14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome - PubMed (original) (raw)
Aki Shionoya, Michael J Gambello, Carlos Cardoso, Richard Leventer, Heather L Ward, Ramses Ayala, Li-Huei Tsai, William Dobyns, David Ledbetter, Shinji Hirotsune, Anthony Wynshaw-Boris
Affiliations
- PMID: 12796778
- DOI: 10.1038/ng1169
14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome
Kazuhito Toyo-oka et al. Nat Genet. 2003 Jul.
Abstract
Heterozygous deletions of 17p13.3 result in the human neuronal migration disorders isolated lissencephaly sequence (ILS) and the more severe Miller-Dieker syndrome (MDS). Mutations in PAFAH1B1 (the gene encoding LIS1) are responsible for ILS and contribute to MDS, but the genetic causes of the greater severity of MDS are unknown. Here, we show that the gene encoding 14-3-3epsilon (YWHAE), one of a family of ubiquitous phosphoserine/threonine-binding proteins, is always deleted in individuals with MDS. Mice deficient in Ywhae have defects in brain development and neuronal migration, similar to defects observed in mice heterozygous with respect to Pafah1b1. Mice heterozygous with respect to both genes have more severe migration defects than single heterozygotes. 14-3-3epsilon binds to CDK5/p35-phosphorylated NUDEL and this binding maintains NUDEL phosphorylation. Similar to LIS1, deficiency of 14-3-3epsilon results in mislocalization of NUDEL and LIS1, consistent with reduction of cytoplasmic dynein function. These results establish a crucial role for 14-3-3epsilon in neuronal development by sustaining the effects of CDK5 phosphorylation and provide a molecular explanation for the differences in severity of human neuronal migration defects with 17p13.3 deletions.
Similar articles
- Lissencephaly and LIS1: insights into the molecular mechanisms of neuronal migration and development.
Wynshaw-Boris A. Wynshaw-Boris A. Clin Genet. 2007 Oct;72(4):296-304. doi: 10.1111/j.1399-0004.2007.00888.x. Clin Genet. 2007. PMID: 17850624 Review. - A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system.
Sasaki S, Shionoya A, Ishida M, Gambello MJ, Yingling J, Wynshaw-Boris A, Hirotsune S. Sasaki S, et al. Neuron. 2000 Dec;28(3):681-96. doi: 10.1016/s0896-6273(00)00146-x. Neuron. 2000. PMID: 11163259 - Responsible Genes for Neuronal Migration in the Chromosome 17p13.3: Beyond Pafah1b1(Lis1), Crk and Ywhae(14-3-3ε).
Liu X, Bennison SA, Robinson L, Toyo-Oka K. Liu X, et al. Brain Sci. 2021 Dec 30;12(1):56. doi: 10.3390/brainsci12010056. Brain Sci. 2021. PMID: 35053800 Free PMC article. Review. - NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein.
Niethammer M, Smith DS, Ayala R, Peng J, Ko J, Lee MS, Morabito M, Tsai LH. Niethammer M, et al. Neuron. 2000 Dec;28(3):697-711. doi: 10.1016/s0896-6273(00)00147-1. Neuron. 2000. PMID: 11163260 - Microdeletions including YWHAE in the Miller-Dieker syndrome region on chromosome 17p13.3 result in facial dysmorphisms, growth restriction, and cognitive impairment.
Nagamani SC, Zhang F, Shchelochkov OA, Bi W, Ou Z, Scaglia F, Probst FJ, Shinawi M, Eng C, Hunter JV, Sparagana S, Lagoe E, Fong CT, Pearson M, Doco-Fenzy M, Landais E, Mozelle M, Chinault AC, Patel A, Bacino CA, Sahoo T, Kang SH, Cheung SW, Lupski JR, Stankiewicz P. Nagamani SC, et al. J Med Genet. 2009 Dec;46(12):825-33. doi: 10.1136/jmg.2009.067637. Epub 2009 Jul 6. J Med Genet. 2009. PMID: 19584063
Cited by
- Epistatic and gene wide effects in YWHA and aromatic amino hydroxylase genes across ADHD and other common neuropsychiatric disorders: Association with YWHAE.
Jacobsen KK, Kleppe R, Johansson S, Zayats T, Haavik J. Jacobsen KK, et al. Am J Med Genet B Neuropsychiatr Genet. 2015 Sep;168(6):423-432. doi: 10.1002/ajmg.b.32339. Epub 2015 Jul 14. Am J Med Genet B Neuropsychiatr Genet. 2015. PMID: 26172220 Free PMC article. - YWHA (14-3-3) protein isoforms and their interactions with CDC25B phosphatase in mouse oogenesis and oocyte maturation.
Eisa AA, De S, Detwiler A, Gilker E, Ignatious AC, Vijayaraghavan S, Kline D. Eisa AA, et al. BMC Dev Biol. 2019 Oct 22;19(1):20. doi: 10.1186/s12861-019-0200-1. BMC Dev Biol. 2019. PMID: 31640562 Free PMC article. - 14-3-3 protein regulation of excitation-contraction coupling.
Thompson WC, Goldspink PH. Thompson WC, et al. Pflugers Arch. 2022 Mar;474(3):267-279. doi: 10.1007/s00424-021-02635-x. Epub 2021 Nov 25. Pflugers Arch. 2022. PMID: 34820713 Free PMC article. Review. - LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein.
Yamada M, Toba S, Yoshida Y, Haratani K, Mori D, Yano Y, Mimori-Kiyosue Y, Nakamura T, Itoh K, Fushiki S, Setou M, Wynshaw-Boris A, Torisawa T, Toyoshima YY, Hirotsune S. Yamada M, et al. EMBO J. 2008 Oct 8;27(19):2471-83. doi: 10.1038/emboj.2008.182. Epub 2008 Sep 11. EMBO J. 2008. PMID: 18784752 Free PMC article. - Comparative Genomic Mapping Implicates LRRK2 for Intellectual Disability and Autism at 12q12, and HDHD1, as Well as PNPLA4, for X-Linked Intellectual Disability at Xp22.31.
Labonne JDJ, Driessen TM, Harris ME, Kong IK, Brakta S, Theisen J, Sangare M, Layman LC, Kim CH, Lim J, Kim HG. Labonne JDJ, et al. J Clin Med. 2020 Jan 19;9(1):274. doi: 10.3390/jcm9010274. J Clin Med. 2020. PMID: 31963867 Free PMC article.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical
Molecular Biology Databases
Research Materials
Miscellaneous