Vassos M Di Forti R Murray C Bonetto S Tosato RM Cantor M Rietschel N Craddock MJ Owen L Peltonen OA Andreassen MM Nothen D St. Clair RA Ophoff M Odonovan D Collier T Werge D Rujescu 2010 A large replication study and meta-analysis in European samples provides further support for association of AHI1 markers with schizophrenia Hum Mol Genet 19 7 1379 1386 10.1093/hmg/ddq009 20071346
26. DE Kaplan J Gayan J Ahn TW Won D Pauls RK Olson JC DeFries F Wood BF Pennington GP Page SD Smith JR Gruen 2002 Evidence for linkage and association with reading disability on 6p21.3-22 Am J Hum Genet 70 5 1287 1298 10.1086/340449 11951179 (Pubitemid 34450578)
27. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D (2002) The human genome browser at UCSC. Genome Res 12(6):996-1006. http://genome.ucsc.edu/ (Pubitemid 34662293)
28. DJ Kleinjan V van Heyningen 1998 Position effect in human genetic disease Hum Mol Genet 7 10 1611 1618 10.1093/hmg/7.10.1611 9735382 (Pubitemid 28464038)
29. CM Leonard JM Kuldau L Maron N Ricciuti B Mahoney M Bengtson C DeBose 2008 Identical neural risk factors predict cognitive deficit in dyslexia and schizophrenia Neuropsychology 22 2 147 158 10.1037/0894-4105.22.2.147 18331156 (Pubitemid 351626503)
30. GR Lyon SE Shaywitz BA Shaywitz 2003 A definition of dyslexia Annals of Dyslexia 53 1 15 10.1007/s11881-003-0001-9
31. C Marino R Giorda M Luisa Lorusso L Vanzin N Salandi M Nobile A Citterio S Beri V Crespi M Battaglia M Molteni 2005 A family-based association study does not support DYX1C1 on 15q21.3 as a candidate gene in developmental dyslexia Eur J Hum Genet 13 4 491 499 10.1038/sj.ejhg.5201356 15702132 (Pubitemid 40520941)
32. H Meng K Hager M Held GP Page RK Olson BF Pennington JC DeFries SD Smith JR Gruen 2005 TDT-association analysis of EKN1 and dyslexia in a Colorado twin cohort Hum Genet 118 1 87 90 10.1007/s00439-005-0017-9 16133186
33. H Meng SD Smith K Hager M Held J Liu RK Olson BF Pennington JC DeFries J Gelernter T O'Reilly-Pol S Somlo P Skudlarski SE Shaywitz BA Shaywitz K Marchione Y Wang M Paramasivam JJ LoTurco GP Page JR Gruen 2005 DCDC2 is associated with reading disability and modulates neuronal development in the brain Proc Natl Acad Sci USA 102 47 17053 17058 10.1073/pnas.0508591102 16278297 (Pubitemid 41692682)
34. L Miscimarra C Stein C Millard A Kluge K Cartier L Freebairn A Hansen L Shriberg HG Taylor B Lewis SK Iyengar 2007 Further evidence of pleiotropy influencing speech and language: analysis of the DYX8 region Hum Hered 63 1 47 58 10.1159/000098727 17230025 (Pubitemid 46192729)
35. J Nopola-Hemmi M Taipale T Haltia AE Lehesjoki A Voutilainen J Kere 2000 Two translocations of chromosome 15q associated with dyslexia J Med Genet 37 10 771 775 10.1136/jmg.37.10.771 11015455
36. J Nopola-Hemmi B Myllyluoma T Haltia M Taipale V Ollikainen T Ahonen A Voutilainen J Kere E Widen 2001 A dominant gene for developmental dyslexia on chromosome 3 J Med Genet 38 10 658 664 10.1136/jmg.38.10.658 11584043 (Pubitemid 32946786)
37. BF Pennington JW Gilger D Pauls SA Smith SD Smith JC DeFries 1991 Evidence for major gene transmission of developmental dyslexia JAMA 266 11 1527 1534 10.1001/jama.266.11.1527 1880884
38. TL Petryshen BJ Kaplan M Fu Liu NS de French R Tobias ML Hughes LL Field 2001 Evidence for a susceptibility locus on chromosome 6q influencing phonological coding dyslexia Am J Med Genet 105 6 507 517 10.1002/ajmg.1475 11496366 (Pubitemid 32729817)
39. MW Pfaffl A Tichopad C Prgomet TP Neuvians 2004 Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-excel-based tool using pair-wise correlations Biotechnol Lett 26 6 509 515 10.1023/B:BILE.0000019559.84305.47 15127793 (Pubitemid 38448421)
40. G Poelmans JJ Engelen J Van Lent-Albrechts HJ Smeets E Schoenmakers B Franke JK Buitelaar M Wuisman-Frerker W Erens J Steyaert C Schrander-Stumpel 2009 Identification of novel dyslexia candidate genes through the analysis of a chromosomal deletion Am J Med Genet B Neuropsychiatr Genet 150B 1 140 147 10.1002/ajmg.b.30787 18521840
41. Raven JC (1994) Standard progressive matrices: sets A, B, C, D and E. Oxford Psychologists Press Ltd, Oxford
42. Raven JC, Court JH, Raven J (1988) Manual for Raven's progressive matrices and vocabulary scales. Section 3, The standard progressive matrices. H. K. Lewis & Co. Ltd., London
43. N Revheim PD Butler I Schechter M Jalbrzikowski G Silipo DC Javitt 2006 Reading impairment and visual processing deficits in schizophrenia Schizophr Res 87 1-3 238 245 10.1016/j.schres.2006.06.022 16890409 (Pubitemid 44428135)
44. GD Rosen J Bai Y Wang CG Fiondella SW Threlkeld JJ LoTurco AM Galaburda 2007 Disruption of neuronal migration by RNAi of Dyx1c1 results in neocortical and hippocampal malformations Cereb Cortex 17 11 2562 2572 10.1093/cercor/bhl162 17218481 (Pubitemid 47537814)
45. TS Scerri SE Fisher C Francks IL MacPhie S Paracchini AJ Richardson JF Stein AP Monaco 2004 Putative functional alleles of DYX1C1 are not associated with dyslexia susceptibility in a large sample of sibling pairs from the UK J Med Genet 41 11 853 857 10.1136/jmg.2004.018341 15520411 (Pubitemid 39524313)
46. G Schulte-Korne T Grimm MM Nothen B Muller-Myhsok S Cichon IR Vogt P Propping H Remschmidt 1998 Evidence for linkage of spelling disability to chromosome 15 Am J Hum Genet 63 1 279 282 10.1086/301919 9634517 (Pubitemid 30428348)
47. SE Shaywitz BA Shaywitz JM Fletcher MD Escobar 1990 Prevalence of reading disability in boys and girls. Results of the Connecticut Longitudinal Study JAMA 264 8 998 1002 10.1001/jama.264.8.998 2376893 (Pubitemid 20260912)
48. SD Smith WJ Kimberling BF Pennington HA Lubs 1983 Specific reading disability: identification of an inherited form through linkage analysis Science 219 4590 1345 1347 10.1126/science.6828864 6828864 (Pubitemid 13109173)
49. M Taipale N Kaminen J Nopola-Hemmi T Haltia B Myllyluoma H Lyytinen K Muller M Kaaranen PJ Lindsberg K Hannula-Jouppi J Kere 2003 A candidate gene for developmental dyslexia encodes a nuclear tetratricopeptide repeat domain protein dynamically regulated in brain Proc Natl Acad Sci USA 100 20 11553 11558 10.1073/pnas.1833911100 12954984 (Pubitemid 37205974)
50. J Tzenova BJ Kaplan TL Petryshen LL Field 2004 Confirmation of a dyslexia susceptibility locus on chromosome 1p34-p36 in a set of 100 Canadian families Am J Med Genet B Neuropsychiatr Genet 127B 1 117 124 10.1002/ajmg.b.20139 15108193 (Pubitemid 38542326)
51. M Uittenbogaard A Chiaramello 2002 Expression of the bHLH transcription factor Tcf12 (ME1) gene is linked to the expansion of precursor cell populations during neurogenesis Brain Res Gene Expr Patterns 1 2 115 121 10.1016/S1567-133X(01)00022-9 15018808
52. IM Veltman JA Veltman G Arkesteijn IM Janssen LE Vissers PJ de Jong AG van Kessel EF Schoenmakers 2003 Chromosomal breakpoint mapping by arrayCGH using flow-sorted chromosomes Biotechniques 35 5 1066 1070 14628681 (Pubitemid 37413430)
53. KG Wigg JM Couto Y Feng B Anderson TD Cate-Carter F Macciardi R Tannock MW Lovett TW Humphries CL Barr 2004 Support for EKN1 as the susceptibility locus for dyslexia on 15q21 Mol Psychiatry 9 12 1111 1121 10.1038/sj.mp.4001543 15249932 (Pubitemid 40065456)
54. KG Wigg Y Feng J Crosbie R Tannock JL Kennedy A Ickowicz M Malone R Schachar CL Barr 2008 Association of ADHD and the Protogenin gene in the chromosome 15q21.3 reading disabilities linkage region Genes Brain Behav 7 8 877 886 10.1111/j.1601-183X.2008.00425.x 19076634
55. EG Willcutt BF Pennington 2000 Comorbidity of reading disability and attention-deficit/hyperactivity disorder: differences by gender and subtype J Learn Disabil 33 2 179 191 10.1177/002221940003300206 15505947
56. J Williams MC O'Donovan 2006 The genetics of developmental dyslexia Eur J Hum Genet 14 6 681 689 10.1038/sj.ejhg.5201575 16721404 (Pubitemid 43797265)
57. World Health Organisation (2010) International statistical classification of diseases and related health problems, 10th Revision, Version for 2007, http://apps.who.int/classifications/apps/icd/icd10online/
58. K Zhou P Asherson P Sham B Franke RJ Anney J Buitelaar R Ebstein M Gill K Brookes C Buschgens D Campbell W Chen H Christiansen E Fliers I Gabriels L Johansson R Marco F Mulas U Muller A Mulligan BM Neale F Rijsdijk N Rommelse H Uebel L Psychogiou X Xu T Banaschewski E Sonuga-Barke J Eisenberg I Manor A Miranda RD Oades H Roeyers A Rothenberger J Sergeant HC Steinhausen E Taylor M Thompson SV Faraone 2008 Linkage to chromosome 1p36 for attention-deficit/ hyperactivity disorder traits in school and home settings Biol Psychiatry 64 7 571 576 10.1016/j.biopsych.2008.02.024 18439570