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

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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.

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References

  1. Feng Y, Walsh CA (2004) Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44:279–293

    Article  CAS  PubMed  Google Scholar 

  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 44:263–277

    Article  CAS  PubMed  Google Scholar 

  3. Ingason A, Rujescu D, Cichon S et al (2011) Copy number variations of chromosome 16p13.1 region associated with schizophrenia. Mol Psychiatry 16:17–25

    Article  CAS  PubMed  Google Scholar 

  4. Malhotra D, Sebat J (2012) CNVs: harbingers of a rare variant revolution in psychiatric genetics. Cell 148:1223–1241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Rees E, Walters JTR, Georgieva L et al (2014) Analysis of copy number variations at 15 schizophrenia-associated loci. Br J Psychiatry 204:108–114

    Article  PubMed  PubMed Central  Google Scholar 

  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 135:1–7

    Article  PubMed  PubMed Central  Google Scholar 

  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 1:175–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 13:868–880

    Article  PubMed  Google Scholar 

  9. Alkuraya FS, Cai X, Emery C et al (2011) Human mutations in NDE1 cause extreme microcephaly with lissencephaly. Am J Hum Genet 88:536–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 88:523–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Guven A, Gunduz A, Bozoglu T, Yalcinkaya C, Tolun A (2012) Novel NDE1 homozygous mutation resulting in microhydranencephaly and not microlyssencephaly. Neurogenetics 13:189–194

    Article  CAS  PubMed  Google Scholar 

  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:1523–1530

    Article  PubMed  CAS  Google Scholar 

  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 6:453–462

    Article  CAS  Google Scholar 

  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 17:2462–2473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 65:1055–1062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 127:441–452

    Article  CAS  PubMed  Google Scholar 

  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 41:744–753

    Article  PubMed  PubMed Central  Google Scholar 

  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 156:261–273

    PubMed  Google Scholar 

  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 227:618–629

    Article  CAS  PubMed  Google Scholar 

  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 26:220–232

    Article  CAS  PubMed  Google Scholar 

  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 473:396–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 116:1151–1159

    Article  CAS  PubMed  Google Scholar 

  23. Oliveira EB, Martins AR, Camargo ACM (1976) Isolation of brain endopeptidases: influence of size and sequence of substrates structurally related to bradykinin. Biochemistry 15:1967–1974

    Article  CAS  PubMed  Google Scholar 

  24. Morris NR (1978) Mitotic mutants of Aspergillus nidulans. Genet Res 26:237–254

    Article  Google Scholar 

  25. Oakley BR, Morris NR (1980) Nuclear movement is β-tubulin-dependent in Aspergillus nidulans. Cell 19:255–262

    Article  CAS  PubMed  Google Scholar 

  26. Xiang X, Beckwith SM, Morris NR (1994) Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc Natl Acad Sci USA 91:2100–2104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 6:297–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 364:717–721

    Article  CAS  PubMed  Google Scholar 

  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 150:681–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Stukenberg PT, Lustig KD, McGarry TJ, King RW, Kuang J, Kirschner MW (1997) Systematic identification of mitotic phosphoproteins. Curr Biol 7:338–348

    Article  CAS  PubMed  Google Scholar 

  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 32:1065–1076

    Article  CAS  PubMed  Google Scholar 

  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 28:665–679

    Article  CAS  PubMed  Google Scholar 

  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 479:57–62

    Article  CAS  PubMed  Google Scholar 

  34. Niethammer M, Smith DS, Ayala R et al (2000) NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28:697–711

    Article  CAS  PubMed  Google Scholar 

  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 28:681–696

    Article  CAS  PubMed  Google Scholar 

  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 336:13–16

    Article  CAS  PubMed  Google Scholar 

  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 9:1415–1425

    Article  CAS  PubMed  Google Scholar 

  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 69:428–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Millar JK, Christie S, Porteous DJ (2003) Yeast two-hybrid screens implicate DISC1 in brain development and function. Biochem Biophys Res Commun 311:1019–1025

    Article  CAS  PubMed  Google Scholar 

  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 12:1591–1608

    Article  CAS  PubMed  Google Scholar 

  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 100:289–294

    Article  CAS  PubMed  Google Scholar 

  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 101:21–33

    Article  CAS  PubMed  Google Scholar 

  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 102:3828–3833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Shmueli A, Segal M, Sapir T et al (2010) Ndel1 palmitoylation: a new mean to regulate cytoplasmic dynein activity. EMBO J 29:107–119

    Article  CAS  PubMed  Google Scholar 

  45. McLysaght A, Makino T, Grayton HM et al (2013) Ohnologs are overrepresented in pathogenic copy number mutations. Proc Natl Acad Sci USA 111:361–366

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Bradshaw NJ, Hennah W, Soares DC (2013) NDE1 and NDEL1: twin neurodevelopmental proteins with similar ‘nature’ but different ‘nurture’. Biomol Concepts 4:447–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 76:672–679

    Article  CAS  Google Scholar 

  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 1730:77–84

    Article  CAS  PubMed  Google Scholar 

  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 449:228–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Bradshaw NJ (2016) Cloning of the promoter of NDE1, a gene implicated in psychiatric and neurodevelopmental disorders through copy number variation. Neuroscience 324:262–270

    Article  CAS  PubMed  Google Scholar 

  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, Rijeka

    Google Scholar 

  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 16:1493–1502

    Article  CAS  PubMed  Google Scholar 

  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, Vienna

    Google Scholar 

  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 89:86–93

    Article  CAS  PubMed  Google Scholar 

  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 55:1114–1121

    Article  CAS  PubMed  Google Scholar 

  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 271:119–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Larney C, Bailey TL, Koopman P (2014) Switching on sex: transcriptional regulation of the testis-determining gene Sry. Development 141:2195–2205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 566:71–76

    Article  CAS  PubMed  Google Scholar 

  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 122:2820–2827

    Article  CAS  PubMed  Google Scholar 

  60. Dewing P, Chiang CWK, Sinchak K et al (2006) Direct regulation of adult brain function by the male-specific factor SRY. Curr Biol 16:415–420

    Article  CAS  PubMed  Google Scholar 

  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 122:260–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 331:1–12

    Article  CAS  PubMed  Google Scholar 

  63. Kandel ER (2012) The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol Brain 5:14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Millar JK, Pickard BS, Mackie S et al (2005) DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signalling. Science 310:1187–1191

    Article  CAS  PubMed  Google Scholar 

  65. Bradshaw NJ, Ogawa F, Antolin-Fontes B et al (2008) DISC1, PDE4B, and NDE1 at the centrosome and synapse. Biochem Biophys Res Commun 377:1091–1096

    Article  CAS  PubMed  Google Scholar 

  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 20:2356–2369

    Article  CAS  PubMed  Google Scholar 

  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 44:809–821

    CAS  PubMed  Google Scholar 

  68. McKenney RJ, Vershinin M, Kunwar A, Vallee RB, Gross SP (2010) LIS1 and NudE induce a persistent dynein force-producing state. Cell 141:304–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 286:44266–44276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Nyarko A, Song Y, Barbar E (2012) Intrinsic disorder in dynein intermediate chain modulates its interactions with NudE and dynactin. J Biol Chem 287:24884–24893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 287:32381–32393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Yerabham ASK, Weiergräber OH, Bradshaw NJ, Korth C (2013) Revisiting disrupted in schizophrenia 1 as a scaffold protein. Biol Chem 394:1425–1437

    Article  CAS  PubMed  Google Scholar 

  73. Carvalho KM, Camargo ACM (1981) Purification of rabbit brain endooligopeptidases and preparation of anti-enzyme antibodies. Biochemistry 20:7082–7088

    Article  CAS  PubMed  Google Scholar 

  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 257:5861–5865

    CAS  PubMed  Google Scholar 

  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 254:5304–5307

    CAS  PubMed  Google Scholar 

  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 257:9265–9267

  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 10:340–348

    Article  CAS  PubMed  Google Scholar 

  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 20:293

    Article  PubMed  Google Scholar 

  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 151:667–672

    Article  CAS  PubMed  Google Scholar 

  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 18:2734–2745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Kinkead B, Nemeroff CB (2002) Neurotensin: an endogenous antipsychotic? Curr Opin Pharmacol 2:99–103

    Article  CAS  PubMed  Google Scholar 

  82. Cáceda R, Kinkead B, Nemeroff CB (2006) Neurotensin: role in psychiatric and neurological diseases. Peptides 27:2385–2404

    Article  PubMed  CAS  Google Scholar 

  83. Boules M, Shaw A, Fredrickson P, Richelson E (2007) Neurotensin agonists: potential in the treatment of schizophrenia. CNS Drugs 21:13–23

    Article  CAS  PubMed  Google Scholar 

  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 157:738–741

    Article  CAS  PubMed  Google Scholar 

  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 51:452–459

    Article  CAS  Google Scholar 

  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 16:754–767

    Article  CAS  PubMed  Google Scholar 

  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 32:898–902

    Article  CAS  PubMed  Google Scholar 

  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 1834:98–111

    Article  CAS  PubMed  Google Scholar 

  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 94:1398–1411

    Article  CAS  PubMed  Google Scholar 

  90. Camargo ACM, Gomes MD, Toffoletto O et al (1994) Structural requirements of bioactive peptides for interaction with endopeptidase 22.19. Neuropeptides 26:281–287

    Article  CAS  PubMed  Google Scholar 

  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 42:1758–1761

    Article  CAS  PubMed  Google Scholar 

  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 70:47–56

    Article  CAS  PubMed  Google Scholar 

  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 15:1467–1481

    Article  CAS  PubMed  Google Scholar 

  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 286:587–593

    Article  CAS  PubMed  Google Scholar 

  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 192:433–445

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 286:1959–1965

    Article  CAS  PubMed  Google Scholar 

  97. McKenney RJ, Weil SJ, Scherer J, Vallee RB (2011) Mutually exclusive cytoplasmic dynein regulation by NudE-LIS1 and dynactin. J Biol Chem 286:39615–39622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 23:1239–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 182:1063–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 31:9043–9054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Pandey JP, Smith DS (2011) A Cdk5-dependent switch regulates Lis1/Ndel1/dynein-driven organelle transport in adult axons. J Neurosci 31:17207–17219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 16:941–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Kikkawa M (2013) Big steps toward understanding dynein. J Cell Biol 202:15–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Cianfrocco MA, DeSantis ME, Leschziner AE, Reck-Peterson SL (2015) Mechanism and regulation of cytoplasmic dynein. Annu Rev Cell Dev Biol 31:83–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Yamada M, Toba S, Yoshida Y et al (2008) LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein. EMBO J 27:2471–2483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 150:975–986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Toropova K, Zou S, Roberts AJ et al (2014) Lis1 regulates dynein by sterically blocking its mechanochemical cycle. eLife 3:e03372

    Article  PubMed Central  Google Scholar 

  108. Toba S, Koyasako K, Yasunaga T, Hirotsune S (2015) Lis1 restricts the conformational changes in cytoplasmic dynein on microtubules. Microscopy (Oxford) 64:419–427

    Article  Google Scholar 

  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 164:557–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Zhang Q, Wang F, Cao J et al (2009) Nudel promotes axonal lysosome clearance and endo-lysosome formation via dynein-mediated transport. Traffic 10:1337–1349

    Article  CAS  PubMed  Google Scholar 

  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 123:202–212

    Article  CAS  PubMed  Google Scholar 

  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 25:7812–7827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 165:709–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 14:342–353

    Article  CAS  PubMed  Google Scholar 

  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 14:785–797

    Article  CAS  PubMed  Google Scholar 

  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 7:553–564

    Article  CAS  PubMed  Google Scholar 

  117. Wan Y, Yang Z, Guo J et al (2012) Misfolded Gβ is recruited to cytoplasmic dynein by Nudel for efficient clearance. Cell Res 22:1140–1154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 1:220–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 17:680–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 14:3113–3128

    Article  CAS  PubMed  Google Scholar 

  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 180:1133–1147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 11:1057–1068

    Article  CAS  PubMed  Google Scholar 

  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 32:11050–11066

    Article  CAS  PubMed  Google Scholar 

  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 29:15520–15530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Yingling J, Youn YH, Darling D et al (2008) Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132:474–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 6:595–608

    Article  CAS  PubMed  Google Scholar 

  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 30:1908–1918

    Article  PubMed  Google Scholar 

  128. Shim SY, Samuels BA, Wang J et al (2008) Ndel1 controls the dynein-mediated transport of vimentin during neurite outgrowth. J Biol Chem 283:12232–12240

    Article  CAS  PubMed  Google Scholar 

  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 22:1270–1284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  130. Pawlisz AS, Feng Y (2011) Three-dimensional regulation of radial glial functions by Lis1-Nde1 and dystrophin glycoprotein complexes. PLoS Biol 9:e1001172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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:e1000116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. Hirohashi Y, Wang Q, Liu Q et al (2006) Centrosomal proteins Nde1 and Su48 form a complex regulated by phosphorylation. Oncogene 25:6048–6055

    Article  CAS  PubMed  Google Scholar 

  133. Vergnolle MAS, Taylor SS (2007) Cenp-F links kinetochores to Ndel1/Nde1/Lis1/Dynein microtubule motor complexes. Curr Biol 17:1173–1179

    Article  CAS  PubMed  Google Scholar 

  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 18:2656–2666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 178:583–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 192:855–871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Raaijmakers JA, Tanenbaum ME, Medema RH (2013) Systematic dissection of dynein regulators in mitosis. J Cell Biol 201:201–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Salina D, Bodoor K, Eckley DM, Schroer TA, Rattner JB, Burke B (2002) Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108:97–107

    Article  CAS  PubMed  Google Scholar 

  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 204:1099–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Tsai M-Y, Wang S, Heidinger JM et al (2006) A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 311:1887–1893

    Article  CAS  PubMed  Google Scholar 

  141. Kuga T, Nie H, Kazami T et al (2014) Lamin B2 prevents chromosome instability by ensuring proper mitotic chromosome segregation. Oncogenesis 3:e94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 11:247–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Wang Y, Jin F, Higgins R, McKnight K (2014) The current view for the silencing of the spindle assembly checkpoint. Cell Cycle 13:1694–1701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 155:1159–1172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 19:4918–4929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 27:352–367

    Article  CAS  PubMed  Google Scholar 

  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 79:254–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Kim S, Zaghloul NA, Bubenshchikova E et al (2011) Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat Cell Biol 13:351–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 34:2424–2440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 212:409–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Houlihan SL, Feng Y (2014) The scaffold protein Nde1 safeguards the brain genome during S phase of early neural progenitor differentiation. eLife 3:e03297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  152. Toth C, Shim SY, Wang J et al (2008) Ndel1 promotes axon regeneration via intermediate filaments. PLoS One 3:e2014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 35:2942–2958

    Article  CAS  Google Scholar 

  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 44:353–361

    Article  CAS  PubMed  Google Scholar 

  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 15:3313–3323

    Article  CAS  PubMed  Google Scholar 

  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

    PubMed  Google Scholar 

  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 268:887–894

    Article  CAS  PubMed  Google Scholar 

  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 17:2441–2455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Hippenmeyer S, Youn YH, Moon HM et al (2010) Genetic mosaic dissection of Lis1 and Ndel1 in neuronal migration. Neuron 68:695–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Jiang Y, Gavrilovici C, Chansard M et al (2016) Ndel1 and Reelin maintain postnatal CA1 hippocampus integrity. J Neuosci 36:6538–6552

    Article  CAS  Google Scholar 

  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 130:1146–1158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 268:276–283

    Article  CAS  PubMed  Google Scholar 

  163. Rauch A, Thiel CT, Schindler D et al (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319:816–819

    Article  CAS  PubMed  Google Scholar 

  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 40:232–236

    Article  CAS  PubMed  Google Scholar 

  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 47:797–802

    Article  CAS  PubMed  Google Scholar 

  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 3:475–485

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  167. Gabriel E, Wason A, Ramani A et al (2016) CPAP promotes timely cilium disassembly to maintain neural progenitor pool. EMBO J 35:803–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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:e61365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Cooper GM, Coe BP, Girirajan S et al (2011) A copy number variation morbidity map of developmental delay. Nat Genet 43:838–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 46:223–232

    Article  CAS  PubMed  Google Scholar 

  171. Nagamani SCS, Erez A, Bader P et al (2011) Phenotypic manifestations of copy number variation in chromosome 16p13.11. Eur J Hum Genet 19:280–286

    Article  PubMed  Google Scholar 

  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 56:541–544

    Article  CAS  PubMed  Google Scholar 

  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:e1000962

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 133:23–32

    Article  PubMed  Google Scholar 

  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 86:707–718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 108:109–116

    Article  PubMed  CAS  Google Scholar 

  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 28:674–682

    Article  CAS  PubMed  Google Scholar 

  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 45:313–319

    Article  PubMed  CAS  Google Scholar 

  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 5:18

    Article  PubMed  PubMed Central  Google Scholar 

  180. Balogh SA, Kwon YT, Denenberg VH (2000) Varying intertrial interval reveals temporally defined memory deficits and enhancements in NTAN1-deficient mice. Learn Mem 7:279–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 20:4135–4148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 70:1109–1114

    Article  PubMed  Google Scholar 

  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:1165–1173

    Article  PubMed  CAS  Google Scholar 

  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:1315–1322

    Article  CAS  Google Scholar 

  185. Need AC, Ge D, Weale ME et al (2009) A genome-wide investigation of SNPs and CNVs in schizophrenia. PLoS Genet 5:e1000373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 53:910–919

    Article  PubMed  PubMed Central  Google Scholar 

  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 19:1579–1585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 376:1401–1408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Rucker JJH, Breen G, Pinto D et al (2013) Genome-wide association analysis of copy number variation in recurrent depressive disorder. Mol Psychiatry 18:183–189

    Article  CAS  PubMed  Google Scholar 

  190. Hennah W, Porteous D (2009) The DISC1 pathway modulates expression of neurodevelopmental, synaptogenic and sensory perception genes. PloS One 4:e4906

  191. Wegelius A, Pankakoski M, Tomppo L et al (2015) An interaction between NDE1 and high birth weight increases schizophrenia susceptibility. Psychiatry Res 230:194–199

    Article  CAS  PubMed  Google Scholar 

  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 47:657–663

    Article  PubMed  Google Scholar 

  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 25:2416–2425

    Article  CAS  PubMed  Google Scholar 

  194. Gadelha A, Coleman J, Breen G et al (2016) Genome-wide investigation of schizophrenia associated plasma Ndel1 enzyme activity. Schizophr Res 172:60–67

    Article  PubMed  Google Scholar 

  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 7:539

    Article  PubMed  PubMed Central  Google Scholar 

  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 59:307–321

    Article  CAS  PubMed  Google Scholar 

  197. Kent WJ, Sugnet CW, Furey TS et al (2002) The Human Genome Browser at UCSC. Genome Res 12:996–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Nadarajah B, Parnavelas JG (2002) Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423–432

    Article  CAS  PubMed  Google Scholar 

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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).

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  1. Department of Neuropathology, Heinrich Heine University, Düsseldorf, Germany

    Nicholas J. Bradshaw

  2. Department of Pharmacology, Universidade Federal de São Paulo (UNIFESP/EPM), São Paulo, Brazil

    Mirian A. F. Hayashi

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Bradshaw, N.J., Hayashi, M.A.F. NDE1 and NDEL1 from genes to (mal)functions: parallel but distinct roles impacting on neurodevelopmental disorders and psychiatric illness. Cell. Mol. Life Sci. 74, 1191–1210 (2017). https://doi.org/10.1007/s00018-016-2395-7

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