Protocadherin Mutations in Neurodevelopmental Disorders

Neuronal and Synaptic Dysfunction in Autism Spectrum Disorder and Intellectual Disability

Volumn , Issue , 2016, Pages 221-231

  Pham, Duyen ^a,b   Tan, Chuan ^a   Homan, Claire ^b   Jolly, Lachlan ^a,b   Gecz, Jozef ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Adhesion molecule; Mutation; Neurodevelopmental disorder; PCDH19; Protocadherin

Indexed keywords

EID: 85011770022     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-800109-7.00014-5     Document Type: Chapter

References (98)

1. Moreno-De-Luca A., Myers S.M., Challman T.D., Moreno-De-Luca D., Evans D.W., Ledbetter D.H. Developmental brain dysfunction: revival and expansion of old concepts based on new genetic evidence. Lancet Neurol 2013, 12(4):406-414.
2. Wills C.D. DSM-5 and neurodevelopmental and other disorders of childhood and adolescence. J Am Acad Psychiatry Law 2014, 42(2):165-172.
3. Andrews G., Pine D.S., Hobbs M.J., Anderson T.M., Sunderland M. Neurodevelopmental disorders: cluster 2 of the proposed meta-structure for DSM-V and ICD-11. Psychol Med 2009, 39(12):2013-2023.
4. Doran C.M., Einfeld S.L., Madden R.H., et al. How much does intellectual disability really cost? First estimates for Australia. J Intellect Dev Disabil 2012, 37(1):42-49.
5. Mullin A.P., Gokhale A., Moreno-De-Luca A., Sanyal S., Waddington J.L., Faundez V. Neurodevelopmental disorders: mechanisms and boundary definitions from genomes, interactomes and proteomes. Transl Psychiatry 2013, 3:e329.
6. Lancet T. Wanted: a global campaign against epilepsy. Lancet 2012, 380(9848):1121.
7. Elsabbagh M., Divan G., Koh Y.J., et al. Global prevalence of autism and other pervasive developmental disorders. Autism Res 2012, 5(3):160-179.
8. SANE Australia. 2014. http://www.sane.org/information/factsheets-podcasts/199-bipolar-disorder.
9. World Health Organization (WHO). 2014. http://www.who.int/mental_health/management/schizophrenia/en/.
10. Clegg J., Gillott A., Jones J. Conceptual issues in neurodevelopmental disorders: lives out of synch. Curr Opin Psychiatry 2013, 26(3):289-294.
11. Coe B.P., Girirajan S., Eichler E.E. The genetic variability and commonality of neurodevelopmental disease. Am J Med Genet C Semin Med Genet 2012, 160C(2):118-129.
12. Sherr E.H., Michelson D.J., Shevell M.I., Moeschler J.B., Gropman A.L., Ashwal S. Neurodevelopmental disorders and genetic testing: current approaches and future advances. Ann Neurol 2013, 74(2):164-170.
13. De Rubeis S., He X., Goldberg A.P., et al. Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 2014, 515(7526):209-215.
14. Homan C.C., Kumar R., Nguyen L.S., et al. Mutations in USP9X are associated with X-linked intellectual disability and disrupt neuronal cell migration and growth. Am J Hum Genet 2014, 94(3):470-478.
15. Kahler A.K., Djurovic S., Kulle B., et al. Association analysis of schizophrenia on 18 genes involved in neuronal migration: MDGA1 as a new susceptibility gene. Am J Med Genet B Neuropsychiatr Genet 2008, 147B(7):1089-1100.
16. Redies C., Hertel N., Hubner C.A. Cadherins and neuropsychiatric disorders. Brain Res 2012, 1470:130-144.
17. Fisher R.S., Acevedo C., Arzimanoglou A., et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia 2014, 55(4):475-482.
18. Srour M., Shevell M. Genetics and the investigation of developmental delay/intellectual disability. Arch Dis Child 2014, 99(4):386-389.
19. Shoubridge C., Fullston T., Gecz J. ARX spectrum disorders: making inroads into the molecular pathology. Hum Mutat 2010, 31(8):889-900.
20. Chopra R., Isom L.L. Untangling the dravet syndrome seizure network: the changing face of a rare genetic epilepsy. Epilepsy Curr 2014, 14(2):86-89.
21. Kim S.Y., Yasuda S., Tanaka H., Yamagata K., Kim H. Non-clustered protocadherin. Cell Adh Migr 2011, 5(2):97-105.
22. Juberg R.C., Hellman C.D. A new familial form of convulsive disorder and mental retardation limited to females. J Pediatr 1971, 79(5):726-732.
23. Ryan S.G., Chance P.F., Zou C.H., Spinner N.B., Golden J.A., Smietana S. Epilepsy and mental retardation limited to females: an X-linked dominant disorder with male sparing. Nat Genet 1997, 17(1):92-95.
24. Dibbens L.M., Tarpey P.S., Hynes K., et al. X-linked protocadherin 19 mutations cause female-limited epilepsy and cognitive impairment. Nat Genet 2008, 40(6):776-781.
25. Kahr I., Vandepoele K., van Roy F. Delta-protocadherins in health and disease. Prog Mol Biol Transl Sci 2013, 116:169-192.
26. Hayashi S., Inoue Y., Kiyonari H., et al. Protocadherin-17 mediates collective axon extension by recruiting actin regulator complexes to interaxonal contacts. Dev Cell 2014, 30(6):673-687.
27. Jamal S.M., Basran R.K., Newton S., Wang Z., Milunsky J.M. Novel de novo PCDH19 mutations in three unrelated females with epilepsy female restricted mental retardation syndrome. Am J Med Genet A 2010, 152A(10):2475-2481.
28. Hynes K., Tarpey P., Dibbens L.M., et al. Epilepsy and mental retardation limited to females with PCDH19 mutations can present de novo or in single generation families. J Med Genet 2010, 47(3):211-216.
29. Higurashi N., Nakamura M., Sugai M., et al. PCDH19-related female-limited epilepsy: further details regarding early clinical features and therapeutic efficacy. Epilepsy Res 2013, 106(1-2):191-199.
30. Depienne C., Bouteiller D., Keren B., et al. Sporadic infantile epileptic encephalopathy caused by mutations in PCDH19 resembles Dravet syndrome but mainly affects females. PLoS Genet 2009, 5(2):e1000381.
31. Depienne C., LeGuern E. PCDH19-related infantile epileptic encephalopathy: an unusual X-linked inheritance disorder. Hum Mutat 2012, 33(4):627-634.
32. Scheffer I.E., Turner S.J., Dibbens L.M., et al. Epilepsy and mental retardation limited to females: an under-recognized disorder. Brain 2008, 131(Pt 4):918-927.
33. Terracciano A., Specchio N., Darra F., et al. Somatic mosaicism of PCDH19 mutation in a family with low-penetrance EFMR. Neurogenetics 2012, 13(4):341-345.
34. Tylki-Szymanska A. Mucopolysaccharidosis type II, Hunter's syndrome. Pediatr Endocrinol Rev 2014, 12(Suppl. 1):107-113.
35. Zafeiriou D.I., Pavlidou E.L., Vargiami E. Diverse clinical and genetic aspects of craniofrontonasal syndrome. Pediatr Neurol 2011, 44(2):83-87.
36. Tan C, Shard C, Ranieri E, Hynes K, Pham DH, Leach D, et al. Mutations of protocadherin 19 in female epilepsy (PCDH19-FE) lead to allopregnanolone deficiency. Hum Mol Genet September 15, 2015, 24(18):5250-5259.
37. Verrotti A., Laus M., Coppola G., Parisi P., Mohn A., Chiarelli F. Catamenial epilepsy: hormonal aspects. Gynecol Endocrinol 2010, 26(11):783-790.
38. Kim S.Y., Chung H.S., Sun W., Kim H. Spatiotemporal expression pattern of non-clustered protocadherin family members in the developing rat brain. Neuroscience 2007, 147(4):996-1021.
39. Krishna K.K., Hertel N., Redies C. Cadherin expression in the somatosensory cortex: evidence for a combinatorial molecular code at the single-cell level. Neuroscience 2011, 175:37-48.
40. Kasnauskiene J., Ciuladaite Z., Preiksaitiene E., et al. A single gene deletion on 4q28.3: PCDH18-a new candidate gene for intellectual disability?. Eur J Med Genet 2012, 55(4):274-277.
41. Hoshina N., Tanimura A., Yamasaki M., et al. Protocadherin 17 regulates presynaptic assembly in topographic corticobasal Ganglia circuits. Neuron 2013, 78(5):839-854.
42. Emond M.R., Biswas S., Blevins C.J., Jontes J.D. A complex of Protocadherin-19 and N-cadherin mediates a novel mechanism of cell adhesion. J Cell Biol 2011, 195(7):1115-1121.
43. Biswas S., Emond M.R., Jontes J.D. Protocadherin-19 and N-cadherin interact to control cell movements during anterior neurulation. J Cell Biol 2010, 191(5):1029-1041.
44. Tai K., Kubota M., Shiono K., Tokutsu H., Suzuki S.T. Adhesion properties and retinofugal expression of chicken protocadherin-19. Brain Res 2010, 1344:13-24.
45. Chen B., Brinkmann K., Chen Z., et al. The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 2014, 156(1-2):195-207.
46. Nakao S., Platek A., Hirano S., Takeichi M. Contact-dependent promotion of cell migration by the OL-protocadherin-Nap1 interaction. J Cell Biol 2008, 182(2):395-410.
47. ILAE Genetic determinants of common epilepsies: a meta-analysis of genome-wide association studies. Lancet Neurol 2014, 13(9):893-903.
48. Miyake K., Hirasawa T., Soutome M., et al. The protocadherins, PCDHB1 and PCDH7, are regulated by MeCP2 in neuronal cells and brain tissues: implication for pathogenesis of Rett syndrome. BMC Neurosci 2011, 12:81.
49. Woods A.G., Wormwood K.L., Wetie A.G., et al. Autism spectrum disorder: an omics perspective. Proteomics Clin Appl 2014, 9(1-2):159-168.
50. APA Diagnostic and statistical manual of mental disorders 2013, American Psychiatric Association, Arlington (VA). 5th ed.
51. Landrigan P.J., Lambertini L., Birnbaum L.S. A research strategy to discover the environmental causes of autism and neurodevelopmental disabilities. Environ Health Perspect 2012, 120(7):a258-a260.
52. Shelton J.F., Hertz-Picciotto I., Pessah I.N. Tipping the balance of autism risk: potential mechanisms linking pesticides and autism. Environ Health Perspect 2012, 120(7):944-951.
53. Abbeduto L., McDuffie A., Thurman A.J. The fragile X syndrome-autism comorbidity: what do we really know?. Front Genet 2014, 5:355.
54. Kohane I.S., McMurry A., Weber G., et al. The co-morbidity burden of children and young adults with autism spectrum disorders. PLoS One 2012, 7(4):e33224.
55. Rosenberg R.E., Law J.K., Yenokyan G., McGready J., Kaufmann W.E., Law P.A. Characteristics and concordance of autism spectrum disorders among 277 twin pairs. Arch Pediatr Adolesc Med 2009, 163(10):907-914.
56. Abrahams B.S., Geschwind D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 2008, 9(5):341-355.
57. Ozonoff S., Young G.S., Carter A., et al. Recurrence risk for autism spectrum disorders: a Baby Siblings Research Consortium study. Pediatrics 2011, 128(3):e488-495.
58. Geschwind D.H. Genetics of autism spectrum disorders. Trends Cogn Sci 2011, 15(9):409-416.
59. O'Roak B.J., Deriziotis P., Lee C., et al. Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat Genet 2011, 43(6):585-589.
60. Anney R., Klei L., Pinto D., et al. Individual common variants exert weak effects on the risk for autism spectrum disorderspi. Hum Mol Genet 2012, 21(21):4781-4792.
61. Talkowski M.E., Minikel E.V., Gusella J.F. Autism spectrum disorder genetics: diverse genes with diverse clinical outcomes. Harv Rev Psychiatry 2014, 22(2):65-75.
62. Gaugler T., Klei L., Sanders S.J., et al. Most genetic risk for autism resides with common variation. Nat Genet 2014, 46(8):881-885.
63. PCDH19 Alliance. 2014. http://www.pcdh19info.org/pcdh19-epilepsy.html.
64. Piton A., Gauthier J., Hamdan F.F., et al. Systematic resequencing of X-chromosome synaptic genes in autism spectrum disorder and schizophrenia. Mol Psychiatry 2011, 16(8):867-880.
65. van Harssel J.J., Weckhuysen S., van Kempen M.J., et al. Clinical and genetic aspects of PCDH19-related epilepsy syndromes and the possible role of PCDH19 mutations in males with autism spectrum disorders. Neurogenetics 2013, 14(1):23-34.
66. Aoki E., Kimura R., Suzuki S.T., Hirano S. Distribution of OL-protocadherin protein in correlation with specific neural compartments and local circuits in the postnatal mouse brain. Neuroscience 2003, 117(3):593-614.
67. Williams E.O., Sickles H.M., Dooley A.L., Palumbos S., Bisogni A.J., Lin D.M. Delta protocadherin 10 is regulated by activity in the mouse main olfactory system. Front Neural Circuits 2011, 5:9.
68. Morrow E.M., Yoo S.Y., Flavell S.W., et al. Identifying autism loci and genes by tracing recent shared ancestry. Science 2008, 321(5886):218-223.
69. Uemura M., Nakao S., Suzuki S.T., Takeichi M., Hirano S. OL-Protocadherin is essential for growth of striatal axons and thalamocortical projections. Nat Neurosci 2007, 10(9):1151-1159.
70. Marshall C.R., Noor A., Vincent J.B., et al. Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet 2008, 82(2):477-488.
71. Asahina H., Masuba A., Hirano S., Yuri K. Distribution of protocadherin 9 protein in the developing mouse nervous system. Neuroscience 2012, 225:88-104.
72. Hertel N., Redies C. Absence of layer-specific cadherin expression profiles in the neocortex of the reeler mutant mouse. Cereb Cortex 2011, 21(5):1105-1117.
73. Anitha A., Thanseem I., Nakamura K., et al. Protocadherin alpha (PCDHA) as a novel susceptibility gene for autism. J Psychiatry Neurosci 2013, 38(3):192-198.
74. Iossifov I., Ronemus M., Levy D., et al. De novo gene disruptions in children on the autistic spectrum. Neuron 2012, 74(2):285-299.
75. Hasegawa S., Hirabayashi T., Kondo T., et al. Constitutively expressed protocadherin-alpha regulates the coalescence and elimination of homotypic olfactory axons through its cytoplasmic region. Front Mol Neurosci 2012, 5:97.
76. Hasegawa S., Hamada S., Kumode Y., et al. The protocadherin-alpha family is involved in axonal coalescence of olfactory sensory neurons into glomeruli of the olfactory bulb in mouse. Mol Cell Neurosci 2008, 38(1):66-79.
77. Katori S., Hamada S., Noguchi Y., et al. Protocadherin-alpha family is required for serotonergic projections to appropriately innervate target brain areas. J Neurosci 2009, 29(29):9137-9147.
78. Kepser L.J., Homberg J.R. The neurodevelopmental effects of serotonin: a behavioural perspective. Behav Brain Res 2014, 277:3-13.
79. Tsai N.P., Wilkerson J.R., Guo W., et al. Multiple autism-linked genes mediate synapse elimination via proteasomal degradation of a synaptic scaffold PSD-95. Cell 2012, 151(7):1581-1594.
80. Potthoff M.J., Olson E.N. MEF2: a central regulator of diverse developmental programs. Development 2007, 134(23):4131-4140.
81. Pfeiffer B.E., Zang T., Wilkerson J.R., et al. Fragile X mental retardation protein is required for synapse elimination by the activity-dependent transcription factor MEF2. Neuron 2010, 66(2):191-197.
82. Dietrich J.B. The MEF2 family and the brain: from molecules to memory. Cell Tissue Res 2013, 352(2):179-190.
83. Rashid A.J., Cole C.J., Josselyn S.A. Emerging roles for MEF2 transcription factors in memory. Genes Brain Behav 2014, 13(1):118-125.
84. Zang T., Maksimova M.A., Cowan C.W., Bassel-Duby R., Olson E.N., Huber K.M. Postsynaptic FMRP bidirectionally regulates excitatory synapses as a function of developmental age and MEF2 activity. Mol Cell Neurosci 2013, 56:39-49.
85. Stratford H.J., Cooper M.J., Di Simplicio M., Blackwell S.E., Holmes E.A. Psychological therapy for anxiety in bipolar spectrum disorders: a systematic review. Clin Psychol Rev 2014, 35C:19-34.
86. Sanches M., Keshavan M.S., Brambilla P., Soares J.C. Neurodevelopmental basis of bipolar disorder: a critical appraisal. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32(7):1617-1627.
87. Smoller J.W., Finn C.T. Family, twin, and adoption studies of bipolar disorder. Am J Med Genet C Semin Med Genet 2003, 123C(1):48-58.
88. Berrettini W. Review of bipolar molecular linkage and association studies. Curr Psychiatry Rep 2002, 4(2):124-129.
89. Vandeleur C.L., Merikangas K.R., Strippoli M.P., Castelao E., Preisig M. Specificity of psychosis, mania and major depression in a contemporary family study. Mol Psychiatry 2014, 19(2):209-213.
90. Schwab S.G., Eckstein G.N., Hallmayer J., et al. Evidence suggestive of a locus on chromosome 5q31 contributing to susceptibility for schizophrenia in German and Israeli families by multipoint affected sib-pair linkage analysis. Mol Psychiatry 1997, 2(2):156-160.
91. Straub R.E., MacLean C.J., Ma Y., et al. Genome-wide scans of three independent sets of 90 Irish multiplex schizophrenia families and follow-up of selected regions in all families provides evidence for multiple susceptibility genes. Mol Psychiatry 2002, 7(6):542-559.
92. Hong K.S., McInnes L.A., Service S.K., et al. Genetic mapping using haplotype and model-free linkage analysis supports previous evidence for a locus predisposing to severe bipolar disorder at 5q31-33. Am J Med Genet B Neuropsychiatr Genet 2004, 125B(1):83-86.
93. Chen W.V., Maniatis T. Clustered protocadherins. Development 2013, 140(16):3297-3302.
94. Pedrosa E., Stefanescu R., Margolis B., et al. Analysis of protocadherin alpha gene enhancer polymorphism in bipolar disorder and schizophrenia. Schizophr Res 2008, 102(1-3):210-219.
95. Durand C.M., Kappeler C., Betancur C., et al. Expression and genetic variability of PCDH11Y, a gene specific to Homo sapiens and candidate for susceptibility to psychiatric disorders. Am J Med Genet B Neuropsychiatr Genet 2006, 141B(1):67-70.
96. Noonan J.P., Li J., Nguyen L., et al. Extensive linkage disequilibrium, a common 16.7-kilobase deletion, and evidence of balancing selection in the human protocadherin alpha cluster. Am J Hum Genet 2003, 72(3):621-635.
97. Bray N.J., Kirov G., Owen R.J., et al. Screening the human protocadherin 8 (PCDH8) gene in schizophrenia. Genes Brain Behav 2002, 1(3):187-191.
98. Dean B., Keriakous D., Scarr E., Thomas E.A. Gene expression profiling in Brodmann's area 46 from subjects with schizophrenia. Aust NZ J Psychiatry 2007, 41(4):308-320.