An EJC factor RBM8a regulates anxiety behaviors

Current Molecular Medicine

Volumn 13, Issue 6, 2013, Pages 887-899

  Alachkar, A ^a,b   Jiang, D ^a   Harrison, M ^a   Zhou, Y ^a   Chen, G ^a   Mao, Y ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adult neurogenesis; Anxiety; EJC; NMD; RBM8a

Indexed keywords

AMPA RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; COMPLEMENTARY DNA; DOUBLECORTIN; EARLY GROWTH RESPONSE FACTOR 1; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; RNA BINDING PROTEIN; RNA BINDING PROTEIN 8A; TAU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPHYSIOLOGY; ELEVATED PLUS MAZE TEST; EXCITATORY POSTSYNAPTIC POTENTIAL; FORCED SWIMMING TEST; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; OPEN FIELD TEST; POLYMERASE CHAIN REACTION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SOCIAL BEHAVIOR; SOCIAL INTERACTION;

EID: 84881357098     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/15665240113139990019     Document Type: Article

References (85)

1. Mendell JT, Sharifi NA, Meyers JL, et al. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat Genet 2004; 36: 1073-1078.
2. Laumonnier F, Shoubridge C, Antar C, et al. Mutations of the UPF3B gene, which encodes a protein widely expressed in neurons, are associated with nonspecific mental retardation with or without autism. Mol Psychiatry 2010; 15: 767-776.
3. Lynch SA, Nguyen LS, Ng LY, et al. Broadening the phenotype associated with mutations in UPF3B: two further cases with renal dysplasia and variable developmental delay. Eur J Med Genet 2012; 55: 476-479.
4. Haldeman-Englert C, Jewett T. 1q21.1 Microdeletion. In: Pagon RA, Bird TD, Dolan CR, Stephens K, Adam MP, editors. GeneReviews™ [Internet]. Seattle (WA): University of Washington, Seattle; 1993.
5. Stefansson H, Rujescu D, Cichon S, et al. Large recurrent microdeletions associated with schizophrenia. Nature 2008; 455: 232-236.
6. Brunetti-Pierri N, Berg JS, Scaglia F, et al. Recurrent reciprocal 1q21.1 deletions and duplications associated with microcephaly or macrocephaly and developmental and behavioral abnormalities. Nat Genet 2008; 40: 1466-1471.
7. Nguyen LS, Kim HG, Rosenfeld JA, et al. Contribution of copy number variants involving nonsense-mediated mRNA decay pathway genes to neuro-developmental disorders. Hum Mol Genet 2013; 22: 1816-1825.
8. Hall GW, Thein S. Nonsense codon mutations in the terminal exon of the beta-globin gene are not associated with a reduction in beta-mRNA accumulation: a mechanism for the phenotype of dominant beta-thalassemia. Blood 1994; 83: 2031-2037.
9. Kerr TP, Sewry CA, Robb SA, Roberts RG. Long mutant dystrophins and variable phenotypes: evasion of nonsense-mediated decay? Hum Genet 2001; 109: 402-407.
10. Tange TO, Nott A, Moore MJ. The ever-increasing complexities of the exon junction complex. Curr Opin Cell Biol 2004; 16: 279-284.
11. Chamieh H, Ballut L, Bonneau F, Le Hir H. NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat Struct Mol Biol 2008; 15: 85-93.
12. Le Hir H, Gatfield D, Izaurralde E, Moore MJ. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J 2001; 20: 4987-4997.
13. Czaplinski K, Ruiz-Echevarria MJ, Paushkin SV, et al. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev 1998; 12: 1665-1677.
14. Kashima I, Yamashita A, Izumi N, et al. Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. Genes Dev 2006; 20: 355-367.
15. Eberle AB, Lykke-Andersen S, Muhlemann O, Jensen TH. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 2009; 16: 49-55.
16. Huntzinger E, Kashima I, Fauser M, et al. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 2008; 14: 2609-2617.
17. Kim VN, Dreyfuss G. Nuclear mRNA binding proteins couple pre-mRNA splicing and post-splicing events. Mol Cells 2001; 12: 1-10.
18. Salicioni AM, Xi M, Vanderveer LA, et al. Identification and structural analysis of human RBM8a and RBM8B: two highly conserved RNA-binding motif proteins that interact with OVCA1, a candidate tumor suppressor. Genomics 2000; 69: 54-62.
19. Isken O, Maquat LE. The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat Rev Genet 2008; 9: 699-712.
20. Chang YF, Imam JS, Wilkinson MF. The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 2007; 76: 51-74.
21. Le Hir H, Izaurralde E, Maquat LE, Moore MJ. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J 2000; 19: 6860-6869.
22. Chuang TW, Peng PJ, Tarn WY. The exon junction complex component Y14 modulates the activity of the methylosome in biogenesis of spliceosomal small nuclear ribonucleoproteins. J Biol Chem 2011; 286: 8722-8728.
23. Dostie J, Dreyfuss G. Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr Biol 2002; 12: 1060-1067.
24. Hachet O, Ephrussi A. Drosophila Y14 shuttles to the posterior of the oocyte and is required for oskar mRNA transport. Curr Biol 2001; 11: 1666-1674.
25. Hachet O, Ephrussi A. Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 2004; 428: 959-963.
26. Michelle L, Cloutier A, Toutant J, et al. Proteins associated with the exon junction complex also control the alternative splicing of apoptotic regulators. Mol Cell Biol 2012; 32: 954-967.
27. Sudo H, Tsuji AB, Sugyo A, et al. Knockdown of COPA, identified by loss-of-function screen, induces apoptosis and suppresses tumor growth in mesothelioma mouse model. Genomics 2010; 95: 210-216.
28. Ohbayashi N, Taira N, Kawakami S, et al. An RNA biding protein, Y14 interacts with and modulates STAT3 activation. Biochem Biophys Res Commun 2008; 372: 475-479.
29. Masse I, Molin L, Mouchiroud L, et al. A novel role for the SMG-1 kinase in lifespan and oxidative stress resistance in Caenorhabditis elegans. PLoS One 2008; 3: e3354.
30. Lew JE, Enomoto S, Berman J. Telomere length regulation and telomeric chromatin require the nonsense-mediated mRNA decay pathway. Mol Cell Biol 1998; 18: 6121-6130.
31. Brumbaugh KM, Otterness DM, Geisen C, et al. The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol Cell 2004; 14: 585-598.
32. Gehen SC, Staversky RJ, Bambara RA, et al. hSMG-1 and ATM sequentially and independently regulate the G1 checkpoint during oxidative stress. Oncogene 2008; 27: 4065-4074.
33. Ma XM, Yoon SO, Richardson CJ, et al. SKAR links pre-mRNA splicing to mTOR/S6K1-mediated enhanced translation efficiency of spliced mRNAs. Cell 2008; 133: 303-313.
34. Isken O, Kim YK, Hosoda N, et al. Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 2008; 133: 314-327.
35. Ashton-Beaucage D, Udell CM, Lavoie H, et al. The exon junction complex controls the splicing of MAPK and other long intron-containing transcripts in Drosophila. Cell 2010; 143: 251-262.
36. Roignant JY, Treisman JE. Exon junction complex subunits are required to splice Drosophila MAP kinase, a large heterochromatic gene. Cell 2010; 143: 238-250.
37. Wittkopp N, Huntzinger E, Weiler C, et al. Nonsense-mediated mRNA decay effectors are essential for zebrafish embryonic development and survival. Mol Cell Biol 2009; 29: 3517-3528.
38. Silver DL, Watkins-Chow DE, Schreck KC, et al. The exon junction complex component Magoh controls brain size by regulating neural stem cell division. Nat Neurosci 2010; 13: 551-558.
39. Giorgi C, Yeo GW, Stone ME, et al. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 2007; 130: 179-191.
40. Long AA, Mahapatra CT, Woodruff EA, et al. The nonsense-mediated decay pathway maintains synapse architecture and synaptic vesicle cycle efficacy. J Cell Sci 2010; 123: 3303-3315.
41. Gehring NH, Neu-Yilik G, Schell T, et al. Y14 and hUpf3b form an NMD-activating complex. Mol Cell 2003; 11: 939-949.
42. Tarpey PS, Raymond FL, Nguyen LS, et al. Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat Genet 2007; 39: 1127-1133.
43. Xu X, Zhang L, Tong P, et al. Exome sequencing identifies UPF3B as the causative gene for a Chinese non-syndrome mental retardation pedigree. Clin Genet 2013; 83: 560-564.
44. Nguyen LS, Jolly L, Shoubridge C, et al. Transcriptome profiling of UPF3B/NMD-deficient lymphoblastoid cells from patients with various forms of intellectual disability. Mol Psychiatry 2012; 17: 1103-1115.
45. Chan WK, Bhalla AD, Le Hir H, et al. A UPF3-mediated regulatory switch that maintains RNA surveillance. Nat Struct Mol Biol 2009; 16: 747-753.
46. Addington AM, Gauthier J, Piton A, et al. A novel frameshift mutation in UPF3B identified in brothers affected with childhood onset schizophrenia and autism spectrum disorders. Mol Psychiatry 2011; 16: 238-239.
47. Szyszka P, Sharp SI, Dedman A, et al. A nonconservative amino acid change in the UPF3B gene in a patient with schizophrenia. Psychiatr Genet 2012; 22: 150-151.
48. Albers CA, Paul DS, Schulze H, et al. Compound inheritance of a low-frequency regulatory SNP and a rare null mutation in exon-junction complex subunit RBM8a causes TAR syndrome. Nat Genet 2012; 44: 435-439, S1-S2.
49. Skorka A, Bielicka-Cymermann J, Gieruszczak-Bialek D, Korniszewski L. Thrombocytopenia-absent radius (tar) syndrome: a case with agenesis of corpus callosum, hypoplasia of cerebellar vermis and horseshoe kidney. Genet Couns 2005; 16: 377-382.
50. Degot S, Le Hir H, Alpy F, et al. Association of the breast cancer protein MLN51 with the exon junction complex via its speckle localizer and RNA binding module. J Biol Chem 2004; 279: 33702-33715.
51. Huang J, Xiong Y, Deng C, et al. Cloning, sequence analysis and identification of a nonsense mutation-mediated mRNA decay of porcine GSTM2 gene. Acta Biochim Biophys Sin (Shanghai) 2007; 39: 560-566.
52. Liu Q, Jiang L, Liu WL, et al. Two novel mutations and evidence for haploinsufficiency of the ADAR gene in dyschromatosis symmetrica hereditaria. Br J Dermatol 2006; 154: 636-642.
53. Mao Y, Lee AW. A novel role for Gab2 in bFGF-mediated cell survival during retinoic acid-induced neuronal differentiation. J Cell Biol 2005; 170: 305-316.
54. Mao Y, Ge X, Frank CL, et al. Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 2009; 136: 1017-1031.
55. Lee FH, Kaidanovich-Beilin O, Roder JC, et al. Genetic inactivation of GSK3alpha rescues spine deficits in Disc1-L100P mutant mice. Schizophr Res 2011; 129: 74-9.
56. Porsolt RD, Le Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977; 266: 730-732.
57. Bourin M, Redrobe JP, Hascoet M, et al. A schematic representation of the psychopharmacological profile of antidepressants. Prog Neuropsychopharmacol Biol Psychiatry 1996; 20: 1389-1402.
58. Wall PM, Messier C. Concurrent modulation of anxiety and memory. Behav Brain Res 2000; 109: 229-241.
59. Santos P, Bittencourt AS, Schenberg LC, Carobrez AP. Elevated T-maze evaluation of anxiety and memory effects of NMDA/glycine-B site ligands injected into the dorsal periaqueductal gray matter and the superior colliculus of rats. Neuropharmacology 2006; 51: 203-212.
60. Sun J, Sun J, Ming GL, Song H. Epigenetic regulation of neurogenesis in the adult mammalian brain. Eur J Neurosci 2011; 33: 1087-1093.
61. Keene JD, Komisarow JM, Friedersdorf MB. RIP-Chip: the isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts. Nat Protoc 2006; 1: 302-307.
62. Kim VN, Yong J, Kataoka N, et al. The Y14 protein communicates to the cytoplasm the position of exon-exon junctions. EMBO J 2001; 20: 2062-2068.
63. Glanzer J, Miyashiro KY, Sul JY, et al. RNA splicing capability of live neuronal dendrites. Proc Natl Acad Sci USA 2005; 102: 16859-16864.
64. Mefford HC, Sharp AJ, Baker C, et al. Recurrent rearrangements of chromosome 1q21.1 and variable pediatric phenotypes. N Engl J Med 2008; 359: 1685-1699.
65. Samuels BA, Hen R. Neurogenesis and affective disorders. Eur J Neurosci 2011; 33: 1152-1159.
66. Ferraiuolo MA, Lee CS, Ler LW, et al. A nuclear translationlike factor eIF4AIII is recruited to the mRNA during splicing and functions in nonsense-mediated decay. Proc Natl Acad Sci USA 2004; 101: 4118-4123.
67. Pellow S, Chopin P, File SE, Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985; 14: 149-167.
68. Nomura S, Shimizu J, Kinjo M, et al. A new behavioral test for antidepressant drugs. Eur J Pharmacol 1982; 83: 171-175.
69. Silverman JL, Yang M, Lord C, Crawley JN. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 2010; 11: 490-502.
70. Kim KS, Lee HJ, Jeong HS, et al. Self-renewal induced efficiently, safely, and effective therapeutically with one regulatable gene in a human somatic progenitor cell. Proc Natl Acad Sci USA 2011; 108: 4876-4881.
71. Santarelli L, Saxe M, Gross C, et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301: 805-809.
72. Chan WK, Huang L, Gudikote JP, et al. An alternative branch of the nonsense-mediated decay pathway. EMBO J 2007; 26: 1820-1830.
73. Sullivan PF, Daly MJ, O'Donovan M. Genetic architectures of psychiatric disorders: the emerging picture and its implications. Nat Rev Genet 2012; 13: 537-551.
74. Malhotra D, Sebat J. CNVs: harbingers of a rare variant revolution in psychiatric genetics. Cell 2012; 148: 1223-1241.
75. Kang JQ, Shen W, Macdonald RL. Two molecular pathways (NMD and ERAD) contribute to a genetic epilepsy associated with the GABA(A) receptor GABRA1 PTC mutation, 975delC, S326fs328X. J Neurosci 2009; 29: 2833-2844.
76. Sala R, Axelson DA, Castro-Fornieles J, et al. Comorbid anxiety in children and adolescents with bipolar spectrum disorders: prevalence and clinical correlates. J Clin Psychiatry 2010; 71: 1344-1350.
77. Lysaker PH, Yanos PT, Outcalt J, Roe D. Association of stigma, self-esteem, and symptoms with concurrent and prospective assessment of social anxiety in schizophrenia. Clin Schizophr Relat Psychoses 2010; 4: 41-48.
78. McLean WH, Irvine AD, Hamill KJ, et al. An unusual N-terminal deletion of the laminin alpha3a isoform leads to the chronic granulation tissue disorder laryngo-onycho-cutaneous syndrome. Hum Mol Genet 2003; 12: 2395-2409.
79. Flaisher-Grinberg S, Einat H. A possible utilization of the mice forced swim test for modeling manic-like increase in vigor and goal-directed behavior. J Pharmacol Toxicol Methods 2009; 59: 141-145.
80. Bannerman DM, Deacon RM, Brady S, et al. A comparison of GluR-A-deficient and wild-type mice on a test battery assessing sensorimotor, affective, and cognitive behaviors. Behav Neurosci 2004; 118: 643-647.
81. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005; 28: 223-250.
82. Luo Y, Shan G, Guo W, et al. Fragile x mental retardation protein regulates proliferation and differentiation of adult neural stem/progenitor cells. PLoS Genet 2010; 6: e1000898.
83. Duan X, Chang JH, Ge S, et al. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 2007; 130: 1146-1158.
84. Zhou M, Li W, Huang S, et al. mTOR Inhibition ameliorates cognitive and affective deficits caused by Disc1 knockdown in adult-born dentate granule neurons. Neuron 2013; 77: 647-654.
85. Koehl M, Abrous DN. A new chapter in the field of memory: adult hippocampal neurogenesis. Eur J Neurosci 2011; 33: 1101-1114.