Functional Properties of Rare Missense Variants of Human CDH13 Found in Adult Attention Deficit/Hyperactivity Disorder (ADHD) Patients

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Mavroconstanti, Thegna ^a,b   Johansson, Stefan ^a,b   Winge, Ingeborg ^a   Knappskog, Per M ^a,b   Haavik, Jan ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ADULT; ANIMAL CELL; ARTICLE; ATTENTION DEFICIT DISORDER; CDH13 GENE; CELL STRAIN HEK293; CHO CELL; CONTROLLED STUDY; EMBRYO; FEMALE; GENE FREQUENCY; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MISSENSE MUTATION; MUTATOR GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SEQUENCE ANALYSIS; WILD TYPE;

ADULT; ANIMALS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CADHERINS; CASE-CONTROL STUDIES; CHO CELLS; COMPUTATIONAL BIOLOGY; CRICETINAE; CRICETULUS; GENOTYPING TECHNIQUES; HEK293 CELLS; HUMANS; MUTATION, MISSENSE;

EID: 84880984788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071445     Document Type: Article

References (59)

1. Mouaffak F, Kebir O, Chayet M, Tordjman S, Vacheron MN, et al. (2011) Association of Disrupted in Schizophrenia 1 (DISC1) missense variants with ultra-resistant schizophrenia. Pharmacogenomics J 11: 267-273.
2. Lepagnol-Bestel AM, Dubertret C, Benmessaoud D, Simonneau M, Ades J, et al. (2010) Association of DISC1 gene with schizophrenia in families from two distinct French and Algerian populations. Psychiatr Genet 20: 298-303.
3. Franke B, Faraone SV, Asherson P, Buitelaar J, Bau CH, et al. (2011) The genetics of attention deficit/hyperactivity disorder in adults, a review. Molecular psychiatry.
4. Rivero O, Sich S, Popp S, Schmitt A, Franke B, et al. (2012) Impact of the ADHD-susceptibility gene CDH13 on development and function of brain networks. European neuropsychopharmacology: the journal of the European College of Neuropsychopharmacology.
5. Neale BM, Lasky-Su J, Anney R, Franke B, Zhou K, et al. (2008) Genome-wide association scan of attention deficit hyperactivity disorder. American journal of medical genetics Part B, Neuropsychiatric genetics: the official publication of the International Society of Psychiatric Genetics 147B: 1337-1344.
6. Lesch KP, Timmesfeld N, Renner TJ, Halperin R, Roser C, et al. (2008) Molecular genetics of adult ADHD: converging evidence from genome-wide association and extended pedigree linkage studies. Journal of neural transmission 115: 1573-1585.
7. Landaas ET, Johansson S, Jacobsen KK, Ribases M, Bosch R, et al. (2010) An international multicenter association study of the serotonin transporter gene in persistent ADHD. Genes, brain, and behavior 9: 449-458.
8. Lantieri F, Glessner JT, Hakonarson H, Elia J, Devoto M, (2010) Analysis of GWAS top hits in ADHD suggests association to two polymorphisms located in genes expressed in the cerebellum. American journal of medical genetics Part B, Neuropsychiatric genetics: the official publication of the International Society of Psychiatric Genetics 153B: 1127-1133.
9. Hinney A, Scherag A, Jarick I, Albayrak O, Putter C, et al. (2011) Genome-wide association study in German patients with attention deficit/hyperactivity disorder. American journal of medical genetics Part B, Neuropsychiatric genetics: the official publication of the International Society of Psychiatric Genetics 156B: 888-897.
10. Stergiakouli E, Hamshere M, Holmans P, Langley K, Zaharieva I, et al. (2012) Investigating the contribution of common genetic variants to the risk and pathogenesis of ADHD. The American journal of psychiatry 169: 186-194.
11. Elia J, Glessner JT, Wang K, Takahashi N, Shtir CJ, et al. (2012) Genome-wide copy number variation study associates metabotropic glutamate receptor gene networks with attention deficit hyperactivity disorder. Nature genetics 44: 78-84.
12. Zhou K, Dempfle A, Arcos-Burgos M, Bakker SC, Banaschewski T, et al. (2008) Meta-analysis of genome-wide linkage scans of attention deficit hyperactivity disorder. American journal of medical genetics Part B, Neuropsychiatric genetics: the official publication of the International Society of Psychiatric Genetics 147B: 1392-1398.
13. Uhl GR, Drgon T, Liu QR, Johnson C, Walther D, et al. (2008) Genome-wide association for methamphetamine dependence: convergent results from 2 samples. Arch Gen Psychiatry 65: 345-355.
14. Treutlein J, Cichon S, Ridinger M, Wodarz N, Soyka M, et al. (2009) Genome-wide association study of alcohol dependence. Arch Gen Psychiatry 66: 773-784.
15. Edwards AC, Aliev F, Bierut LJ, Bucholz KK, Edenberg H, et al. (2012) Genome-wide association study of comorbid depressive syndrome and alcohol dependence. Psychiatr Genet 22: 31-41.
16. Vestal DJ, Ranscht B, (1992) Glycosyl phosphatidylinositol-anchored T-cadherin mediates calcium-dependent, homophilic cell adhesion. The Journal of cell biology 119: 451-461.
17. Ranscht B, Dours-Zimmermann MT, (1991) T-cadherin, a novel cadherin cell adhesion molecule in the nervous system lacks the conserved cytoplasmic region. Neuron 7: 391-402.
18. Zhou S, Matsuyoshi N, Liang SB, Takeuchi T, Ohtsuki Y, et al. (2002) Expression of T-cadherin in Basal keratinocytes of skin. The Journal of investigative dermatology 118: 1080-1084.
19. Dames SA, Bang E, Haussinger D, Ahrens T, Engel J, et al. (2008) Insights into the low adhesive capacity of human T-cadherin from the NMR structure of Its N-terminal extracellular domain. The Journal of biological chemistry 283: 23485-23495.
20. Fredette BJ, Miller J, Ranscht B, (1996) Inhibition of motor axon growth by T-cadherin substrata. Development 122: 3163-3171.
21. Rubina K, Kalinina N, Potekhina A, Efimenko A, Semina E, et al. (2007) T-cadherin suppresses angiogenesis in vivo by inhibiting migration of endothelial cells. Angiogenesis 10: 183-195.
22. Kyriakakis E, Philippova M, Joshi MB, Pfaff D, Bochkov V, et al. (2010) T-cadherin attenuates the PERK branch of the unfolded protein response and protects vascular endothelial cells from endoplasmic reticulum stress-induced apoptosis. Cellular signalling 22: 1308-1316.
23. Philippova M, Ivanov D, Joshi MB, Kyriakakis E, Rupp K, et al. (2008) 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. Molecular and cellular biology 28: 4004-4017.
24. Rubina K, Talovskaya E, Cherenkov V, Ivanov D, Stambolsky D, et al. (2005) LDL induces intracellular signalling and cell migration via atypical LDL-binding protein T-cadherin. Molecular and cellular biochemistry 273: 33-41.
25. Takeuchi T, Misaki A, Liang SB, Tachibana A, Hayashi N, et al. (2000) 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. Journal of neurochemistry 74: 1489-1497.
26. Wu Y, Li Y, Lange EM, Croteau-Chonka DC, Kuzawa CW, et al. (2010) Genome-wide association study for adiponectin levels in Filipino women identifies CDH13 and a novel uncommon haplotype at KNG1-ADIPOQ. Human molecular genetics 19: 4955-4964.
27. Morisaki H, Yamanaka I, Iwai N, Miyamoto Y, Kokubo Y, et al. (2012) CDH13 gene coding T-cadherin influences variations in plasma adiponectin levels in the Japanese population. Human mutation 33: 402-410.
28. Fava C, Danese E, Montagnana M, Sjogren M, Almgren P, et al. (2011) A variant upstream of the CDH13 adiponectin receptor gene and metabolic syndrome in Swedes. The American journal of cardiology 108: 1432-1437.
29. Chung CM, Lin TH, Chen JW, Leu HB, Yang HC, et al. (2011) A genome-wide association study reveals a quantitative trait locus of adiponectin on CDH13 that predicts cardiometabolic outcomes. Diabetes 60: 2417-2423.
30. Denzel MS, Scimia MC, Zumstein PM, Walsh K, Ruiz-Lozano P, et al. (2010) T-cadherin is critical for adiponectin-mediated cardioprotection in mice. The Journal of clinical investigation 120: 4342-4352.
31. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American journal of human genetics 81: 559-575.
32. Halmoy A, Fasmer OB, Gillberg C, Haavik J, (2009) Occupational outcome in adult ADHD: impact of symptom profile, comorbid psychiatric problems, and treatment: a cross-sectional study of 414 clinically diagnosed adult ADHD patients. Journal of attention disorders 13: 175-187.
33. Johansson S, Halleland H, Halmoy A, Jacobsen KK, Landaas ET, et al. (2008) Genetic analyses of dopamine related genes in adult ADHD patients suggest an association with the DRD5-microsatellite repeat, but not with DRD4 or SLC6A3 VNTRs. American journal of medical genetics Part B, Neuropsychiatric genetics: the official publication of the International Society of Psychiatric Genetics 147B: 1470-1475.
34. Bava KA, Gromiha MM, Uedaira H, Kitajima K, Sarai A, (2004) ProTherm, version 4.0: thermodynamic database for proteins and mutants. Nucleic Acids Res 32: D120-121.
35. Ciatto C, Bahna F, Zampieri N, VanSteenhouse HC, Katsamba PS, et al. (2010) T-cadherin structures reveal a novel adhesive binding mechanism. Nature structural & molecular biology 17: 339-347.
36. Sim NL, Kumar P, Hu J, Henikoff S, Schneider G, et al. (2012) SIFT web server: predicting effects of amino acid substitutions on proteins. Nucleic Acids Res 40: W452-457.
37. Kumar P, Henikoff S, Ng PC, (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073-1081.
38. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249.
39. Capriotti E, Fariselli P, Casadio R, (2005) I-Mutant2.0: predicting stability changes upon mutation from the protein sequence or structure. Nucleic Acids Res 33: W306-310.
40. Capriotti E, Fariselli P, Rossi I, Casadio R, (2008) A three-state prediction of single point mutations on protein stability changes. BMC Bioinformatics 9Suppl 2: S6.
41. Thomas P, Smart TG, (2005) HEK293 cell line: a vehicle for the expression of recombinant proteins. J Pharmacol Toxicol Methods 51: 187-200.
42. Franke B, Neale BM, Faraone SV, (2009) Genome-wide association studies in ADHD. Human genetics 126: 13-50.
43. Poelmans G, Pauls DL, Buitelaar JK, Franke B, (2011) Integrated genome-wide association study findings: identification of a neurodevelopmental network for attention deficit hyperactivity disorder. The American journal of psychiatry 168: 365-377.
44. Daoud H, Valdmanis PN, Gros-Louis F, Belzil V, Spiegelman D, et al. (2011) Resequencing of 29 candidate genes in patients with familial and sporadic amyotrophic lateral sclerosis. Archives of neurology 68: 587-593.
45. Kohannim O, Hibar DP, Stein JL, Jahanshad N, Hua X, et al. (2012) Discovery and Replication of Gene Influences on Brain Structure Using LASSO Regression. Front Neurosci 6: 115.
46. Kleppe R, Knappskog PM, Haavik J, (2001) [Why do mutations cause disease-a protein chemical perspective]. Tidsskr Nor Laegeforen 121: 2717-2720.
47. Masoodi TA, Al Shammari SA, Al-Muammar MN, Alhamdan AA, (2012) Screening and Evaluation of Deleterious SNPs in APOE Gene of Alzheimer's Disease. Neurol Res Int 2012: 480609.
48. George Priya Doss C, Nagasundaram N, Tanwar H, (2012) Predicting the impact of deleterious single point mutations in SMAD gene family using structural bioinformatics approach. Interdiscip Sci 4: 103-115.
49. Joshi MB, Kyriakakis E, Pfaff D, Rupp K, Philippova M, et al. (2009) Extracellular cadherin repeat domains EC1 and EC5 of T-cadherin are essential for its ability to stimulate angiogenic behavior of endothelial cells. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 23: 4011-4021.
50. Mousavi M, Bereau V, Duhayon C, Guionneau P, Sutter JP, (2012) First magnets based on thiocyanato-bridges. Chemical communications 48: 10028-10030.
51. Kuzmenko YS, Stambolsky D, Kern F, Bochkov VN, Tkachuk VA, et al. (1998) Characteristics of smooth muscle cell lipoprotein binding proteins (p105/p130) as T-cadherin and regulation by positive and negative growth regulators. Biochemical and biophysical research communications 246: 489-494.
52. Resink TJ, Kuzmenko YS, Kern F, Stambolsky D, Bochkov VN, et al. (1999) LDL binds to surface-expressed human T-cadherin in transfected HEK293 cells and influences homophilic adhesive interactions. FEBS letters 463: 29-34.
53. Philippova M, Joshi MB, Kyriakakis E, Pfaff D, Erne P, et al. (2009) A guide and guard: the many faces of T-cadherin. Cellular signalling 21: 1035-1044.
54. Andreeva AV, Kutuzov MA, Tkachuk VA, Voyno-Yasenetskaya TA, (2009) T-cadherin is located in the nucleus and centrosomes in endothelial cells. American journal of physiology Cell physiology 297: C1168-1177.
55. Zandy NL, Playford M, Pendergast AM, (2007) Abl tyrosine kinases regulate cell-cell adhesion through Rho GTPases. Proceedings of the National Academy of Sciences of the United States of America 104: 17686-17691.
56. Muise AM, Walters TD, Glowacka WK, Griffiths AM, Ngan BY, et al. (2009) Polymorphisms in E-cadherin (CDH1) result in a mis-localised cytoplasmic protein that is associated with Crohn's disease. Gut 58: 1121-1127.
57. Udenfriend S, Kodukula K, (1995) How glycosylphosphatidylinositol-anchored membrane proteins are made. Annu Rev Biochem 64: 563-591.
58. Zuppinger C, Schaub MC, Eppenberger HM, (2000) Dynamics of early contact formation in cultured adult rat cardiomyocytes studied by N-cadherin fused to green fluorescent protein. J Mol Cell Cardiol 32: 539-555.
59. Quadri SK, Sun L, Islam MN, Shapiro L, Bhattacharya J, (2012) Cadherin selectivity filter regulates endothelial sieving properties. Nat Commun 3: 1099.