De Novo Loss-of-Function Mutations in USP9X Cause a Female-Specific Recognizable Syndrome with Developmental Delay and Congenital Malformations

American Journal of Human Genetics

Volumn 98, Issue 2, 2016, Pages 373-381

  Reijnders, Margot R F ^a   Zachariadis, Vasilios ^b   Latour, Brooke ^a,c   Jolly, Lachlan ^d   Mancini, Grazia M ^e   Pfundt, Rolph ^a   Wu, Ka Man ^a,c   Van Ravenswaaij Arts, Conny M A ^f   Veenstra Knol, Hermine E ^f   Anderlid, Britt Marie M ^b,g   Wood, Stephen A ^h   Cheung, Sau Wai ⁱ   Barnicoat, Angela ^j   Probst, Frank ⁱ   Magoulas, Pilar ⁱ   Brooks, Alice S ^e   Malmgren, Helena ^b,g   Harila Saari, Arja ^g   Marcelis, Carlo M ^a   Vreeburg, Maaike ^k   Hobson, Emma ^l   Sutton, V Reid ⁱ   Stark, Zornitza ^m   Vogt, Julie ⁿ   Cooper, Nicola ^o   Lim, Jiin Ying ^p   Price, Sue ^q   Lai, Angeline Hwei Meeng ^p   Domingo, Deepti ^d   Reversade, Bruno ^r,s   Gecz, Jozef ^d   Gilissen, Christian ^a   Brunner, Han G ^a,k   Kini, Usha ^q   Roepman, Ronald ^a,c   Nordgren, Ann ^b,g   Kleefstra, Tjitske ^a   more..

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b KAROLINSKA INSTITUTE   (Sweden)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF ADELAIDE   (Australia)

^e SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^f UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^g KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^h GRIFFITH UNIVERSITY   (Australia)

ⁱ BAYLOR COLLEGE OF MEDICINE   (United States)

^j GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^k MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^l CHAPEL ALLERTON HOSPITAL   (United Kingdom)

^m MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

ⁿ BIRMINGHAM WOMEN S HOSPITAL   (United Kingdom)

^o BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^p KK WOMEN'S AND CHILDREN'S HOSPITAL   (Singapore)

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

^r INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^s University of Amsterdam   (Netherlands)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINASE; MESSENGER RNA; UBIQUITIN SPECIFIC PROTEASE 9; UNCLASSIFIED DRUG; UBIQUITIN THIOLESTERASE; USP9X PROTEIN, HUMAN;

ABDOMINAL WALL DEFECT; ADULT; ANUS ATRESIA; ARTICLE; ASYMMETRIC HYPOMASTIA; AXONEME; BIFID UVULA; BRAIN MALFORMATION; CHILD; CHOANA ATRESIA; CLEFT PALATE; CLINICAL ARTICLE; COHORT ANALYSIS; CONGENITAL HEART MALFORMATION; CONGENITAL MALFORMATION; DEVELOPMENTAL DISORDER; EXON; EYE MALFORMATION; FEMALE; GENE EXPRESSION; GENETIC SCREENING; HIP DYSPLASIA; HUMAN; INTELLECTUAL IMPAIRMENT; LOSS OF FUNCTION MUTATION; NONSENSE MEDIATED MRNA DECAY; PHENOTYPE; POLYDACTYLY; PRIORITY JOURNAL; SACRAL DIMPLE; SCHOOL CHILD; SCOLIOSIS; SHORT STATURE; SKIN FIBROBLAST; TOOTH MALFORMATION; UROGENITAL TRACT MALFORMATION; X CHROMOSOME INACTIVATION; YOUNG ADULT; ADOLESCENT; CHOANAL ATRESIA; DEVELOPMENTAL DISABILITIES; GENETICS; INTELLECTUAL DISABILITY; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; X CHROMOSOMAL INHERITANCE;

ADOLESCENT; BASE SEQUENCE; CHILD; CHILD, PRESCHOOL; CHOANAL ATRESIA; DEVELOPMENTAL DISABILITIES; FEMALE; GENES, X-LINKED; GENETIC TESTING; HUMANS; INTELLECTUAL DISABILITY; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; UBIQUITIN THIOLESTERASE; X CHROMOSOME INACTIVATION; YOUNG ADULT;

EID: 84957811593     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2015.12.015     Document Type: Article

References (51)

1. H.A. Lubs, R.E. Stevenson, and C.E. Schwartz Fragile X and X-linked intellectual disability: four decades of discovery Am. J. Hum. Genet. 90 2012 579 590
2. 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
3. P.S. Tarpey, R. Smith, E. Pleasance, A. Whibley, S. Edkins, C. Hardy, S. O'Meara, C. Latimer, E. Dicks, A. Menzies, and et al. A systematic, large-scale resequencing screen of X-chromosome coding exons in mental retardation Nat. Genet. 41 2009 535 543
4. 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 21 2016 133 148
5. A.C. Whibley, V. Plagnol, P.S. Tarpey, F. Abidi, T. Fullston, M.K. Choma, C.A. Boucher, L. Shepherd, L. Willatt, G. Parkin, and et al. Fine-scale survey of X chromosome copy number variants and indels underlying intellectual disability Am. J. Hum. Genet. 87 2010 173 188
6. 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
7. A.T. Vulto-van Silfhout, J.Y. Hehir-Kwa, B.W. van Bon, J.H. Schuurs-Hoeijmakers, S. Meader, C.J. Hellebrekers, I.J. Thoonen, A.P. de Brouwer, H.G. Brunner, C. Webber, and et al. Clinical significance of de novo and inherited copy-number variation Hum. Mutat. 34 2013 1679 1687
8. M.J. Stevens-Kroef, E. van den Berg, D. Olde Weghuis, A. Geurts van Kessel, R. Pfundt, M. Linssen-Wiersma, M. Benjamins, T. Dijkhuizen, P.J. Groenen, and A. Simons Identification of prognostic relevant chromosomal abnormalities in chronic lymphocytic leukemia using microarray-based genomic profiling Mol. Cytogenet. 7 2014 3
9. M. Brett, J. McPherson, Z.J. Zang, A. Lai, E.S. Tan, I. Ng, L.C. Ong, B. Cham, P. Tan, S. Rozen, and E.C. Tan Massively parallel sequencing of patients with intellectual disability, congenital anomalies and/or autism spectrum disorders with a targeted gene panel PLoS ONE 9 2014 e93409
10. C.F. Wright, T.W. Fitzgerald, W.D. Jones, S. Clayton, J.F. McRae, M. van Kogelenberg, D.A. King, K. Ambridge, D.M. Barrett, T. Bayzetinova, et al. DDD study Genetic diagnosis of developmental disorders in the DDD study: a scalable analysis of genome-wide research data Lancet 385 2015 1305 1314
11. J. Wiszniewska, W. Bi, C. Shaw, P. Stankiewicz, S.H. Kang, A.N. Pursley, S. Lalani, P. Hixson, T. Gambin, C.H. Tsai, and et al. Combined array CGH plus SNP genome analyses in a single assay for optimized clinical testing Eur. J. Hum. Genet. 22 2014 79 87
12. F.R. Lepri, R. Scavelli, M.C. Digilio, M. Gnazzo, S. Grotta, M.L. Dentici, E. Pisaneschi, P. Sirleto, R. Capolino, A. Baban, and et al. Diagnosis of Noonan syndrome and related disorders using target next generation sequencing BMC Med. Genet. 15 2014 14
13. A.C. Faesen, M.P. Luna-Vargas, and T.K. Sixma The role of UBL domains in ubiquitin-specific proteases Biochem. Soc. Trans. 40 2012 539 545
14. M. Murtaza, L.A. Jolly, J. Gecz, and S.A. Wood La FAM fatale: USP9X in development and disease Cell. Mol. Life Sci. 72 2015 2075 2089
15. 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
16. 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
17. M.H. Jones, R.A. Furlong, H. Burkin, I.J. Chalmers, G.M. Brown, O. Khwaja, and N.A. Affara The Drosophila developmental gene fat facets has a human homologue in Xp11.4 which escapes X-inactivation and has related sequences on Yq11.2 Hum. Mol. Genet. 5 1996 1695 1701
18. 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
19. J.A. Fischer-Vize, G.M. Rubin, and R. Lehmann The fat facets gene is required for Drosophila eye and embryo development Development 116 1992 985 1000
20. S. Dupont, A. Mamidi, M. Cordenonsi, M. Montagner, L. Zacchigna, M. Adorno, G. Martello, M.J. Stinchfield, S. Soligo, L. Morsut, and et al. FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination Cell 136 2009 123 135
21. G. Friocourt, C. Kappeler, Y. Saillour, F. Fauchereau, M.S. Rodriguez, N. Bahi, M.C. Vinet, P. Chafey, K. Poirier, S. Taya, and et al. Doublecortin interacts with the ubiquitin protease DFFRX, which associates with microtubules in neuronal processes Mol. Cell. Neurosci. 28 2005 153 164
22. Y. Xie, M. Avello, M. Schirle, E. McWhinnie, Y. Feng, E. Bric-Furlong, C. Wilson, R. Nathans, J. Zhang, M.W. Kirschner, and 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
23. P. Agrawal, Y.T. Chen, B. Schilling, B.W. Gibson, and R.E. Hughes Ubiquitin-specific peptidase 9, X-linked (USP9X) modulates activity of mammalian target of rapamycin (mTOR) J. Biol. Chem. 287 2012 21164 21175
24. S. Taya, T. Yamamoto, M. Kanai-Azuma, S.A. Wood, and K. Kaibuchi The deubiquitinating enzyme Fam interacts with and stabilizes beta-catenin Genes Cells 4 1999 757 767
25. S. Taya, T. Yamamoto, K. Kano, Y. Kawano, A. Iwamatsu, T. Tsuchiya, K. Tanaka, M. Kanai-Azuma, S.A. Wood, J.S. Mattick, and K. Kaibuchi The Ras target AF-6 is a substrate of the fam deubiquitinating enzyme J. Cell Biol. 142 1998 1053 1062
26. R. Mouchantaf, B.A. Azakir, P.S. McPherson, S.M. Millard, S.A. Wood, and A. Angers The ubiquitin ligase itch is auto-ubiquitylated in vivo and in vitro but is protected from degradation by interacting with the deubiquitylating enzyme FAM/USP9X J. Biol. Chem. 281 2006 38738 38747
27. A.K. Al-Hakim, A. Zagorska, L. Chapman, M. Deak, M. Peggie, and D.R. Alessi Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains Biochem. J. 411 2008 249 260
28. C. Luise, M. Capra, M. Donzelli, G. Mazzarol, M.G. Jodice, P. Nuciforo, G. Viale, P.P. Di Fiore, and S. Confalonieri An atlas of altered expression of deubiquitinating enzymes in human cancer PLoS ONE 6 2011 e15891
29. M. Schwickart, X. Huang, J.R. Lill, J. Liu, R. Ferrando, D.M. French, H. Maecker, K. O'Rourke, F. Bazan, J. Eastham-Anderson, and et al. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival Nature 463 2010 103 107
30. H.V. Firth, J.A. Hurst, and J.G. Hall Clinical Genetics 2009 Oxford University Press New York
31. X. Deng, J.B. Berletch, D.K. Nguyen, and C.M. Disteche X chromosome regulation: diverse patterns in development, tissues and disease Nat. Rev. Genet. 15 2014 367 378
32. 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
33. J.B. Berletch, F. Yang, J. Xu, L. Carrel, and C.M. Disteche Genes that escape from X inactivation Hum. Genet. 130 2011 237 245
34. C. Yang, A.G. Chapman, A.D. Kelsey, J. Minks, A.M. Cotton, and C.J. Brown X-chromosome inactivation: molecular mechanisms from the human perspective Hum. Genet. 130 2011 175 185
35. 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
36. L. Carrel, and H.F. Willard X-inactivation profile reveals extensive variability in X-linked gene expression in females Nature 434 2005 400 404
37. Z. Talebizadeh, S.D. Simon, and M.G. Butler X chromosome gene expression in human tissues: male and female comparisons Genomics 88 2006 675 681
38. C. Zweier, C. Kraus, L. Brueton, T. Cole, F. Degenhardt, H. Engels, G. Gillessen-Kaesbach, L. Graul-Neumann, D. Horn, J. Hoyer, and et al. A new face of Borjeson-Forssman-Lehmann syndrome? De novo mutations in PHF6 in seven females with a distinct phenotype J. Med. Genet. 50 2013 838 847
39. S.B. Peeters, A.M. Cotton, and C.J. Brown Variable escape from X-chromosome inactivation: identifying factors that tip the scales towards expression BioEssays 36 2014 746 756
40. L. Snijders Blok, E. Madsen, J. Juusola, C. Gilissen, D. Baralle, M.R. Reijnders, H. Venselaar, C. Helsmoortel, M.T. Cho, A. Hoischen, et al. DDD Study Mutations in DDX3X are a common cause of unexplained intellectual disability with gender-specific effects on Wnt signaling Am. J. Hum. Genet. 97 2015 343 352
41. J. Xu, S. Taya, K. Kaibuchi, and A.P. Arnold Sexually dimorphic expression of Usp9x is related to sex chromosome complement in adult mouse brain Eur. J. Neurosci. 21 2005 3017 3022
42. C.C. Homan, R. Kumar, L.S. Nguyen, E. Haan, F.L. Raymond, F. Abidi, M. Raynaud, C.E. Schwartz, S.A. Wood, J. Gecz, and L.A. Jolly Mutations in USP9X are associated with X-linked intellectual disability and disrupt neuronal cell migration and growth Am. J. Hum. Genet. 94 2014 470 478
43. L. Paemka, V.B. Mahajan, S.N. Ehaideb, J.M. Skeie, M.C. Tan, S. Wu, A.J. Cox, L.P. Sowers, J. Gecz, L. Jolly, and et al. Seizures are regulated by ubiquitin-specific peptidase 9 X-linked (USP9X), a de-ubiquitinase PLoS Genet. 11 2015 e1005022
44. I. Iossifov, B.J. O'Roak, S.J. Sanders, M. Ronemus, N. Krumm, D. Levy, H.A. Stessman, K.T. Witherspoon, L. Vives, K.E. Patterson, and et al. The contribution of de novo coding mutations to autism spectrum disorder Nature 515 2014 216 221
45. E. Nagy, and L.E. Maquat A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance Trends Biochem. Sci. 23 1998 198 199
46. B.P. Lewis, R.E. Green, and S.E. Brenner Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans Proc. Natl. Acad. Sci. USA 100 2003 189 192
47. 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
48. S.M. Ware, M.G. Aygun, and F. Hildebrandt Spectrum of clinical diseases caused by disorders of primary cilia Proc. Am. Thorac. Soc. 8 2011 444 450
49. R.W. Tucker, A.B. Pardee, and K. Fujiwara Centriole ciliation is related to quiescence and DNA synthesis in 3T3 cells Cell 17 1979 527 535
50. I.A. Vorobjev, and Chentsov YuS Centrioles in the cell cycle. I. Epithelial cells J. Cell Biol. 93 1982 938 949
51. R.Z. Murray, L.A. Jolly, and S.A. Wood The FAM deubiquitylating enzyme localizes to multiple points of protein trafficking in epithelia, where it associates with E-cadherin and beta-catenin Mol. Biol. Cell 15 2004 1591 1599