Immune-related pathways including HLA-DRB1*13:02 are associated with panic disorder

Brain, Behavior, and Immunity

Volumn 46, Issue , 2015, Pages 96-103

  Shimada Sugimoto, Mihoko ^a   Otowa, Takeshi ^a   Miyagawa, Taku ^a   Khor, Seik Soon ^a   Kashiwase, Koichi ^b   Sugaya, Nagisa ^c   Kawamura, Yoshiya ^d   Umekage, Tadashi ^e   Kojima, Hiroto ^f   Saji, Hiroh ^f   Miyashita, Akinori ^g   Kuwano, Ryozo ^g   Kaiya, Hisanobu ^h   Kasai, Kiyoto ^a   Tanii, Hisashi ⁱ   Okazaki, Yuji ^j   Tokunaga, Katsushi ^a   Sasaki, Tsukasa ^e  

^a UNIVERSITY OF TOKYO   (Japan)

^b Japanese Red Cross Kanto Koshinetsu Block Blood Center   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d Department of Psychiatry   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f Japanese Red Cross Kanto Koshinetsu Block Blood Center   (Japan)

^g NIIGATA UNIVERSITY   (Japan)

^h Medical Corporation Warakukai   (Japan)

ⁱ MIE UNIVERSITY   (Japan)

^j TOKYO METROPOLITAN MATSUZAWA HOSPITAL   (Japan)

more..

Author keywords

Genome wide association study; HLA B; HLA DRB1; Human leukocyte antigen; Immunity; Panic disorder; Pathway analysis

Indexed keywords

ARTICLE; CONTROLLED STUDY; FEMALE; GENE FREQUENCY; GENE FUNCTION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; HISTOCOMPATIBILITY GENE; HLA B GENE; HLA DRB1 13:02 GENE; HLA TYPING; HUMAN; IMMUNOGENETICS; MAJOR CLINICAL STUDY; MALE; MENTAL PATIENT; MOLECULAR PATHOLOGY; NEUROIMMUNOLOGY; PANIC; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; ADULT; GENETIC PREDISPOSITION; GENETICS; HAPLOTYPE; MIDDLE AGED;

HLA DRB1 ANTIGEN;

ADULT; FEMALE; GENE FREQUENCY; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HAPLOTYPES; HLA-DRB1 CHAINS; HUMANS; MALE; MIDDLE AGED; PANIC DISORDER; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84928829401     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.01.002     Document Type: Article

References (65)

1. Diagnostic and Statistical Manual of Mental Disorders 1994, American Psychiatric Association, American Psychiatric Press, Washington, DC. fourth ed.
2. Bachen E.A., Chesney M.A., Criswell L.A. Prevalence of mood and anxiety disorders in women with systemic lupus erythematosus. Arthritis Rheum. 2009, 61:822-829.
3. Bergmann C.C., Parra B., Hinton D.R., Chandran R., Morrison M., Stohlman S.A. Perforin-mediated effector function within the central nervous system requires IFN-gamma-mediated MHC up-regulation. J Immunol. 2003, 170:3204-3213.
4. Boulanger L.M. Immune proteins in brain development and synaptic plasticity. Neuron 2009, 64:93-109.
5. Crowe R.R., Noyes R., Pauls D.L., Slymen D. A family study of panic disorder. Arch. Gen. Psychiatry 1983, 40:1065-1069.
6. Debnath M., Busson M., Jamain S., Etain B., Hamdani N., Oliveira J., Boukouaci W., Amokrane K., Moins-Teisserenc H., Lajnef M., Bengoufa D., Malafosse A., Bellivier F., Henry C., Kahn J.P., Krishnamoorthy R., Charron D., Leboyer M., Tamouza R. The HLA-G low expressor genotype is associated with protection against bipolar disorder. Hum. Immunol. 2013, 74:593-597.
7. Deckert J., Catalano M., Syagailo Y.V., Bosi M., Okladnova O., Di Bella D., Nöthen M.M., Maffei P., Franke P., Fritze J., Maier W., Propping P., Beckmann H., Bellodi L., Lesch K.P. Excess of high activity monoamine oxidase A gene promoter alleles in female patients with panic disorder. Hum. Mol. Genet. 1999, 8:621-624.
8. Deckert J., Nöthen M.M., Franke P., Delmo C., Fritze J., Knapp M., Maier W., Beckmann H., Propping P. Systematic mutation screening and association study of the A1 and A2a adenosine receptor genes in panic disorder suggest a contribution of the A2a gene to the development of disease. Mol. Psychiatry 1998, 3:81-85.
9. Domschke K., Freitag C.M., Kuhlenbäumer G., Schirmacher A., Sand P., Nyhuis P., Jacob C., Fritze J., Franke P., Rietschel M., Garritsen H.S., Fimmers R., Nöthen M.M., Lesch K.P., Stögbauer F., Deckert J. Association of the functional V158M catechol-O-methyl-transferase polymorphism with panic disorder in women. Int. J. Neuropsychopharmacol. 2004, 7:183-188.
10. Eaton W.W., Kessler R.C., Wittchen H.U., Magee W.J. Panic and panic disorder in the United States. Am. J. Psychiatry 1994, 151:413-420.
11. Ebihara M., Ohba H., Hattori E., Yamada K., Yoshikawa T. Transcriptional activities of cholecystokinin promoter haplotypes and their relevance to panic disorder susceptibility. Am. J. Med. Genet. B, Neuropsychiatr. Genet. 2003, 118B:32-35.
12. Erhardt A., Akula N., Schumacher J., Czamara D., Karbalai N., Müller-Myhsok B., Mors O., Borglum A., Kristensen A.S., Woldbye D.P., Koefoed P., Eriksson E., Maron E., Metspalu A., Nurnberger J., Philibert R.A., Kennedy J., Domschke K., Reif A., Deckert J., Otowa T., Kawamura Y., Kaiya H., Okazaki Y., Tanii H., Tokunaga K., Sasaki T., Ioannidis J.P., McMahon F.J., Binder E.B. Replication and meta-analysis of TMEM132D gene variants in panic disorder. Transl. Psychiatry 2012, 2:e156.
13. Erhardt A., Czibere L., Roeske D., Lucae S., Unschuld P.G., Ripke S., Specht M., Kohli M.A., Kloiber S., Ising M., Heck A., Pfister H., Zimmermann P., Lieb R., Pütz B., Uhr M., Weber P., Deussing J.M., Gonik M., Bunck M., Kebler M.S., Frank E., Hohoff C., Domschke K., Krakowitzky P., Maier W., Bandelow B., Jacob C., Deckert J., Schreiber S., Strohmaier J., Nöthen M., Cichon S., Rietschel M., Bettecken T., Keck M.E., Landgraf R., Müller-Myhsok B., Holsboer F., Binder E.B. TMEM132D, a new candidate for anxiety phenotypes: evidence from human and mouse studies. Mol. Psychiatry 2011, 16:647-663.
14. Favreau H., Bacon S.L., Labrecque M., Lavoie K.L. Prospective impact of panic disorder and panic-anxiety on asthma control, health service use, and quality of life in adult patients with asthma over a 4-year follow-up. Psychosom. Med. 2014, 76:147-155.
15. Figueiredo T.C., de Oliveira J.R. Reconsidering the association between the major histocompatibility complex and bipolar disorder. J. Mol. Neurosci. 2012, 47:26-30.
16. Freeman M.P., Freeman S.A., McElroy S.L. The comorbidity of bipolar and anxiety disorders: prevalence, psychobiology, and treatment issues. J. Affect. Disord. 2002, 68:1-23.
17. Goldstein R.B., Wickramaratne P.J., Horwath E., Weissman M.M. Familial aggregation and phenomenology of 'early'-onset (at or before age 20years) panic disorder. Arch. Gen. Psychiatry 1997, 54:271-278.
18. Goodwin R.D., Pagura J., Cox B., Sareen J. Asthma and mental disorders in Canada: impact on functional impairment and mental health service use. J. Psychosom. Res. 2010, 68:165-173.
19. Hamilton S.P., Slager S.L., De Leon A.B., Heiman G.A., Klein D.F., Hodge S.E., Weissman M.M., Fyer A.J., Knowles J.A. Evidence for genetic linkage between a polymorphism in the adenosine 2A receptor and panic disorder. Neuropsychopharmacology 2004, 29:558-565.
20. Hamilton S.P., Slager S.L., Heiman G.A., Deng Z., Haghighi F., Klein D.F., Hodge S.E., Weissman M.M., Fyer A.J., Knowles J.A. Evidence for a susceptibility locus for panic disorder near the catechol-O-methyltransferase gene on chromosome 22. Biol. Psychiatry 2002, 51:591-601.
21. Hamo L., Stohlman S.A., Otto-Duessel M., Bergmann C.C. Distinct regulation of MHC molecule expression on astrocytes and microglia during viral encephalomyelitis. Glia 2007, 55:1169-1177.
22. Hattori E., Yamada K., Toyota T., Yoshitsugu K., Toru M., Shibuya H., Yoshikawa T. Association studies of the CT repeat polymorphism in the 5' upstream region of the cholecystokinin B receptor gene with panic disorder and schizophrenia in Japanese subjects. Am. J. Med. Genet. 2001, 105:779-782.
23. Hettema J.M., Neale M.C., Kendler K.S. A review and meta-analysis of the genetic epidemiology of anxiety disorders. Am. J. Psychiatry. 2001, 158:1568-1578.
24. Holoshitz J. The quest for better understanding of HLA-disease association: scenes from a road less travelled by. Discov. Med 2013, 16:93-101.
25. Huang D.W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
26. Inada Y., Yoneda H., Koh J., Sakai J., Himei A., Kinoshita Y., Akabame K., Hiraoka Y., Sakai T. Positive association between panic disorder and polymorphism of the serotonin 2A receptor gene. Psychiatry Res. 2003, 118:25-31.
27. International Schizophrenia Consortium Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 2009, 460:748-752.
28. Johnson W.G., Buyske S., Mars A.E., Sreenath M., Stenroos E.S., Williams T.A., Stein R., Lambert G.H. HLA-DR4 as a risk allele for autism acting in mothers of probands possibly during pregnancy. Arch. Pediatr. Adolesc. Med. 2009, 163:542-546.
29. Khor, S.S., Yang, W., Kawashima, M., Kamitsuji, S., Zheng, X., Nishida, N., Sawai, H., Toyoda, H., Miyagawa, T., Honda, M., Kamatani, N., Tokunaga, K., in press. High-accuracy imputation for HLA class I and II genes based on high-resolution SNP data of population-specific references. Pharmacogenomics J.
30. Lavoie K.L., Cartier A., Labrecque M., Bacon S.L., Lemière C., Malo J.L., Lacoste G., Barone S., Verrier P., Ditto B. Are psychiatric disorders associated with worse asthma control and quality of life in asthma patients?. Respir. Med. 2005, 99:1249-1257.
31. Liu J.Z., Mcrae A.F., Nyholt D.R., Medland S.E., Wray N.R., Brown K.M., Hayward N.K., Montgomery G.W., Visscher P.M., Martin N.G., Macgregor S. A versatile gene-based test for genome-wide association studies. Am. J. Hum. Genet. 2010, 87:139-145. AMFS Investigators.
32. MacKinnon D.F., McMahon F.J., Simpson S.G., McInnis M.G., DePaulo J.R. Panic disorder with familial bipolar disorder. Biol. Psychiatry 1997, 42:90-95.
33. MacKinnon D.F., Zandi P.P., Cooper J., Potash J.B., Simpson S.G., Gershon E., Nurnberger J., Reich T., DePaulo J.R. Comorbid bipolar disorder and panic disorder in families with a high prevalence of bipolar disorder. Am. J. Psychiatry 2002, 159:30-35.
34. Manfro G.G., Pollack M.H., Otto M.W., Worthington J.J., Rosenbaum J.F., Scott E.L., Kradin R.L. Cell-surface expression of L-selectin (CD62L) by blood lymphocytes: correlates with affective parameters and severity of panic disorder. Depress. Anxiety 2000, 11:31-37.
35. Marazziti D., Ambrogi F., Vanacore R., Mignani V., Savino M., Palego L., Cassano G.B., Akiskal H.S. Immune cell imbalance in major depressive and panic disorders. Neuropsychobiology 1992, 26:23-26.
36. Maron E., Lang A., Tasa G., Liivlaid L., Tõru I., Must A., Vasar V., Shlik J. Associations between serotonin-related gene polymorphisms and panic disorder. Int. J. Neuropsychopharmacol. 2005, 8:261-266.
37. Na H.R., Kang E.H., Lee J.H., Yu B.H. The genetic basis of panic disorder. J. Korean Med. Sci. 2011, 26:701-710.
38. Nahar Z., Khanum S., Harun S., Islam S.N., Sobhan A., Islam S., Hasnat A. Immunoglobulin levels in panic disorder patients. Pak. J. Pharm. Sci. 2012, 25:149-153.
39. Navarrete C.V. The HLA system in blood transfusion. Baillieres Best Pract. Res. Clin. Haematol. 2000, 13:511-532.
40. Otowa T., Kawamura Y., Nishida N., Sugaya N., Koike A., Yoshida E., Inoue K., Yasuda S., Nishimura Y., Liu X., Konishi Y., Nishimura F., Shimada T., Kuwabara H., Tochigi M., Kakiuchi C., Umekage T., Miyagawa T., Miyashita A., Shimizu E., Akiyoshi J., Someya T., Kato T., Yoshikawa T., Kuwano R., Kasai K., Kato N., Kaiya H., Tokunaga K., Okazaki Y., Tanii H., Sasaki T. Meta-analysis of genome-wide association studies for panic disorder in the Japanese population. Transl. Psychiatry 2012, 2:e186.
41. Otowa T., Tanii H., Sugaya N., Yoshida E., Inoue K., Yasuda S., Shimada T., Kawamura Y., Tochigi M., Minato T., Umekage T., Miyagawa T., Nishida N., Tokunaga K., Okazaki Y., Kaiya H., Sasaki T. Replication of a genome-wide association study of panic disorder in a Japanese population. J. Hum. Genet. 2010, 55:91-96.
42. Otowa T., Yoshida E., Sugaya N., Yasuda S., Nishimura Y., Inoue K., Tochigi M., Umekage T., Miyagawa T., Nishida N., Tokunaga K., Tanii H., Sasaki T., Kaiya H., Okazaki Y. Genome-wide association study of panic disorder in the Japanese population. J. Hum. Genet. 2009, 54:122-126.
43. Park J.E., Kim S.W., Park Q., Jeong D.U., Yu B.H. Lymphocyte subsets and mood states in panic disorder patients. J. Korean Med. Sci. 2005, 20:215-219.
44. Perini G.I., Zara M., Carraro C., Tosin C., Gava F., Santucci M.G., Valverde S., De Franchis G. Psychoimmunoendocrine aspects of panic disorder. Hum. Psychopharmacol. Clin. Exp. 1995, 10:461-465.
45. Perna G., Bertani A., Politi E., Colombo G., Bellodi L. Asthma and panic attacks. Biol. Psychiatry 1997, 42:625-630.
46. Ramanan V.K., Shen L., Moore J.H., Saykin A.J. Pathway analysis of genomic data: concepts, methods, and prospects for future development. Trends Genet. 2012, 28:323-332.
47. Rapaport M.H. Circulating lymphocyte phenotypic surface markers in anxiety disorder patients and normal volunteers. Biol. Psychiatry 1998, 43:458-463.
48. Rothe C., Gutknecht L., Freitag C., Tauber R., Mössner R., Franke P., Fritze J., Wagner G., Peikert G., Wenda B., Sand P., Jacob C., Rietschel M., Nöthen M.M., Garritsen H., Fimmers R., Deckert J., Lesch K.P. Association of a functional 1019C>G 5-HT1A receptor gene polymorphism with panic disorder with agoraphobia. Int. J. Neuropsychopharmacol. 2004, 7:189-192.
49. Rothe C., Koszycki D., Bradwejn J., King N., De Luca V., Shaikh S., Franke P., Garritsen H., Fritze J., Deckert J., Kennedy J.L. Association study of serotonin-2A receptor gene polymorphism and panic disorder in patients from Canada and Germany. Neurosci. Lett. 2004, 363:276-279.
50. Rothe C., Koszycki D., Bradwejn J., King N., Deluca V., Tharmalingam S., Macciardi F., Deckert J., Kennedy J.L. Association of the Val158Met catechol O-methyltransferase genetic polymorphism with panic disorder. Neuropsychopharmacology 2006, 31:2237-2242.
51. Schizophrenia Working Group of the Psychiatric Genomics Consortium Biological insights from 108 schizophrenia-associated genetic loci. Nature 2014, 511:421-427.
52. Schleifer S.J., Keller S.E., Bartlett J.A. Panic disorder and immunity: few effects on circulating lymphocytes, mitogen response, and NK cell activity. Brain Behav. Immun. 2002, 16:698-705.
53. Shatz C.J. MHC class I: an unexpected role in neuronal plasticity. Neuron 2009, 64:40-45.
54. Shi J., Levinson D.F., Duan J., Sanders A.R., Zheng Y., Pe'er I., Dudbridge F., Holmans P.A., Whittemore A.S., Mowry B.J., Olincy A., Amin F., Cloninger C.R., Silverman J.M., Buccola N.G., Byerley W.F., Black D.W., Crowe R.R., Oksenberg J.R., Mirel D.B., Kendler K.S., Freedman R., Gejman P.V. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 2009, 460:753-757.
55. Stefansson H., Ophoff R.A., Steinberg S., Andreassen O.A., Cichon S., Rujescu D., Werge T., Pietiläinen O.P., Mors O., Mortensen P.B., Sigurdsson E., Gustafsson O., Nyegaard M., Tuulio-Henriksson A., Ingason A., Hansen T., Suvisaari J., Lonnqvist J., Paunio T., Børglum A.D., Hartmann A., Fink-Jensen A., Nordentoft M., Hougaard D., Norgaard-Pedersen B., Böttcher Y., Olesen J., Breuer R., Möller H.J., Giegling I., Rasmussen H.B., Timm S., Mattheisen M., Bitter I., Réthelyi J.M., Magnusdottir B.B., Sigmundsson T., Olason P., Masson G., Gulcher J.R., Haraldsson M., Fossdal R., Thorgeirsson T.E., Thorsteinsdottir U., Ruggeri M., Tosato S., Franke B., Strengman E., Kiemeney L.A., Melle I., Djurovic S., Abramova L., Kaleda V., Sanjuan J., de Frutos R., Bramon E., Vassos E., Fraser G., Ettinger U., Picchioni M., Walker N., Toulopoulou T., Need A.C., Ge D., Yoon J.L., Shianna K.V., Freimer N.B., Cantor R.M., Murray R., Kong A., Golimbet V., Carracedo A., Arango C., Costas J., Jönsson E.G., Terenius L., Agartz I., Petursson H., Nöthen M.M., Rietschel M., Matthews P.M., Muglia P., Peltonen L., St.Clair D., Goldstein D.B., Stefansson K., Collier D.A. Common variants conferring risk of schizophrenia. Nature 2009, 460:744-747. Genetic Risk and Outcome in Psychosis (GROUP).
56. Takei N., Miyashita A., Tsukie T., Arai H., Asada T., Imagawa M., Shoji M., Higuchi S., Urakami K., Kimura H., Kakita A., Takahashi H., Tsuji S., Kanazawa I., Ihara Y., Odani S., Kuwano R. Genetic association study on in and around the APOE in late-onset Alzheimer disease in Japanese. Genomics 2009, 93:441-448. The Japanese Genetic Study Consortium for Alzheimer Disease.
57. Tokunaga K., Omoto K., Akaza T., Akiyama N., Amemiya H., Naito S., Sasazuki T., Satoh H., Juji T. Haplotype study on C4 polymorphism in Japanese. Associations with MHC alleles, complotypes, and HLA-complement haplotypes. Immunogenetics 1985, 22:359-365.
58. Torres A.R., Maciulis A., Stubbs E.G., Cutler A., Odell D. The transmission disequilibrium test suggests that HLA-DR4 and DR13 are linked to autism spectrum disorder. Hum. Immunol. 2002, 63:311-316.
59. Wang K., Li M., Hakonarson H. Analysing biological pathways in genome-wide association studies. Nat. Rev. Genet. 2010, 11:843-854.
60. Wang Z., Valdes J., Noyes R., Zoega T., Crowe R.R. Possible association of a cholecystokinin promotor polymorphism (CCK-36CT) with panic disorder. Am. J. Med. Genet. 1998, 81:228-234.
61. Warren R.P., Singh V.K., Cole P., Odell J.D., Pingree C.B., Warren W.L., DeWitt C.W., McCullough M. Possible association of the extended MHC haplotype B44-SC30-DR4 with autism. Immunogenetics 1992, 36:203-207.
62. Woo J.M., Yoon K.S., Yu B.H. Catechol O-methyltransferase genetic polymorphism in panic disorder. Am. J. Psychiatry 2002, 159:1785-1787.
63. Young S., Pfaff D., Lewandowski K.E., Ravichandran C., Cohen B.M., Öngür D. Anxiety disorder comorbidity in bipolar disorder, schizophrenia and schizoaffective disorder. Psychopathology 2013, 46:176-185.
64. Zhang K., Chang S., Cui S., Guo L., Zhang L., Wang J. ICSNPathway: identify candidate causal SNPs and pathways from genome-wide association study by one analytical framework. Nucleic Acids Res. 2011, 39:W437-W443.
65. Zhang K., Cui S., Chang S., Zhang L., Wang J. I-GSEA4GWAS: a web server for identification of pathways/gene sets associated with traits by applying an improved gene set enrichment analysis to genome-wide association study. Nucleic Acids Res. 2010, 38:W90-W95.