Rbm8a haploinsufficiency disrupts embryonic cortical development resulting in microcephaly

Journal of Neuroscience

Volumn 35, Issue 18, 2015, Pages 7003-7018

  Mao, Hanqian ^a   Pilaz, Louis Jan ^a   McMahon, John J ^a   Golzio, Christelle ^a   Wu, Danwei ^a   Shi, Lei ^a   Katsanis, Nicholas ^a   Silver, Debra L ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cortical development; Embryonic; Microcephaly; Neurogenesis; Radial glia; rbm8a

Indexed keywords

MESSENGER RNA; PEPTIDES AND PROTEINS; RNA BINDING MOTIF PROTEIN 8A; UNCLASSIFIED DRUG; RBM8A PROTEIN, HUMAN; RNA BINDING PROTEIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; EMBRYONIC CORTICAL DEVELOPMENT; FEMALE; GLIA CELL; HAPLOINSUFFICIENCY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MALE; MICROCEPHALY; MOUSE; NEOCORTEX; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ZEBRA FISH; ANIMAL; BIOSYNTHESIS; BRAIN CORTEX; C57BL MOUSE; CELL CULTURE; EMBRYO DEVELOPMENT; EMBRYOLOGY; GENETICS; HUMAN; METABOLISM; ORGANOGENESIS; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYONIC DEVELOPMENT; HAPLOINSUFFICIENCY; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROCEPHALY; ORGANOGENESIS; RNA-BINDING PROTEINS;

EID: 84929340848     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0018-15.2015     Document Type: Article

References (64)

1. Addington AM, Gauthier J, Piton A, Hamdan FF, Raymond A, Gogtay N, Miller R, Tossell J, Bakalar J, Inoff-Germain G, Gochman P, Long R, Rapoport JL, Rouleau GA (2011) A novel frameshift mutation in UPF3B identified in brothers affected with childhood onset schizophrenia and autism spectrum disorders. Mol Psychiatry 16:238-239. CrossRef Medline
2. Alachkar, A, Jiang, D, Harrison, M, Zhou, Y, Chen, G, and Mao, Y (2013) An EJC factor RBM8a regulates anxiety behaviors. Curr Mol Med 6:887-899. Medline
3. Albers CA, Paul DS, Schulze H, Freson K, Stephens JC, Smethurst PA, Jolley JD, Cvejic A, Kostadima M, Bertone P, Breuning MH, Debili N, Deloukas P, Favier R, Fiedler J, Hobbs CM, Huang N, Hurles ME, Kiddle G, Krapels I, et al. (2012) Compound inheritance of a low-frequency regulatory SNP and a rare null mutation in exon-junction complex subunit RBM8A causes TAR syndrome. Nat Genet 44:435-439, S1-S2. CrossRef Medline
4. Arai Y, Pulvers JN, Haffner C, Schilling B, Nüsslein I, Calegari F, Huttner WB (2011) Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2:154. CrossRef Medline
5. Ashton-Beaucage D, Udell CM, Lavoie H, Baril C, Lefrançois M, Chagnon P, Gendron P, Caron-Lizotte O, Bonneil E, Thibault P, Therrien M (2010) The exon junction complex controls the splicing of MAPK and other long intron-containing transcripts in Drosophila. Cell 143:251-262. CrossRef Medline
6. Ayoub AE, Oh S, Xie Y, Leng J, Cotney J, Dominguez MH, Noonan JP, Rakic P (2011) Transcriptional programs in transient embryonic zones of the cerebral cortex defined by high-resolution mRNA sequencing. Proc Natl Acad Sci U S A 108:14950-14955. CrossRef Medline
7. Beunders G, Voorhoeve E, Golzio C, Pardo LM, Rosenfeld JA, Talkowski ME, Simonic I, Lionel AC, Vergult S, Pyatt RE, van de Kamp J, Nieuwint A, Weiss MM, Rizzu P, Verwer LE, van Spaendonk RM, Shen Y, Wu BL, Yu T, Yu Y, et al. (2013) Exonic deletions in AUTS2 cause a syndromic form of intellectual disability and suggest a critical role for the C terminus. Am J Hum Genet 92:210-220. CrossRef Medline
8. Blumenthal I, Ragavendran A, Erdin S, Klei L, Sugathan A, Guide JR, Manavalan P, Zhou JQ, Wheeler VC, Levin JZ, Ernst C, Roeder K, Devlin B, Gusella JF, Talkowski ME (2014) AR TICLETranscriptional consequences of 16pll.2 deletion and duplication in mouse cortex and multiplex autism families. Am J Hum Genet 94:870-883. CrossRef Medline
9. Bono F, Gehring NH (2011) Assembly, disassembly and recycling: the dynamics of exon junction complexes. RNA Biol 8:24-29. CrossRef Medline
10. Bono F, Ebert J, Lorentzen E, Conti E (2006) The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 126:713-725. CrossRef Medline
11. Brunetti-Pierri N, Berg JS, Scaglia F, Belmont J, Bacino CA, Sahoo T, Lalani SR, Graham B, Lee B, Shinawi M, Shen J, Kang SH, Pursley A, Lotze T, Kennedy G, Lansky-Shafer S, Weaver C, Roeder ER, Grebe, TA, Arnold GL, et al. (2008) Recurrent reciprocal lq21.1 deletions and duplications associated with microcephaly or macrocephaly and developmental and behavioral abnormalities. Nat Genet 40:1466-1471. CrossRef Medline
12. Carvalho CM, Vasanth S, Shinawi M, Russell C, Ramocki MB, Brown CW, Graakjaer J, Skytte AB, Vianna-Morgante AM, Krepischi AC, Patel GS, Immken L, Aleck K, Lim C, Cheung SW, Rosenberg C, Katsanis N, Lupski JR (2014) Dosage changes of a segment at 17pl3.1 lead to intellectual disability and microcephaly as a result of complex genetic interaction of multiple genes. Am J Hum Genet 95:565-578. CrossRef Medline
13. Chen JF, Zhang Y, Wilde J, Hansen KC, Lai F, Niswander L (2014) Microcephaly disease gene Wdr62 regulates mitotic progression of embryonic neural stem cells and brain size. Nat Commun 5:3885. CrossRef Medline
14. Chou SJ, Perez-Garcia CG, Kroll TT, O'Leary DD (2009) Lhx2 specifies regional fate in Emxl lineage of telencephalic progenitors generating cerebral cortex. Nat Neurosci 12:1381-1389. CrossRef Medline
15. Daguenet E, Baguet A, Degot S, Schmidt U, Alpy F, Wendling C, Spiegelhalter C, Kessler P, Rio MC, Le Hir H, Bertrand E, Tomasetto C (2012) Perispeckles are major assembly sites for the exon junction core complex. Mol Biol Cell 23:1765-1782. CrossRef Medline
16. DeBoer EM, Kraushar ML, Hart RP, Rasin MR (2013) Post-transcriptional regulatory elements and spatiotemporal specification of neocortical stem cells and projection neurons. Neuroscience 248: 499-528. CrossRef Medline
17. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (2005) Pax6, Tbr2, and Tbrl are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247-251. CrossRef Medline
18. Favaro FP, Alvizi L, Zechi-Ceide RM, Bertola D, Felix TM, de Souza J, Raskin S, Twigg SR, Weiner AM, Armas P, Margarit E, Calcaterra NB, Andersen GR, McGowan SJ, Wilkie AO, Richieri-Costa A, de Almeida ML, Passos-Bueno MR (2014) A noncoding expansion in EIF4A3 causes Richieri-Costa-Pereira syndrome, a craniofacial disorder associated with limb defects. Am J Hum Genet 94:120-128. CrossRef Medline
19. Feng Y, Walsh CA (2004) Mitotic spindle regulation by Ndel controls cerebral cortical size. Neuron 44:279-293. CrossRef Medline
20. Fietz SA, Huttner WB (2011) Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr Opin Neurobiol 21:23-35. CrossRef Medline
21. Franco SJ, Müller U (2013) Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex. Neuron 77:19-34. CrossRef Medline
22. Fromer M, Pocklington AJ, Kavanagh DH, Williams HJ, Dwyer S, Gormley P, Georgieva L, Rees E, Palta P, Ruderfer DM, Carrera N, Humphreys I, Johnson JS, Roussos P, Barker DD, Banks E, Milanova V, Grant SG, Hannon E, Rose SA, et al. (2014) De novo mutations in schizophrenia implicate synaptic networks. Nature 506:179-184. CrossRef Medline
23. Gehring NH, Lamprinaki S, Hentze MW, Kulozik AE (2009) The hierarchy of exon-junction complex assembly by the spliceosome explains key features of mammalian nonsense-mediated mRNA decay. PLoS Biol 7:el000120. CrossRef Medline
24. Golzio C, Wilier J, Talkowski ME, Oh EC, Taniguchi Y, Jacquemont S, Rey-mond A, Sun M, Sawa A, Gusella JF, Kamiya A, Beckmann JS, Katsanis N (2012) KCTD13 is a major driver of mirrored neuroanatomical phenotypes of the 16pl 1.2 copy number variant. Nature 485:363-367. CrossRef Medline
25. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR (2002) Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emxl-expressing lineage. J Neurosci 22:6309-6314. Medline
26. Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M (2006) Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295:263-277. CrossRef Medline
27. Greig LC, Woodworth MB, Galazo MJ, Padmanabhan H, Macklis JD (2013) Molecular logic of neocortical projection neuron specification, development and diversity. Nat Rev Neurosci 14:755-769. CrossRef Medline
28. Haydar TF, Kuan CY, Flavell RA, Rakic P (1999) The role of cell death in regulating the size and shape of the mammalian forebrain. Cereb Cortex 9:621-626. CrossRef Medline
29. Hu WF, Chahrour MH, Walsh CA (2014) The diverse genetic landscape of neurodevelopmental disorders. Annu Rev Genomics Hum Genet 15:195-213. CrossRef Medline
30. Insolera R, Bazzi H, Shao W, Anderson KV, Shi SH (2014) Cortical neuro-genesis in the absence ofcentrioles. Nat Neurosci 17:1528-1535. CrossRef Medline
31. International Schizophrenia Consortium (2008) Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 455:237-241. CrossRef Medline
32. Kataoka N, Diem MD, Kim VN, Yong J, Dreyfuss G (2001) Magoh, a human homolog of Drosophila mago nashi protein, is a component of the splicing-dependent exon-exon junction complex. EMBO J 20:6424-6433. CrossRef Medline
33. Kim S, Lehtinen MK, Sessa A, Zappaterra MW, Cho SH, Gonzalez D, Boggan B, Austin CA, Wijnholds J, Gambello MJ, Malicki J, La Mantia AS, Broccoli V, Walsh CA (2010) The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron 66:69-84. CrossRef Medline
34. Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, Hodge R, Attardo A, Bell C, Huttner WB, Hevner RF (2009) Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex 19:2439-2450. CrossRef Medline
35. Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS, Hurles ME, Homfray T, Penninger JM, Jackson AP, Knoblich JA (2013) Cerebral organoids model human brain development and microcephaly. Nature 501:373-379. CrossRef Medline
36. Lange C, Huttner WB, Calegari F (2009) Cdk4/cyclinDl overexpression in neural stem cells shortens Gl, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5:320-331. CrossRef Medline
37. Lau CK, Diem MD, Dreyfuss G, Van Duyne GD (2003) Structure of the Y14-Magoh core of the exon junction complex. Curr Biol 13:933-941. CrossRef Medline
38. Marthiens V, Rujano MA, Pennetier C, Tessier S, Paul-Gilloteaux P, Basto R (2013) Centrosome amplification causes microcephaly. Nat Cell Biol 15: 731-740. CrossRef Medline
39. McMahon JJ, Shi L, Silver DL (2014) Generation of a Magoh conditional allele in mice. Genesis 52:752-758. CrossRef Medline
40. Mefford HC, Sharp AJ, Baker C, Itsara A, Jiang Z, Buysse K, Huang S, Maloney VK, Crolla JA, Baralle D, Collins A, Mercer C, Norga K, de Ravel T, Devriendt K, Bongers EM, de Leeuw N, Reardon W, Gimelli S, Bena F, et al. (2008) Recurrent rearrangements of chromosome 1 q21.1 and variable pediatric phenotypes. N Engl J Med 359:1685-1699. CrossRef Medline
41. Muromoto R, Taira N, Ikeda O, Shiga K, Kamitani S, Togi S, Kawakami S, Sekine Y, Nanbo A, Oritani K, Matsuda T (2009) The exon-junction complex proteins, Y14 and MAGOH regulate STAT3 activation. Biochem Biophys Res Commun 382:63-68. CrossRef Medline
42. Nguyen LS, Kim HG, Rosenfeld JA, Shen Y, Gusella JF, Lacassie Y, Layman LC, Shaffer LG, Gécz J (2013) Contribution of copy number variants involving nonsense-mediated mRNA decay pathway genes to neuro-developmental disorders. Hum Mol Genet 22:1816-1825. CrossRef Medline
43. Nguyen LS, Wilkinson MF, Gecz J (2014) Nonsense-mediated mRNA decay: inter-individual variability and human disease. Neurosci Biobehav Rev 46:175-186. CrossRef Medline
44. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714-720. CrossRef Medline
45. Palacios IM, Gatfìeld D, St Johnston D, Izaurralde E (2004) An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427:753-757. CrossRef Medline
46. Pilaz LJ, Patti D, Marcy G, Oilier E, Pfister S, Douglas RJ, Betizeau M, Gautier E, Cortay V, Doerflinger N, Kennedy H, Dehay C (2009) Forced Gl-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc Natl Acad Sci U S A 106:21924-21929. CrossRef Medline
47. Roignant JY, Treisman JE (2010) Exon junction complex subunits are required to splice Drosophila MAP kinase, a large heterochromatic gene. Cell 143:238-250. CrossRef Medline
48. Rosenfeld JA, Traylor RN, Schaefer GB, McPherson EW, Ballif BC, Klopocki E, Mundlos S, Shaffer LG, Aylsworth AS, 1 q21.1 Study Group (2012) Proximal microdeletions and microduplications of lq21.1 contribute to variable abnormal phenotypes. Eur J Hum Genet 20:754-761. CrossRef Medline
49. Sahara S, O'Leary DD (2009) FgflO regulates transition period of cortical stem cell differentiation to radial glia controlling generation of neurons and basal progenitors. Neuron 63:48-62. CrossRef Medline
50. Saito T (2006) In vivo electroporation in the embryonic mouse central nervous system. Nat Protoc 1:1552-1558. CrossRef Medline
51. Sharp AJ, Hansen S, Selzer RR, Cheng Z, Regan R, Hurst JA, Stewart H, Price SM, Blair E, Hennekam RC, Fitzpatrick CA, Segraves R, Richmond TA, Guiver C, Albertson DG, Pinkel D, Eis PS, Schwartz S, Knight SJ, Eichler EE (2006) Discovery of previously unidentified genomic disorders from the duplication architecture of the human genome. Nat Genet 38:1038-1042. CrossRef Medline
52. Shibuya T, Tange TØ, Sonenberg N, Moore MJ (2004) eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nat Struct Mol Biol 11:346-351. CrossRef Medline
53. Silver DL, Watkins-Chow DE, SchreckKC, Pierfelice TJ, Larson DM, Burnetti AJ, Liaw HJ, Myung K, Walsh CA, Gaiano N, Pavan WJ (2010) The exon junction complex component Magoh controls brain size by regulating neural stem cell division. Nat Neurosci 13:551-558. CrossRef Medline
54. Silver DL, Leeds KE, Hwang HW, Miller EE, Pavan WJ (2013) The EJC component Magoh regulates proliferation and expansion of neural crest-derived melanocytes. Dev Biol 375:172-181. CrossRef Medline
55. Singh KK, Wachsmuth L, Kulozik AE, GehringNH (2013) Two mammalian MAGOH genes contribute to exon junction complex composition and nonsense-mediated decay. RNA Biol 10:1291-1298. CrossRef Medline
56. Sugathan A, Biagioli M, Golzio C, Erdin S, Blumenthal I, Manavalan P, Ra-gavendran A, Brand H, Lucente D, Miles J, Sheridan SD, Stortchevoi A, Kellis M, Haggarty SJ, Katsanis N, Gusella JF, Talkowski ME (2014) CHD8 regulates neurodevelopmental pathways associated with autism spectrum disorder in neural progenitors. Proc Natl Acad Sci U S A 111: E4468-E4477. CrossRef Medline
57. Sun Y, Goderie SK, Temple S (2005) Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 45:873-886. CrossRef Medline
58. Tange TØ, Shibuya T, Jurica MS, Moore MJ (2005) Biochemical analysis of the EJC reveals two new factors and a stable tetrameric protein core. RNA 11:1869-1883. CrossRef Medline
59. Tarpey PS, Raymond FL, Nguyen LS, Rodriguez J, Hackett A, Vandeleur L, Smith R, Shoubridge C, Edkins S, Stevens C, O'Meara S, Tofts C, Bar-thorpe S, Buck G, Cole J, Halliday K, Hills K, Jones D, Mironenko T, Perry J, et al. (2007) Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat Genet 39:1127-1133. CrossRef Medline
60. Togi S, Shiga K, Muromoto R, Kato M, Souma Y, Sekine Y, Kon S, Oritani K, Matsuda T (2013) Y14 positively regulates TNF-α-induced NF-κB transcriptional activity via interacting RIP1 and TRADD beyond an exon junction complex protein. J Immunol 191:1436-1444. CrossRef Medline
61. Vasistha NA, García-Moreno F, Arora S, Cheung AFP, Arnold SJ, Robertson EJ, Molnár Z (2014) Cortical and clonal contribution of Tbr2 expressing progenitors in the developing mouse brain. Cereb Cortex. Advance online publication. Retrieved June 13, 2014. doi: 10.1093/cercor/bhul25.
62. Visel A, Thaller C, Eichele G (2004) GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 32:D552-D556. CrossRef Medline
63. Xie Y, Jüschke C, Esk C, Hirotsune S, Knoblich JA (2013) The phosphatase PP4c controls spindle orientation to maintain proliferative symmetric divisions in the developing neocortex. Neuron 79:254-265. CrossRef Medline
64. Yingling J, Youn YH, Darling D, Toyo-Oka K, Pramparo T, Hirotsune S, Wynshaw-Boris A (2008) Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132:474-486. CrossRef Medline