Mutations in USP9X are associated with x-linked intellectual disability and disrupt neuronal cell migration and growth

American Journal of Human Genetics

Volumn 94, Issue 3, 2014, Pages 470-478

  Homan, Claire C ^a   Kumar, Raman ^b,c   Nguyen, Lam Son ^c   Haan, Eric ^c,d   Raymond, F Lucy ^e   Abidi, Fatima ^f   Raynaud, Martine ^g,h   Schwartz, Charles E ^f   Wood, Stephen A ⁱ   Gecz, Jozef ^a,b,c   Jolly, Lachlan A ^c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b CHILD HEALTH RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d WOMEN S AND CHILDREN S HOSPITAL   (Australia)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f GREENWOOD GENETIC CENTER   (United States)

^g UNIVERSITY HOSPITAL OF TOURS   (France)

^h CHRU de Tours   (France)

ⁱ GRIFFITH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINASE; UNCLASSIFIED DRUG; USP9X PROTEIN; ARID1B PROTEIN; PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DISRUPTION; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; FEMALE; GENE ONTOLOGY; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; GROWTH CONE; HUMAN; KNOCKOUT MOUSE; LIQUID CHROMATOGRAPHY; LOSS OF FUNCTION MUTATION; MALE; MOUSE; NERVE CELL CULTURE; NERVE CELL GROWTH; NEURAL STEM CELL; NEURONAL CELL MIGRATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEOMICS; TANDEM MASS SPECTROMETRY; WILD TYPE; X CHROMOSOME LINKAGE; X LINKED MENTAL RETARDATION; BRAIN DEVELOPMENT; CELL GROWTH; CLINICAL ASSESSMENT; EMBRYO; GENE MUTATION; INTELLECTUAL IMPAIRMENT; NERVE FIBER GROWTH; PROTEIN DEPLETION; UBIQUITINATION; X LINKED INTELLECTUAL DISABILITY;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CHROMOSOMES, HUMAN, X; CYTOSKELETON; DNA-BINDING PROTEINS; FAMILY HEALTH; FEMALE; GENES, X-LINKED; GENETIC VARIATION; HUMANS; INTELLECTUAL DISABILITY; MALE; MICE; MICE, KNOCKOUT; MUTATION; MUTATION, MISSENSE; NEUROGENESIS; NEURONS; PHENOTYPE; TIME FACTORS; TRANSCRIPTION FACTORS; UBIQUITIN THIOLESTERASE;

EID: 84896768982     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2014.02.004     Document Type: Article

References (36)

1. H.H. Ropers Genetics of early onset cognitive impairment Annu. Rev. Genomics Hum. Genet. 11 2010 161 187
2. J. Gécz, C. Shoubridge, and M. Corbett The genetic landscape of intellectual disability arising from chromosome X Trends Genet. 25 2009 308 316
3. P.S. Tarpey, R. Smith, E. Pleasance, A. Whibley, S. Edkins, C. Hardy, S. O'Meara, C. Latimer, E. Dicks, and A. Menzies et al. A systematic, large-scale resequencing screen of X-chromosome coding exons in mental retardation Nat. Genet. 41 2009 535 543
4. A.C. Whibley, V. Plagnol, P.S. Tarpey, F. Abidi, T. Fullston, M.K. Choma, C.A. Boucher, L. Shepherd, L. Willatt, and G. Parkin et al. Fine-scale survey of X chromosome copy number variants and indels underlying intellectual disability Am. J. Hum. Genet. 87 2010 173 188
5. C. Shoubridge, P.S. Tarpey, F. Abidi, S.L. Ramsden, S. Rujirabanjerd, J.A. Murphy, J. Boyle, M. Shaw, A. Gardner, and A. Proos et al. Mutations in the guanine nucleotide exchange factor gene IQSEC2 cause nonsyndromic intellectual disability Nat. Genet. 42 2010 486 488
6. J. Hoyer, A.B. Ekici, S. Endele, B. Popp, C. Zweier, A. Wiesener, E. Wohlleber, A. Dufke, E. Rossier, and C. Petsch et al. Haploinsufficiency of ARID1B, a member of the SWI/SNF-a chromatin-remodeling complex, is a frequent cause of intellectual disability Am. J. Hum. Genet. 90 2012 565 572
7. P.Y. Khut, B. Tucker, M. Lardelli, and S.A. Wood Evolutionary and expression analysis of the zebrafish deubiquitylating enzyme, usp9 Zebrafish 4 2007 95 101
8. S. Petrovski, Q. Wang, E.L. Heinzen, A.S. Allen, and D.B. Goldstein Genic intolerance to functional variation and the interpretation of personal genomes PLoS Genet. 9 2013 e1003709
9. S.A. Wood, W.S. Pascoe, K. Ru, T. Yamada, J. Hirchenhain, R. Kemler, and J.S. Mattick Cloning and expression analysis of a novel mouse gene with sequence similarity to the Drosophila fat facets gene Mech. Dev. 63 1997 29 38
10. M. Schwickart, X. Huang, J.R. Lill, J. Liu, R. Ferrando, D.M. French, H. Maecker, K. O'Rourke, F. Bazan, and J. Eastham-Anderson et al. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival Nature 463 2010 103 107
11. S. Stegeman, L.A. Jolly, S. Premarathne, J. Gecz, L.J. Richards, A. Mackay-Sim, and S.A. Wood Loss of Usp9x disrupts cortical architecture, hippocampal development and TGFβ-mediated axonogenesis PLoS ONE 8 2013 e68287
12. J.G. Gleeson, P.T. Lin, L.A. Flanagan, and C.A. Walsh Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons Neuron 23 1999 257 271
13. G. Friocourt, C. Kappeler, Y. Saillour, F. Fauchereau, M.S. Rodriguez, N. Bahi, M.C. Vinet, P. Chafey, K. Poirier, and S. Taya et al. Doublecortin interacts with the ubiquitin protease DFFRX, which associates with microtubules in neuronal processes Mol. Cell. Neurosci. 28 2005 153 164
14. V. des Portes, F. Francis, J.M. Pinard, I. Desguerre, M.L. Moutard, I. Snoeck, L.C. Meiners, F. Capron, R. Cusmai, and S. Ricci et al. doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH) Hum. Mol. Genet. 7 1998 1063 1070
15. K. Angata, and M. Fukuda Roles of polysialic acid in migration and differentiation of neural stem cells Methods Enzymol. 479 2010 25 36
16. P.J. Ocbina, M.L. Dizon, L. Shin, and F.G. Szele Doublecortin is necessary for the migration of adult subventricular zone cells from neurospheres Mol. Cell. Neurosci. 33 2006 126 135
17. P. Durbec, I. Franceschini, F. Lazarini, and M. Dubois-Dalcq In vitro migration assays of neural stem cells Methods Mol. Biol. 438 2008 213 225
18. T.A. Deuel, J.S. Liu, J.C. Corbo, S.Y. Yoo, L.B. Rorke-Adams, and C.A. Walsh Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth Neuron 49 2006 41 53
19. X. Fu, K.J. Brown, C.C. Yap, B. Winckler, J.K. Jaiswal, and J.S. Liu Doublecortin (Dcx) family proteins regulate filamentous actin structure in developing neurons J. Neurosci. 33 2013 709 721
20. D.C. Jean, P.W. Baas, and M.M. Black A novel role for doublecortin and doublecortin-like kinase in regulating growth cone microtubules Hum. Mol. Genet. 21 2012 5511 5527
21. H. Koizumi, H. Higginbotham, T. Poon, T. Tanaka, B.C. Brinkman, and J.G. Gleeson Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain Nat. Neurosci. 9 2006 779 786
22. H. Koizumi, T. Tanaka, and J.G. Gleeson Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration Neuron 49 2006 55 66
23. L.A. Jolly, V. Taylor, and S.A. Wood USP9X enhances the polarity and self-renewal of embryonic stem cell-derived neural progenitors Mol. Biol. Cell 20 2009 2015 2029
24. T. Tanaka, H. Koizumi, and J.G. Gleeson The doublecortin and doublecortin-like kinase 1 genes cooperate in murine hippocampal development Cereb. Cortex 16 Suppl 1 2006 i69 i73
25. G. Dennis Jr., B.T. Sherman, D.A. Hosack, J. Yang, W. Gao, H.C. Lane, and R.A. Lempicki DAVID: Database for Annotation, Visualization, and Integrated Discovery Genome Biol. 4 2003 3
26. S. Girirajan, and E.E. Eichler Phenotypic variability and genetic susceptibility to genomic disorders Hum. Mol. Genet. 19 R2 2010 R176 R187
27. M. Pantaleon, M. Kanai-Azuma, J.S. Mattick, K. Kaibuchi, P.L. Kaye, and S.A. Wood FAM deubiquitylating enzyme is essential for preimplantation mouse embryo development Mech. Dev. 109 2001 151 160
28. Y. Feng, and C.A. Walsh Protein-protein interactions, cytoskeletal regulation and neuronal migration Nat. Rev. Neurosci. 2 2001 408 416
29. J.S. Liu Molecular genetics of neuronal migration disorders Curr. Neurol. Neurosci. Rep. 11 2011 171 178
30. S. Dupont, A. Mamidi, M. Cordenonsi, M. Montagner, L. Zacchigna, M. Adorno, G. Martello, M.J. Stinchfield, S. Soligo, and L. Morsut et al. FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination Cell 136 2009 123 135
31. M.J. Stinchfield, N.T. Takaesu, J.C. Quijano, A.M. Castillo, N. Tiusanen, O. Shimmi, E. Enzo, S. Dupont, S. Piccolo, and S.J. Newfeld Fat facets deubiquitylation of Medea/Smad4 modulates interpretation of a Dpp morphogen gradient Development 139 2012 2721 2729
32. Y. Xie, M. Avello, M. Schirle, E. McWhinnie, Y. Feng, E. Bric-Furlong, C. Wilson, R. Nathans, J. Zhang, and M.W. Kirschner et al. Deubiquitinase FAM/USP9X interacts with the E3 ubiquitin ligase SMURF1 protein and protects it from ligase activity-dependent self-degradation J. Biol. Chem. 288 2013 2976 2985
33. J.A. Fischer, and E. Overstreet Fat facets does a Highwire act at the synapse Bioessays 24 2002 13 16
34. L. Huang, L.A. Jolly, S. Willis-Owen, A. Gardner, R. Kumar, E. Douglas, C. Shoubridge, D. Wieczorek, A. Tzschach, and M. Cohen et al. A noncoding, regulatory mutation implicates HCFC1 in nonsyndromic intellectual disability Am. J. Hum. Genet. 91 2012 694 702
35. M.A. Corbett, M. Bahlo, L. Jolly, Z. Afawi, A.E. Gardner, K.L. Oliver, S. Tan, A. Coffey, J.C. Mulley, and L.M. Dibbens et al. A focal epilepsy and intellectual disability syndrome is due to a mutation in TBC1D24 Am. J. Hum. Genet. 87 2010 371 375
36. L.A. Jolly, C.C. Homan, R. Jacob, S. Barry, and J. Gecz The UPF3B gene, implicated in intellectual disability, autism, ADHD and childhood onset schizophrenia regulates neural progenitor cell behaviour and neuronal outgrowth Hum. Mol. Genet. 22 2013 4673 4687