Reciprocal Xp11.4p11.3 microdeletion/microduplication spanning USP9X, DDX3X, and CASK genes in two patients with syndromic intellectual disability.
CASK
DDX3X
USP9X
Xp11.4 deletion
Xp11.4 duplication
Journal
American journal of medical genetics. Part A
ISSN: 1552-4833
Titre abrégé: Am J Med Genet A
Pays: United States
ID NLM: 101235741
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
revised:
02
02
2022
received:
17
09
2021
accepted:
05
02
2022
pubmed:
4
3
2022
medline:
18
5
2022
entrez:
3
3
2022
Statut:
ppublish
Résumé
Only a few patients with deletions or duplications at Xp11.4, bridging USP9X, DDX3X, and CASK genes, have been described so far. Here, we report on a female harboring a de novo Xp11.4p11.3 deletion and a male with an overlapping duplication inherited from an unaffected mother, presenting with syndromic intellectual disability. We discuss the role of USP9X, DDX3X, and CASK genes in human development and describe the effects of Xp11.4 deletion and duplications in female and male patients, respectively.
Identifiants
pubmed: 35238482
doi: 10.1002/ajmg.a.62694
doi:
Substances chimiques
USP9X protein, human
0
Ubiquitin Thiolesterase
EC 3.4.19.12
DDX3X protein, human
EC 3.6.1.-
DEAD-box RNA Helicases
EC 3.6.4.13
Types de publication
Case Reports
Langues
eng
Sous-ensembles de citation
IM
Pagination
1836-1847Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Agrawal, P., Chen, Y. T., Schilling, B., Gibson, B. W., & Hughes, R. E. (2012). Ubiquitin-specific peptidase 9, X-linked (USP9X) modulates activity of mammalian target of rapamycin (mTOR). Journal of Biological Chemistry, 287(25), 21164-21175. https://doi.org/10.1074/jbc.M111.328021
Al-Hakim, A. K., Zagorska, A., Chapman, L., Deak, M., Peggie, M., & Alessi, D. R. (2008). Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. Biochemical Journal, 411, 249-260. https://doi.org/10.1042/BJ20080067
Allen, R. C., Zoghbi, H. Y., Moseley, A. B., Rosenblatt, H. M., & Belmont, J. W. (1992). Methylation of HpaII and HhaI sites near the polymorphic CAG repeat in the human androgen-receptor gene correlates with X chromosome inactivation. The American Journal of Human Genetics, 51, 1229-1239.
Amos-Landgraf, J. M., Cottle, A., Plenge, R. M., Friez, M., Schwartz, C. E., Longshore, J., & Willard, H. F. (2006). X chromosome-inactivation patterns of 1,005 phenotypically unaffected females. The American Journal of Human Genetics, 79, 493-499. https://doi.org/10.1086/507565
Atasoy, D., Schoch, S., Ho, A., Nadasy, K. A., Liu, X., Zhang, W., Mukherjee, K., Nosyreva, E. D., Fernandez-Chacon, R., Missler, M., Kavalali, E. T., & Südhof, T. C. (2007). Deletion of CASK in mice is lethal and impairs synaptic function. Proceedings of the National Academy of Sciences of the United States of America, 104, 2525-2530. https://doi.org/10.1073/pnas.0611003104
Au, P. Y. B., Huang, L., Broley, S., Gallagher, L., Creede, E., Lahey, D., Ordorica, S., Mina, K., Boycott, K. M., Baynam, G., & Dyment, D. A. (2017). Two females with mutations in USP9X highlight the variable expressivity of the intellectual disability syndrome. European Journal of Medical Genetics, 60, 359-364. https://doi.org/10.1016/j.ejmg.2017.03.013
Belmont, J. W. (1996). Genetic control of X inactivation and processes leading to X-inactivation skewing. The American Journal of Human Genetics, 58, 1101-1108.
Bertelli, M. O., Munir, K., Harris, J., & Salvador-Carulla, L. (2016). “Intellectual developmental disorders”: Reflections on the international consensus document for redefining “mental retardation-intellectual disability” in ICD-11. Advances in Mental Health and Intellectual Disabilities, 10, 36-58. https://doi.org/10.1108/AMHID-10-2015-0050
Bethea, C. L., Kim, A., & Cameron, J. L. (2013). Function and innervation of the locus ceruleus in a macaque model of functional hypothalamic amenorrhea. Neurobiology of Disease, 50, 96-106. https://doi.org/10.1016/j.nbd.2012.10.009
Brett, M., McPherson, J., Zang, Z. J., Lai, A., Tan, E. S., Ng, I., Ong, L. C., Cham, B., Tan, P., Rozen, S., & Tan, E. C. (2014). Massively parallel sequencing of patients with intellectual disability, congenital anomalies and/or autism spectrum disorders with a targeted gene panel. PLoS One, 9, e93409. https://doi.org/10.1371/journal.pone.0093409
Brown, C. J., & Robinson, W. P. (2000). The causes and consequences of random and non-random X chromosome inactivation in humans. Clinical Genetics, 58, 353-363. https://doi.org/10.1034/j.1399-0004.2000.580504.x
Burglen, L., Chantot-Bastaraud, S., Garel, C., Milh, M., Touraine, R., Zanni, G., Petit, F., Afenjar, A., Goizet, C., Barresi, S., Coussement, A., Ioos, C., Lazaro, L., Joriot, S., Desguerre, I., Lacombe, D., des Portes, V., Bertini, E., Siffroi, J. P., … Rodriguez, D. (2012). Spectrum of pontocerebellar hypoplasia in 13 girls and boys with CASK mutations: Confirmation of a recognizable phenotype and first description of a male mosaic patient. Orphanet Journal of Rare Diseases, 7, 18. https://doi.org/10.1186/1750-1172-17-18
Busque, L., Paquette, Y., Provost, S., Roy, D. C., Levine, R. L., Mollica, L., & Gilliland, D. G. (2009). Skewing of X-inactivation ratios in blood cells of aging women is confirmed by independent methodologies. Blood, 113, 3472-3474. https://doi.org/10.1182/blood-2008-12-195677
Chelly, J., Khelfaoui, M., Francis, F., Chérif, B., & Bienvenu, T. (2006). Genetics and pathophysiology of mental retardation. European Journal of Medical Genetics, 14, 701-713. https://doi.org/10.1038/sj.ejhg.5201595
Dupont, S., Mamidi, A., Cordenonsi, M., Montagner, M., Zacchigna, L., Adorno, M., Martello, G., Stinchfield, M. J., Soligo, S., Morsut, L., Inui, M., Moro, S., Modena, N., Argenton, F., Newfeld, S. J., & Piccolo, S. (2009). FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell, 136, 123-135. https://doi.org/10.1016/j.cell.2008.10.051
Friocourt, G., Kappeler, C., Saillour, Y., Fauchereau, F., Rodriguez, M. S., Bahi, N., Vinet, M. C., Chafey, P., Poirier, K., Taya, S., Wood, S. A., Dargemont, C., Francis, F., & Chelly, J. (2005). Doublecortin interacts with the ubiquitin protease DFFRX, which associates with microtubules in neuronal processes. Molecular and Cellular Neuroscience, 28, 153-164. https://doi.org/10.1016/j.mcn.2004.09.005
Froyen, G., van Esch, H., Bauters, M., Hollanders, K., Frints, S. G., Vermeesch, J. R., Devriendt, K., Fryns, J. P., & Marynen, P. (2007). Detection of genomic copy number changes in patients with idiopathic mental retardation by high-resolution X-array-CGH: Important role for increased gene dosage of XLMR genes. Human Mutation, 28, 1034-1042. https://doi.org/10.1002/humu.20564
Garbelli, A., Beermann, S., di Cicco, G., Dietrich, U., & Maga, G. (2011). 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, e19810. https://doi.org/10.1371/journal.pone.0019810
Giorda, R., Bonaglia, M. C., Beri, S., Fichera, M., Novara, F., Magini, P., Urquhart, J., Sharkey, F. H., Zucca, C., Grasso, R., Marelli, S., Castiglia, L., di Benedetto, D., Musumeci, S. A., Vitello, G. A., Failla, P., Reitano, S., Avola, E., Bisulli, F., … Zuffardi, O. (2009). Complex segmental duplications mediate a recurrent dup(X)(p11.22-p11.23) associated with mental retardation, speech delay, and EEG anomalies in males and females. The American Journal of Human Genetics, 85, 394-400. https://doi.org/10.1016/j.ajhg.2009.08.001
Harripaul, R., Vasli, N., Mikhailov, A., Rafiq, M. A., Mittal, K., Windpassinger, C., Sheikh, T. I., Noor, A., Mahmood, H., Downey, S., Johnson, M., Vleuten, K., Bell, L., Ilyas, M., Khan, F. S., Khan, V., Moradi, M., Ayaz, M., Naeem, F., … Vincent, J. B. (2018). Mapping autosomal recessive intellectual disability: Combined microarray and exome sequencing identifies 26 novel candidate genes in 192 consanguineous families. Molecular Psychiatry, 23, 973-984. https://doi.org/10.1038/mp.2017.60
Hayashi, S., Okamoto, N., Chinen, Y., Takanashi, J., Makita, Y., Hata, A., Imoto, I., & Inazawa, J. (2012). Novel intragenic duplications and mutations of CASK in patients with mental retardation and microcephaly with pontine and cerebellar hypoplasia (MICPCH). Human Genetics, 131(1), 99-110. https://doi.org/10.1007/s00439-011-1047-0
Hsueh, Y. P. (2006). The role of the MAGUK protein CASK in neural development and synaptic function. Current Medicinal Chemistry, 13, 1915-1927. https://doi.org/10.2174/092986706777585040
Hsueh, Y. P., Wang, T. F., Yang, F. C., & Sheng, M. (2000). Nuclear translocation and transcription regulation by the membrane-associated guanylate kinase CASK/LIN-2. Nature, 404, 298-302. https://doi.org/10.1038/35005118
Hsueh, Y. P., Yang, F. C., Kharazia, V., Naisbitt, S., Cohen, A. R., Weinberg, R. J., & Sheng, M. (1998). Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. Journal of Cell Biology, 142, 139-151. https://doi.org/10.1083/jcb.142.1.139
Iwase, S., Bérubé, N. G., Zhou, Z., Kasri, N. N., Battaglioli, E., Scandaglia, M., & Barco, A. (2017). Epigenetic etiology of intellectual disability. Journal of Neuroscience, 37, 10773-10782. https://doi.org/10.1523/JNEUROSCI.1840-17
Johnson, B. V., Kumar, R., Oishi, S., Alexander, S., Kasherman, M., Vega, M. S., Ivancevic, A., Gardner, A., Domingo, D., Corbett, M., Parnell, E., Yoon, S., Oh, T., Lines, M., Lefroy, H., Kini, U., van Allen, M., Grønborg, S., Mercier, S., … Johnson, B. V. (2020). Partial loss of USP9X function leads to a male neurodevelopmental and behavioral disorder converging on transforming growth factor beta signaling. Biological Psychiatry, 15(87), 100-112. https://doi.org/10.1016/j.biopsych.2019.05.028
Jolly, L. A., Taylor, V., & Wood, S. A. (2009). USP9X enhances the polarity and self-renewal of embryonic stem cell-derived neural progenitors. Molecular Biology of the Cell, 20, 2015-2029. https://doi.org/10.1091/mbc.e08-06-0596
Jones, M. H., Furlong, R. A., Burkin, H., Chalmers, I. J., Brown, G. M., Khwaja, O., & Affara, N. A. (1996). The Drosophila developmental gene fat facets has a human homologue in Xp11.4 which escapes X-inactivation and has related sequences on Yq11.2. Human Molecular Genetics, 5, 1695-1701. https://doi.org/10.1093/hmg/5.11.1695
Kasim, V., Wu, S., Taira, K., & Miyagishi, M. (2013). Determination of the role of DDX3 a factor involved in mammalian RNAi pathway using an shRNA-expression library. PLoS ONE, 8, e59445. https://doi.org/10.1371/journal.pone.0059445
Khut, P. Y., Tucker, B., Lardelli, M., & Wood, S. A. (2007). Evolutionary and expression analysis of the zebrafish deubiquitylating enzyme, usp9. Zebrafish, 4, 95-101. https://doi.org/10.1089/zeb.2006.0502
Laverty, H. G., & Wilson, J. B. (1998). Murine CASK is disrupted in a sex-linked cleft palate mouse mutant. Genomics, 53, 29-41. https://doi.org/10.1006/geno.1998.5479
Lennox, A. L., Hoye, M. L., Jiang, R., Johnson-Kerner, B. L., Suit, L. A., Venkataramanan, S., Sheehan, C. J., Alsina, F. C., Fregeau, B., Aldinger, K. A., Moey, C., Lobach, I., Afenjar, A., Babovic-Vuksanovic, D., Bézieau, S., Blackburn, P. R., Bunt, J., Burglen, L., Campeau, P. M., … Sherr, E. H. (2020). Pathogenic DDX3X mutations impair RNA metabolism and neurogenesis during fetal cortical development. Neuron, 106, 404-420.e8. https://doi.org/10.1016/j.neuron.2020.01.042
Leonard, H., & Wen, X. (2002). The epidemiology of mental retardation: Challenges and opportunities in the new millennium. Mental Retardation and Developmental Disabilities Research Reviews, 8, 117-134. https://doi.org/10.1002/mrdd.10031
Linsalata, A. E., He, F., Malik, A. M., Glineburg, M. R., Green, K. M., Natla, S., Flores, B. N., Krans, A., Archbold, H. C., Fedak, S. J., Barmada, S. J., & Todd, P. K. (2019). DDX3X and specific initiation factors modulate FMR1 repeat-associated non-AUG-initiated translation. EMBO Reports, 20, e47498. https://doi.org/10.15252/embr.201847498
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Miller, D. T., Adam, M. P., Aradhya, S., Biesecker, L. G., Brothman, A. R., Carter, N. P., Church, D. M., Crolla, J. A., Eichler, E. E., Epstein, C. J., Faucett, W. A., Feuk, L., Friedman, J. M., Hamosh, A., Jackson, L., Kaminsky, E. B., Kok, K., Krantz, I. D., Kuhn, R. M., … Ledbetter, D. H. (2010). Consensus statement: Chromosomal microarray is a first-tier clinical diagnostic test for individuals with developmental disabilities or congenital anomalies. The American Journal of Human Genetics, 86, 749-764. https://doi.org/10.1016/j.ajhg.2010.04.006
Moog, U., Bierhals, T., Brand, K., Bautsch, J., Biskup, S., Brune, T., Denecke, J., de Die-Smulders, C. E., Evers, C., Hempel, M., Henneke, M., Yntema, H., Menten, B., Pietz, J., Pfundt, R., Schmidtke, J., Steinemann, D., Stumpel, C. T., van Maldergem, L., … Moog, U. (2015). Phenotypic and molecular insights into CASK-related disorders in males. Orphanet Journal of Rare Diseases, 10, 44. https://doi.org/10.1186/s13023-015-0256-3
Mouchantaf, R., Azakir, B. A., McPherson, P. S., Millard, S. M., Wood, S. A., & Angers, A. (2006). 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. Journal of Biological Chemistry, 281, 38738-38747. https://doi.org/10.1074/jbc.M605959200
Mukherjee, K., Patel, P. A., Rajan, D. S., LaConte, L. E. W., Srivastava, S., & Mukherjee, K. (2020). Survival of a male patient harboring CASK Arg27Ter mutation to adolescence. Molecular Genetics & Genomic Medicine, 8, e1426. https://doi.org/10.1002/mgg3.1426
Murtaza, M., Lachlan, A. J., Jozef, G., & Stephen, A. W. (2015). La FAM fatale: USP9X in development and disease. Cellular and Molecular Life Sciences, 72, 2075-2089. https://doi.org/10.1007/s00018-015-1851-0
Najm, J., Horn, D., Wimplinger, I., Golden, J. A., Chizhikov, V. V., Sudi, J., Christian, S. L., Ullmann, R., Kuechler, A., Haas, C. A., Flubacher, A., Charnas, L. R., Uyanik, G., Frank, U., Klopocki, E., Dobyns, W. B., & Kutsche, K. (2008). Mutations of CASK cause an X-linked brain malformation phenotype with microcephaly and hypoplasia of the brainstem and cerebellum. Nature Genetics, 40, 1065-1067. https://doi.org/10.1038/ng.194
Nakamura, K., Nishiyama, K., Kodera, H., Nakashima, M., Tsurusaki, Y., & Miyake, N. (2014). A de novo CASK mutation in pontocerebellar hypoplasia type 3 with early myoclonic epilepsy and tetralogy of Fallot. Brain and Development, 36, 272-273. https://doi.org/10.1016/j.braindev.2013.03.007
Neri, G., Schwartz, C. E., Lubs, H. A., & Stevenson, R. E. (2018). X-linked intellectual disability update 2017. The American Journal of Human Genetics. Part A, 176, 1375-1388. https://doi.org/10.1002/ajmg.a.38710
Nicola, P., Blackburn, P. R., Rasmussen, K. J., Bertsch, N. L., Klee, E. W., Hasadsri, L., Pichurin, P. N., Rankin, J., Raymond, F. L., DDD Study, & Clayton-Smith, J. (2019). De novo DDX3X missense variants in males appear viable and contribute to syndromic intellectual disability. The American Journal of Human Genetics. Part A, 179, 570-578. https://doi.org/10.1002/ajmg.a.61061
Nyhan, W. L., Bakay, B., Connor, J. D., Marks, J. F., & Keele, D. K. (1970). Hemizygous expression of glucose-6-phosphate dehydrogenase in erythrocytes of heterozygotes for the Lesch-Nyhan syndrome. Proceedings of the National Academy of Sciences of the United States of America, 65, 214-218. https://doi.org/10.1073/pnas.65.1.214
Palka, C., de Marco, S., Alfonsi, M., Matricardi, M., Erricchiello, E., Morizio, E., Guanciali Franchi, P., Calabrese, G., Mohn, A., & Chiarelli, F. (2018). Discovering a familial Xp11.4 microduplication: Does the mother matter? Meta Gene, 16, 90-95. https://doi.org/10.1016/j.mgene.2018.02.001
Plenge, R. M., Stevenson, R. A., Lubs, H. A., Schwartz, C. E., & Willard, H. F. (2002). Skewed X-chromosome inactivation is a common feature of X-linked mental retardation disorders. The American Journal of Human Genetics, 71, 168-173. https://doi.org/10.1086/341123
Reijnders, M. R., Zachariadis, V., Latour, B., Jolly, L., Mancini, G. M., Pfundt, R., Wu, K. M., van Ravenswaaij-Arts, C. M., Veenstra-Knol, H. E., Anderlid, B. M., Wood, S. A., Cheung, S. W., Barnicoat, A., Probst, F., Magoulas, P., Brooks, A. S., Malmgren, H., Harila-Saari, A., Marcelis, C. M., … Kleefstra, T. (2016). De novo loss-of-function mutations in USP9X cause a female-specific recognizable syndrome with developmental delay and congenital malformations. The American Journal of Human Genetics, 98, 373-381. https://doi.org/10.1016/j.ajhg.2015.12.015
Rodriguez-Revenga, L., Mila, M., Rosenberg, C., Lamb, A., & Lee, C. (2007). Structural variation in the human genome: The impact of copy number variants on clinical diagnosis. Genetics in Medicine, 9, 600-606. https://doi.org/10.1097/gim.0b013e318149e1e3
Saitsu, H., Kato, M., Osaka, H., Moriyama, N., Horita, H., & Nishiyama, K. (2012). CASK aberrations in male patients with Ohtahara syndrome and cerebellar hypoplasia. Epilepsia, 53, 1441-1449. https://doi.org/10.1111/j.1528-1167.2012.03548.x
Schröder, M. (2010). Human DEAD-box protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation. Biochemical Pharmacology, 79, 297-306. https://doi.org/10.1016/j.bcp.2009.08.032
Sharp, A., Robinson, D., & Jacobs, P. (2000). Age-and tissue-specific variation of X chromosome inactivation ratios in normal women. Human Genetics, 107, 343-349. https://doi.org/10.1007/s004390000382
Srivastava, S., McMillan, R., Willis, J., Clark, H., Chavan, V., Liang, C., Zhang, H., Hulver, M., & Mukherjee, K. (2016). X-linked intellectual disability gene CASK regulates postnatal brain growth in a non-cell autonomous manner. Acta Neuropathologica Communications, 4, 30. https://doi.org/10.1186/s40478-016-0295-6
Stageman, S., Jolly, L. A., Premarathne, S., Gecz, J., Richards, L. J., Mackay-Sim, A., & Wood, S. A. (2013). Loss of Usp9x disrupts cortical architecture, hippocampal development and TGFbeta-mediated axonogenesis. PLoS ONE, 5(8), e68287. https://doi.org/10.1371/journal.pone.0068287
Stevenson, D., Laverty, H. G., Wenwieser, S., Douglas, M., & Wilson, J. B. (2000). Mapping and expression analysis of the human CASK gene. Mammalian Genome, 11, 934-937. https://doi.org/10.1007/s003350010170
Takanashi, J., Okamoto, N., Yamamoto, Y., Hayashi, S., Arai, H., & Takahashi, Y. (2012). Clinical and radiological features of Japanese patients with a severe phenotype due to CASK mutations. The American Journal of Human Genetics, 158A, 3112-3118. https://doi.org/10.1002/ajmg.a.35640
Taya, S., Yamamoto, T., Kanai-Azuma, M., Wood, S. A., & Kaibuchi, K. (1999). The deubiquitinating enzyme fam interacts with and stabilizes beta-catenin. Genes to Cells, 4, 757-767. https://doi.org/10.1046/j.1365-2443.1999.00297.x
Taya, S., Yamamoto, T., Kano, K., Kawano, Y., Iwamatsu, A., Tsuchiya, T., Tanaka, K., Kanai-Azuma, M., Wood, S. A., Mattick, J. S., & Kaibuchi, K. (1998). The Ras target AF-6 is a substrate of the fam deubiquitinating enzyme. Journal of Cell Biology, 142, 1053-1062. https://doi.org/10.1083/jcb.142.4.1053
Willard, H. F. (2000). The sex chromosomes and X chromosome inactivation. In D. L. Valle, S. Antonarakis, A. Ballabio, A. L. Beaudet, & G. A. Mitchell (Eds.), The online metabolic and molecular bases of inherited disease. McGraw Hill. https://doi.org/10.1036/ommbid.371
Wood, S. A., Pascoe, W. S., Ru, K., Yamada, T., Hirchenhain, J., Kemler, R., & Mattick, J. S. (1997). Cloning and expression analysis of a novel mouse gene with sequence similarity to the Drosophila fat facets gene. Mechanisms of Development, 63, 29-38. https://doi.org/10.1016/s0925-4773(97)00672-2
Xie, Y., Avello, M., Schirle, M., McWhinnie, E., Feng, Y., Bric-Furlong, E., Wilson, C., Nathans, R., Zhang, J., Kirschner, M. W., Huang, S. M., & Cong, F. (2013). Deubiquitinase FAM/USP9X interacts with the E3 ubiquitin ligase SMURF1 protein and protects it from ligase activity-dependent self-degradation. Journal of Biological Chemistry, 288, 2976-2985. https://doi.org/10.1074/jbc.M112.430066
Zheng, C. Y., Seabold, G. K., Horak, M., & Petralia, R. S. (2011). MAGUKs, synaptic development, and synaptic plasticity. The Neuroscientist, 17, 493-512. https://doi.org/10.1177/1073858410386384