Homozygous and heterozygous disruptions of ANK3: At the crossroads of neurodevelopmental and psychiatric disorders

Human Molecular Genetics

Volumn 22, Issue 10, 2013, Pages 1960-1970

  Iqbal, Zafar ^a,b,c   Vandeweyer, Geert ^d   Van der voet, Monique ^a,b,c   Waryah, Ali Muhammad ^e,f,g   Zahoor, Muhammad Yasir ^e,f   Besseling, Judith A ^a,b,c   Roca, Laura Tomas ^a,b,c   Vulto van silfhout, Anneke T ^a   Nijhof, Bonnie ^a,b,c   Kramer, Jamie M ^a,b,c   Van der Aa, Nathalie ^d   Ansar, Muhammad ^a,e,h   Peeters, Hilde ⁱ   Helsmoortel, Céline ^d   Gilissen, Christian ^a   Vissers, Lisenka E L M ^a   Veltman, Joris A ^a   De brouwer, Arjan P M ^a   Frank kooy, R ^d   Riazuddin, Sheikh ^e,f   Schenck, Annette ^a,b,c   Van bokhoven, Hans ^a,b,c   Rooms, Liesbeth ^d   more..

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY   (Netherlands)

^d ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^e UNIVERSITY OF THE PUNJAB   (Pakistan)

^f ALLAMA IQBAL MEDICAL COLLEGE   (Pakistan)

^g LIAQUAT UNIVERSITY OF MEDICAL AND HEALTH SCIENCES   (Pakistan)

^h KING EDWARD MEDICAL UNIVERSITY   (Pakistan)

ⁱ UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN 3 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATTENTION DEFICIT DISORDER; AUTISM; BORDERLINE STATE; COGNITIVE DEFECT; DROSOPHILA; FRAMESHIFT MUTATION; GENE DISRUPTION; GENE TRANSLOCATION; HETEROZYGOTE; HOMOZYGOTE; HUMAN; INTELLECTUAL IMPAIRMENT; KARYOTYPING; MENTAL DISEASE; NONHUMAN; PRIORITY JOURNAL; SHORT TERM MEMORY; SLEEP DISORDER;

ADULT; ANIMALS; ANKYRINS; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; FEMALE; FRAMESHIFT MUTATION; GENE KNOCKDOWN TECHNIQUES; HETEROZYGOTE; HOMOZYGOTE; HUMANS; INFANT; MALE; MENTAL DISORDERS; NEUROGENESIS; SLEEP DISORDERS;

EID: 84877045763     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt043     Document Type: Article

References (74)

1. WHO (2001) World Health Report 2001: Mental Health: New Understanding, New Hope. Geneva, Switzerland.
2. Curry, C.J., Stevenson, R.E., Aughton, D., Byrne, J., Carey, J.C., Cassidy, S., Cunniff, C., Graham, J.M. Jr, Jones, M.C., Kaback, M.M. et al. (1997) Evaluation of mental retardation: recommendations of a consensus conference. Am. J. Med. Genet., 72, 468-477.
3. Stevenson, R.E., Procopio-Allen, A.M., Schroer, R.J. and Collins, J.S. (2003) Genetic syndromes among individuals with mental retardation. Am. J. Med. Genet., 123A, 29-32.
4. van Bokhoven, H. (2011) Genetic and epigenetic networks in intellectual disabilities. Annu. Rev. Genet., 45, 81-104.
5. Vandeweyer, G. and Kooy, R.F. (2009) Balanced translocations in mental retardation. Hum. Genet., 126, 133-147.
6. Gillberg, C. and Billstedt, E. (2000) Autism and Asperger syndrome: coexistence with other clinical disorders. Acta Psychiatr. Scand., 102, 321-330.
7. Geschwind, D.H. (2008) Autism: many genes, common pathways? Cell, 135, 391-395.
8. Polanczyk, G., de Lima, M.S., Horta, B.L., Biederman, J. and Rohde, L.A. (2007) The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am. J. Psychiatry, 164, 942-948.
9. Faraone, S.V. and Mick, E. (2010) Molecular genetics of attention deficit hyperactivity disorder. Psychiatr. Clin. North Am., 33, 159-180.
10. Hagerman, P.J. (2008) The fragile X prevalence paradox. J. Med. Genet., 45, 498-499.
11. Lichtenstein, P., Carlstrom, E., Rastam, M., Gillberg, C. and Anckarsater, H. (2010) The genetics of autism spectrum disorders and related neuropsychiatric disorders in childhood. Am. J. Psychiatry, 167, 1357-1363.
12. Bakker, S.C., van der Meulen, E.M., Buitelaar, J.K., Sandkuijl, L.A., Pauls, D.L., Monsuur, A.J., van 't Slot, R., Minderaa, R.B., Gunning, W.B., Pearson, P.L. et al. (2003) A whole-genome scan in 164 Dutch sib pairs with attention-deficit/hyperactivity disorder: suggestive evidence for linkage on chromosomes 7p and 15q. Am. J. Hum. Genet., 72, 1251-1260.
13. Lionel, A.C., Crosbie, J., Barbosa, N., Goodale, T., Thiruvahindrapuram, B., Rickaby, J., Gazzellone, M., Carson, A.R., Howe, J.L., Wang, Z. et al. (2011) Rare copy number variation discovery and cross-disorder comparisons identify risk genes for ADHD. Sci. Transl. Med., 3, 95ra75.
14. Talkowski, M.E., Rosenfeld, J.A., Blumenthal, I., Pillalamarri, V., Chiang, C., Heilbut, A., Ernst, C., Hanscom, C., Rossin, E., Lindgren, A.M. et al. (2012) Sequencing chromosomal abnormalities reveals neurodevelopmental loci that confer risk across diagnostic boundaries. Cell, 149, 525-537.
15. Awadalla, P., Gauthier, J., Myers, R.A., Casals, F., Hamdan, F.F., Griffing, A.R., Cote, M., Henrion, E., Spiegelman, D., Tarabeux, J. et al. (2010) Direct measure of the de novo mutation rate in autism and schizophrenia cohorts. Am. J. Hum. Genet., 87, 316-324.
16. Hamdan, F.F., Gauthier, J., Araki, Y., Lin, D.T., Yoshizawa, Y., Higashi, K., Park, A.R., Spiegelman, D., Dobrzeniecka, S., Piton, A. et al. (2011) Excess of de novo deleterious mutations in genes associated with glutamatergic systems in nonsyndromic intellectual disability. Am. J. Hum. Genet., 88, 306-316.
17. Tesli, M., Koefoed, P., Athanasiu, L., Mattingsdal, M., Gustafsson, O., Agartz, I., Rimol, L.M., Brown, A., Wirgenes, K.V., Smorr, L.L. et al. (2011) Association analysis of ANK3 gene variants in nordic bipolar disorder and schizophrenia case-control samples. Am. J. Med. Genet. B. Neuropsychiatr. Genet., 156B, 969-974.
18. Ferreira, M.A., O'Donovan, M.C., Meng, Y.A., Jones, I.R., Ruderfer, D.M., Jones, L., Fan, J., Kirov, G., Perlis, R.H., Green, E.K. et al. (2008) Collaborative genome-wide association analysis supports a role for ANK3 and CACNA1C in bipolar disorder. Nat. Genet., 40, 1056-1058.
19. Schulze, T.G., Detera-Wadleigh, S.D., Akula, N., Gupta, A., Kassem, L., Steele, J., Pearl, J., Strohmaier, J., Breuer, R., Schwarz, M. et al. (2009) Two variants in Ankyrin 3 (ANK3) are independent genetic risk factors for bipolar disorder. Mol. Psychiatr., 14, 487-491.
20. Klopocki, E., Schulze, H., Strauss, G., Ott, C.E., Hall, J., Trotier, F., Fleischhauer, S., Greenhalgh, L., Newbury-Ecob, R.A., Neumann, L.M. et al. (2007) Complex inheritance pattern resembling autosomal recessive inheritance involving a microdeletion in thrombocytopenia-absent radius syndrome. Am. J. Hum. Genet., 80, 232-240.
21. Gella, A., Segura, M., Durany, N., Pfuhlmann, B., Stober, G. and Gawlik, M. (2011) Is Ankyrin a genetic risk factor for psychiatric phenotypes? BMC Psychiatry, 11, 103.
22. Green, E.K., Hamshere, M., Forty, L., Gordon-Smith, K., Fraser, C., Russell, E., Grozeva, D., Kirov, G., Holmans, P., Moran, J.L. et al. (2012) Replication of bipolar disorder susceptibility alleles and identification of two novel genome-wide significant associations in a new bipolar disorder case-control sample. Mol. Psychiatr, [epub ahead of print].
23. Yuan, A., Yi, Z., Wang, Q., Sun, J., Li, Z., Du, Y., Zhang, C., Yu, T., Fan, J., Li, H. et al. (2012) ANK3 as a risk gene for schizophrenia: new data in han Chinese and meta analysis. Am. J. Med. Genet. B. Neuropsychiatr. Genet., 159B, 997-1005.
24. Athanasiu, L., Mattingsdal, M., Kahler, A.K., Brown, A., Gustafsson, O., Agartz, I., Giegling, I., Muglia, P., Cichon, S., Rietschel, M. et al. (2010) Gene variants associated with schizophrenia in a Norwegian genome-wide study are replicated in a large European cohort. J. Psychiatr. Res., 44, 748-753.
25. Vicari, S. and Carlesimo, G.A. (2006) Short-term memory deficits are not uniform in Down and Williams syndromes. Neuropsychol. Rev., 16, 87-94.
26. Poirier, M., Martin, J.S., Gaigg, S.B. and Bowler, D.M. (2011) Short-term memory in autism spectrum disorder. J. Abnorm. Psychol., 120, 247-252.
27. Bolden, J., Rapport, M.D., Raiker, J.S., Sarver, D.E. and Kofler, M.J. (2012) Understanding phonological memory deficits in boys with attention-deficit/hyperactivity disorder (ADHD): dissociation of short-term storage and articulatory rehearsal processes. J. Abnorm. Child Psychol., 40, 999-1011.
28. Vandeweyer, G., Reyniers, E., Wuyts, W., Rooms, L. and Kooy, R.F. (2011) CNV-WebStore: online CNV analysis, storage and interpretation. BMC Bioinformatics, 12, 4.
29. Chen, J.M., Cooper, D.N., Ferec, C., Kehrer-Sawatzki, H. and Patrinos, G.P. (2010) Genomic rearrangements in inherited disease and cancer. Semin. Cancer Biol., 20, 222-233.
30. Swanberg, S.E., Nagarajan, R.P., Peddada, S., Yasui, D.H. and LaSalle, J.M. (2009) Reciprocal co-regulation of EGR2 and MECP2 is disrupted in Rett syndrome and autism. Hum. Mol. Genet., 18, 525-534.
31. Castermans, D., Vermeesch, J.R., Fryns, J.P., Steyaert, J.G., Van de Ven, W.J., Creemers, J.W. and Devriendt, K. (2007) Identification and characterization of the TRIP8 and REEP3 genes on chromosome 10q21.3 as novel candidate genes for autism. Eur. J. Hum. Genet., 15, 422-431.
32. Poot, M., Eleveld, M.J., van 't Slot, R., Ploos van Amstel, H.K. and Hochstenbach, R. (2010) Recurrent copy number changes in mentally retarded children harbour genes involved in cellular localization and the glutamate receptor complex. Eur. J. Hum. Genet., 18, 39-46.
33. Durbin,R.M., Altshuler, D.L.,Abecasis,G.R.,Bentley,D.R.,Chakravarti, A., Clark, A.G., Collins, F.S., De La Vega, F.M., Donnelly, P. and Egholm, M. (2010)Amap of human genome variation frompopulation-scale sequencing. Nature, 467, 1061-1073.
34. Nagy, E. and Maquat, L.E. (1998) A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci., 23, 198-199.
35. Green, R.E., Lewis, B.P., Hillman, R.T., Blanchette, M., Lareau, L.F., Garnett, A.T., Rio, D.C. and Brenner, S.E. (2003) Widespread predicted nonsense-mediated mRNA decay of alternatively-spliced transcripts of human normal and disease genes. Bioinformatics, 19 (Suppl. 1), i118-i121.
36. Gatto, C.L. and Broadie, K. (2011) Drosophila modeling of heritable neurodevelopmental disorders. Curr. Opin. Neurobiol., 21, 834-841.
37. Bouley, M., Tian, M.Z., Paisley, K., Shen, Y.C., Malhotra, J.D. and Hortsch, M. (2000) The L1-type cell adhesion molecule neuroglian influences the stability of neural ankyrin in the Drosophila embryo but not its axonal localization. J. Neurosci., 20, 4515-4523.
38. Hortsch, M., Paisley, K.L., Tian, M.Z., Qian, M., Bouley, M. and Chandler, R. (2002) The axonal localization of large Drosophila ankyrin2 protein isoforms is essential for neuronal functionality. Mol. Cell Neurosci., 20, 43-55.
39. Koch, I., Schwarz, H., Beuchle, D., Goellner, B., Langegger, M. and Aberle, H. (2008) Drosophila ankyrin 2 is required for synaptic stability. Neuron, 58, 210-222.
40. Pielage, J., Cheng, L., Fetter, R.D., Carlton, P.M., Sedat, J.W. and Davis, G.W. (2008) A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron, 58, 195-209.
41. Scott, L.J., Muglia, P., Kong, X.Q., Guan, W., Flickinger, M., Upmanyu, R., Tozzi, F., Li, J.Z., Burmeister, M., Absher, D. et al. (2009) Genome-wide association and meta-analysis of bipolar disorder in individuals of European ancestry. Proc. Natl Acad. Sci. USA, 106, 7501-7506.
42. Morgan, A.R., Hamilton, G., Turic, D., Jehu, L., Harold, D., Abraham, R., Hollingworth, P., Moskvina, V., Brayne, C., Rubinsztein, D.C. et al. (2008) Association analysis of 528 intra-genic SNPs in a region of chromosome 10 linked to late onset Alzheimer's disease. Am. J. Med. Genet. B. Neuropsychiatr. Genet., 147B, 727-731.
43. Psychiatric GWAS Consortium Bipolar Disorder Working Group. (2011) Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nat. Genet., 43, 977-983.
44. Ruberto, G., Vassos, E., Lewis, C.M., Tatarelli, R., Girardi, P., Collier, D. and Frangou, S. (2011) The cognitive impact of the ANK3 risk variant for bipolar disorder: initial evidence of selectivity to signal detection during sustained attention. PloS One, 6, e16671.
45. Hatzimanolis, A., Smyrnis, N., Avramopoulos, D., Stefanis, C.N., Evdokimidis, I. and Stefanis, N.C. (2012) Bipolar disorder ANK3 risk variant effect on sustained attention is replicated in a large healthy population. Psychiatr. Genet., 22, 210-213.
46. Christakou, A., Murphy, C.M., Chantiluke, K., Cubillo, A.I., Smith, A.B., Giampietro, V., Daly, E., Ecker, C., Robertson, D. et al. MRC AIMS Consortium. (2012) Disorder-specific functional abnormalities during sustained attention in youth with Attention Deficit Hyperactivity Disorder (ADHD) and with autism. Mol. Psychiatr, 18, 264.
47. Weissman, A.S., Chu, B.C., Reddy, L.A. and Mohlman, J. (2012) Attention mechanisms in children with anxiety disorders and in children with attention deficit hyperactivity disorder: implications for research and practice. J. Clin. Child Adolesc. Psychol., 41, 117-126.
48. Roussos, P., Katsel, P., Davis, K.L., Bitsios, P., Giakoumaki, S.G., Jogia, J., Rozsnyai, K., Collier, D., Frangou, S., Siever, L.J. et al. (2012) Molecular and genetic evidence for abnormalities in the nodes of Ranvier in schizophrenia. Arch. Gen. Psychiatr., 69, 7-15.
49. Kosaka, T., Komada, M. and Kosaka, K. (2008) Sodium channel cluster, betaIV-spectrin and ankyrinG positive hot spots on dendritic segments of parvalbumin-containing neurons and some other neurons in the mouse and rat main olfactory bulbs. Neurosci. Res., 62, 176-186.
50. Kordeli, E., Lambert, S., Bennett, V. and Ankyrin, G. (1995) A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J. Biol. Chem., 270, 2352-2359.
51. Lambert, S., Davis, J.Q. and Bennett, V. (1997) Morphogenesis of the node of Ranvier: co-clusters of ankyrin and ankyrin-binding integral proteins define early developmental intermediates. J. Neurosci., 17, 7025-7036.
52. Custer, A.W., Kazarinova-Noyes, K., Sakurai, T., Xu, X., Simon, W., Grumet, M. and Shrager, P. (2003) The role of the ankyrin-binding protein NrCAM in node of Ranvier formation. J. Neurosci., 23, 10032-10039.
53. Sobotzik, J.M., Sie, J.M., Politi, C., Del Turco, D., Bennett, V., Deller, T. and Schultz, C. (2009) AnkyrinG is required to maintain axo-dendritic polarity in vivo. Proc. Natl Acad. Sci. USA, 106, 17564-17569.
54. Rueckert, E.H., Barker, D., Ruderfer, D., Bergen, S.E., O'Dushlaine, C., Luce, C.J., Sheridan, S.D., Theriault, K.M., Chambert, K., Moran, J. et al. (2012) Cis-acting regulation of brain-specific ANK3 gene expression by a genetic variant associated with bipolar disorder. Mol. Psychiatr, [epub ahead of print].
55. Sebat, J., Lakshmi, B., Malhotra, D., Troge, J., Lese-Martin, C., Walsh, T., Yamrom, B., Yoon, S., Krasnitz, A., Kendall, J. et al. (2007) Strong association of de novo copy number mutations with autism. Science, 316, 445-449.
56. Bi, C., Wu, J., Jiang, T., Liu, Q., Cai, W., Yu, P., Cai, T., Zhao, M., Jiang, Y.H. and Sun, Z.S. (2012) Mutations of ANK3 identified by exome sequencing are associated with autism ausceptibility. Hum. Mut., 33, 1635-1638.
57. Sanders, S.J., Murtha, M.T., Gupta, A.R., Murdoch, J.D., Raubeson, M.J., Willsey, A.J., Ercan-Sencicek, A.G., DiLullo, N.M., Parikshak, N.N., Stein, J.L. et al. (2012) De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature, 485, 237-241.
58. Kooy, R.F., Van der Aa, N., Vandeweyer, G., Reyniers, E. and Rooms, L. (2010) Genetic overlaps in mental retardation, autism and schizophrenia. Monogr. Hum. Genet., 18, 126-136.
59. Carroll, L.S. and Owen, M.J. (2009) Genetic overlap between autism, schizophrenia and bipolar disorder. Genome Med., 1, 102.
60. Guilmatre, A., Dubourg, C., Mosca, A.L., Legallic, S., Goldenberg, A., Drouin-Garraud, V., Layet, V., Rosier, A., Briault, S., Bonnet-Brilhault, F. et al. (2009) Recurrent rearrangements in synaptic and neurodevelopmental genes and shared biologic pathways in schizophrenia, autism, and mental retardation. Arch Gen. Psychiatr., 66, 947-956.
61. Pavlowsky, A., Chelly, J. and Billuart, P. (2012) Emerging major synaptic signaling pathways involved in intellectual disability. Mol. Psychiatr., 17, 682-693.
62. Rooms, L., Reyniers, E., van Luijk, R., Scheers, S., Wauters, J. and Kooy, R.F. (2004) Screening for subtelomeric rearrangements using genetic markers in 70 patients with unexplained mental retardation. Ann. Genet., 47, 53-59.
63. Veltman, I.M., Veltman, J.A., Arkesteijn, G., Janssen, I.M., Vissers, L.E., de Jong, P.J., van Kessel, A.G. and Schoenmakers, E.F. (2003) Chromosomal breakpoint mapping by arrayCGH using flow-sorted chromosomes. Biotechniques, 35, 1066-1070.
64. Rozen, S. and Skaletsky, H. (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol., 132, 365-386.
65. Markham, N.R. and Zuker, M. (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol. Biol., 453, 3-31.
66. Vandeweyer, G., Van der Aa, N., Ceulemans, B., van Bon, B., Rooms, L. and Kooy, R.F. (2012) A de novo balanced t(2;6)(p15;p22.3) in a patient with West Syndrome disrupts a lnc-RNA. Epilepsy Res., 99, 346-349.
67. Van der Aa, N., Rooms, L., Vandeweyer, G., van den Ende, J., Reyniers, E., Fichera, M., Romano, C., Delle Chiaie, B., Mortier, G., Menten, B. et al. (2009) Fourteen new cases contribute to the characterization of the 7q11.23 microduplication syndrome. Eur. J. Med. Genet., 52, 94-100.
68. Nannya, Y., Sanada, M., Nakazaki, K., Hosoya, N., Wang, L., Hangaishi, A., Kurokawa, M., Chiba, S., Bailey, D.K., Kennedy, G.C. et al. (2005) A robust algorithm for copy number detection using high-density oligonucleotide single nucleotide polymorphism genotyping arrays. Cancer Res., 65, 6071-6079.
69. Hoischen, A., Gilissen, C., Arts, P., Wieskamp, N., van der Vliet, W., Vermeer, S., Steehouwer, M., de Vries, P., Meijer, R., Seiqueros, J. et al. (2010) Massively parallel sequencing of ataxia genes after array-based enrichment. Hum. Mut., 31, 494-499.
70. Gilissen, C., Arts, H.H., Hoischen, A., Spruijt, L., Mans, D.A., Arts, P., van Lier, B., Steehouwer, M., van Reeuwijk, J., Kant, S.G. et al. (2010) Exome sequencing identifies WDR35 variants involved in Sensenbrenner syndrome. Am. J. Hum. Genet., 87, 418-423.
71. Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
72. Siegel, R.W. and Hall, J.C. (1979) Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc. Natl Acad. Sci. USA, 76, 3430-3434.
73. Keleman, K., Kruttner, S., Alenius, M. and Dickson, B.J. (2007) Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat. Neurosci., 10, 1587-1593.
74. Koolen, D.A., Kramer, J.M., Neveling, K., Nillesen, W.M., Moore-Barton, H.L., Elmslie, F.V., Toutain, A., Amiel, J., Malan, V., Tsai, A.C. et al. (2012) Mutations in the chromatin modifier gene KANSL1 cause the 17q21.31 microdeletion syndrome. Nat. Genet., 44, 639-641.