Mutations in DDX3X Are a Common Cause of Unexplained Intellectual Disability with Gender-Specific Effects on Wnt Signaling

American Journal of Human Genetics

Volumn 97, Issue 2, 2015, Pages 343-352

  Snijders Blok, Lot ^a   Madsen, Erik ^b   Juusola, Jane ^c   Gilissen, Christian ^a   Baralle, Diana ^d   Reijnders, Margot R F ^a   Venselaar, Hanka ^e   Helsmoortel, Céline ^f   Cho, Megan T ^c   Hoischen, Alexander ^a   Vissers, Lisenka E L M ^a   Koemans, Tom S ^a   Wissink Lindhout, Willemijn ^a   Eichler, Evan E ^g,h   Romano, Corrado ⁱ   Van Esch, Hilde ^j   Stumpel, Connie ^k   Vreeburg, Maaike ^k   Smeets, Eric ^k   Oberndorff, Karin ^l   Van Bon, Bregje W M ^a,m   Shaw, Marie ^m   Gecz, Jozef ^m   Haan, Eric ^m,n   Bienek, Melanie ^o   Jensen, Corinna ^o   Loeys, Bart L ^f   Van Dijck, Anke ^f   Innes, A Micheil ^p   Racher, Hilary ^p   Vermeer, Sascha ^q   Di Donato, Nataliya ^r   Rump, Andreas ^r   Tatton Brown, Katrina ^s   Parker, Michael J ^t   Henderson, Alex ^u   Lynch, Sally A ^v   Fryer, Alan ^w   Ross, Alison ^x   Vasudevan, Pradeep ^y   Kini, Usha ^z   Newbury Ecob, Ruth ^aa   Chandler, Kate ^ab   Male, Alison ^ac   Dijkstra, Sybe ^ad   Schieving, Jolanda ^a   Giltay, Jacques ^ae   Van gassen, Koen L I ^ae   Schuurs Hoeijmakers, Janneke ^a   Tan, Perciliz L ^b   Pediaditakis, Igor ^b   Haas, Stefan A ^o   Retterer, Kyle ^c   Reed, Patrick ^c   Monaghan, Kristin G ^c   Haverfield, Eden ^c   Natowicz, Marvin ^af   Myers, Angela ^ag   Kruer, Michael C ^ag,ah   Stein, Quinn ^ah   Strauss, Kevin A ^ai   Brigatti, Karlla W ^ai   Keating, Katherine ^aj   Burton, Barbara K ^aj   Kim, Katherine H ^aj   Charrow, Joel ^aj   Norman, Jennifer ^ak   Foster Barber, Audrey ^al   Kline, Antonie D ^am   Kimball, Amy ^am   Zackai, Elaine ^an   Harr, Margaret ^an   Fox, Joyce ^ao   McLaughlin, Julie ^ao   Lindstrom, Kristin ^ah   Haude, Katrina M ^ap   Van Roozendaal, Kees ^k   Brunner, Han ^a,k   Chung, Wendy K ^aq   Kooy, R Frank ^f   Pfundt, Rolph ^a   Kalscheuer, Vera ^o   Mehta, Sarju G ^ar   Katsanis, Nicholas ^b   Kleefstra, Tjitske ^a   more..

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c GENEDX   (United States)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF ANTWERP   (Belgium)

^g UNIVERSITY OF WASHINGTON   (United States)

^h HOWARD HUGHES MEDICAL INSTITUTE   (United States)

ⁱ OASI RESEARCH INSTITUTE IRCCS   (Italy)

^j UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^k MAASTRICHT UNIVERSITY   (Netherlands)

^l Sittard Geleen Heerlen   (Netherlands)

^m UNIVERSITY OF ADELAIDE   (Australia)

ⁿ South Australian Clinical Genetics Service   (Australia)

^o MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^p UNIVERSITY OF CALGARY   (Canada)

^q UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^r DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^s ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^t SHEFFIELD CHILDREN S HOSPITAL   (United Kingdom)

^u NEWCASTLE UPON TYNE HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^v Temple Street Children's Hospital   (Ireland)

^w LIVERPOOL WOMEN S HOSPITAL   (United Kingdom)

^x Clinical Genetics Service   (United Kingdom)

^y LEICESTER ROYAL INFIRMARY   (United Kingdom)

^z OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^aa University Hospital   (United Kingdom)

^ab ST MARY S HOSPITAL   (United Kingdom)

^ac GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^ad Organisation for People with Intellectual Disabilities   (Netherlands)

^ae UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^af LERNER RESEARCH INSTITUTE   (United States)

^ag Sanford Children's Specialty Clinic   (United States)

^ah PHOENIX CHILDREN'S HOSPITAL   (United States)

^ai FRANKLIN AND MARSHALL COLLEGE   (United States)

^aj CHILDREN'S MEMORIAL HOSPITAL   (United States)

^ak Integris Pediatric Neurology   (United States)

^al UNIVERSITY OF CALIFORNIA   (United States)

^am GREATER BALTIMORE MEDICAL CENTER   (United States)

^an CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^ao Northwell Health   (United States)

^ap UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^aq NewYork Presbyterian Hospital   (United States)

^ar ADDENBROOKE S HOSPITAL   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; WNT PROTEIN; DDX3X PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR DISORDER; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CORPUS CALLOSUM AGENESIS; DDX3X GENE; DE NOVO MUTATION; DISEASE TRANSMISSION; EPILEPSY; FEMALE; FRAMESHIFT MUTATION; GENE; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENETIC VARIABILITY; HUMAN; IN VIVO STUDY; INTELLECTUAL IMPAIRMENT; LOSS OF FUNCTION MUTATION; MALE; MISSENSE MUTATION; MOTOR DYSFUNCTION; MUSCLE HYPOTONIA; NONHUMAN; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; RECESSIVE INHERITANCE; SEX DIFFERENCE; WNT SIGNALING PATHWAY; AMINO ACID SUBSTITUTION; ANIMAL; ANIMAL EMBRYO; CASE REPORT; DNA SEQUENCE; EXOME; GENE DOSAGE; GENETICS; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; SEXUAL DEVELOPMENT; ZEBRA FISH;

DANIO RERIO;

AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; DEAD-BOX RNA HELICASES; EMBRYO, NONMAMMALIAN; EXOME; FEMALE; GENE DOSAGE; HUMANS; INTELLECTUAL DISABILITY; MALE; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PHENOTYPE; SEQUENCE ANALYSIS, DNA; SEX CHARACTERISTICS; WNT SIGNALING PATHWAY; ZEBRAFISH;

EID: 84938978665     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2015.07.004     Document Type: Article

References (45)

1. N. Roeleveld, G.A. Zielhuis, and F. Gabreëls The prevalence of mental retardation: a critical review of recent literature Dev. Med. Child Neurol. 39 1997 125 132
2. H. Leonard, and X. Wen The epidemiology of mental retardation: challenges and opportunities in the new millennium Ment. Retard. Dev. Disabil. Res. Rev. 8 2002 117 134
3. P.K. Maulik, M.N. Mascarenhas, C.D. Mathers, T. Dua, and S. Saxena Prevalence of intellectual disability: a meta-analysis of population-based studies Res. Dev. Disabil. 32 2011 419 436
4. K. Van Naarden Braun, D. Christensen, N. Doernberg, L. Schieve, C. Rice, L. Wiggins, D. Schendel, and M. Yeargin-Allsopp Trends in the prevalence of autism spectrum disorder, cerebral palsy, hearing loss, intellectual disability, and vision impairment, metropolitan Atlanta, 1991-2010 PLoS ONE 10 2015 e0124120
5. R.L. Schalock, S.A. Borthwick-Duffy, V.J. Bradley, W.H.E. Buntinx, D.L. Coulter, E.M. Craig, S.C. Gomez, Y. Lachapelle, R. Luckasson, A. Reeve, and et al. Intellectual Disability: Definition, Classification, and Systems of Supports 2010 American Association on Intellectual and Developmental Disabilities
6. A. Piton, C. Redin, and J.L. Mandel XLID-causing mutations and associated genes challenged in light of data from large-scale human exome sequencing Am. J. Hum. Genet. 93 2013 368 383
7. H. Hu, S.A. Haas, J. Chelly, H. Van Esch, M. Raynaud, A.P. de Brouwer, S. Weinert, G. Froyen, S.G. Frints, F. Laumonnier, and et al. X-exome sequencing of 405 unresolved families identifies seven novel intellectual disability genes Mol. Psychiatry 2015 10.1038/mp.2014.193 Published online February 3, 2015
8. W.B. Dobyns, A. Filauro, B.N. Tomson, A.S. Chan, A.W. Ho, N.T. Ting, J.C. Oosterwijk, and C. Ober Inheritance of most X-linked traits is not dominant or recessive, just X-linked Am. J. Med. Genet. A. 129A 2004 136 143
9. M. Morleo, and B. Franco Dosage compensation of the mammalian X chromosome influences the phenotypic variability of X-linked dominant male-lethal disorders J. Med. Genet. 45 2008 401 408
10. K. Neveling, I. Feenstra, C. Gilissen, L.H. Hoefsloot, E.J. Kamsteeg, A.R. Mensenkamp, R.J. Rodenburg, H.G. Yntema, L. Spruijt, S. Vermeer, and et al. A post-hoc comparison of the utility of sanger sequencing and exome sequencing for the diagnosis of heterogeneous diseases Hum. Mutat. 34 2013 1721 1726
11. J. de Ligt, M.H. Willemsen, B.W. van Bon, T. Kleefstra, H.G. Yntema, T. Kroes, A.T. Vulto-van Silfhout, D.A. Koolen, P. de Vries, C. Gilissen, and et al. Diagnostic exome sequencing in persons with severe intellectual disability N. Engl. J. Med. 367 2012 1921 1929
12. K. Retterer, J. Scuffins, D. Schmidt, R. Lewis, D. Pineda-Alvarez, A. Stafford, L. Schmidt, S. Warren, F. Gibellini, A. Kondakova, and et al. Assessing copy number from exome sequencing and exome array CGH based on CNV spectrum in a large clinical cohort Genet. Med. 2014 10.1038/gim.2014.160 Published online November 6, 2014
13. Deciphering Developmental Disorders Study Large-scale discovery of novel genetic causes of developmental disorders Nature 519 2015 223 228
14. B.T. Lahn, and D.C. Page Functional coherence of the human Y chromosome Science 278 1997 675 680
15. A.M. Cotton, E.M. Price, M.J. Jones, B.P. Balaton, M.S. Kobor, and C.J. Brown Landscape of DNA methylation on the X chromosome reflects CpG density, functional chromatin state and X-chromosome inactivation Hum. Mol. Genet. 24 2015 1528 1539
16. L. Carrel, and H.F. Willard X-inactivation profile reveals extensive variability in X-linked gene expression in females Nature 434 2005 400 404
17. R.C. Allen, H.Y. Zoghbi, A.B. Moseley, H.M. Rosenblatt, and J.W. Belmont Methylation of HpaII and HhaI sites near the polymorphic CAG repeat in the human androgen-receptor gene correlates with X chromosome inactivation Am. J. Hum. Genet. 51 1992 1229 1239
18. L. Busque, R. Mio, J. Mattioli, E. Brais, N. Blais, Y. Lalonde, M. Maragh, and D.G. Gilliland Nonrandom X-inactivation patterns in normal females: lyonization ratios vary with age Blood 88 1996 59 65
19. C. Gilissen, J.Y. Hehir-Kwa, D.T. Thung, M. van de Vorst, B.W. van Bon, M.H. Willemsen, M. Kwint, I.M. Janssen, A. Hoischen, A. Schenck, and et al. Genome sequencing identifies major causes of severe intellectual disability Nature 511 2014 344 347
20. M. Abdelhaleem RNA helicases: regulators of differentiation Clin. Biochem. 38 2005 499 503
21. A. Garbelli, S. Beermann, G. Di Cicco, U. Dietrich, and G. Maga A motif unique to the human DEAD-box protein DDX3 is important for nucleic acid binding, ATP hydrolysis, RNA/DNA unwinding and HIV-1 replication PLoS ONE 6 2011 e19810
22. Q. Li, P. Zhang, C. Zhang, Y. Wang, R. Wan, Y. Yang, X. Guo, R. Huo, M. Lin, Z. Zhou, and J. Sha DDX3X regulates cell survival and cell cycle during mouse early embryonic development J. Biomed. Res. 28 2014 282 291
23. M. Schröder Human DEAD-box protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation Biochem. Pharmacol. 79 2010 297 306
24. V. Kasim, S. Wu, K. Taira, and M. Miyagishi Determination of the role of DDX3 a factor involved in mammalian RNAi pathway using an shRNA-expression library PLoS ONE 8 2013 e59445
25. C.M. Cruciat, C. Dolde, R.E. de Groot, B. Ohkawara, C. Reinhard, H.C. Korswagen, and C. Niehrs RNA helicase DDX3 is a regulatory subunit of casein kinase 1 in Wnt-β-catenin signaling Science 339 2013 1436 1441
26. G. Bellipanni, M. Varga, S. Maegawa, Y. Imai, C. Kelly, A.P. Myers, F. Chu, W.S. Talbot, and E.S. Weinberg Essential and opposing roles of zebrafish β-catenins in the formation of dorsal axial structures and neurectoderm Development 133 2006 1299 1309
27. L. Caneparo, Y.-L. Huang, N. Staudt, M. Tada, R. Ahrendt, O. Kazanskaya, C. Niehrs, and C. Houart Dickkopf-1 regulates gastrulation movements by coordinated modulation of Wnt/β catenin and Wnt/PCP activities, through interaction with the Dally-like homolog Knypek Genes Dev. 21 2007 465 480
28. C. Kelly, A.J. Chin, J.L. Leatherman, D.J. Kozlowski, and E.S. Weinberg Maternally controlled (beta)-catenin-mediated signaling is required for organizer formation in the zebrafish Development 127 2000 3899 3911
29. G.M. Kelly, D.F. Erezyilmaz, and R.T. Moon Induction of a secondary embryonic axis in zebrafish occurs following the overexpression of beta-catenin Mech. Dev. 53 1995 261 273
30. S. Kumar, M. Žigman, T.R. Patel, B. Trageser, J.C. Gross, K. Rahm, M. Boutros, D. Gradl, H. Steinbeisser, T. Holstein, and et al. Molecular dissection of Wnt3a-Frizzled8 interaction reveals essential and modulatory determinants of Wnt signaling activity BMC Biol. 12 2014 44
31. A.C. Lekven, C.J. Thorpe, J.S. Waxman, and R.T. Moon Zebrafish wnt8 encodes two wnt8 proteins on a bicistronic transcript and is required for mesoderm and neurectoderm patterning Dev. Cell 1 2001 103 114
32. T.N. Turner, K. Sharma, E.C. Oh, Y.P. Liu, R.L. Collins, M.X. Sosa, D.R. Auer, H. Brand, S.J. Sanders, D. Moreno-De-Luca, and et al. Loss of δ-catenin function in severe autism Nature 520 2015 51 56
33. M. Westerfield The Zebrafish Book 1995 University of Oregon Press Eugene, OR
34. W. Wu, A. Glinka, H. Delius, and C. Niehrs Mutual antagonism between dickkopf1 and dickkopf2 regulates Wnt/beta-catenin signalling Curr. Biol. 10 2000 1611 1614
35. C.L. Andoniadou, M. Signore, R.M. Young, C. Gaston-Massuet, S.W. Wilson, E. Fuchs, and J.P. Martinez-Barbera HESX1- and TCF3-mediated repression of Wnt/β-catenin targets is required for normal development of the anterior forebrain Development 138 2011 4931 4942
36. F.J. Najm, A.M. Lager, A. Zaremba, K. Wyatt, A.V. Caprariello, D.C. Factor, R.T. Karl, T. Maeda, R.H. Miller, and P.J. Tesar Transcription factor-mediated reprogramming of fibroblasts to expandable, myelinogenic oligodendrocyte progenitor cells Nat. Biotechnol. 31 2013 426 433
37. R.A. Mentink, T.C. Middelkoop, L. Rella, N. Ji, C.Y. Tang, M.C. Betist, A. van Oudenaarden, and H.C. Korswagen Cell intrinsic modulation of Wnt signaling controls neuroblast migration in C. elegans Dev. Cell 31 2014 188 201
38. S. Zhang, J. Li, R. Lea, K. Vleminckx, and E. Amaya Fezf2 promotes neuronal differentiation through localised activation of Wnt/β-catenin signalling during forebrain development Development 141 2014 4794 4805
39. A. Kuechler, M.H. Willemsen, B. Albrecht, C.A. Bacino, D.W. Bartholomew, H. van Bokhoven, M.J. van den Boogaard, N. Bramswig, C. Büttner, K. Cremer, and et al. De novo mutations in beta-catenin (CTNNB1) appear to be a frequent cause of intellectual disability: expanding the mutational and clinical spectrum Hum. Genet. 134 2015 97 109
40. V. Tucci, T. Kleefstra, A. Hardy, I. Heise, S. Maggi, M.H. Willemsen, H. Hilton, C. Esapa, M. Simon, M.T. Buenavista, and et al. Dominant β-catenin mutations cause intellectual disability with recognizable syndromic features J. Clin. Invest. 124 2014 1468 1482
41. A. Rauch, D. Wieczorek, E. Graf, T. Wieland, S. Endele, T. Schwarzmayr, B. Albrecht, D. Bartholdi, J. Beygo, N. Di Donato, and et al. Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exome sequencing study Lancet 380 2012 1674 1682
42. T. Sekiguchi, H. Iida, J. Fukumura, and T. Nishimoto Human DDX3Y, the Y-encoded isoform of RNA helicase DDX3, rescues a hamster temperature-sensitive ET24 mutant cell line with a DDX3X mutation Exp. Cell Res. 300 2004 213 222
43. H.J. Ditton, J. Zimmer, C. Kamp, E. Rajpert-De Meyts, and P.H. Vogt The AZFa gene DBY (DDX3Y) is widely transcribed but the protein is limited to the male germ cells by translation control Hum. Mol. Genet. 13 2004 2333 2341
44. C. Foresta, A. Ferlin, and E. Moro Deletion and expression analysis of AZFa genes on the human Y chromosome revealed a major role for DBY in male infertility Hum. Mol. Genet. 9 2000 1161 1169
45. A. Ferlin, E. Moro, A. Rossi, B. Dallapiccola, and C. Foresta The human Y chromosome's azoospermia factor b (AZFb) region: sequence, structure, and deletion analysis in infertile men J. Med. Genet. 40 2003 18 24