Cadherin-13, a risk gene for ADHD and comorbid disorders, impacts GABAergic function in hippocampus and cognition

Translational Psychiatry

Volumn 5, Issue 10, 2015, Pages

  Rivero, O ^a   Selten, M M ^b   Sich, S ^a   Popp, S ^a   Bacmeister, L ^a   Amendola, E ^c   Negwer, M ^b   Schubert, D ^b   Proft, F ^a   Kiser, D ^a   Schmitt, A G ^a   Gross, C ^c   Kolk, S M ^b   Strekalova, T ^d   Van Den Hove, D ^d   Resink, T J ^e   Nadif Kasri, N ^b   Lesch, K P ^a,d  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b RADBOUD UNIVERSITY   (Netherlands)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^d MAASTRICHT UNIVERSITY   (Netherlands)

^e UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID RECEPTOR; CADHERIN; CADHERIN 13; CALBINDIN; CALRETININ; GEPHYRIN; GLUTAMATE DECARBOXYLASE; GLYCOSYLPHOSPHATIDYLINOSITOL; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE; PARVALBUMIN; POSTSYNAPTIC DENSITY PROTEIN 95; SOMATOSTATIN; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; 4 AMINOBUTYRIC ACID; H-CADHERIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENTION DEFICIT DISORDER; BRAIN ELECTROPHYSIOLOGY; CELLULAR DISTRIBUTION; CLINICAL EVALUATION; COGNITION; COGNITIVE DEFECT; COMORBIDITY; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ENZYME INACTIVATION; GABAERGIC SYSTEM; GENE EXPRESSION; GENETIC RISK; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; INTERNEURON; LEARNING DISORDER; LOCOMOTION; MALE; MEMORY DISORDER; MOUSE; NEUROMODULATION; NONHUMAN; PHENOTYPIC VARIATION; PYRAMIDAL NERVE CELL; RISK ASSESSMENT; RISK FACTOR; STRATUM ORIENS; SYNAPTIC TRANSMISSION; ANIMAL; DISEASE MODEL; GENETICS; LEARNING; MEMORY; MENTAL DISEASE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; TUMOR SUPPRESSOR GENE;

ANIMALS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CADHERINS; DISEASE MODELS, ANIMAL; GAMMA-AMINOBUTYRIC ACID; GENES, TUMOR SUPPRESSOR; HIPPOCAMPUS; INTERNEURONS; LEARNING; MEMORY; MICE; PSYCHOPATHOLOGY; SYNAPTIC TRANSMISSION;

EID: 84977763654     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.152     Document Type: Article

References (81)

1. Hirano S, Takeichi M. Cadherins in brain morphogenesis and wiring. Physiol Rev 2012; 92: 597-634.
2. Philippova M, Joshi MB, Kyriakakis E, Pfaff D, Erne P, Resink TJ. A guide and guard: The many faces of T-cadherin. Cell Signal 2009; 21: 1035-1044.
3. Ranscht B, Dours-Zimmermann MT. T-cadherin, a novel cadherin cell adhesion molecule in the nervous system lacks the conserved cytoplasmic region. Neuron 1991; 7: 391-402.
4. Rivero O, Sich S, Popp S, Schmitt A, Franke B, Lesch KP. Impact of the ADHDsusceptibility gene CDH13 on development and function of brain networks. Eur Neuropsychopharmacol 2013; 23: 492-507.
5. Arias-Vasquez A, Altink ME, Rommelse NN, Slaats-Willemse DI, Buschgens CJ, Fliers EA et al. CDH13 is associated with working memory performance in attention deficit/hyperactivity disorder. Genes Brain Behav 2011; 10: 844-851.
6. Doyle A, Faraone SV, MgGrath L, Thermenos H, Juelich R, Chaponis J et al. Multivariate association of CDH13 variants and cortical thickness in ADHD. Biol Psychiatry 2014; 75: 347S.
7. Edwards AC, Aliev F, Bierut LJ, Bucholz KK, Edenberg H, Hesselbrock V et al. Genome-wide association study of comorbid depressive syndrome and alcohol dependence. Psychiatr Genet 2012; 22: 31-41.
8. Hart AB, Engelhardt BE, Wardle MC, Sokoloff G, Stephens M, de Wit H et al. Genome-wide association study of d-Amphetamine response in healthy volunteers identifies putative associations, including cadherin 13 (CDH13). PLoS One 2012; 7: E42646.
9. Lesch KP, Timmesfeld N, Renner TJ, Halperin R, Roser C, Nguyen TT et al. Molecular genetics of adult ADHD: Converging evidence from genome-wide association and extended pedigree linkage studies. J Neural Transm 2008; 115: 1573-1585.
10. Mavroconstanti T, Halmoy A, Haavik J. Decreased serum levels of adiponectin in adult attention deficit hyperactivity disorder. Psychiatry Res 2014; 216: 123-130.
11. Neale BM, Lasky-Su J, Anney R, Franke B, Zhou K, Maller JB et al. Genome-wide association scan of attention deficit hyperactivity disorder. Am J Med Genet B Neuropsychiatr Genet 2008; 147B: 1337-1344.
12. Neale BM, Medland SE, Ripke S, Asherson P, Franke B, Lesch KP et al. Meta-Analysis of genome-wide association studies of attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 2010; 49: 884-897.
13. Treutlein J, Cichon S, Ridinger M, Wodarz N, Soyka M, Zill P et al. Genome-wide association study of alcohol dependence. Arch Gen Psychiatry 2009; 66: 773-784.
14. Uhl GR, Drgon T, Johnson C, Li CY, Contoreggi C, Hess J et al. Molecular genetics of addiction and related heritable phenotypes: Genome-wide association approaches identify 'connectivity constellation' and drug target genes with pleiotropic effects. Ann N Y Acad Sci 2008; 1141: 318-381.
15. Uhl GR, Drgon T, Liu QR, Johnson C, Walther D, Komiyama T et al. Genome-wide association for methamphetamine dependence: Convergent results from 2 samples. Arch Gen Psychiatry 2008; 65: 345-355.
16. Yang J, Wang S, Yang Z, Hodgkinson CA, Iarikova P, Ma JZ et al. The contribution of rare and common variants in 30 genes to risk nicotine dependence. Mol Psychiatry; e-pub ahead of print 2 December 2014; doi: 10.1038/mp.2014.156.
17. Zhou K, Dempfle A, Arcos-Burgos M, Bakker SC, Banaschewski T, Biederman J et al. Meta-Analysis of genome-wide linkage scans of attention deficit hyperactivity disorder. Am J Med Genet B Neuropsychiatr Genet 2008; 147B: 1392-1398.
18. Sibille E, Wang Y, Joeyen-Waldorf J, Gaiteri C, Surget A, Oh S et al. A molecular signature of depression in the amygdala. Am J Psychiatry 2009; 166: 1011-1024.
19. Sanders SJ, Ercan-Sencicek AG, Hus V, Luo R, Murtha MT, Moreno-De-Luca D et al. Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism. Neuron 2011; 70: 863-885.
20. Borglum AD, Demontis D, Grove J, Pallesen J, Hollegaard MV, Pedersen CB et al. Genome-wide study of association and interaction with maternal cytomegalovirus infection suggests new schizophrenia loci. Mol Psychiatry 2014; 19: 325-333.
21. Xu W, Cohen-Woods S, Chen Q, Noor A, Knight J, Hosang G et al. Genome-wide association study of bipolar disorder in Canadian and UK populations corroborates disease loci including SYNE1 and CSMD1. BMC Med Genet 2014; 15: 2.
22. Terracciano A, Sanna S, Uda M, Deiana B, Usala G, Busonero F et al. Genome-wide association scan for five major dimensions of personality. Mol Psychiatry 2010; 15: 647-656.
23. Tiihonen J, Rautiainen MR, Ollila HM, Repo-Tiihonen E, Virkkunen M, Palotie A et al. Genetic background of extreme violent behavior. Mol Psychiatry 2014; 20: 786-792.
24. Bai S, Ghoshal K, Jacob ST. Identification of T-cadherin as a novel target of DNA methyltransferase 3B and its role in the suppression of nerve growth factormediated neurite outgrowth in PC12 cells. J Biol Chem 2006; 281: 13604-13611.
25. Ciatto C, Bahna F, Zampieri N, VanSteenhouse HC, Katsamba PS, Ahlsen G et al. Tcadherin structures reveal a novel adhesive binding mechanism. Nat Struct Mol Biol 2010; 17: 339-347.
26. Fredette BJ, Miller J, Ranscht B. Inhibition of motor axon growth by T-cadherin substrata. Development 1996; 122: 3163-3171.
27. Fredette BJ, Ranscht B. T-cadherin expression delineates specific regions of the developing motor axon-hindlimb projection pathway. J Neurosci 1994; 14: 7331-7346.
28. Takeuchi T, Misaki A, Liang SB, Tachibana A, Hayashi N, Sonobe H et al. Expression of T-cadherin (CDH13, H-Cadherin) in human brain and its characteristics as a negative growth regulator of epidermal growth factor in neuroblastoma cells. J Neurochem 2000; 74: 1489-1497.
29. Hayano Y, Zhao H, Kobayashi H, Takeuchi K, Norioka S, Yamamoto N. The role of T-cadherin in axonal pathway formation in neocortical circuits. Development 2014; 141: 4784-4793.
30. Paradis S, Harrar DB, Lin Y, Koon AC, Hauser JL, Griffith EC et al. An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 2007; 53: 217-232.
31. Schwenk F, Baron U, Rajewsky K. A cre-Transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 1995; 23: 5080-5081.
32. Nadif Kasri N, Nakano-Kobayashi A, Van Aelst L. Rapid synthesis of the X-linked mental retardation protein OPHN1 mediates mGluR-dependent LTD through interaction with the endocytic machinery. Neuron 2011; 72: 300-315.
33. Tricoire L, Pelkey KA, Erkkila BE, Jeffries BW, Yuan X, McBain CJ. A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J Neurosci 2011; 31: 10948-10970.
34. Marx M, Gunter RH, Hucko W, Radnikow G, Feldmeyer D. Improved biocytin labeling and neuronal 3D reconstruction. Nat Protoc 2012; 7: 394-407.
35. Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J. The Hippocampus Book. Oxford University Press: New York, NY, USA, 2006.
36. Miyoshi G, Butt SJ, Takebayashi H, Fishell G. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J Neurosci 2007; 27: 7786-7798.
37. Steward O, Falk PM. Selective localization of polyribosomes beneath developing synapses: A quantitative analysis of the relationships between polyribosomes and developing synapses in the hippocampus and dentate gyrus. J Comp Neurol 1991; 314: 545-557.
38. Hebbard LW, Garlatti M, Young LJ, Cardiff RD, Oshima RG, Ranscht B. T-cadherin supports angiogenesis and adiponectin association with the vasculature in a mouse mammary tumor model. Cancer Res 2008; 68: 1407-1416.
39. Williams NM, Zaharieva I, Martin A, Langley K, Mantripragada K, Fossdal R et al. Rare chromosomal deletions and duplications in attention-deficit hyperactivity disorder: A genome-wide analysis. Lancet 2010; 376: 1401-1408.
40. Lionel AC, Crosbie J, Barbosa N, Goodale T, Thiruvahindrapuram B, Rickaby J et al. Rare copy number variation discovery and cross-disorder comparisons identify risk genes for ADHD. Sci Transl Med 2011; 3: 95ra75.
41. Jinno S, Kosaka T. Cellular architecture of the mouse hippocampus: A quantitative aspect of chemically defined GABAergic neurons with stereology. Neurosci Res 2006; 56: 229-245.
42. Marin O. Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 2012; 13: 107-120.
43. Ramamoorthi K, Lin Y. The contribution of GABAergic dysfunction to neurodevelopmental disorders. Trends Mol Med 2011; 17: 452-462.
44. Kluge C, Stoppel C, Szinyei C, Stork O, Pape HC. Role of the somatostatin system in contextual fear memory and hippocampal synaptic plasticity. Learn Mem 2008; 15: 252-260.
45. Fiederling A, Ewert R, Andreyeva A, Jungling K, Gottmann K. E-cadherin is required at GABAergic synapses in cultured cortical neurons. Neurosci Lett 2011; 501: 167-172.
46. Li Y, Xiao H, Chiou TT, Jin H, Bonhomme B, Miralles CP et al. Molecular and functional interaction between protocadherin-gammaC5 and GABAA receptors. J Neurosci 2012; 32: 11780-11797.
47. Najarro EH, Wong L, Zhen M, Carpio EP, Goncharov A, Garriga G et al. Caenorhabditis elegans flamingo cadherin fmi-1 regulates GABAergic neuronal development. J Neurosci 2012; 32: 4196-4211.
48. Nikitczuk JS, Patil SB, Matikainen-Ankney BA, Scarpa J, Shapiro ML, Benson DL et al. N-cadherin regulates molecular organization of excitatory and inhibitory synaptic circuits in adult hippocampus in vivo. Hippocampus 2014; 24: 943-962.
49. Johnston D, Amaral DG. Hippocampus. In: Sheperd GM (ed). The Synaptic Organization of the Brain. Oxford University Press: New York, NY, USA, 2003, pp 455-498.
50. Edden RA, Crocetti D, Zhu H, Gilbert DL, Mostofsky SH. Reduced GABA concentration in attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 2012; 69: 750-753.
51. Ahrens S, Jaramillo S, Yu K, Ghosh S, Hwang GR, Paik R et al. ErbB4 regulation of a thalamic reticular nucleus circuit for sensory selection. Nat Neurosci 2015; 18: 104-111.
52. Kremkow J, Aertsen A, Kumar A. Gating of signal propagation in spiking neural networks by balanced and correlated excitation and inhibition. J Neurosci 2010; 30: 15760-15768.
53. Olshausen BA, Anderson CH, Van Essen DC. A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information. J Neurosci 1993; 13: 4700-4719.
54. Vogels TP, Abbott LF. Signal propagation and logic gating in networks of integrate-And-fire neurons. J Neurosci 2005; 25: 10786-10795.
55. Farzan F, Barr MS, Levinson AJ, Chen R, Wong W, Fitzgerald PB et al. Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia. Brain 2010; 133(Pt 5): 1505-1514.
56. Fazzari P, Paternain AV, Valiente M, Pla R, Lujan R, Lloyd K et al. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 2010; 464: 1376-1380.
57. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005; 6: 312-324.
58. Ongur D, Prescot AP, McCarthy J, Cohen BM, Renshaw PF. Elevated gammaaminobutyric acid levels in chronic schizophrenia. Biol Psychiatry 2010; 68: 667-670.
59. Neddens J, Buonanno A. Selective populations of hippocampal interneurons express ErbB4 and their number and distribution is altered in ErbB4 knockout mice. Hippocampus 2010; 20: 724-744.
60. Vullhorst D, Neddens J, Karavanova I, Tricoire L, Petralia RS, McBain CJ et al. Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J Neurosci 2009; 29: 12255-12264.
61. Chen YJ, Zhang M, Yin DM, Wen L, Ting A, Wang P et al. ErbB4 in parvalbuminpositive interneurons is critical for neuregulin 1 regulation of long-Term potentiation. Proc Natl Acad Sci USA 2010; 107: 21818-21823.
62. Shamir A, Kwon OB, Karavanova I, Vullhorst D, Leiva-Salcedo E, Janssen MJ et al. The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J Neurosci 2012; 32: 2988-2997.
63. Gibson JR, Huber KM, Sudhof TC. Neuroligin-2 deletion selectively decreases inhibitory synaptic transmission originating from fast-spiking but not from somatostatin-positive interneurons. J Neurosci 2009; 29: 13883-13897.
64. Foldy C, Malenka RC, Sudhof TC. Autism-Associated neuroligin-3 mutations commonly disrupt tonic endocannabinoid signaling. Neuron 2013; 78: 498-509.
65. Aloy EM, Weinmann O, Pot C, Kasper H, Dodd DA, Rulicke T et al. Synaptic destabilization by neuronal Nogo-A. Brain Cell Biol 2006; 35: 137-156.
66. Andreyeva A, Nieweg K, Horstmann K, Klapper S, Muller-Schiffmann A, Korth C et al. C-Terminal fragment of N-cadherin accelerates synapse destabilization by amyloid-beta. Brain 2012; 135(Pt 7): 2140-2154.
67. Philippova M, Ivanov D, Joshi MB, Kyriakakis E, Rupp K, Afonyushkin T et al. Identification of proteins associating with glycosylphosphatidylinositol-Anchored T-cadherin on the surface of vascular endothelial cells: Role for Grp78/BiP in T-cadherin-dependent cell survival. Mol Cell Biol 2008; 28: 4004-4017.
68. Joshi MB, Ivanov D, Philippova M, Erne P, Resink TJ. Integrin-linked kinase is an essential mediator for T-cadherin-dependent signaling via Akt and GSK3beta in endothelial cells. FASEB J 2007; 21: 3083-3095.
69. Philippova M, Ivanov D, Allenspach R, Takuwa Y, Erne P, Resink T. RhoA and Rac mediate endothelial cell polarization and detachment induced by T-cadherin. FASEB J 2005; 19: 588-590.
70. Oosterlaan J, Logan GD, Sergeant JA. Response inhibition in AD/HD, CD, comorbid AD/HD+CD, anxious, and control children: A meta-Analysis of studies with the stop task. J Child Psychol Psychiatry 1998; 39: 411-425.
71. Oosterlaan J, Sergeant JA. Response inhibition and response re-engagement in attention-deficit/hyperactivity disorder, disruptive, anxious and normal children. Behav Brain Res 1998; 94: 33-43.
72. Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF. Validity of the executive function theory of attention-deficit/hyperactivity disorder: A metaanalytic review. Biol Psychiatry 2005; 57: 1336-1346.
73. Kleschevnikov AM, Belichenko PV, Villar AJ, Epstein CJ, Malenka RC, Mobley WC. Hippocampal long-Term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J Neurosci 2004; 24: 8153-8160.
74. Reeves RH, Irving NG, Moran TH, Wohn A, Kitt C, Sisodia SS et al. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat Genet 1995; 11: 177-184.
75. Costa RM, Federov NB, Kogan JH, Murphy GG, Stern J, Ohno M et al. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 2002; 415: 526-530.
76. Amitai N, Markou A. Comparative effects of different test day challenges on performance in the 5-choice serial reaction time task. Behav Neurosci 2011; 125: 764-774.
77. Gratten J, Wray NR, Keller MC, Visscher PM. Large-scale genomics unveils the genetic architecture of psychiatric disorders. Nat Neurosci 2014; 17: 782-790.
78. Denzel MS, Scimia MC, Zumstein PM, Walsh K, Ruiz-Lozano P, Ranscht B. T-cadherin is critical for adiponectin-mediated cardioprotection in mice. J Clin Invest 2010; 120: 4342-4352.
79. Geissler J, Lesch KP. A lifetime of attention-deficit/hyperactivity disorder: Diagnostic challenges, treatment and neurobiological mechanisms. Expert Rev Neurother 2011; 11: 1467-1484.
80. Bolivar VJ. Intrasession and intersession habituation in mice: From inbred strain variability to linkage analysis. Neurobiol Learn Mem 2009; 92: 206-214.
81. Lesch KP, Araragi N, Waider J, van den Hove D, Gutknecht L. Targeting brain serotonin synthesis: Insights into neurodevelopmental disorders with long-Term outcomes related to negative emotionality, aggression and antisocial behaviour. Philos Trans R Soc Lond B Biol Sci 2012; 367: 2426-2443.