Excessive UBE3A dosage impairs retinoic acid signaling and synaptic plasticity in autism spectrum disorders (original) (raw)

• Huguet G, Ey E, Bourgeron T . The genetic landscapes of autism spectrum disorders. Annu Rev Genomics Hum Genet 2013; 14:191–213.
  Article CAS Google Scholar
• Zoghbi HY, Bear MF . Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb Perspect Biol 2012; 4.
  Article Google Scholar
• Abrahams BS, Geschwind DH . Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 2008; 9:341–355.
  Article CAS Google Scholar
• Glessner JT, Wang K, Cai G, et al. Autism genome-wide copy number variation reveals ubiquitin and neuronal genes. Nature 2009; 459:569–573.
  Article CAS Google Scholar
• De Rubeis S, He X, Goldberg AP, et al. Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 2014; 515:209–215.
  Article CAS Google Scholar
• Iossifov I, O'Roak BJ, Sanders SJ, et al. The contribution of de novo coding mutations to autism spectrum disorder. Nature 2014; 515:216–221.
  Article CAS Google Scholar
• Sanders SJ, He X, Willsey AJ, et al. Insights into autism spectrum disorder genomic architecture and biology from 71 risk loci. Neuron 2015; 87:1215–1233.
  Article CAS Google Scholar
• Wang T, Guo H, Xiong B, et al. De novo genic mutations among a Chinese autism spectrum disorder cohort. Nat Commun 2016; 7:13316.
  Article CAS Google Scholar
• Doan RN, Bae BI, Cubelos B, et al. Mutations in human accelerated regions disrupt cognition and social behavior. Cell 2016; 167:341–354.
  Article CAS Google Scholar
• Toro R, Konyukh M, Delorme R, et al. Key role for gene dosage and synaptic homeostasis in autism spectrum disorders. Trends Genet 2010; 26:363–372.
  Article CAS Google Scholar
• Santini E, Klann E . Reciprocal signaling between translational control pathways and synaptic proteins in autism spectrum disorders. Sci Signal 2014; 7:re10.
  Article Google Scholar
• Schanen NC . Epigenetics of autism spectrum disorders. Hum Mol Genet 2006; 15:R138–R150.
  Article CAS Google Scholar
• Nurmi EL, Bradford Y, Chen Y, et al. Linkage disequilibrium at the Angelman syndrome gene UBE3A in autism families. Genomics 2001; 77:105–113.
  Article CAS Google Scholar
• Baron CA . Genomic and functional profiling of duplicated chromosome 15 cell lines reveal regulatory alterations in UBE3A-associated ubiquitin-proteasome pathway processes. Hum Mol Genet 2006; 15:853–869.
  Article CAS Google Scholar
• Noor A, Dupuis L, Mittal K, et al. 15q11.2 Duplication encompassing only the UBE3A gene is associated with developmental delay and neuropsychiatric phenotypes. Hum Mutat 2015; 36:689–693.
  Article CAS Google Scholar
• Smith SE, Zhou YD, Zhang G, et al. Increased gene dosage of Ube3a results in autism traits and decreased glutamate synaptic transmission in mice. Sci Transl Med 2011; 3:103ra197.
  Article Google Scholar
• Yi JJ, Berrios J, Newbern JM, et al. An autism-linked mutation disables phosphorylation control of UBE3A. Cell 2015; 162:795–807.
  Article CAS Google Scholar
• Grabbe C, Husnjak K, Dikic I . The spatial and temporal organization of ubiquitin networks. Nat Rev Mol Cell Biol 2011; 12:295–307.
  Article CAS Google Scholar
• Hershko A, Ciechanover A, Varshavsky A . Basic Medical Research Award. The ubiquitin system. Nat Med 2000; 6:1073–1081.
  Article CAS Google Scholar
• Kerscher O, Felberbaum R, Hochstrasser M . Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 2006; 22:159–180.
  Article CAS Google Scholar
• Komander D, Rape M . The ubiquitin code. Annu Rev Biochem 2012; 81:203–229.
  Article CAS Google Scholar
• Swatek KN, Komander D . Ubiquitin modifications. Cell Res 2016; 26:399–422.
  Article CAS Google Scholar
• Sell GL, Margolis SS . From UBE3A to Angelman syndrome: a substrate perspective. Front Neurosci 2015; 9:322.
  Article Google Scholar
• Kumar S, Duester G . SnapShot: retinoic acid signaling. Cell 2011; 147:1422.
  Article CAS Google Scholar
• Shearer KD, Stoney PN, Morgan PJ, McCaffery PJ . A vitamin for the brain. Trends Neurosci 2012; 35:733–741.
  Article CAS Google Scholar
• Rhinn M, Dolle P . Retinoic acid signalling during development. Development 2012; 139:843–858.
  Article CAS Google Scholar
• Cunningham TJ, Duester G . Mechanisms of retinoic acid signalling and its roles in organ and limb development. Nat Rev Mol Cell Biol 2015; 16:110–123.
  Article CAS Google Scholar
• Chen L, Lau AG, Sarti F . Synaptic retinoic acid signaling and homeostatic synaptic plasticity. Neuropharmacology 2014; 78:3–12.
  Article CAS Google Scholar
• Aoto J, Nam CI, Poon MM, Ting P, Chen L . Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 2008; 60:308–320.
  Article CAS Google Scholar
• Chen N, Napoli JL . All-trans-retinoic acid stimulates translation and induces spine formation in hippocampal neurons through a membrane-associated RARα. FASEB J 2008; 22:236–245.
  Article CAS Google Scholar
• Koppaka V, Thompson DC, Chen Y, et al. Aldehyde dehydrogenase inhibitors: a comprehensive review of the pharmacology, mechanism of action, substrate specificity, and clinical application. Pharmacol Rev 2012; 64:520–539.
  Article CAS Google Scholar
• Keren-Kaplan T, Attali I, Motamedchaboki K, et al. Synthetic biology approach to reconstituting the ubiquitylation cascade in bacteria. EMBO J 2012; 31:378–390.
  Article CAS Google Scholar
• Moreb JS, Zucali JR, Ostmark B, Benson NA . Heterogeneity of aldehyde dehydrogenase expression in lung cancer cell lines is revealed by Aldefluor flow cytometry-based assay. Cytometry B Clin Cytom 2007; 72:281–289.
  Article Google Scholar
• Jiang YH, Armstrong D, Albrecht U, et al. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 1998; 21:799–811.
  Article CAS Google Scholar
• Yamamoto Y, Huibregtse JM, Howley PM . The human _E6_-AP gene (UBE3A) encodes three potential protein isoforms generated by differential splicing. Genomics 1997; 41:263–266.
  Article CAS Google Scholar
• Kumar S, Talis AL, Howley PM . Identification of HHR23A as a substrate for E6-associated protein-mediated ubiquitination. J Biol Chem 1999; 274:18785–18792.
  Article CAS Google Scholar
• Louria-Hayon I, Alsheich-Bartok O, Levav-Cohen Y, et al. E6AP promotes the degradation of the PML tumor suppressor. Cell Death Differ 2009; 16:1156–1166.
  Article CAS Google Scholar
• Zaaroor-Regev D, de Bie P, Scheffner M, et al. Regulation of the polycomb protein Ring1B by self-ubiquitination or by E6-AP may have implications to the pathogenesis of Angelman syndrome. Proc Natl Acad Sci USA 2010; 107:6788–6793.
  Article CAS Google Scholar
• Li W, Yao A, Zhi H, et al. Angelman syndrome protein Ube3a regulates synaptic growth and endocytosis by inhibiting BMP signaling in Drosophila. PLoS Genet 2016; 12:e1006062.
  Article Google Scholar
• Huibregtse JM, Scheffner M, Howley PM . Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol Cell Biol 1993; 13:4918–4927.
  Article CAS Google Scholar
• Ansari T, Brimer N, Vande Pol SB . Peptide interactions stabilize and restructure human papillomavirus type 16 E6 to interact with p53. J Virol 2012; 86:11386–11391.
  Article CAS Google Scholar
• Moretti A, Li J, Donini S, et al. Crystal structure of human aldehyde dehydrogenase 1A3 complexed with NAD+ and retinoic acid. Sci Rep 2016; 6:35710.
  Article CAS Google Scholar
• Storms RW, Trujillo AP, Springer JB, et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci USA 1999; 96:9118–9123.
  Article CAS Google Scholar
• Han EB, Stevens CF . Development regulates a switch between post- and presynaptic strengthening in response to activity deprivation. Proc Natl Acad Sci USA 2009; 106:10817–10822.
  Article CAS Google Scholar
• Bicks LK, Koike H, Akbarian S, Morishita H . Prefrontal cortex and social cognition in mouse and man. Front Psychol 2015; 6:1805.
  Article Google Scholar
• Barak B, Feng G . Neurobiology of social behavior abnormalities in autism and Williams syndrome. Nat Neurosci 2016; 19:647–655.
  Article CAS Google Scholar
• Chow ML, Pramparo T, Winn ME, et al. Age-dependent brain gene expression and copy number anomalies in autism suggest distinct pathological processes at young versus mature ages. PLoS Genet 2012; 8:e1002592.
  Article CAS Google Scholar
• Stoner R, Chow ML, Boyle MP, et al. Patches of disorganization in the neocortex of children with autism. N Engl J Med 2014; 370:1209–1219.
  Article CAS Google Scholar
• Duffney LJ, Zhong P, Wei J, et al. Autism-like deficits in _Shank3_-deficient mice are rescued by targeting actin regulators. Cell Rep 2015; 11:1400–1413.
  Article CAS Google Scholar
• Lein ES, Hawrylycz MJ, Ao N, et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007; 445:168–176.
  Article CAS Google Scholar
• Kane MA, Napoli JL . Quantification of endogenous retinoids. Methods Mol Biol 2010; 652:1–54.
  Article CAS Google Scholar
• Evans JE, McCaffery P . HPLC/MS(N) analysis of retinoids. Methods Mol Biol 2010; 652:149–162.
  Article CAS Google Scholar
• Ramocki MB, Peters SU, Tavyev YJ, et al. Autism and other neuropsychiatric symptoms are prevalent in individuals with MeCP2 duplication syndrome. Ann Neurol 2009; 66:771–782.
  Article CAS Google Scholar
• Durand CM, Betancur C, Boeckers TM, et al. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat Genet 2007; 39:25–27.
  Article CAS Google Scholar
• Zweier C, de Jong EK, Zweier M, et al. CNTNAP2 and NRXN1 are mutated in autosomal-recessive Pitt-Hopkins-like mental retardation and determine the level of a common synaptic protein in Drosophila. Am J Hum Genet 2009; 85:655–666.
  Article CAS Google Scholar
• Ramocki MB, Zoghbi HY . Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 2008; 455:912–918.
  Article CAS Google Scholar
• Misner DL, Jacobs S, Shimizu Y, et al. Vitamin A deprivation results in reversible loss of hippocampal long-term synaptic plasticity. Proc Natl Acad Sci USA 2001; 98:11714–11719.
  Article CAS Google Scholar
• Sarti F, Schroeder J, Aoto J, Chen L . Conditional RARα knockout mice reveal acute requirement for retinoic acid and RARα in homeostatic plasticity. Front Mol Neurosci 2012; 5:16.
  Article CAS Google Scholar
• Wan C, Shi Y, Zhao X, et al. Positive association between ALDH1A2 and schizophrenia in the Chinese population. Prog Neuropsychopharmacol Biol Psychiatry 2009; 33:1491–1495.
  Article CAS Google Scholar
• Galter D, Buervenich S, Carmine A, Anvret M, Olson L . ALDH1 mRNA: presence in human dopamine neurons and decreases in substantia nigra in Parkinson's disease and in the ventral tegmental area in schizophrenia. Neurobiol Dis 2003; 14:637–647.
  Article CAS Google Scholar
• Fares-Taie L, Gerber S, Chassaing N, et al. ALDH1A3 mutations cause recessive anophthalmia and microphthalmia. Am J Hum Genet 2013; 92:265–270.
  Article CAS Google Scholar
• Ramamoorthy S, Nawaz Z . E6-associated protein (E6-AP) is a dual function coactivator of steroid hormone receptors. Nucl Recept Signal 2008; 6:e006.
  Article Google Scholar
• Krishnan V, Stoppel DC, Nong Y, et al. Autism gene Ube3a and seizures impair sociability by repressing VTA Cbln1. Nature 2017; 543:507–512.
  Article CAS Google Scholar
• Sztainberg Y, Zoghbi HY . Lessons learned from studying syndromic autism spectrum disorders. Nat Neurosci 2016; 19:1408–1417.
  Article CAS Google Scholar
• Delorme R, Ey E, Toro R, et al. Progress toward treatments for synaptic defects in autism. Nat Med 2013; 19:685–694.
  Article CAS Google Scholar
• Xia K, Guo H, Hu Z, et al. Common genetic variants on 1p13.2 associate with risk of autism. Mol Psychiatry 2013; 19:1212–1219.
  Article Google Scholar
• Nava C, Keren B, Mignot C, et al. Prospective diagnostic analysis of copy number variants using SNP microarrays in individuals with autism spectrum disorders. Eur J Hum Genet 2013; 22:71–78.
  Article Google Scholar
• Benn P, Delach J . Human lymphocyte culture and chromosome analysis. CSH Protoc 2008; 2008:pdbprot5035.
  Google Scholar
• Xu X, Tao Y, Gao X, et al. A CRISPR-based approach for targeted DNA demethylation. Cell Discov 2016; 2:16009.
  Article CAS Google Scholar
• Anderson MA, Gusella JF . Use of cyclosporin A in establishing Epstein-Barr virus-transformed human lymphoblastoid cell lines. In Vitro 1984; 20:856–858.
  Article CAS Google Scholar
• Xu J . Preparation, culture, and immortalization of mouse embryonic fibroblasts. Curr Protoc Mol Biol 2005; Chapter 28:Unit 28.1.
  PubMed Google Scholar
• Hsu PD, Scott DA, Weinstein JA, et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 2013; 31:827–832.
  Article CAS Google Scholar
• Liu H, Naismith JH . An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol 2008; 8:91.
  Article Google Scholar
• Liu Z, Chen P, Gao H, et al. Ubiquitylation of autophagy receptor Optineurin by HACE1 activates selective autophagy for tumor suppression. Cancer Cell 2014; 26:106–120.
  Article Google Scholar
• Sztainberg Y, Chen H-m, Swann JW, et al. Reversal of phenotypes in MECP2 duplication mice using genetic rescue or antisense oligonucleotides. Nature 2015; 528:123–126.
  Article CAS Google Scholar