JAKMIP1, a Novel Regulator of Neuronal Translation, Modulates Synaptic Function and Autistic-like Behaviors in Mouse

Neuron

Volumn 88, Issue 6, 2015, Pages 1173-1191

  Berg, Jamee M ^a,b   Lee, Changhoon ^a   Chen, Leslie ^a   Galvan, Laurie ^a   Cepeda, Carlos ^a   Chen, Jane Y ^a   Peñagarikano, Olga ^a   Stein, Jason L ^a   Li, Alvin ^a   Oguro Ando, Asami ^a   Miller, Jeremy A ^a   Vashisht, Ajay A ^a   Starks, Mary E ^a   Kite, Elyse P ^a   Tam, Eric ^a   Gdalyahu, Amos ^a,b   Al Sharif, Noor B ^a   Burkett, Zachary D ^c   White, Stephanie A ^c   Fears, Scott C ^a   Levine, Michael S ^a   Wohlschlegel, James A ^a   Geschwind, Daniel H ^a,b   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX HELICASE 5; DEAD BOX PROTEIN; FRAGILE X MENTAL RETARDATION PROTEIN; JANUS KINASE AND MICROTUBULE INTERACTING PROTEIN 1; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POLY(A) BINDING PROTEIN CYTOPLASMIC 1; POLYADENYLIC ACID BINDING PROTEIN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; JAKMIP1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTISM; CONTROLLED STUDY; CORPUS STRIATUM; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MOUSE; NEOCORTEX; NONHUMAN; PERINATAL PERIOD; POLYSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEOMICS; RNA TRANSLATION; RNA TRANSPORT; SIGNAL TRANSDUCTION; SOCIAL DISABILITY; STEREOTYPY; SYNAPTOGENESIS; VOCALIZATION; ANIMAL; C57BL MOUSE; GENE REGULATORY NETWORK; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; PROCEDURES; PROTEIN SYNTHESIS; SYNAPSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTISM SPECTRUM DISORDER; GENE REGULATORY NETWORKS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PROTEIN BIOSYNTHESIS; PROTEOMICS; RNA-BINDING PROTEINS; SYNAPSES;

EID: 84949032593     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.10.031     Document Type: Article

References (73)

1. Abrahams B.S., Geschwind D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 2008, 9:341-355.
2. Berg J.M., Geschwind D.H. Autism genetics: searching for specificity and convergence. Genome Biol. 2012, 13:247.
3. Bodfish J. Repetitive Behaviors in Individuals with Autism Spectrum Disorders 2011, Oxford University Press.
4. Burkett Z.D., Day N.F., Peñagarikano O., Geschwind D.H., White S.A. VoICE: a semi-automated pipeline for standardizing vocal analysis across models. Sci. Rep. 2015, 5:10237.
5. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 2008, 28:264-278.
6. Couve A., Restituito S., Brandon J.M., Charles K.J., Bawagan H., Freeman K.B., Pangalos M.N., Calver A.R., Moss S.J. Marlin-1, a novel RNA-binding protein associates with GABA receptors. J. Biol. Chem. 2004, 279:13934-13943.
7. Crawley J.N., Paylor R. A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm. Behav. 1997, 31:197-211.
8. Darnell J.C., Van Driesche S.J., Zhang C., Hung K.Y., Mele A., Fraser C.E., Stone E.F., Chen C., Fak J.J., Chi S.W., et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 2011, 146:247-261.
9. De Rubeis S., Bagni C. Regulation of molecular pathways in the Fragile X Syndrome: insights into Autism Spectrum Disorders. J. Neurodev. Disord. 2011, 3:257-269.
10. De Rubeis S., He X., Goldberg A.P., Poultney C.S., Samocha K., Cicek A.E., Kou Y., Liu L., Fromer M., Walker S., et al. Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 2014, 515:209-215. DDD Study, Homozygosity Mapping Collaborative for AutismHomozygosity Mapping Collaborative for Autism, UK10K ConsortiumUK10K Consortium.
11. Deacon R.M. Assessing nest building in mice. Nat. Protoc. 2006, 1:1117-1119.
12. Deacon R.M. Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nat. Protoc. 2006, 1:122-124.
13. del Prete M.J., Vernal R., Dolznig H., Müllner E.W., Garcia-Sanz J.A. Isolation of polysome-bound mRNA from solid tissues amenable for RT-PCR and profiling experiments. RNA 2007, 13:414-421.
14. Dictenberg J.B., Swanger S.A., Antar L.N., Singer R.H., Bassell G.J. A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev. Cell 2008, 14:926-939.
15. Dieterich D.C., Hodas J.J., Gouzer G., Shadrin I.Y., Ngo J.T., Triller A., Tirrell D.A., Schuman E.M. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 2010, 13:897-905.
16. Diagnostic and Statistical Manual of Mental Disorders 2013, DSM-V, American Psychiatric Association. Fifth Edition.
17. Ebert D.H., Greenberg M.E. Activity-dependent neuronal signalling and autism spectrum disorder. Nature 2013, 493:327-337.
18. Ellegood J., Anagnostou E., Babineau B.A., Crawley J.N., Lin L., Genestine M., DiCicco-Bloom E., Lai J.K., Foster J.A., Peñagarikano O., et al. Clustering autism: using neuroanatomical differences in 26 mouse models to gain insight into the heterogeneity. Mol. Psychiatry 2015, 20:118-125.
19. Fernández E., Rajan N., Bagni C. The FMRP regulon: from targets to disease convergence. Front. Neurosci. 2013, 7:191.
20. Fogel B.L., Wexler E., Wahnich A., Friedrich T., Vijayendran C., Gao F., Parikshak N., Konopka G., Geschwind D.H. RBFOX1 regulates both splicing and transcriptional networks in human neuronal development. Hum. Mol. Genet. 2012, 21:4171-4186.
21. Gebauer F., Hentze M.W. Molecular mechanisms of translational control. Nat. Rev. Mol. Cell Biol. 2004, 5:827-835.
22. Gkogkas C.G., Khoutorsky A., Ran I., Rampakakis E., Nevarko T., Weatherill D.B., Vasuta C., Yee S., Truitt M., Dallaire P., et al. Autism-related deficits via dysregulated eIF4E-dependent translational control. Nature 2013, 493:371-377.
23. Greco B., Managò F., Tucci V., Kao H.T., Valtorta F., Benfenati F. Autism-related behavioral abnormalities in synapsin knockout mice. Behav. Brain Res. 2013, 251:65-74.
24. Heiman M., Schaefer A., Gong S., Peterson J.D., Day M., Ramsey K.E., Suárez-Fariñas M., Schwarz C., Stephan D.A., Surmeier D.J., et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 2008, 135:738-748.
25. 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 2014, 515:216-221.
26. Jiang Y.H., Ehlers M.D. Modeling autism by SHANK gene mutations in mice. Neuron 2013, 78:8-27.
27. Jin J., Smith F.D., Stark C., Wells C.D., Fawcett J.P., Kulkarni S., Metalnikov P., O'Donnell P., Taylor P., Taylor L., et al. Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 2004, 14:1436-1450.
28. Kaminsky E.B., Kaul V., Paschall J., Church D.M., Bunke B., Kunig D., Moreno-De-Luca D., Moreno-De-Luca A., Mulle J.G., Warren S.T., et al. An evidence-based approach to establish the functional and clinical significance of copy number variants in intellectual and developmental disabilities. Genet. Med. 2011, 13:777-784.
29. Kanai Y., Dohmae N., Hirokawa N. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 2004, 43:513-525.
30. Kang H.J., Kawasawa Y.I., Cheng F., Zhu Y., Xu X., Li M., Sousa A.M., Pletikos M., Meyer K.A., Sedmak G., et al. Spatio-temporal transcriptome of the human brain. Nature 2011, 478:483-489.
31. Kedia S., Chattarji S. Marble burying as a test of the delayed anxiogenic effects of acute immobilisation stress in mice. J. Neurosci. Methods 2014, 233:150-154.
32. Kelleher R.J., Bear M.F. The autistic neuron: troubled translation?. Cell 2008, 135:401-406.
33. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256:675-677.
34. Kim E., Sheng M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 2004, 5:771-781.
35. Lai J.K., Sobala-Drozdowski M., Zhou L., Doering L.C., Faure P.A., Foster J.A. Temporal and spectral differences in the ultrasonic vocalizations of fragile X knock out mice during postnatal development. Behav. Brain Res. 2014, 259:119-130.
36. Langen M., Durston S., Kas M.J., van Engeland H., Staal W.G. The neurobiology of repetitive behavior: . . .and men. Neurosci. Biobehav. Rev. 2011, 35:356-365.
37. Lipton J.O., Sahin M. The neurology of mTOR. Neuron 2014, 84:275-291.
38. Moon J., Beaudin A.E., Verosky S., Driscoll L.L., Weiskopf M., Levitsky D.A., Crnic L.S., Strupp B.J. Attentional dysfunction, impulsivity, and resistance to change in a mouse model of fragile X syndrome. Behav. Neurosci. 2006, 120:1367-1379.
39. Muddashetty R.S., Kelić S., Gross C., Xu M., Bassell G.J. Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J. Neurosci. 2007, 27:5338-5348.
40. Nakatani J., Tamada K., Hatanaka F., Ise S., Ohta H., Inoue K., Tomonaga S., Watanabe Y., Chung Y.J., Banerjee R., et al. Abnormal behavior in a chromosome-engineered mouse model for human 15q11-13 duplication seen in autism. Cell 2009, 137:1235-1246.
41. Nishimura Y., Martin C.L., Vazquez-Lopez A., Spence S.J., Alvarez-Retuerto A.I., Sigman M., Steindler C., Pellegrini S., Schanen N.C., Warren S.T., Geschwind D.H. Genome-wide expression profiling of lymphoblastoid cell lines distinguishes different forms of autism and reveals shared pathways. Hum. Mol. Genet. 2007, 16:1682-1698.
42. Njung'e K., Handley S.L. Effects of 5-HT uptake inhibitors, agonists and antagonists on the burying of harmless objects by mice; a putative test for anxiolytic agents. Br. J. Pharmacol. 1991, 104:105-112.
43. O'Roak B.J., Vives L., Fu W., Egertson J.D., Stanaway I.B., Phelps I.G., Carvill G., Kumar A., Lee C., Ankenman K., et al. Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science 2012, 338:1619-1622.
44. Parikshak N.N., Luo R., Zhang A., Won H., Lowe J.K., Chandran V., Horvath S., Geschwind D.H. Integrative functional genomic analyses implicate specific molecular pathways and circuits in autism. Cell 2013, 155:1008-1021.
45. Peça J., Feliciano C., Ting J.T., Wang W., Wells M.F., Venkatraman T.N., Lascola C.D., Fu Z., Feng G. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 2011, 472:437-442.
46. Peñagarikano O., Abrahams B.S., Herman E.I., Winden K.D., Gdalyahu A., Dong H., Sonnenblick L.I., Gruver R., Almajano J., Bragin A., et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 2011, 147:235-246.
47. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106:274-285.
48. Poultney C.S., Goldberg A.P., Drapeau E., Kou Y., Harony-Nicolas H., Kajiwara Y., De Rubeis S., Durand S., Stevens C., Rehnström K., et al. Identification of small exonic CNV from whole-exome sequence data and application to autism spectrum disorder. Am. J. Hum. Genet. 2013, 93:607-619.
49. Prasad T.S., Kandasamy K., Pandey A. Human Protein Reference Database and Human Proteinpedia as discovery tools for systems biology. Methods Mol. Biol. 2009, 577:67-79.
50. Presti M.F., Watson C.J., Kennedy R.T., Yang M., Lewis M.H. Behavior-related alterations of striatal neurochemistry in a mouse model of stereotyped movement disorder. Pharmacol. Biochem. Behav. 2004, 77:501-507.
51. Santini E., Huynh T.N., MacAskill A.F., Carter A.G., Pierre P., Ruggero D., Kaphzan H., Klann E. Exaggerated translation causes synaptic and behavioural aberrations associated with autism. Nature 2013, 493:411-415.
52. Santoro M.R., Bray S.M., Warren S.T. Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu. Rev. Pathol. 2012, 7:219-245.
53. Sawicka K., Zukin R.S. Dysregulation of mTOR signaling in neuropsychiatric disorders: therapeutic implications. Neuropsychopharmacology 2012, 37:305-306.
54. Scattoni M.L., Ricceri L., Crawley J.N. Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters. Genes Brain Behav. 2011, 10:44-56.
55. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 2010, 11:490-502.
56. Steinberg J., Webber C. The roles of FMRP-regulated genes in autism spectrum disorder: single- and multiple-hit genetic etiologies. Am. J. Hum. Genet. 2013, 93:825-839.
57. Steindler C., Li Z., Algarté M., Alcover A., Libri V., Ragimbeau J., Pellegrini S. Jamip1 (marlin-1) defines a family of proteins interacting with janus kinases and microtubules. J. Biol. Chem. 2004, 279:43168-43177.
58. Szatmari P., Paterson A.D., Zwaigenbaum L., Roberts W., Brian J., Liu X.Q., Vincent J.B., Skaug J.L., Thompson A.P., Senman L., et al. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat. Genet. 2007, 39:319-328. Autism Genome Project Consortium.
59. Szczypka M.S., Kwok K., Brot M.D., Marck B.T., Matsumoto A.M., Donahue B.A., Palmiter R.D. Dopamine production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron 2001, 30:819-828.
60. Thomas A., Burant A., Bui N., Graham D., Yuva-Paylor L.A., Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl.) 2009, 204:361-373.
61. Todd P.K., Mack K.J., Malter J.S. The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95. Proc. Natl. Acad. Sci. USA 2003, 100:14374-14378.
62. Tzetis M., Kitsiou-Tzeli S., Frysira H., Xaidara A., Kanavakis E. The clinical utility of molecular karyotyping using high-resolution array-comparative genomic hybridization. Expert Rev. Mol. Diagn. 2012, 12:449-457.
63. Vidal R.L., Valenzuela J.I., Luján R., Couve A. Cellular and subcellular localization of Marlin-1 in the brain. BMC Neurosci. 2009, 10:37.
64. Villacé P., Marión R.M., Ortín J. The composition of Staufen-containing RNA granules from human cells indicates their role in the regulated transport and translation of messenger RNAs. Nucleic Acids Res. 2004, 32:2411-2420.
65. Voineagu I., Wang X., Johnston P., Lowe J.K., Tian Y., Horvath S., Mill J., Cantor R.M., Blencowe B.J., Geschwind D.H. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 2011, 474:380-384.
66. Wang C.C., Held R.G., Chang S.C., Yang L., Delpire E., Ghosh A., Hall B.J. A critical role for GluN2B-containing NMDA receptors in cortical development and function. Neuron 2011, 72:789-805. 10.1016/j.neuron.2011.09.023.
67. Waung M.W., Huber K.M. Protein translation in synaptic plasticity: mGluR-LTD, Fragile X. Curr. Opin. Neurobiol. 2009, 19:319-326.
68. Wohlschlegel J.A. Identification of SUMO-conjugated proteins and their SUMO attachment sites using proteomic mass spectrometry. Methods Mol. Biol. 2009, 497:33-49.
69. Won H., Lee H.R., Gee H.Y., Mah W., Kim J.I., Lee J., Ha S., Chung C., Jung E.S., Cho Y.S., et al. Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function. Nature 2012, 486:261-265.
70. Yang M., Crawley J.N. Simple behavioral assessment of mouse olfaction. Curr. Protoc. Neurosci. 2009, Chapter 8:Unit 8.24.
71. Zaĭchenko M.I., Vanetsian G.L., Merzhanova G.Kh. [Differences in behavior of impulsive and self-controlled rats in the open-field and light-dark tests]. Zh. Vyssh. Nerv. Deiat. Im. I P Pavlova 2011, 61:340-350.
72. Zalfa F., Giorgi M., Primerano B., Moro A., Di Penta A., Reis S., Oostra B., Bagni C. The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 2003, 112:317-327.
73. Zalfa F., Eleuteri B., Dickson K.S., Mercaldo V., De Rubeis S., di Penta A., Tabolacci E., Chiurazzi P., Neri G., Grant S.G., Bagni C. A new function for the fragile X mental retardation protein in regulation of PSD-95 mRNA stability. Nat. Neurosci. 2007, 10:578-587.