De Novo Disruption of the Proteasome Regulatory Subunit PSMD12 Causes a Syndromic Neurodevelopmental Disorder

American Journal of Human Genetics

Volumn 100, Issue 2, 2017, Pages 352-363

  Küry, Sébastien ^a   Besnard, Thomas ^a   Ebstein, Frédéric ^b   Khan, Tahir N ^c   Gambin, Tomasz ^d,e,f   Douglas, Jessica ^g   Bacino, Carlos A ^d,h   Sanders, Stephan J ⁱ   Lehmann, Andrea ^b   Latypova, Xénia ^a   Khan, Kamal ^c   Pacault, Mathilde ^a   Sacharow, Stephanie ^g   Glaser, Kimberly ^j   Bieth, Eric ^a   Perrin Sabourin, Laurence ^a   Jacquemont, Marie Line ^a   Cho, Megan T ^k   Roeder, Elizabeth ^d   Denommé Pichon, Anne Sophie ^a   Monaghan, Kristin G ^k   Yuan, Bo ^d,h   Xia, Fan ^d,h   Simon, Sylvain ^a   Bonneau, Dominique ^a   Parent, Philippe ^a   Gilbert Dussardier, Brigitte ^a   Odent, Sylvie ^a   Toutain, Annick ^a   Pasquier, Laurent ^a   Barbouth, Deborah ^j   Shaw, Chad A ^d,h   Patel, Ankita ^d,h   Smith, Janice L ^d,h   Bi, Weimin ^d,h   Schmitt, Sébastien ^a   Deb, Wallid ^a   Nizon, Mathilde ^a   Mercier, Sandra ^a   Vincent, Marie ^a   Rooryck, Caroline ^a   Malan, Valérie ^a   Briceño, Ignacio ^l   Gómez, Alberto ^l   Nugent, Kimberly M ^d   Gibson, James B ^m   Cogné, Benjamin ^a   Lupski, James R ^d,n   Stessman, Holly A F ^o   Eichler, Evan E ^o,p   Retterer, Kyle ^k   Yang, Yaping ^d,h   Redon, Richard ^a   Katsanis, Nicholas ^c   Rosenfeld, Jill A ^d   Kloetzel, Peter Michael ^b   Golzio, Christelle ^c   Bézieau, Stéphane ^a   Stankiewicz, Paweł ^d,f,h   Isidor, Bertrand ^a   more..

^a NANTES UNIVERSITY HOSPITAL   (France)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e WARSAW UNIVERSITY OF TECHNOLOGY   (Poland)

^f INSTITUTE OF MOTHER AND CHILD   (Poland)

^g BOSTON CHILDREN S HOSPITAL   (United States)

^h BAYLOR GENETICS   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^k GENEDX   (United States)

^l PONTIFICIA UNIVERSIDAD JAVERIANA   (Colombia)

^m Section of Clinical Genetics and Metabolism'Specially for Children   (United States)

ⁿ TEXAS CHILDREN S HOSPITAL   (United States)

^o UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^p HOWARD HUGHES MEDICAL INSTITUTE   (United States)

more..

Author keywords

intellectual disability; proteasome 26S; PSMD12; RPN5; syndromic neurodevelopmental disorder; ubiquitin

Indexed keywords

PROTEASOME; PROTEASOME 26S SUBUNIT NON ATPASE 12; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; 26S PROTEASOME NON-ATPASE REGULATORY SUBUNIT 13;

ABNORMAL BEHAVIOR; ADOLESCENT; ADULT; AGENESIS; ARTICLE; BRAIN ATROPHY; CHILD; CLINICAL ARTICLE; COLOBOMA; CONGENITAL HEART MALFORMATION; CONGENITAL MALFORMATION; CRANIOFACIAL MALFORMATION; CRISPR CAS SYSTEM; CRISPR CAS9 SYSTEM; CRYPTORCHISM; DEMYELINATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; EYE MALFORMATION; FACE DYSMORPHIA; FEEDING DIFFICULTY; FEMALE; GENE DELETION; GENITAL MALFORMATION; GROWTH DISORDER; HEARING IMPAIRMENT; HEART VENTRICLE SEPTUM DEFECT; HUMAN; HYDRONEPHROSIS; HYPERTELORISM; HYPOPLASIA; HYPOSPADIAS; INTELLECTUAL IMPAIRMENT; KIDNEY DYSPLASIA; KIDNEY MALFORMATION; KIDNEY TUBULE; LOW SET EAR; MALE; MENTAL DISEASE; MICROCEPHALY; MOLECULAR PATHOLOGY; MOTOR DYSFUNCTION; MUSCLE HYPOTONIA; NEUROPATHOLOGY; PATENT DUCTUS ARTERIOSUS; PERIVENTRIC HYPOMYELINATION; POINT MUTATION; PRESCHOOL CHILD; PRIORITY JOURNAL; RETROGNATHIA; SCHOOL CHILD; SEIZURE; SKELETON MALFORMATION; SPEECH DELAY; STRABISMUS; SYNDACTYLY; THUMB; TONIC SEIZURE; VISUAL IMPAIRMENT; YOUNG ADULT; ZEBRA FISH; ANIMAL; CASE REPORT; COPY NUMBER VARIATION; DISEASE MODEL; DOWN REGULATION; GENETICS; INFANT; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ANIMALS; CHILD; CHILD, PRESCHOOL; DISEASE MODELS, ANIMAL; DNA COPY NUMBER VARIATIONS; DOWN-REGULATION; FEMALE; GENE DELETION; HUMANS; INFANT; INTELLECTUAL DISABILITY; MALE; MICROCEPHALY; NEURODEVELOPMENTAL DISORDERS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEASOME ENDOPEPTIDASE COMPLEX; ZEBRAFISH;

EID: 85010903957     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2017.01.003     Document Type: Article

References (63)

1. 1 Sullivan, J.A., Shirasu, K., Deng, X.W., The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nat. Rev. Genet. 4 (2003), 948–958.
2. 2 Goldberg, A.L., Protein degradation and protection against misfolded or damaged proteins. Nature 426 (2003), 895–899.
3. 3 Hershko, A., Ciechanover, A., The ubiquitin system. Annu. Rev. Biochem. 67 (1998), 425–479.
4. 4 Finley, D., Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78 (2009), 477–513.
5. 5 Murata, S., Yashiroda, H., Tanaka, K., Molecular mechanisms of proteasome assembly. Nat. Rev. Mol. Cell Biol. 10 (2009), 104–115.
6. 6 Voges, D., Zwickl, P., Baumeister, W., The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68 (1999), 1015–1068.
7. 7 Hamilton, A.M., Zito, K., Breaking it down: the ubiquitin proteasome system in neuronal morphogenesis. Neural Plast., 2013, 2013, 196848.
8. 8 Tai, H.C., Schuman, E.M., Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat. Rev. Neurosci. 9 (2008), 826–838.
9. 9 Cajigas, I.J., Will, T., Schuman, E.M., Protein homeostasis and synaptic plasticity. EMBO J. 29 (2010), 2746–2752.
10. 10 Hegde, A.N., Haynes, K.A., Bach, S.V., Beckelman, B.C., Local ubiquitin-proteasome-mediated proteolysis and long-term synaptic plasticity. Front. Mol. Neurosci., 7, 2014, 96.
11. 11 Acconcia, F., Sigismund, S., Polo, S., Ubiquitin in trafficking: the network at work. Exp. Cell Res. 315 (2009), 1610–1618.
12. 12 Schwarz, L.A., Patrick, G.N., Ubiquitin-dependent endocytosis, trafficking and turnover of neuronal membrane proteins. Mol. Cell. Neurosci. 49 (2012), 387–393.
13. 13 Dantuma, N.P., Bott, L.C., The ubiquitin-proteasome system in neurodegenerative diseases: precipitating factor, yet part of the solution. Front. Mol. Neurosci., 7, 2014, 70.
14. 14 Fecto, F., Esengul, Y.T., Siddique, T., Protein recycling pathways in neurodegenerative diseases. Alzheimers Res. Ther., 6, 2014, 13.
15. 15 Kishino, T., Lalande, M., Wagstaff, J., UBE3A/E6-AP mutations cause Angelman syndrome. Nat. Genet. 15 (1997), 70–73.
16. 16 Basel-Vanagaite, L., Dallapiccola, B., Ramirez-Solis, R., Segref, A., Thiele, H., Edwards, A., Arends, M.J., Miró, X., White, J.K., Désir, J., et al. Deficiency for the ubiquitin ligase UBE3B in a blepharophimosis-ptosis-intellectual-disability syndrome. Am. J. Hum. Genet. 91 (2012), 998–1010.
17. 17 Froyen, G., Corbett, M., Vandewalle, J., Jarvela, I., Lawrence, O., Meldrum, C., Bauters, M., Govaerts, K., Vandeleur, L., Van Esch, H., et al. Submicroscopic duplications of the hydroxysteroid dehydrogenase HSD17B10 and the E3 ubiquitin ligase HUWE1 are associated with mental retardation. Am. J. Hum. Genet. 82 (2008), 432–443.
18. 18 Hao, Y.H., Fountain, M.D. Jr., Fon Tacer, K., Xia, F., Bi, W., Kang, S.H., Patel, A., Rosenfeld, J.A., Le Caignec, C., Isidor, B., et al. USP7 Acts as a Molecular Rheostat to Promote WASH-Dependent Endosomal Protein Recycling and Is Mutated in a Human Neurodevelopmental Disorder. Mol. Cell 59 (2015), 956–969.
19. 19 Homan, C.C., Kumar, R., Nguyen, L.S., Haan, E., Raymond, F.L., Abidi, F., Raynaud, M., Schwartz, C.E., Wood, S.A., Gecz, J., Jolly, L.A., 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.
20. 20 Sobreira, N., Schiettecatte, F., Valle, D., Hamosh, A., GeneMatcher: a matching tool for connecting investigators with an interest in the same gene. Hum. Mutat. 36 (2015), 928–930.
21. 21 Firth, H.V., Richards, S.M., Bevan, A.P., Clayton, S., Corpas, M., Rajan, D., Van Vooren, S., Moreau, Y., Pettett, R.M., Carter, N.P., DECIPHER: Database of Chromosomal Imbalance and Phenotype in Humans Using Ensembl Resources. Am. J. Hum. Genet. 84 (2009), 524–533.
22. 22 Isidor, B., Küry, S., Rosenfeld, J.A., Besnard, T., Schmitt, S., Joss, S., Davies, S.J., Lebel, R.R., Henderson, A., Schaaf, C.P., et al. De Novo Truncating Mutations in the Kinetochore-Microtubules Attachment Gene CHAMP1 Cause Syndromic Intellectual Disability. Hum. Mutat. 37 (2016), 354–358.
23. 23 Retterer, K., Juusola, J., Cho, M.T., Vitazka, P., Millan, F., Gibellini, F., Vertino-Bell, A., Smaoui, N., Neidich, J., Monaghan, K.G., et al. Clinical application of whole-exome sequencing across clinical indications. Genet. Med. 18 (2016), 696–704.
24. 24 Iossifov, I., O'Roak, B.J., Sanders, S.J., Ronemus, M., Krumm, N., Levy, D., Stessman, H.A., Witherspoon, K.T., Vives, L., Patterson, K.E., et al. The contribution of de novo coding mutations to autism spectrum disorder. Nature 515 (2014), 216–221.
25. 25 Bainbridge, M.N., Wang, M., Wu, Y., Newsham, I., Muzny, D.M., Jefferies, J.L., Albert, T.J., Burgess, D.L., Gibbs, R.A., Targeted enrichment beyond the consensus coding DNA sequence exome reveals exons with higher variant densities. Genome Biol., 12, 2011, R68.
26. 26 Yang, Y., Muzny, D.M., Reid, J.G., Bainbridge, M.N., Willis, A., Ward, P.A., Braxton, A., Beuten, J., Xia, F., Niu, Z., et al. Clinical whole-exome sequencing for the diagnosis of mendelian disorders. N. Engl. J. Med. 369 (2013), 1502–1511.
27. 27 Boone, P.M., Bacino, C.A., Shaw, C.A., Eng, P.A., Hixson, P.M., Pursley, A.N., Kang, S.H., Yang, Y., Wiszniewska, J., Nowakowska, B.A., et al. Detection of clinically relevant exonic copy-number changes by array CGH. Hum. Mutat. 31 (2010), 1326–1342.
28. 28 Wiszniewska, J., Bi, W., Shaw, C., Stankiewicz, P., Kang, S.H., Pursley, A.N., Lalani, S., Hixson, P., Gambin, T., Tsai, C.H., 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.
29. 29 MacDonald, J.R., Ziman, R., Yuen, R.K., Feuk, L., Scherer, S.W., The Database of Genomic Variants: a curated collection of structural variation in the human genome. Nucleic Acids Res. 42 (2014), D986–D992.
30. 30 Gomes, A.V., Genetics of proteasome diseases. Scientifica (Cairo), 2013, 2013, 637629.
31. 31 Bhattacharyya, S., Yu, H., Mim, C., Matouschek, A., Regulated protein turnover: snapshots of the proteasome in action. Nat. Rev. Mol. Cell Biol. 15 (2014), 122–133.
32. 32 Sharon, M., Taverner, T., Ambroggio, X.I., Deshaies, R.J., Robinson, C.V., Structural organization of the 19S proteasome lid: insights from MS of intact complexes. PLoS Biol., 4, 2006, e267.
33. 33 Glickman, M.H., Rubin, D.M., Coux, O., Wefes, I., Pfeifer, G., Cjeka, Z., Baumeister, W., Fried, V.A., Finley, D., A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94 (1998), 615–623.
34. 34 Rubin, D.M., Glickman, M.H., Larsen, C.N., Dhruvakumar, S., Finley, D., Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 17 (1998), 4909–4919.
35. 35 Book, A.J., Smalle, J., Lee, K.H., Yang, P., Walker, J.M., Casper, S., Holmes, J.H., Russo, L.A., Buzzinotti, Z.W., Jenik, P.D., Vierstra, R.D., The RPN5 subunit of the 26s proteasome is essential for gametogenesis, sporophyte development, and complex assembly in Arabidopsis. Plant Cell 21 (2009), 460–478.
36. 36 Yen, H.C., Espiritu, C., Chang, E.C., Rpn5 is a conserved proteasome subunit and required for proper proteasome localization and assembly. J. Biol. Chem. 278 (2003), 30669–30676.
37. 37 Collins, S.R., Miller, K.M., Maas, N.L., Roguev, A., Fillingham, J., Chu, C.S., Schuldiner, M., Gebbia, M., Recht, J., Shales, M., et al. Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446 (2007), 806–810.
38. 38 Maytal-Kivity, V., Pick, E., Piran, R., Hofmann, K., Glickman, M.H., The COP9 signalosome-like complex in S. cerevisiae and links to other PCI complexes. Int. J. Biochem. Cell Biol. 35 (2003), 706–715.
39. 39 Huang, N., Lee, I., Marcotte, E.M., Hurles, M.E., Characterising and predicting haploinsufficiency in the human genome. PLoS Genet., 6, 2010, e1001154.
40. 40 Lek, M., Karczewski, K.J., Minikel, E.V., Samocha, K.E., Banks, E., Fennell, T., O'Donnell-Luria, A.H., Ware, J.S., Hill, A.J., Cummings, B.B., et al., Exome Aggregation Consortium. Analysis of protein-coding genetic variation in 60,706 humans. Nature 536 (2016), 285–291.
41. 41 Kim, H.M., Yu, Y., Cheng, Y., Structure characterization of the 26S proteasome. Biochim. Biophys. Acta 1809 (2011), 67–79.
42. 42 Yu, Z., Kleifeld, O., Lande-Atir, A., Bsoul, M., Kleiman, M., Krutauz, D., Book, A., Vierstra, R.D., Hofmann, K., Reis, N., et al. Dual function of Rpn5 in two PCI complexes, the 26S proteasome and COP9 signalosome. Mol. Biol. Cell 22 (2011), 911–920.
43. 43 Peters, L.Z., Karmon, O., David-Kadoch, G., Hazan, R., Yu, T., Glickman, M.H., Ben-Aroya, S., The protein quality control machinery regulates its misassembled proteasome subunits. PLoS Genet., 11, 2015, e1005178.
44. 44 Ebstein, F., Lehmann, A., Kloetzel, P.M., The FAT10- and ubiquitin-dependent degradation machineries exhibit common and distinct requirements for MHC class I antigen presentation. Cell. Mol. Life Sci. 69 (2012), 2443–2454.
45. 45 Bochmann, I., Ebstein, F., Lehmann, A., Wohlschlaeger, J., Sixt, S.U., Kloetzel, P.M., Dahlmann, B., T lymphocytes export proteasomes by way of microparticles: a possible mechanism for generation of extracellular proteasomes. J. Cell. Mol. Med. 18 (2014), 59–68.
46. 46 Seifert, U., Bialy, L.P., Ebstein, F., Bech-Otschir, D., Voigt, A., Schröter, F., Prozorovski, T., Lange, N., Steffen, J., Rieger, M., et al. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 142 (2010), 613–624.
47. 47 Dambacher, C.M., Worden, E.J., Herzik, M.A., Martin, A., Lander, G.C., Atomic structure of the 26S proteasome lid reveals the mechanism of deubiquitinase inhibition. eLife, 5, 2016, e13027.
48. 48 Boehringer, J., Riedinger, C., Paraskevopoulos, K., Johnson, E.O., Lowe, E.D., Khoudian, C., Smith, D., Noble, M.E., Gordon, C., Endicott, J.A., Structural and functional characterization of Rpn12 identifies residues required for Rpn10 proteasome incorporation. Biochem. J. 448 (2012), 55–65.
49. 49 Bolar, N.A., Golzio, C., Živná, M., Hayot, G., Van Hemelrijk, C., Schepers, D., Vandeweyer, G., Hoischen, A., Huyghe, J.R., Raes, A., et al. Heterozygous Loss-of-Function SEC61A1 Mutations Cause Autosomal-Dominant Tubulo-Interstitial and Glomerulocystic Kidney Disease with Anemia. Am. J. Hum. Genet. 99 (2016), 174–187.
50. 50 Borck, G., Hög, F., Dentici, M.L., Tan, P.L., Sowada, N., Medeira, A., Gueneau, L., Thiele, H., Kousi, M., Lepri, F., et al. BRF1 mutations alter RNA polymerase III-dependent transcription and cause neurodevelopmental anomalies. Genome Res. 25 (2015), 155–166.
51. 51 Dauber, A., Golzio, C., Guenot, C., Jodelka, F.M., Kibaek, M., Kjaergaard, S., Leheup, B., Martinet, D., Nowaczyk, M.J., Rosenfeld, J.A., et al. SCRIB and PUF60 are primary drivers of the multisystemic phenotypes of the 8q24.3 copy-number variant. Am. J. Hum. Genet. 93 (2013), 798–811.
52. 52 Gordon, C.T., Weaver, K.N., Zechi-Ceide, R.M., Madsen, E.C., Tavares, A.L., Oufadem, M., Kurihara, Y., Adameyko, I., Picard, A., Breton, S., et al. Mutations in the endothelin receptor type A cause mandibulofacial dysostosis with alopecia. Am. J. Hum. Genet. 96 (2015), 519–531.
53. 53 Isrie, M., Breuss, M., Tian, G., Hansen, A.H., Cristofoli, F., Morandell, J., Kupchinsky, Z.A., Sifrim, A., Rodriguez-Rodriguez, C.M., Dapena, E.P., et al. Mutations in Either TUBB or MAPRE2 Cause Circumferential Skin Creases Kunze Type. Am. J. Hum. Genet. 97 (2015), 790–800.
54. 54 Kague, E., Gallagher, M., Burke, S., Parsons, M., Franz-Odendaal, T., Fisher, S., Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS ONE, 7, 2012, e47394.
55. 55 Pardo-Martin, C., Allalou, A., Medina, J., Eimon, P.M., Wählby, C., Fatih Yanik, M., High-throughput hyperdimensional vertebrate phenotyping. Nat. Commun., 4, 2013, 1467.
56. 56 Bartnik, M., Nowakowska, B., Derwińska, K., Wiśniowiecka-Kowalnik, B., Kędzior, M., Bernaciak, J., Ziemkiewicz, K., Gambin, T., Sykulski, M., Bezniakow, N., et al. Application of array comparative genomic hybridization in 256 patients with developmental delay or intellectual disability. J. Appl. Genet. 55 (2014), 125–144.
57. 57 Vergult, S., Dauber, A., Delle Chiaie, B., Van Oudenhove, E., Simon, M., Rihani, A., Loeys, B., Hirschhorn, J., Pfotenhauer, J., Phillips, J.A. 3rd, et al. 17q24.2 microdeletions: a new syndromal entity with intellectual disability, truncal obesity, mood swings and hallucinations. Eur. J. Hum. Genet. 20 (2012), 534–539.
58. 58 Cooper, E.M., Cutcliffe, C., Kristiansen, T.Z., Pandey, A., Pickart, C.M., Cohen, R.E., K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-associated Brcc36 and proteasomal Poh1. EMBO J. 28 (2009), 621–631.
59. 59 Notwell, J.H., Heavner, W.E., Darbandi, S.F., Katzman, S., McKenna, W.L., Ortiz-Londono, C.F., Tastad, D., Eckler, M.J., Rubenstein, J.L., McConnell, S.K., et al. TBR1 regulates autism risk genes in the developing neocortex. Genome Res. 26 (2016), 1013–1022.
60. 60 Burrage, L.C., Eble, T.N., Hixson, P.M., Roney, E.K., Cheung, S.W., Franco, L.M., A mosaic 2q24.2 deletion narrows the critical region to a 0.4 Mb interval that includes TBR1, TANK, and PSMD14. Am. J. Med. Genet. A. 161A (2013), 841–844.
61. 61 Blake, J., Riddell, A., Theiss, S., Gonzalez, A.P., Haase, B., Jauch, A., Janssen, J.W., Ibberson, D., Pavlinic, D., Moog, U., et al. Sequencing of a patient with balanced chromosome abnormalities and neurodevelopmental disease identifies disruption of multiple high risk loci by structural variation. PLoS ONE, 9, 2014, e90894.
62. 62 Verma, R., Aravind, L., Oania, R., McDonald, W.H., Yates, J.R. 3rd, Koonin, E.V., Deshaies, R.J., Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298 (2002), 611–615.
63. 63 de Ligt, J., Willemsen, M.H., van Bon, B.W., Kleefstra, T., Yntema, H.G., Kroes, T., Vulto-van Silfhout, A.T., Koolen, D.A., de Vries, P., Gilissen, C., et al. Diagnostic exome sequencing in persons with severe intellectual disability. N. Engl. J. Med. 367 (2012), 1921–1929.