An Autism-Linked Mutation Disables Phosphorylation Control of UBE3A

Cell

Volumn 162, Issue 4, 2015, Pages 795-807

  Yi, Jason J ^a   Berrios, Janet ^a   Newbern, Jason M ^b   Snider, William D ^a   Philpot, Benjamin D ^a   Hahn, Klaus M ^a   Zylka, Mark J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYCLIC AMP DEPENDENT PROTEIN KINASE; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3A; UNCLASSIFIED DRUG; UBE3A PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN CELL CULTURE; BRAIN DEVELOPMENT; CLUSTER ANALYSIS; CONTROLLED STUDY; DENDRITIC SPINE; DEVELOPMENT; EMBRYO; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; GENE DELETION; GENETIC CODE; HAPPY PUPPET SYNDROME; HUMAN; HUMAN CELL; IN VITRO STUDY; MISSENSE MUTATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; UBIQUITINATION; ANIMAL; BRAIN; C57BL MOUSE; CHEMISTRY; ENZYME STABILITY; GENETICS; MAMMALIAN EMBRYO; METABOLISM; MUTAGENESIS; PATHOLOGY; PHOSPHORYLATION;

ANGELMAN SYNDROME; ANIMALS; AUTISTIC DISORDER; BRAIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DENDRITIC SPINES; EMBRYO, MAMMALIAN; ENZYME STABILITY; FEMALE; HUMANS; MICE, INBRED C57BL; MUTAGENESIS; MUTATION, MISSENSE; PHOSPHORYLATION; UBIQUITIN-PROTEIN LIGASES;

EID: 84939220718     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.06.045     Document Type: Article

References (44)

1. U. Albrecht, J.S. Sutcliffe, B.M. Cattanach, C.V. Beechey, D. Armstrong, G. Eichele, and A.L. Beaudet Imprinted expression of the murine Angelman syndrome gene, Ube3a, in hippocampal and Purkinje neurons Nat. Genet. 17 1997 75 78
2. C. Camprubí, M. Guitart, E. Gabau, M.D. Coll, S. Villatoro, S. Oltra, M. Roselló, I. Ferrer, S. Monfort, C. Orellana, and F. Martínez Novel UBE3A mutations causing Angelman syndrome: different parental origin for single nucleotide changes and multiple nucleotide deletions or insertions Am. J. Med. Genet. A. 149A 2009 343 348
3. J.A. Chen, O. Peñagarikano, T.G. Belgard, V. Swarup, and D.H. Geschwind The emerging picture of autism spectrum disorder: genetics and pathology Annu. Rev. Pathol. 10 2015 111 144
4. P. Cohen Immune diseases caused by mutations in kinases and components of the ubiquitin system Nat. Immunol. 15 2014 521 529
5. E.M. Cooper, A.W. Hudson, J. Amos, J. Wagstaff, and P.M. Howley Biochemical analysis of Angelman syndrome-associated mutations in the E3 ubiquitin ligase E6-associated protein J. Biol. Chem. 279 2004 41208 41217
6. P. de Bie, and A. Ciechanover Ubiquitination of E3 ligases: self-regulation of the ubiquitin system via proteolytic and non-proteolytic mechanisms Cell Death Differ. 18 2011 1393 1402
7. S. De Rubeis, X. He, A.P. Goldberg, C.S. Poultney, K. Samocha, A.E. Cicek, Y. Kou, L. Liu, M. Fromer, S. Walker, et al. DDD Study Homozygosity Mapping Collaborative for Autism UK10K Consortium Synaptic, transcriptional and chromatin genes disrupted in autism Nature 515 2014 209 215
8. N.D. Germain, P.F. Chen, A.M. Plocik, H. Glatt-Deeley, J. Brown, J.J. Fink, K.A. Bolduc, T.M. Robinson, E.S. Levine, L.T. Reiter, and et al. Gene expression analysis of human induced pluripotent stem cell-derived neurons carrying copy number variants of chromosome 15q11-q13.1 Mol. Autism 5 2014 44
9. J.T. Glessner, K. Wang, G. Cai, O. Korvatska, C.E. Kim, S. Wood, H. Zhang, A. Estes, C.W. Brune, J.P. Bradfield, and et al. Autism genome-wide copy number variation reveals ubiquitin and neuronal genes Nature 459 2009 569 573
10. P.L. Greer, R. Hanayama, B.L. Bloodgood, A.R. Mardinly, D.M. Lipton, S.W. Flavell, T.K. Kim, E.C. Griffith, Z. Waldon, R. Maehr, and et al. The Angelman Syndrome protein Ube3A regulates synapse development by ubiquitinating arc Cell 140 2010 704 716
11. A. Hogart, D. Wu, J.M. LaSalle, and N.C. Schanen The comorbidity of autism with the genomic disorders of chromosome 15q11.2-q13 Neurobiol. Dis. 38 2010 181 191
12. H.S. Huang, J.A. Allen, A.M. Mabb, I.F. King, J. Miriyala, B. Taylor-Blake, N. Sciaky, J.W. Dutton Jr., H.M. Lee, X. Chen, and et al. Topoisomerase inhibitors unsilence the dormant allele of Ube3a in neurons Nature 481 2012 185 189
13. J.M. Huibregtse, M. Scheffner, and P.M. Howley Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins Mol. Cell. Biol. 13 1993 4918 4927
14. J.J. Hutsler, and H. Zhang Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders Brain Res. 1309 2010 83 94
15. 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
16. A.D. Jacobson, A. MacFadden, Z. Wu, J. Peng, and C.W. Liu Autoregulation of the 26S proteasome by in situ ubiquitination Mol. Biol. Cell 25 2014 1824 1835
17. Y.H. Jiang, D. Armstrong, U. Albrecht, C.M. Atkins, J.L. Noebels, G. Eichele, J.D. Sweatt, and A.L. Beaudet Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation Neuron 21 1998 799 811
18. T. Kishino, M. Lalande, and J. Wagstaff UBE3A/E6-AP mutations cause Angelman syndrome Nat. Genet. 15 1997 70 73
19. H.S. Ko, Y. Lee, J.H. Shin, S.S. Karuppagounder, B.S. Gadad, A.J. Koleske, O. Pletnikova, J.C. Troncoso, V.L. Dawson, and T.M. Dawson Phosphorylation by the c-Abl protein tyrosine kinase inhibits parkin's ubiquitination and protective function Proc. Natl. Acad. Sci. USA 107 2010 16691 16696
20. S. Kumar, A.L. Talis, and P.M. Howley Identification of HHR23A as a substrate for E6-associated protein-mediated ubiquitination J. Biol. Chem. 274 1999 18785 18792
21. A. Lemak, A. Yee, I. Bezsonova, S. Dhe-Paganon, and C.H. Arrowsmith Zn-binding AZUL domain of human ubiquitin protein ligase Ube3A J. Biomol. NMR 51 2011 185 190
22. Y. Lu, M. Allen, A.R. Halt, M. Weisenhaus, R.F. Dallapiazza, D.D. Hall, Y.M. Usachev, G.S. McKnight, and J.W. Hell Age-dependent requirement of AKAP150-anchored PKA and GluR2-lacking AMPA receptors in LTP EMBO J. 26 2007 4879 4890
23. Y. Lu, X.M. Zha, E.Y. Kim, S. Schachtele, M.E. Dailey, D.D. Hall, S. Strack, S.H. Green, D.A. Hoffman, and J.W. Hell A kinase anchor protein 150 (AKAP150)-associated protein kinase A limits dendritic spine density J. Biol. Chem. 286 2011 26496 26506
24. A.M. Mabb, M.C. Judson, M.J. Zylka, and B.D. Philpot Angelman syndrome: insights into genomic imprinting and neurodevelopmental phenotypes Trends Neurosci. 34 2011 293 303
25. P. Malzac, H. Webber, A. Moncla, J.M. Graham, M. Kukolich, C. Williams, R.A. Pagon, L.A. Ramsdell, T. Kishino, and J. Wagstaff Mutation analysis of UBE3A in Angelman syndrome patients Am. J. Hum. Genet. 62 1998 1353 1360
26. S.S. Margolis, J. Salogiannis, D.M. Lipton, C. Mandel-Brehm, Z.P. Wills, A.R. Mardinly, L. Hu, P.L. Greer, J.B. Bikoff, H.Y. Ho, and et al. EphB-mediated degradation of the RhoA GEF Ephexin5 relieves a developmental brake on excitatory synapse formation Cell 143 2010 442 455
27. A. Noor, L. Dupuis, K. Mittal, A.C. Lionel, C.R. Marshall, S.W. Scherer, T. Stockley, J.B. Vincent, R. Mendoza-Londono, and D.J. Stavropoulos 15q11.2 Duplication Encompassing Only the UBE3A Gene Is Associated with Developmental Delay and Neuropsychiatric Phenotypes Hum. Mutat. 36 2015 689 693
28. U. Nuber, S.E. Schwarz, and M. Scheffner The ubiquitin-protein ligase E6-associated protein (E6-AP) serves as its own substrate Eur. J. Biochem. 254 1998 643 649
29. R.K. Pandya, J.R. Partridge, K.R. Love, T.U. Schwartz, and H.L. Ploegh A structural element within the HUWE1 HECT domain modulates self-ubiquitination and substrate ubiquitination activities J. Biol. Chem. 285 2010 5664 5673
30. C. Piochon, A.D. Kloth, G. Grasselli, H.K. Titley, H. Nakayama, K. Hashimoto, V. Wan, D.H. Simmons, T. Eissa, J. Nakatani, and et al. Cerebellar plasticity and motor learning deficits in a copy-number variation mouse model of autism Nat. Commun. 5 2014 5586
31. P. Pisani, D.M. Parkin, F. Bray, and J. Ferlay Estimates of the worldwide mortality from 25 cancers in 1990 Int. J. Cancer 83 1999 18 29
32. V.P. Ronchi, J.M. Klein, D.J. Edwards, and A.L. Haas The active form of E6-associated protein (E6AP)/UBE3A ubiquitin ligase is an oligomer J. Biol. Chem. 289 2014 1033 1048
33. C. Rougeulle, H. Glatt, and M. Lalande The Angelman syndrome candidate gene, UBE3A/E6-AP, is imprinted in brain Nat. Genet. 17 1997 14 15
34. B. Sadikovic, P. Fernandes, V.W. Zhang, P.A. Ward, I. Miloslavskaya, W. Rhead, R. Rosenbaum, R. Gin, B. Roa, and P. Fang Mutation Update for UBE3A variants in Angelman syndrome Hum. Mutat. 35 2014 1407 1417
35. M. Sato, and M.P. Stryker Genomic imprinting of experience-dependent cortical plasticity by the ubiquitin ligase gene Ube3a Proc. Natl. Acad. Sci. USA 107 2010 5611 5616
36. Z. Songyang, S. Blechner, N. Hoagland, M.F. Hoekstra, H. Piwnica-Worms, and L.C. Cantley Use of an oriented peptide library to determine the optimal substrates of protein kinases Curr. Biol. 4 1994 973 982
37. A.I. Su, T. Wiltshire, S. Batalov, H. Lapp, K.A. Ching, D. Block, J. Zhang, R. Soden, M. Hayakawa, G. Kreiman, and et al. A gene atlas of the mouse and human protein-encoding transcriptomes Proc. Natl. Acad. Sci. USA 101 2004 6062 6067
38. G. Tang, K. Gudsnuk, S.H. Kuo, M.L. Cotrina, G. Rosoklija, A. Sosunov, M.S. Sonders, E. Kanter, C. Castagna, A. Yamamoto, and et al. Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits Neuron 83 2014 1131 1143
39. N. Urraca, J. Cleary, V. Brewer, E.K. Pivnick, K. McVicar, R.L. Thibert, N.C. Schanen, C. Esmer, D. Lamport, and L.T. Reiter The interstitial duplication 15q11.2-q13 syndrome includes autism, mild facial anomalies and a characteristic EEG signature Autism Res. 6 2013 268 279
40. T.H. Vu, and A.R. Hoffman Imprinting of the Angelman syndrome gene, UBE3A, is restricted to brain Nat. Genet. 17 1997 12 13
41. J.M. Walboomers, M.V. Jacobs, M.M. Manos, F.X. Bosch, J.A. Kummer, K.V. Shah, P.J. Snijders, J. Peto, C.J. Meijer, and N. Muñoz Human papillomavirus is a necessary cause of invasive cervical cancer worldwide J. Pathol. 189 1999 12 19
42. M.L. Wallace, A.C. Burette, R.J. Weinberg, and B.D. Philpot Maternal loss of Ube3a produces an excitatory/inhibitory imbalance through neuron type-specific synaptic defects Neuron 74 2012 793 800
43. K. Yashiro, T.T. Riday, K.H. Condon, A.C. Roberts, D.R. Bernardo, R. Prakash, R.J. Weinberg, M.D. Ehlers, and B.D. Philpot Ube3a is required for experience-dependent maturation of the neocortex Nat. Neurosci. 12 2009 777 783
44. H. Yasuda, A.L. Barth, D. Stellwagen, and R.C. Malenka A developmental switch in the signaling cascades for LTP induction Nat. Neurosci. 6 2003 15 16