De Novo Mutations in DENR Disrupt Neuronal Development and Link Congenital Neurological Disorders to Faulty mRNA Translation Re-initiation.

Haas, Matilda A.; Ngo, Linh; Li, Shan Shan; Schleich, Sibylle; Qu, Zhengdong; Vanyai, Hannah K.; Cullen, Hayley D.; Cardona-Alberich, Aida; Gladwyn-Ng, Ivan; Pagnamenta, Alistair T.; Taylor, Jenny C.; Stewart, Helen; Kini, Usha; Duncan, Kent E.; Teleman, Aurelio A.; Keays, David A.; Heng, Julian I.-T.

doi:10.1016/j.celrep.2016.04.090

Article (Scientific journals)

De Novo Mutations in DENR Disrupt Neuronal Development and Link Congenital Neurological Disorders to Faulty mRNA Translation Re-initiation.

Haas, Matilda A.; Ngo, Linh; Li, Shan Shan et al.

2016 • In Cell Reports

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https://hdl.handle.net/2268/197726

DOI
10.1016/j.celrep.2016.04.090

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27239039

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Abstract :

[en] Disruptions to neuronal mRNA translation are hypothesized to underlie human neurodevelopmental syndromes. Notably, the mRNA translation re-initiation factor DENR is a regulator of eukaryotic translation and cell growth, but its mammalian functions are unknown. Here, we report that Denr influences the migration of murine cerebral cortical neurons in vivo with its binding partner Mcts1, whereas perturbations to Denr impair the long-term positioning, dendritic arborization, and dendritic spine characteristics of postnatal projection neurons. We characterized de novo missense mutations in DENR (p.C37Y and p.P121L) detected in two unrelated human subjects diagnosed with brain developmental disorder to find that each variant impairs the function of DENR in mRNA translation re-initiation and disrupts the migration and terminal branching of cortical neurons in different ways. Thus, our findings link human brain disorders to impaired mRNA translation re-initiation through perturbations in DENR (OMIM: 604550) function in neurons.

Disciplines :

Human health sciences: Multidisciplinary, general & others

Author, co-author :

Haas, Matilda A.

Ngo, Linh

Li, Shan Shan

Schleich, Sibylle

Qu, Zhengdong

Vanyai, Hannah K.

Cullen, Hayley D.

Cardona-Alberich, Aida

Gladwyn-Ng, Ivan ; Université de Liège > Giga - Neurosciences

Pagnamenta, Alistair T.

More authors (7 more)

Language :

English

Title :

De Novo Mutations in DENR Disrupt Neuronal Development and Link Congenital Neurological Disorders to Faulty mRNA Translation Re-initiation.

Publication date :

2016

Journal title :

Cell Reports

eISSN :

2211-1247

Publisher :

Elsevier

Peer reviewed :

Peer Reviewed verified by ORBi

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Available on ORBi :

since 02 June 2016

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Barkovich A.J., Kuzniecky R.I., Jackson G.D., Guerrini R., Dobyns W.B. A developmental and genetic classification for malformations of cortical development. Neurology 2005, 65:1873-1887.
Barkovich A.J., Guerrini R., Kuzniecky R.I., Jackson G.D., Dobyns W.B. A developmental and genetic classification for malformations of cortical development: update 2012. Brain 2012, 135:1348-1369.
Barnes A.P., Polleux F. Establishment of axon-dendrite polarity in developing neurons. Annu. Rev. Neurosci. 2009, 32:347-381.
Borck G., Shin B.S., Stiller B., Mimouni-Bloch A., Thiele H., Kim J.R., Thakur M., Skinner C., Aschenbach L., Smirin-Yosef P., et al. eIF2γ mutation that disrupts eIF2 complex integrity links intellectual disability to impaired translation initiation. Mol. Cell 2012, 48:641-646.
Breuss M., Heng J.I., Poirier K., Tian G., Jaglin X.H., Qu Z., Braun A., Gstrein T., Ngo L., Haas M., et al. Mutations in the β-tubulin gene TUBB5 cause microcephaly with structural brain abnormalities. Cell Rep. 2012, 2:1554-1562.
Bron R., Vermeren M., Kokot N., Andrews W., Little G.E., Mitchell K.J., Cohen J. Boundary cap cells constrain spinal motor neuron somal migration at motor exit points by a semaphorin-plexin mechanism. Neural Dev. 2007, 2:21.
Bugiani M., Boor I., Powers J.M., Scheper G.C., van der Knaap M.S. Leukoencephalopathy with vanishing white matter: a review. J. Neuropathol. Exp. Neurol. 2010, 69:987-996.
Causeret F., Terao M., Jacobs T., Nishimura Y.V., Yanagawa Y., Obata K., Hoshino M., Nikolic M. The p21-activated kinase is required for neuronal migration in the cerebral cortex. Cereb. Cortex 2009, 19:861-875.
Chen J.A., Peñagarikano O., Belgard T.G., Swarup V., Geschwind D.H. The emerging picture of autism spectrum disorder: genetics and pathology. Annu. Rev. Pathol. 2015, 10:111-144.
Dmitriev S.E., Terenin I.M., Andreev D.E., Ivanov P.A., Dunaevsky J.E., Merrick W.C., Shatsky I.N. GTP-independent tRNA delivery to the ribosomal P-site by a novel eukaryotic translation factor. J. Biol. Chem. 2010, 285:26779-26787.
Firth A.E., Brierley I. Non-canonical translation in RNA viruses. J. Gen. Virol. 2012, 93:1385-1409.
Forrest A.R., Kawaji H., Rehli M., Baillie J.K., de Hoon M.J., Haberle V., Lassmann T., Kulakovskiy I.V., Lizio M., Itoh M., et al. A promoter-level mammalian expression atlas. Nature 2014, 507:462-470. FANTOM Consortium and the RIKEN PMI and CLST (DGT).
Gladwyn-Ng I.E., Li S.S., Qu Z., Davis J.M., Ngo L., Haas M., Singer J., Heng J.I. Bacurd2 is a novel interacting partner to Rnd2 which controls radial migration within the developing mammalian cerebral cortex. Neural Dev. 2015, 10:9.
Haas M.A., Bell D., Slender A., Lana-Elola E., Watson-Scales S., Fisher E.M., Tybulewicz V.L., Guillemot F. Alterations to dendritic spine morphology, but not dendrite patterning, of cortical projection neurons in Tc1 and Ts1Rhr mouse models of Down syndrome. PLoS ONE 2013, 8:e78561.
Harris K.D., Mrsic-Flogel T.D. Cortical connectivity and sensory coding. Nature 2013, 503:51-58.
Heng J.I., Nguyen L., Castro D.S., Zimmer C., Wildner H., Armant O., Skowronska-Krawczyk D., Bedogni F., Matter J.M., Hevner R., Guillemot F. Neurogenin 2 controls cortical neuron migration through regulation of Rnd2. Nature 2008, 455:114-118.
Heng J.I., Chariot A., Nguyen L. Molecular layers underlying cytoskeletal remodelling during cortical development. Trends Neurosci. 2010, 33:38-47.
Hering H., Sheng M. Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2001, 2:880-888.
Hinnebusch A.G., Lorsch J.R. The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harb. Perspect. Biol. 2012, 4. pii: a011544.
Holt C.E., Schuman E.M. The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 2013, 80:648-657.
Janich P., Arpat A.B., Castelo-Szekely V., Lopes M., Gatfield D. Ribosome profiling reveals the rhythmic liver translatome and circadian clock regulation by upstream open reading frames. Genome Res. 2015, 25:1848-1859.
Kasperaitis M.A., Voorma H.O., Thomas A.A. The amino acid sequence of eukaryotic translation initiation factor 1 and its similarity to yeast initiation factor SUI1. FEBS Lett. 1995, 365:47-50.
Kelleher R.J., Bear M.F. The autistic neuron: troubled translation?. Cell 2008, 135:401-406.
Kriegstein A.R., Noctor S.C. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 2004, 27:392-399.
Li W., Wang X., Van Der Knaap M.S., Proud C.G. Mutations linked to leukoencephalopathy with vanishing white matter impair the function of the eukaryotic initiation factor 2B complex in diverse ways. Mol. Cell. Biol. 2004, 24:3295-3306.
Liu L., Lei J., Sanders S.J., Willsey A.J., Kou Y., Cicek A.E., Klei L., Lu C., He X., Li M., et al. DAWN: a framework to identify autism genes and subnetworks using gene expression and genetics. Mol. Autism 2014, 5:22.
LoTurco J.J., Bai J. The multipolar stage and disruptions in neuronal migration. Trends Neurosci. 2006, 29:407-413.
Lunter G., Goodson M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 2011, 21:936-939.
Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 2004, 5:793-807.
Mazan-Mamczarz K., Gartenhaus R.B. Post-transcriptional control of the MCT-1-associated protein DENR/DRP by RNA-binding protein AUF1. Cancer Genomics Proteomics 2007, 4:233-239.
Nadarajah B., Alifragis P., Wong R.O., Parnavelas J.G. Ventricle-directed migration in the developing cerebral cortex. Nat. Neurosci. 2002, 5:218-224.
Nadarajah B., Alifragis P., Wong R.O., Parnavelas J.G. Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb. Cortex 2003, 13:607-611.
Neale B.M., Kou Y., Liu L., Ma'ayan A., Samocha K.E., Sabo A., Lin C.F., Stevens C., Wang L.S., Makarov V., et al. Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 2012, 485:242-245.
Ngo L., Haas M., Qu Z., Li S.S., Zenker J., Teng K.S., Gunnersen J.M., Breuss M., Habgood M., Keays D.A., Heng J.I. TUBB5 and its disease-associated mutations influence the terminal differentiation and dendritic spine densities of cerebral cortical neurons. Hum. Mol. Genet. 2014, 23:5147-5158.
Niblock M.M., Brunso-Bechtold J.K., Riddle D.R. Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J. Neurosci. 2000, 20:4165-4176.
Noctor S.C., Martínez-Cerdeño V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 2004, 7:136-144.
Reinert L.S., Shi B., Nandi S., Mazan-Mamczarz K., Vitolo M., Bachman K.E., He H., Gartenhaus R.B. MCT-1 protein interacts with the cap complex and modulates messenger RNA translational profiles. Cancer Res. 2006, 66:8994-9001.
Rimmer A., Phan H., Mathieson I., Iqbal Z., Twigg S.R., Wilkie A.O., McVean G., Lunter G. Integrating mapping-, assembly- and haplotype-based approaches for calling variants in clinical sequencing applications. Nat. Genet. 2014, 46:912-918. WGS500 Consortium.
Schleich S., Strassburger K., Janiesch P.C., Koledachkina T., Miller K.K., Haneke K., Cheng Y.S., Küchler K., Stoecklin G., Duncan K.E., Teleman A.A. DENR-MCT-1 promotes translation re-initiation downstream of uORFs to control tissue growth. Nature 2014, 512:208-212.
Skabkin M.A., Skabkina O.V., Dhote V., Komar A.A., Hellen C.U., Pestova T.V. Activities of ligatin and MCT-1/DENR in eukaryotic translation initiation and ribosomal recycling. Genes Dev. 2010, 24:1787-1801.
Skabkin M.A., Skabkina O.V., Hellen C.U., Pestova T.V. Reinitiation and other unconventional posttermination events during eukaryotic translation. Mol. Cell 2013, 51:249-264.
Stoner R., Chow M.L., Boyle M.P., Sunkin S.M., Mouton P.R., Roy S., Wynshaw-Boris A., Colamarino S.A., Lein E.S., Courchesne E. Patches of disorganization in the neocortex of children with autism. N. Engl. J. Med. 2014, 370:1209-1219.
Tabata H., Nakajima K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 2003, 23:9996-10001.
Wegiel J., Kuchna I., Nowicki K., Imaki H., Wegiel J., Marchi E., Ma S.Y., Chauhan A., Chauhan V., Bobrowicz T.W., et al. The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol. 2010, 119:755-770.
Zinoviev A., Hellen C.U., Pestova T.V. Multiple mechanisms of reinitiation on bicistronic calicivirus mRNAs. Mol. Cell 2015, 57:1059-1073.