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Cellular and Molecular Life Sciences

, Volume 74, Issue 7, pp 1191–1210 | Cite as

NDE1 and NDEL1 from genes to (mal)functions: parallel but distinct roles impacting on neurodevelopmental disorders and psychiatric illness

  • Nicholas J. BradshawEmail author
  • Mirian A. F. Hayashi
Review

Abstract

NDE1 (Nuclear Distribution Element 1, also known as NudE) and NDEL1 (NDE-Like 1, also known as NudEL) are the mammalian homologues of the fungus nudE gene, with important and at least partially overlapping roles for brain development. While a large number of studies describe the various properties and functions of these proteins, many do not directly compare the similarities and differences between NDE1 and NDEL1. Although sharing a high degree structural similarity and multiple common cellular roles, each protein presents several distinct features that justify their parallel but also unique functions. Notably both proteins have key binding partners in dynein, LIS1 and DISC1, which impact on neurodevelopmental and psychiatric illnesses. Both are implicated in schizophrenia through genetic and functional evidence, with NDE1 also strongly implicated in microcephaly, as well as other neurodevelopmental and psychiatric conditions through copy number variation, while NDEL1 possesses an oligopeptidase activity with a unique potential as a biomarker in schizophrenia. In this review, we aim to give a comprehensive overview of the various cellular roles of these proteins in a “bottom-up” manner, from their biochemistry and protein–protein interactions on the molecular level, up to the consequences for neuronal differentiation, and ultimately to their importance for correct cortical development, with direct consequences for the pathophysiology of neurodevelopmental and mental illness.

Keywords

Dynein Microtubules Neurodevelopment Neuron differentiation Oligopeptidase activity Schizophrenia 

Notes

Acknowledgments

NJB was supported by the Forschungskommission der Medizinischen Fakultät der Heinrich-Heine-Universität Düsseldorf (9772547) and the Fritz Thyssen Stiftung (10.14.2.140). MAFH was supported by the Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq, 477760/2010-4; 557753/2010-4; 508113/2010-5; 311815/2012-0; 475739/2013-2).

References

  1. 1.
    Feng Y, Walsh CA (2004) Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44:279–293PubMedCrossRefGoogle Scholar
  2. 2.
    Shu T, Ayala R, Nguyen M-D, Xie Z, Gleeson JG, Tsai L-H (2004) Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron 44:263–277PubMedCrossRefGoogle Scholar
  3. 3.
    Ingason A, Rujescu D, Cichon S et al (2011) Copy number variations of chromosome 16p13.1 region associated with schizophrenia. Mol Psychiatry 16:17–25PubMedCrossRefGoogle Scholar
  4. 4.
    Malhotra D, Sebat J (2012) CNVs: harbingers of a rare variant revolution in psychiatric genetics. Cell 148:1223–1241PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Rees E, Walters JTR, Georgieva L et al (2014) Analysis of copy number variations at 15 schizophrenia-associated loci. Br J Psychiatry 204:108–114PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Grozeva D, Conrad DF, Barnes CP et al (2012) Independent estimation of the frequency of rare CNVs in the UK population confirms their role in schizophrenia. Schizophr Res 135:1–7PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Johnstone M, Maclean A, Heyrman L et al (2015) Copy number variations in DISC1 and DISC1-interacting partners in major mental illness. Mol Neuropsychiatry 1:175–190PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Sahoo T, Theisen A, Rosenfeld JA et al (2011) Copy number variants of schizophrenia susceptibility loci are associated with a spectrum of speech and developmental delays and behavior problems. Genet Med 13:868–880PubMedCrossRefGoogle Scholar
  9. 9.
    Alkuraya FS, Cai X, Emery C et al (2011) Human mutations in NDE1 cause extreme microcephaly with lissencephaly. Am J Hum Genet 88:536–547PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Bakircioglu M, Carvalho OP, Khurshid M et al (2011) The essential role of centrosomal NDE1 in human cerebral cortex neurogenesis. Am J Hum Genet 88:523–535PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Guven A, Gunduz A, Bozoglu T, Yalcinkaya C, Tolun A (2012) Novel NDE1 homozygous mutation resulting in microhydranencephaly and not microlyssencephaly. Neurogenetics 13:189–194PubMedCrossRefGoogle Scholar
  12. 12.
    Paciorkowski AR, Keppler-Noreuil K, Robinson L et al (2013) Deletion 16p13.11 uncovers NDE1 mutations on the non-deleted homolog and extends the spectrum of severe microcephaly to include fetal brain disruption. Am J Med Genet 161A:1523–1530PubMedCrossRefGoogle Scholar
  13. 13.
    Hennah W, Tomppo L, Hiekkalinna T et al (2007) Families with the risk allele of DISC1 reveal a link between schizophrenia and another component of the same molecular pathway, NDE1. Hum Mol Genet 6:453–462CrossRefGoogle Scholar
  14. 14.
    Burdick KE, Kamiya A, Hodgkinson CA et al (2008) Elucidating the relationship between DISC1, NDEL1, and NDE1 and the risk for schizophrenia: evidence of epistasis and competitive binding. Hum Mol Genet 17:2462–2473PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Tomppo L, Hennah W, Lahermo P et al (2009) Association between genes of Disrupted in Schizophrenia 1 (DISC1) interactors and schizophrenia supports the role of the DISC1 pathway in the etiology of major mental illnesses. Biol Psychiatry 65:1055–1062PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Nicodemus KK, Callicott JH, Higier RG et al (2010) Evidence of statistical epistasis between DISC1, CIT and NDEL1 impacting risk for schizophrenia: biological validation with functional neuroimaging. Hum Genet 127:441–452PubMedCrossRefGoogle Scholar
  17. 17.
    Kimura H, Tsuboi D, Wang C et al (2014) Identification of rare, single-nucleotide mutations in NDE1 and their contributions to schizophrenia susceptibility. Schizophr Bull 41:744–753PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Rocha e Silva M, Beraldo WT, Rosenfeld G (1949) Bradykinin, a hypotensive and smooth muscle stimulating factor released from plasma globulin by snake venoms and by trypsin. Am J Physiol 156:261–273PubMedGoogle Scholar
  19. 19.
    Tanabe A, Shiraishi M, Negishi M, Saito N, Tanabe M, Sasaki Y (2012) MARCKS dephosphorylation is involved in bradykinin-induced neurite outgrowth in neuroblastoma SH-SY5Y cells. J Cell Physiol 227:618–629PubMedCrossRefGoogle Scholar
  20. 20.
    Lu Z, Cui M, Zhao H, Wang T, Shen Y, Dong Q (2014) Tissue kallikrein mediates neurite outgrowth through epidermal growth factor receptor and flotillin-2 pathway in vitro. Cell Signal 26:220–232PubMedCrossRefGoogle Scholar
  21. 21.
    Huang D, Liang C, Zhang F et al (2016) Inflammatory mediator bradykinin increases population of sensory neurons expressing functional T-type Ca2+ channels. Biochem Biophys Res Commun 473:396–402PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Camargo ACM, Caldo H, Emson PC (1983) Degradation of neurotensin by rabbit brain endo-oligopeptidase A and endo-oligopeptidase B (proline-endopeptidase). Biochem Biophys Res Commun 116:1151–1159PubMedCrossRefGoogle Scholar
  23. 23.
    Oliveira EB, Martins AR, Camargo ACM (1976) Isolation of brain endopeptidases: influence of size and sequence of substrates structurally related to bradykinin. Biochemistry 15:1967–1974PubMedCrossRefGoogle Scholar
  24. 24.
    Morris NR (1978) Mitotic mutants of Aspergillus nidulans. Genet Res 26:237–254CrossRefGoogle Scholar
  25. 25.
    Oakley BR, Morris NR (1980) Nuclear movement is β-tubulin-dependent in Aspergillus nidulans. Cell 19:255–262PubMedCrossRefGoogle Scholar
  26. 26.
    Xiang X, Beckwith SM, Morris NR (1994) Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc Natl Acad Sci USA 91:2100–2104PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Xiang X, Osmani AH, Osmani SA, Xin M, Morris NR (1995) NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol Biol Cell 6:297–310PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Reiner O, Carrozzo R, Shen Y et al (1993) Isolation of a Miller–Dicker lissencephaly gene containing G protein β-subunit-like repeats. Nature 364:717–721PubMedCrossRefGoogle Scholar
  29. 29.
    Efimov VP, Morris NR (2000) The LIS1-related NUDF protein of Aspergillus nidulans interacts with the coiled-coil domain of the NUDE/RO11 protein. J Cell Biol 150:681–688PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Stukenberg PT, Lustig KD, McGarry TJ, King RW, Kuang J, Kirschner MW (1997) Systematic identification of mitotic phosphoproteins. Curr Biol 7:338–348PubMedCrossRefGoogle Scholar
  31. 31.
    Minke PF, Lee IH, Tinsley JH, Bruno KS, Plamann M (1999) Neurospora crassa ro-10 and ro-11 genes encode novel proteins required for nuclear distribution. Mol Microbiol 32:1065–1076PubMedCrossRefGoogle Scholar
  32. 32.
    Feng Y, Olson EC, Stukenberg PT, Flanagan LA, Kirschner MW, Walsh CA (2000) LIS1 regulates CNS lamination by interacting with mNudE, a central component of the centrosome. Neuron 28:665–679PubMedCrossRefGoogle Scholar
  33. 33.
    Kitagawa M, Umezu M, Aoki J, Koizumi H, Arai H, Inoue K (2000) Direct association of LIS1, the lissencephaly gene product, with a mammalian homologue of a fungal nuclear distribution protein, rNUDE. FEBS Lett 479:57–62PubMedCrossRefGoogle Scholar
  34. 34.
    Niethammer M, Smith DS, Ayala R et al (2000) NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28:697–711PubMedCrossRefGoogle Scholar
  35. 35.
    Sasaki S, Shionoya A, Ishida M et al (2000) A LIS1/NUDEL/cytoplasmic dyenin heavy chain complex in the developing and adult nervous system. Neuron 28:681–696PubMedCrossRefGoogle Scholar
  36. 36.
    St Clair D, Blackwood D, Muir W et al (1990) Association within a family of a balanced autosomal translocation with major mental illness. Lancet 336:13–16PubMedCrossRefGoogle Scholar
  37. 37.
    Millar JK, Wilson-Annan JC, Anderson S et al (2000) Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum Mol Genet 9:1415–1425PubMedCrossRefGoogle Scholar
  38. 38.
    Blackwood DHR, Fordyce A, Walker MT, St. Clair DM, Porteous DJ, Muir WJ (2001) Schizophrenia and affective disorders - Cosegregation with a translocation at chromosome 1q42 that directly disrupts brain-expressed genes: clinical and P300 findings in a family. Am J Hum Genet 69:428–433PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Millar JK, Christie S, Porteous DJ (2003) Yeast two-hybrid screens implicate DISC1 in brain development and function. Biochem Biophys Res Commun 311:1019–1025PubMedCrossRefGoogle Scholar
  40. 40.
    Morris JA, Kandpal G, Ma L, Austin CP (2003) DISC1 (Disrupted-In-Schizophrenia 1) is a centrosome-associated protein that interacts with MAP1A, MIPT3, ATF4/5 and NUDEL: regulation and loss of interaction with mutation. Hum Mol Genet 12:1591–1608PubMedCrossRefGoogle Scholar
  41. 41.
    Ozeki Y, Tomoda T, Kleiderlein J et al (2003) Disrupted-in-Schizophrenia-1 (DISC-1): mutant truncation prevents binding to NudE-like (NUDEL) and inhibits neurite outgrowth. Proc Natl Acad Sci USA 100:289–294PubMedCrossRefGoogle Scholar
  42. 42.
    Sweeney KJ, Prokscha A, Eichele G (2001) NudE-L, a novel Lis1-interacting protein, belongs to a family of vertebrate coiled-coil proteins. Mech Dev 101:21–33PubMedCrossRefGoogle Scholar
  43. 43.
    Hayashi MAF, Portaro FCV, Bastos MF et al (2005) Inhibition of NUDEL (nuclear distribution element-like)-oligopeptidase activity by disrupted-in-schizophrenia 1. Proc Natl Acad Sci USA 102:3828–3833PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Shmueli A, Segal M, Sapir T et al (2010) Ndel1 palmitoylation: a new mean to regulate cytoplasmic dynein activity. EMBO J 29:107–119PubMedCrossRefGoogle Scholar
  45. 45.
    McLysaght A, Makino T, Grayton HM et al (2013) Ohnologs are overrepresented in pathogenic copy number mutations. Proc Natl Acad Sci USA 111:361–366PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Bradshaw NJ, Hennah W, Soares DC (2013) NDE1 and NDEL1: twin neurodevelopmental proteins with similar ‘nature’ but different ‘nurture’. Biomol Concepts 4:447–464PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Drerup CM, Ahlgren SC, Morris JA (2007) Expression profiles of ndel1a and ndel1b, two orthologs of the NudE-Like gene, in the zebrafish. Gene Expr Patterns 76:672–679CrossRefGoogle Scholar
  48. 48.
    Guerreiro JR, Winnischofer SMB, Bastos MF et al (2005) Cloning and characterization of the human and rabbit NUDEL-oligopeptidase promoters and their negative regulation. Biochim Biophys Acta 1730:77–84PubMedCrossRefGoogle Scholar
  49. 49.
    Bradshaw NJ, Christie S, Soares DC, Carlyle BC, Porteous DJ, Millar JK (2009) NDE1 and NDEL1: multimerisation, alternate splicing and DISC1 interaction. Neurosci Lett 449:228–233PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Bradshaw NJ (2016) Cloning of the promoter of NDE1, a gene implicated in psychiatric and neurodevelopmental disorders through copy number variation. Neuroscience 324:262–270PubMedCrossRefGoogle Scholar
  51. 51.
    Yan CYI, Vieceli FM, Kanno TY, Turri JAO, Hayashi MAF (2012) Gene expression in embryonic neural development and stem cell differentiation. In: Sato K-I (ed) Embryogenesis. InTech, RijekaGoogle Scholar
  52. 52.
    Hayashi MAF, Guerreiro JR, Cassola AC et al (2010) Long-term culture of mouse embryonic stem cell-derived adherent neurospheres and functional neurons. Tissue Eng Part C Methods 16:1493–1502PubMedCrossRefGoogle Scholar
  53. 53.
    Kerkis I, Hayashi MAF, Lizier NF, Cassola AC, Pereira LV, Kerkis A (2011) Pluripotent stem cells as an in vitro model of neuronal differentiation. In: Kallos MS (ed) Embryonic stem cells—differentiation and pluripotent alternatives. InTech, ViennaGoogle Scholar
  54. 54.
    Hayashi MAF, Pires RS, Reboucas NA, Britto LRG, Camargo ACM (2001) Expression of endo-oligopeptidase A in the rat central nervous system: a non-radioactive in situ hybridization study. Mol Brain Res 89:86–93PubMedCrossRefGoogle Scholar
  55. 55.
    Oliveira ES, Leite PEP, Spillantini MG, Camargo ACM, Hunt SP (1990) Localization of endo-oligopeptidase (EC 3.4.22.19) in the rat nervous tissue. J Neurochem 55:1114–1121PubMedCrossRefGoogle Scholar
  56. 56.
    Pei Z, Lang B, Fragoso YD et al (2014) The expression and roles of Nde1 and Ndel1 in the adult mammalian central nervous system. Neuroscience 271:119–136PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Larney C, Bailey TL, Koopman P (2014) Switching on sex: transcriptional regulation of the testis-determining gene Sry. Development 141:2195–2205PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Yamaguchi N, Takanezawa Y, Koizumi H, Umezu-Goto M, Aoki J, Arai H (2004) Expression of NUDEL in manchette and its implication in spermatogenesis. FEBS Lett 566:71–76PubMedCrossRefGoogle Scholar
  59. 59.
    Ding C, Liang X, Ma L, Yuan X, Zhu X (2009) Opposing effects of Ndel1 and α1 or α2 on cytoplasmic dynein through competitive binding to Lis1. J Cell Sci 122:2820–2827PubMedCrossRefGoogle Scholar
  60. 60.
    Dewing P, Chiang CWK, Sinchak K et al (2006) Direct regulation of adult brain function by the male-specific factor SRY. Curr Biol 16:415–420PubMedCrossRefGoogle Scholar
  61. 61.
    Czech DP, Lee J, Sim H, Parish CL, Vilain E, Harley VR (2012) The human testis-determining factor SRY localizes in midbrain dopamine neurons and regulates multiple components of catecholamine synthesis and metabolism. J Neurochem 122:260–271PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Choi Y-S, Lee B, Hansen K et al (2016) Status epilepticus stimulates NDEL1 expression via the CREB/CRE pathway in the adult mouse brain. Neuroscience 331:1–12PubMedCrossRefGoogle Scholar
  63. 63.
    Kandel ER (2012) The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol Brain 5:14PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Millar JK, Pickard BS, Mackie S et al (2005) DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signalling. Science 310:1187–1191PubMedCrossRefGoogle Scholar
  65. 65.
    Bradshaw NJ, Ogawa F, Antolin-Fontes B et al (2008) DISC1, PDE4B, and NDE1 at the centrosome and synapse. Biochem Biophys Res Commun 377:1091–1096PubMedCrossRefGoogle Scholar
  66. 66.
    Collins DM, Murdoch H, Dunlop AJ et al (2008) Ndel1 alters its conformation by sequestering cAMP-specific phosphodiesterase-4D3 (PDE4D3) in a manner that is dynamically regulated through Protein Kinase A (PKA). Cell Signal 20:2356–2369PubMedCrossRefGoogle Scholar
  67. 67.
    Tarricone C, Perrina F, Monzani S et al (2004) Coupling PAF signaling to dynein regulation: structure of LIS1 in complex with PAF-acetylhydrolase. Neuron 44:809–821PubMedGoogle Scholar
  68. 68.
    McKenney RJ, Vershinin M, Kunwar A, Vallee RB, Gross SP (2010) LIS1 and NudE induce a persistent dynein force-producing state. Cell 141:304–314PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Narayanan S, Arthanari H, Wolfe MS, Wagner G (2011) Molecular characterization of disrupted in schizophrenia-1 risk variant S704C reveals the formation of altered oligomeric assembly. J Biol Chem 286:44266–44276PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Nyarko A, Song Y, Barbar E (2012) Intrinsic disorder in dynein intermediate chain modulates its interactions with NudE and dynactin. J Biol Chem 287:24884–24893PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Soares DC, Bradshaw NJ, Zou J et al (2012) The mitosis and neurodevelopment proteins NDE1 and NDEL1 form dimers, tetramers, and polymers with a folded back structure in solution. J Biol Chem 287:32381–32393PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Yerabham ASK, Weiergräber OH, Bradshaw NJ, Korth C (2013) Revisiting disrupted in schizophrenia 1 as a scaffold protein. Biol Chem 394:1425–1437PubMedCrossRefGoogle Scholar
  73. 73.
    Carvalho KM, Camargo ACM (1981) Purification of rabbit brain endooligopeptidases and preparation of anti-enzyme antibodies. Biochemistry 20:7082–7088PubMedCrossRefGoogle Scholar
  74. 74.
    Andrews PC, Minth CD, Dixon JE (1982) Immunochemical characterization of a proline endopeptidase from rat brain. Its relationship to proline endopeptidase from other tissues and from other species. J Biol Chem 257:5861–5865PubMedGoogle Scholar
  75. 75.
    Camargo AC, Caldo H, Reis ML (1979) Susceptibility of a peptide derived from bradykinin to hydrolysis by brain eno-oligopeptidases and pancreatic proteinases. J Biol Chem 254:5304–5307PubMedGoogle Scholar
  76. 76.
    de Camargo AC, da Fonseca MJ, Caldo H, de Morais Carvalho K (1982) Influence of the carboxyl terminus of luteinizing hormone-releasing hormone and bradykinin on hydrolysis by brain endo-oligopeptidases. J Biol Chem 257:9265–9267Google Scholar
  77. 77.
    Penttinen A, Tenorio-Laranga J, Siikanen A, Morawski M, Roner S, Garcia-Horsman JA (2011) Prolyl oligopeptidase: a rising star on the stage of neuroinflammation research. CNS Neurol Disord Drug Targets 10:340–348PubMedCrossRefGoogle Scholar
  78. 78.
    Männistö PT, Venäläinen J, Jalkanen A, García-Horsman JA (2007) Prolyl oligopeptidase: a potential target for the treatment of cognitive disorders. Drug News Perspect 20:293PubMedCrossRefGoogle Scholar
  79. 79.
    Deng J, Lamb JR, Mckeown AP et al (2013) Identification of altered dipeptidyl-peptidase activities as potential biomarkers for unipolar depression. J Affect Disorders 151:667–672PubMedCrossRefGoogle Scholar
  80. 80.
    Williams RSB, Eames M, Ryves WJ, Viggars J, Harwood AJ (1999) Loss of a prolyl oligopeptidase confers resistance to lithium by elevation of inositol (1,4,5) trisphosphate. EMBO J 18:2734–2745PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Kinkead B, Nemeroff CB (2002) Neurotensin: an endogenous antipsychotic? Curr Opin Pharmacol 2:99–103PubMedCrossRefGoogle Scholar
  82. 82.
    Cáceda R, Kinkead B, Nemeroff CB (2006) Neurotensin: role in psychiatric and neurological diseases. Peptides 27:2385–2404PubMedCrossRefGoogle Scholar
  83. 83.
    Boules M, Shaw A, Fredrickson P, Richelson E (2007) Neurotensin agonists: potential in the treatment of schizophrenia. CNS Drugs 21:13–23PubMedCrossRefGoogle Scholar
  84. 84.
    Kost NV, Meshavkin VK, Khashaba EY et al (2014) Neurotensin-like peptides as potential antipsychotics: modulation of the serotonin system. Bull Exp Biol Med 157:738–741PubMedCrossRefGoogle Scholar
  85. 85.
    Jacchieri SG, Gomes MD, Juliano L, Camargo ACM (1998) A comparative conformational analysis of thimet oligopeptidase (EC 3.4.24.15) substrates. J Peptide Res 51:452–459CrossRefGoogle Scholar
  86. 86.
    Hayashi MAF, Felicori LF, Fresqui MAC, Yonamine CM (2015) Protein-protein and peptide-protein interactions of NudE-like 1 (Ndel1): a protein involved in schizophrenia. Curr Protein Pept Sci 16:754–767PubMedCrossRefGoogle Scholar
  87. 87.
    Schechter I, Berger A (1968) On the active site of proteases. III. Mapping the active site of papain; specific peptide inhibitors of papain. Biochem Biophys Res Commun 32:898–902PubMedCrossRefGoogle Scholar
  88. 88.
    Szeltner Z, Juhász T, Szamosi I et al (2013) The loops facing the active site of prolyl oligopeptidase are crucial components in substrate gating and specificity. Biochim Biophys Acta 1834:98–111PubMedCrossRefGoogle Scholar
  89. 89.
    Kaszuba K, Róg T, Danne R et al (2012) Molecular dynamics, crystallography and mutagenesis studies on the substrate gating mechanism of prolyl oligopeptidase. Biochimie 94:1398–1411PubMedCrossRefGoogle Scholar
  90. 90.
    Camargo ACM, Gomes MD, Toffoletto O et al (1994) Structural requirements of bioactive peptides for interaction with endopeptidase 22.19. Neuropeptides 26:281–287PubMedCrossRefGoogle Scholar
  91. 91.
    Camargo ACM, Almeida MLC, Emson PC (1984) Involvement of endo-oligopeptidases A and B in the degradation of neurotensin by rabbit brain. J Neurochem 42:1758–1761PubMedCrossRefGoogle Scholar
  92. 92.
    Toffoletto O, Camargo ACM, Oliveira EB, Metters KM, Rossier J (1988) Liberation of enkephalins from enkephalin-containing peptides by brain endo-oligopeptidase A. Biochimie 70:47–56PubMedCrossRefGoogle Scholar
  93. 93.
    Derewenda U, Tarricone C, Choi WC et al (2007) The structure of the coiled-coil domain of Ndel1 and the basis of its interaction with Lis1, the causal protein of Miller–Dieker lissencephaly. Structure 15:1467–1481PubMedCrossRefGoogle Scholar
  94. 94.
    Wang S, Zheng Y (2011) Identification of a novel dynein-binding domain in Nudel essential for spindle pole organization in Xenopus egg extracts. J Biol Chem 286:587–593PubMedCrossRefGoogle Scholar
  95. 95.
    Żyłkiewicz E, Kijańska M, Choi W-C, Derewenda U, Derewenda ZS, Stukenberg PT (2011) The N-terminal coiled-coil of Ndel1 is a regulated scaffold that recruits LIS1 to dynein. J Cell Biol 192:433–445PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Torisawa T, Nakayama A, Ky Furuta, Yamada M, Hirotsune S, Toyoshima YY (2011) Functional dissection of LIS1 and NDEL1 towards understanding the molecular mechanism of cytoplasmic dynein regulation. J Biol Chem 286:1959–1965PubMedCrossRefGoogle Scholar
  97. 97.
    McKenney RJ, Weil SJ, Scherer J, Vallee RB (2011) Mutually exclusive cytoplasmic dynein regulation by NudE-LIS1 and dynactin. J Biol Chem 286:39615–39622PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Yan X, Li F, Liang Y et al (2003) Human Nudel and NudE as regulators of cytoplasmic dynein in poleward protein transport along the mitotic spindle. Mol Cell Biol 23:1239–1250PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Hebbar S, Mesngon MT, Guillotte AM, Desai B, Ayala R, Smith DS (2008) Lis1 and Ndel1 influence the timing of nuclear envelope breakdown in neural stem cells. J Cell Biol 182:1063–1071PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Bradshaw NJ, Soares DC, Carlyle BC et al (2011) PKA phosphorylation of NDE1 is DISC1/PDE4 dependent and modulates its interaction with LIS1 and NDEL1. J Neurosci 31:9043–9054PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Pandey JP, Smith DS (2011) A Cdk5-dependent switch regulates Lis1/Ndel1/dynein-driven organelle transport in adult axons. J Neurosci 31:17207–17219PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Gao FJ, Hebbar S, Gao XA et al (2015) GSK-3β phosphorylation of cytoplasmic dynein reduces Ndel1 binding to intermediate chains and alters dynein motility. Traffic 16:941–961PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Kikkawa M (2013) Big steps toward understanding dynein. J Cell Biol 202:15–23PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Cianfrocco MA, DeSantis ME, Leschziner AE, Reck-Peterson SL (2015) Mechanism and regulation of cytoplasmic dynein. Annu Rev Cell Dev Biol 31:83–108PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Yamada M, Toba S, Yoshida Y et al (2008) LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein. EMBO J 27:2471–2483PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Huang J, Roberts AJ, Leschziner AE, Reck-Peterson SL (2012) Lis1 acts as a “clutch” between the ATPase and microtubule-binding domains of the dynein motor. Cell 150:975–986PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Toropova K, Zou S, Roberts AJ et al (2014) Lis1 regulates dynein by sterically blocking its mechanochemical cycle. eLife 3:e03372PubMedCentralCrossRefGoogle Scholar
  108. 108.
    Toba S, Koyasako K, Yasunaga T, Hirotsune S (2015) Lis1 restricts the conformational changes in cytoplasmic dynein on microtubules. Microscopy (Oxford) 64:419–427CrossRefGoogle Scholar
  109. 109.
    Liang Y, Yu W, Li Y et al (2004) Nudel functions in membrane traffic mainly through association with Lis1 and cytoplasmic dynein. J Cell Biol 164:557–566PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Zhang Q, Wang F, Cao J et al (2009) Nudel promotes axonal lysosome clearance and endo-lysosome formation via dynein-mediated transport. Traffic 10:1337–1349PubMedCrossRefGoogle Scholar
  111. 111.
    Lam C, Vergnolle MAS, Thorpe L, Woodman PG, Allan VJ (2010) Functional interplay between LIS1, NDE1 and NDEL1 in dynein-dependent organelle positioning. J Cell Sci 123:202–212PubMedCrossRefGoogle Scholar
  112. 112.
    Sasaki S, Mori D, Toyo-oka K et al (2005) Complete loss of Ndel1 results in neuronal migration defects and early embryonic lethality. Mol Cell Biol 25:7812–7827PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165:709–721PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Shen Y, Li N, Wu S et al (2008) Nudel binds Cdc42GAP to modulate Cdc42 activity at the leading edge of migrating cells. Dev Cell 14:342–353PubMedCrossRefGoogle Scholar
  115. 115.
    Shao C-Y, Zhu J, Xie Y-J et al (2013) Distinct functions of nuclear distribution proteins LIS1, Ndel1 and NudCL in regulating axonal mitochondrial transport. Traffic 14:785–797PubMedCrossRefGoogle Scholar
  116. 116.
    Ogawa F, Murphy LC, Malavasi ELV et al (2016) NDE1 and GSK3β associate with TRAK1 and regulate axonal mitochondrial motility: identification of cyclic AMP as a novel modulator of axonal mitochondrial trafficking. ACS Chem Neurosci 7:553–564PubMedCrossRefGoogle Scholar
  117. 117.
    Wan Y, Yang Z, Guo J et al (2012) Misfolded Gβ is recruited to cytoplasmic dynein by Nudel for efficient clearance. Cell Res 22:1140–1154PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Segal M, Soifer I, Petzold H, Howard J, Elbaum M, Reiner O (2012) Ndel1-derived peptides modulate bidirectional transport of injected beads in the squid giant axon. Biol Open 1:220–231PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Guo J, Yang Z, Song W et al (2006) Nudel contributes to microtubule anchoring at the mother centriole and is involved in both dynein-dependent and -independent centrosomal protein assembly. Mol Biol Cell 17:680–689PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Toyo-oka K, Sasaki S, Yano Y et al (2005) Recruitment of katanin p60 by phosphorylated NDEL1, an LIS1 interacting protein, is essential for mitotic cell division and neuronal migration. Hum Mol Genet 14:3113–3128PubMedCrossRefGoogle Scholar
  121. 121.
    Toyo-oka K, Mori D, Yano Y et al (2008) Protein phosphatase 4 catalytic subunit regulates Cdk1 activity and microtubule organization via NDEL1 dephosphorylation. J Cell Biol 180:1133–1147PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Mori D, Yamada M, Mimori-Kiyosue Y et al (2009) An essential role of the aPKC-Aurora A-NDEL1 pathway on neurite elongation by modulation of microtubule dynamics. Nat Cell Biol 11:1057–1068PubMedCrossRefGoogle Scholar
  123. 123.
    Takitoh T, Kumamoto K, Wang C-C et al (2012) Activation of Aurora-A is essential for neuronal migration via modulation of microtubule organization. J Neurosci 32:11050–11066PubMedCrossRefGoogle Scholar
  124. 124.
    Youn YH, Pramparo T, Hirotsune S, Wynshaw-Boris A (2009) Distinct dose-dependent cortical neuronal migration and neurite extension defects in Lis1 and Ndel1 mutant mice. J Neurosci 29:15520–15530PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Yingling J, Youn YH, Darling D et al (2008) Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132:474–486PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Nguyen MD, Shu T, Sanada K et al (2004) A NUDEL-dependent mechanism of neurofilament assembly regulates the integrity of CNS neurons. Nat Cell Biol 6:595–608PubMedCrossRefGoogle Scholar
  127. 127.
    Blizzard CA, King AE, Vickers J, Dickson T (2013) Cortical murine neurons lacking the neurofilament light chain protein have an attenuated response to injury in vitro. J Neurotrauma 30:1908–1918PubMedCrossRefGoogle Scholar
  128. 128.
    Shim SY, Samuels BA, Wang J et al (2008) Ndel1 controls the dynein-mediated transport of vimentin during neurite outgrowth. J Biol Chem 283:12232–12240PubMedCrossRefGoogle Scholar
  129. 129.
    Wu S, Ma L, Wu Y, Zeng R, Zhu X (2012) Nudel is crucial for the WAVE complex assembly in vivo by selectively promoting subcomplex stability and formation through direct interactions. Cell Res 22:1270–1284PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Pawlisz AS, Feng Y (2011) Three-dimensional regulation of radial glial functions by Lis1-Nde1 and dystrophin glycoprotein complexes. PLoS Biol 9:e1001172PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Shan Y, Yu L, Li Y et al (2009) Nudel and FAK as antagonizing strength modulators of nascent adhesions through paxillin. PLoS Biol 7:e1000116PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Hirohashi Y, Wang Q, Liu Q et al (2006) Centrosomal proteins Nde1 and Su48 form a complex regulated by phosphorylation. Oncogene 25:6048–6055PubMedCrossRefGoogle Scholar
  133. 133.
    Vergnolle MAS, Taylor SS (2007) Cenp-F links kinetochores to Ndel1/Nde1/Lis1/Dynein microtubule motor complexes. Curr Biol 17:1173–1179PubMedCrossRefGoogle Scholar
  134. 134.
    Liang Y, Yu W, Li Y et al (2007) Nudel modulates kinetochore association and function of cytoplasmic dynein in M phase. Mol Biol Cell 18:2656–2666PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Stehman SA, Chen Y, McKenney RJ, Vallee RB (2007) NudE and NudEL are required for mitotic progression and are involved in dynein recruitment to kinetochores. J Cell Biol 178:583–594PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Bolhy S, Bouhlel I, Dultz E et al (2011) A Nup133-dependent NPC-anchored network tethers centrosomes to the nuclear envelope in prophase. J Cell Biol 192:855–871PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Raaijmakers JA, Tanenbaum ME, Medema RH (2013) Systematic dissection of dynein regulators in mitosis. J Cell Biol 201:201–215PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Salina D, Bodoor K, Eckley DM, Schroer TA, Rattner JB, Burke B (2002) Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108:97–107PubMedCrossRefGoogle Scholar
  139. 139.
    Turgay Y, Champion L, Balazs C et al (2014) SUN proteins facilitate the removal of membranes from chromatin during nuclear envelope breakdown. J Cell Biol 204:1099–1109PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Tsai M-Y, Wang S, Heidinger JM et al (2006) A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 311:1887–1893PubMedCrossRefGoogle Scholar
  141. 141.
    Kuga T, Nie H, Kazami T et al (2014) Lamin B2 prevents chromosome instability by ensuring proper mitotic chromosome segregation. Oncogenesis 3:e94PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Ma L, Tsai M-Y, Wang S et al (2009) Requirement for Nudel and dynein for assembly of the lamin B spindle matrix. Nat Cell Biol 11:247–256PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Wang Y, Jin F, Higgins R, McKnight K (2014) The current view for the silencing of the spindle assembly checkpoint. Cell Cycle 13:1694–1701PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Howell BJ, McEwen BF, Canman JC et al (2001) Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J Cell Biol 155:1159–1172PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Mische S, He Y, Ma L, Li M, Serr M, Hays TS (2008) Dynein light intermediate chain: an essential subunit that contributes to spindle checkpoint inactivation. Mol Biol Cell 19:4918–4929PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Mori D, Yano Y, Toyo-oka K et al (2007) NDEL1 phosphorylation by Aurora-A Kinase is essential for centrosomal maturation, separation, and TACC3 recruitment. Mol Cell Biol 27:352–367PubMedCrossRefGoogle Scholar
  147. 147.
    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 79:254–265PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Kim S, Zaghloul NA, Bubenshchikova E et al (2011) Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat Cell Biol 13:351–360PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Maskey D, Marlin MC, Kim S et al (2015) Cell cycle-dependent ubiquitylation and destruction of NDE1 by CDK5-FBW7 regulates ciliary length. EMBO J 34:2424–2440PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Inaba H, Goto H, Kasahara K et al (2016) Ndel1 suppresses ciliogenesis in proliferating cells by regulating the trichoplein–Aurora A pathway. J Cell Biol 212:409–423PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Houlihan SL, Feng Y (2014) The scaffold protein Nde1 safeguards the brain genome during S phase of early neural progenitor differentiation. eLife 3:e03297PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Toth C, Shim SY, Wang J et al (2008) Ndel1 promotes axon regeneration via intermediate filaments. PLoS One 3:e2014PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Okamoto M, Iguchi T, Hattori T et al (2015) DBZ regulates cortical cell positioning and neurite development by sustaining the anterograde transport of Lis1 and DISC1 through control of Ndel1 dual-phosphorylation. J Neuosci 35:2942–2958CrossRefGoogle Scholar
  154. 154.
    Hayashi MAF, Guerreiro JR, Charych E et al (2010) Assessing the role of endooligopeptidase activity of Ndel1 (nuclear-distribution gene E homolog like-1) in neurite outgrowth. Mol Cell Neurosci 44:353–361PubMedCrossRefGoogle Scholar
  155. 155.
    Kamiya A, Tomoda T, Chang J et al (2006) DISC1-NDEL1/NUDEL protein interaction, an essential component for neurite outgrowth, is modulated by genetic variations of DISC1. Hum Mol Genet 15:3313–3323PubMedCrossRefGoogle Scholar
  156. 156.
    Saito A, Taniguchi Y, Kim S-H et al (2016) Developmental alcohol exposure impairs activity-dependent S-Nitrosylation of NDEL1 for neuronal maturation. Cereb Cortex. doi: 10.1093/cercor/bhw201 PubMedGoogle Scholar
  157. 157.
    Portaro FCV, Hayashi MAF, Silva CL, de Camargo ACM (2001) Free ATP inhibits thimet oligopeptidase (EC 3.4.24.15) activity, induces autophosphorylation in vitro, and controls oligopeptide degradation in macrophage. Eur J Biochem 268:887–894PubMedCrossRefGoogle Scholar
  158. 158.
    Pawlisz AS, Mutch C, Wynshaw-Boris A, Chenn A, Walsh CA, Feng Y (2008) Lis1-Nde1 dependent neuronal fate control determines cerebral cortical size and lamination. Hum Mol Genet 17:2441–2455PubMedPubMedCentralCrossRefGoogle Scholar
  159. 159.
    Hippenmeyer S, Youn YH, Moon HM et al (2010) Genetic mosaic dissection of Lis1 and Ndel1 in neuronal migration. Neuron 68:695–709PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Jiang Y, Gavrilovici C, Chansard M et al (2016) Ndel1 and Reelin maintain postnatal CA1 hippocampus integrity. J Neuosci 36:6538–6552CrossRefGoogle Scholar
  161. 161.
    Duan X, Chang JH, Ge S et al (2007) Disrupted-in-schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130:1146–1158PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Wu Q, Li Y, Shu Y et al (2014) NDEL1 was decreased in the CA3 region but increased in the hippocampal blood vessel network during the spontaneous seizure period after pilocarpine-induced status epilepticus. Neuroscience 268:276–283PubMedCrossRefGoogle Scholar
  163. 163.
    Rauch A, Thiel CT, Schindler D et al (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319:816–819PubMedCrossRefGoogle Scholar
  164. 164.
    Griffith E, Walker S, Martin C-A et al (2008) Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat Genet 40:232–236PubMedCrossRefGoogle Scholar
  165. 165.
    Willems M, Geneviève D, Borck G et al (2010) Molecular analysis of pericentrin gene (PCNT) in a series of 24 Seckel/microcephalic osteodysplastic primordial dwarfism type II (MOPD II) families. J Med Genet 47:797–802PubMedCrossRefGoogle Scholar
  166. 166.
    Belzil C, Asada N, K-i Ishiguro et al (2014) p600 regulates spindle orientation in apical neural progenitors and contributes to neurogenesis in the developing neocortex. Biol Open 3:475–485PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Gabriel E, Wason A, Ramani A et al (2016) CPAP promotes timely cilium disassembly to maintain neural progenitor pool. EMBO J 35:803–819PubMedPubMedCentralCrossRefGoogle Scholar
  168. 168.
    Tropeano M, Ahn JW, Dobson RJB et al (2013) Male-biased autosomal effect of 16p13.11 copy number variation in neurodevelopmental disorders. PLoS One 8:e61365PubMedPubMedCentralCrossRefGoogle Scholar
  169. 169.
    Cooper GM, Coe BP, Girirajan S et al (2011) A copy number variation morbidity map of developmental delay. Nat Genet 43:838–846PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Hannes FD, Sharp AJ, Mefford HC et al (2009) Recurrent reciprocal deletions and duplications of 16p13.11: the deletion is a risk factor for MR/MCA while the duplication may be a rare benign variant. J Med Genet 46:223–232PubMedCrossRefGoogle Scholar
  171. 171.
    Nagamani SCS, Erez A, Bader P et al (2011) Phenotypic manifestations of copy number variation in chromosome 16p13.11. Eur J Hum Genet 19:280–286PubMedCrossRefGoogle Scholar
  172. 172.
    Ramalingam A, Zhou X-G, Fiedler SD et al (2011) 16p13.11 duplication is a risk factor for a wide spectrum of neuropsychiatric disorders. J Hum Genet 56:541–544PubMedCrossRefGoogle Scholar
  173. 173.
    Mefford HC, Muhle H, Ostertag P et al (2010) Genome-wide copy number variation in epilepsy: novel susceptibility loci in idiopathic generalized and focal epilepsies. PLoS Genet 6:e1000962PubMedPubMedCentralCrossRefGoogle Scholar
  174. 174.
    de Kovel CGF, Trucks H, Helbig I et al (2010) Recurrent microdeletions at 15q11.2 and 16p13.11 predispose to idiopathic generalized epilepsies. Brain 133:23–32PubMedCrossRefGoogle Scholar
  175. 175.
    Heinzen EL, Radtke RA, Urban TJ et al (2010) Rare deletions at 16p13.11 predispose to a diverse spectrum of sporadic epilepsy syndromes. Am J Hum Genet 86:707–718PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    Jähn JA, von Spiczak S, Muhle H et al (2014) Iterative phenotyping of 15q11.2, 15q13.3 and 16p13.11 microdeletion carriers in pediatric epilepsies. Epilepsy Res 108:109–116PubMedCrossRefGoogle Scholar
  177. 177.
    Ullmann R, Turner G, Kirchhoff M et al (2007) Array CGH identifies reciprocal 16p13.1 duplications and deletions that predispose to autism and/or mental retardation. Hum Mutat 28:674–682PubMedCrossRefGoogle Scholar
  178. 178.
    Gümüşlü KE, Savli H, Sünnetçi D et al (2015) A CGH array study in nonsyndromic (primary) autism patients: deletions on 16p13.11, 16p11.2, 1q21.1, 2q21.1q21.2, and 8p23.1. Turk J Med Sci 45:313–319PubMedCrossRefGoogle Scholar
  179. 179.
    Siu W-K, Lam C-W, Mak CM et al (2016) Diagnostic yield of array CGH in patients with autism spectrum disorder in Hong Kong. Clin Transl Med 5:18PubMedPubMedCentralCrossRefGoogle Scholar
  180. 180.
    Balogh SA, Kwon YT, Denenberg VH (2000) Varying intertrial interval reveals temporally defined memory deficits and enhancements in NTAN1-deficient mice. Learn Mem 7:279–286PubMedPubMedCentralCrossRefGoogle Scholar
  181. 181.
    Kwon YT, Balogh SA, Davydov IV et al (2000) Altered activity, social behavior, and spatial memory in mice lacking the NTAN1p amidase and the asparagine branch of the N-end rule pathway. Mol Cell Biol 20:4135–4148PubMedPubMedCentralCrossRefGoogle Scholar
  182. 182.
    Rees E, Moskvina V, Owen MJ, O’Donovan MC, Kirov G (2011) De novo rates and selection of schizophrenia-associated copy number variants. Biol Psychiatry 70:1109–1114PubMedCrossRefGoogle Scholar
  183. 183.
    Brownstein CA, Kleiman RJ, Engle EC et al (2016) Overlapping 16p13.11 deletion and gain of copies variations associated with childhood onset psychosis include genes with mechanistic implications for autism associated pathways: two case reports. Am J Med Genet 170A:1165–1173PubMedCrossRefGoogle Scholar
  184. 184.
    Quintela I, Barros F, Lago-Leston R, Castro-Gago M, Carracedo A, Eiris J (2015) A maternally inherited 16p13.11-p12.3 duplication concomitant with a de novo SOX5 deletion in a male patient with global developmental delay, disruptive and obsessive behaviors and minor dysmorphic features. Am J Med Genet 167A:1315–1322CrossRefGoogle Scholar
  185. 185.
    Need AC, Ge D, Weale ME et al (2009) A genome-wide investigation of SNPs and CNVs in schizophrenia. PLoS Genet 5:e1000373PubMedPubMedCentralCrossRefGoogle Scholar
  186. 186.
    McGrath LM, Yu D, Marshall C et al (2014) Copy number variation in obsessive-compulsive disorder and Tourette syndrome: a cross-disorder study. J Am Acad Child Adolesc Psychiatry 53:910–919PubMedPubMedCentralCrossRefGoogle Scholar
  187. 187.
    Mefford HC, Cooper GM, Zerr T et al (2009) A method for rapid, targeted CNV genotyping identifies rare variants associated with neurocognitive disease. Genome Res 19:1579–1585PubMedPubMedCentralCrossRefGoogle Scholar
  188. 188.
    Williams NM, Zaharieva I, Martin A et al (2010) Rare chromosomal deletions and duplications in attention-deficit hyperactivity disorder: a genome-wide analysis. Lancet 376:1401–1408PubMedPubMedCentralCrossRefGoogle Scholar
  189. 189.
    Rucker JJH, Breen G, Pinto D et al (2013) Genome-wide association analysis of copy number variation in recurrent depressive disorder. Mol Psychiatry 18:183–189PubMedCrossRefGoogle Scholar
  190. 190.
    Hennah W, Porteous D (2009) The DISC1 pathway modulates expression of neurodevelopmental, synaptogenic and sensory perception genes. PloS One 4:e4906Google Scholar
  191. 191.
    Wegelius A, Pankakoski M, Tomppo L et al (2015) An interaction between NDE1 and high birth weight increases schizophrenia susceptibility. Psychiatry Res 230:194–199PubMedCrossRefGoogle Scholar
  192. 192.
    Gadelha A, Machado MFM, Yonamine CM et al (2013) Plasma Ndel1 enzyme activity is reduced in patients with schizophrenia—a potential biomarker? J Psychiatr Res 47:657–663PubMedCrossRefGoogle Scholar
  193. 193.
    Ota VK, Noto C, Santoro ML et al (2015) Increased expression of NDEL1 and MBP genes in the peripheral blood of antipsychotic-naïve patients with first-episode psychosis. Eur Neuropsychopharmacol 25:2416–2425PubMedCrossRefGoogle Scholar
  194. 194.
    Gadelha A, Coleman J, Breen G et al (2016) Genome-wide investigation of schizophrenia associated plasma Ndel1 enzyme activity. Schizophr Res 172:60–67PubMedCrossRefGoogle Scholar
  195. 195.
    Sievers F, Wilm A, Dineen D et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539PubMedPubMedCentralCrossRefGoogle Scholar
  196. 196.
    Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321PubMedCrossRefGoogle Scholar
  197. 197.
    Kent WJ, Sugnet CW, Furey TS et al (2002) The Human Genome Browser at UCSC. Genome Res 12:996–1006PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Nadarajah B, Parnavelas JG (2002) Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423–432PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  1. 1.Department of NeuropathologyHeinrich Heine UniversityDüsseldorfGermany
  2. 2.Department of PharmacologyUniversidade Federal de São Paulo (UNIFESP/EPM)São PauloBrazil

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