Genome-Wide Significant Association Signals in IPO11-HTR1A Region Specific for Alcohol and Nicotine Codependence

Alcoholism: Clinical and Experimental Research

Volumn 37, Issue 5, 2013, Pages 730-739

  Zuo, Lingjun ^a   Zhang, Xiang Yang ^b   Wang, Fei ^a   Li, Chiang Shan R ^a   Lu, Lingeng ^a   Ye, Liefu ^c   Zhang, Heping ^d   Krystal, John H ^a   Deng, Hong Wen ^e   Luo, Xingguang ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c FUJIAN PROVINCIAL HOSPITAL   (China)

^d YALE UNIVERSITY   (United States)

^e TULANE UNIVERSITY   (United States)

Author keywords

Alcohol and Nicotine Codependence; cis eQTL; GWAS; HTR1A; IPO11

Indexed keywords

HTR1A PROTEIN; IPO11 PROTEIN; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG;

ADULT; ALCOHOLISM; ARTICLE; AUSTRALIA; BRAIN TISSUE; CHROMOSOME 5Q; CONTROLLED STUDY; EUROPE; FEMALE; GENE LOCUS; GENETIC ASSOCIATION; GENETIC RISK; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MENTAL DISEASE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TOBACCO DEPENDENCE; UNITED STATES;

ADULT; AFRICAN AMERICANS; ALCOHOLISM; BETA KARYOPHERINS; CASE-CONTROL STUDIES; CHROMOSOMES, HUMAN, PAIR 5; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; RECEPTOR, SEROTONIN, 5-HT1A; TOBACCO USE DISORDER;

EID: 84876806246     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/acer.12032     Document Type: Article

References (36)

1. American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders. 4th ed. American Psychiatric Press, Washington, DC.
2. Bierut LJ, Agrawal A, Bucholz KK, Doheny KF, Laurie C, Pugh E, Fisher S, Fox L, Howells W, Bertelsen S, Hinrichs AL, Almasy L, Breslau N, Culverhouse RC, Dick DM, Edenberg HJ, Foroud T, Grucza RA, Hatsukami D, Hesselbrock V, Johnson EO, Kramer J, Krueger RF, Kuperman S, Lynskey M, Mann K, Neuman RJ, Nothen MM, Nurnberger JI Jr, Porjesz B, Ridinger M, Saccone NL, Saccone SF, Schuckit MA, Tischfield JA, Wang JC, Rietschel M, Goate AM, Rice JP (2010) A genome-wide association study of alcohol dependence. Proc Natl Acad Sci U S A 107:5082-5087.
3. Bierut LJ, Madden PA, Breslau N, Johnson EO, Hatsukami D, Pomerleau OF, Swan GE, Rutter J, Bertelsen S, Fox L, Fugman D, Goate AM, Hinrichs AL, Konvicka K, Martin NG, Montgomery GW, Saccone NL, Saccone SF, Wang JC, Chase GA, Rice JP, Ballinger DG (2007) Novel genes identified in a high-density genome wide association study for nicotine dependence. Hum Mol Genet 16:24-35.
4. Bucholz KK, Cadoret R, Cloninger CR, Dinwiddie SH, Hesselbrock VM, Nurnberger JI Jr, Reich T, Schmidt I, Schuckit MA (1994) A new, semi-structured psychiatric interview for use in genetic linkage studies: a report on the reliability of the SSAGA. J Stud Alcohol 55:149-158.
5. Carmelli D, Swan GE, Robinette D (1993) The relationship between quitting smoking and changes in drinking in World War II veteran twins. J Subst Abuse 5:103-116.
6. Edenberg HJ, Bierut LJ, Boyce P, Cao M, Cawley S, Chiles R, Doheny KF, Hansen M, Hinrichs T, Jones K, Kelleher M, Kennedy GC, Liu G, Marcus G, McBride C, Murray SS, Oliphant A, Pettengill J, Porjesz B, Pugh EW, Rice JP, Rubano T, Shannon S, Steeke R, Tischfield JA, Tsai YY, Zhang C, Begleiter H (2005) Description of the data from the Collaborative Study on the Genetics of Alcoholism (COGA) and single-nucleotide polymorphism genotyping for Genetic Analysis Workshop 14. BMC Genet 6(Suppl 1):S2.
7. Edenberg HJ, Dick DM, Xuei X, Tian H, Almasy L, Bauer LO, Crowe RR, Goate A, Hesselbrock V, Jones K, Kwon J, Li TK, Nurnberger JI Jr, O'Connor SJ, Reich T, Rice J, Schuckit MA, Porjesz B, Foroud T, Begleiter H (2004) Variations in GABRA2, encoding the alpha 2 subunit of the GABA(A) receptor, are associated with alcohol dependence and with brain oscillations. Am J Hum Genet 74:705-714.
8. Edenberg HJ, Koller DL, Xuei X, Wetherill L, McClintick JN, Almasy L, Bierut LJ, Bucholz KK, Goate A, Aliev F, Dick D, Hesselbrock V, Hinrichs A, Kramer J, Kuperman S, Nurnberger JI Jr, Rice JP, Schuckit MA, Taylor R, Todd Webb B, Tischfield JA, Porjesz B, Foroud T (2010) Genome-wide association study of alcohol dependence implicates a region on chromosome 11. Alcohol Clin Exp Res 34:840-852.
9. Grant BF, Hasin DS, Chou SP, Stinson FS, Dawson DA (2004) Nicotine dependence and psychiatric disorders in the United States: results from the national epidemiologic survey on alcohol and related conditions. Arch Gen Psychiatry 61:1107-1115.
10. Heath AC, Whitfield JB, Martin NG, Pergadia ML, Goate AM, Lind PA, McEvoy BP, Schrage AJ, Grant JD, Chou YL, Zhu R, Henders AK, Medland SE, Gordon SD, Nelson EC, Agrawal A, Nyholt DR, Bucholz KK, Madden PA, Montgomery GW (2011) A quantitative-trait genome-wide association study of alcoholism risk in the community: findings and implications. Biol Psychiatry 70:513-518.
11. Heinzen EL, Ge D, Cronin KD, Maia JM, Shianna KV, Gabriel WN, Welsh-Bohmer KA, Hulette CM, Denny TN, Goldstein DB (2008) Tissue-specific genetic control of splicing: implications for the study of complex traits. PLoS Biol 6:e1.
12. Horvath S, Xu X, Laird NM (2001) The family based association test method: strategies for studying general genotype-phenotype associations. Eur J Hum Genet 9:301-306.
13. Johnson C, Drgon T, Walther D, Uhl GR (2011) Genomic regions identified by overlapping clusters of nominally-positive SNPs from genome-wide studies of alcohol and illegal substance dependence. PLoS ONE 6:e19210.
14. Kerns RT, Ravindranathan A, Hassan S, Cage MP, York T, Sikela JM, Williams RW, Miles MF (2005) Ethanol-responsive brain region expression networks: implications for behavioral responses to acute ethanol in DBA/2J versus C57BL/6J mice. J Neurosci 25:2255-2266.
15. Lee YS, Choi SW, Han DH, Kim DJ, Joe KH (2009) Clinical manifestation of alcohol withdrawal symptoms related to genetic polymorphisms of two serotonin receptors and serotonin transporter. Eur Addict Res 15:39-46.
16. Lemonde S, Turecki G, Bakish D, Du L, Hrdina PD, Bown CD, Sequeira A, Kushwaha N, Morris SJ, Basak A, Ou XM, Albert PR (2003) Impaired repression at a 5-hydroxytryptamine 1A receptor gene polymorphism associated with major depression and suicide. J Neurosci 23:8788-8799.
17. Li J, Ji L (2005) Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity (Edinb) 95:221-227.
18. Lind PA, Macgregor S, Vink JM, Pergadia ML, Hansell NK, de Moor MH, Smit AB, Hottenga JJ, Richter MM, Heath AC, Martin NG, Willemsen G, de Geus EJ, Vogelzangs N, Penninx BW, Whitfield JB, Montgomery GW, Boomsma DI, Madden PA (2010) A genomewide association study of nicotine and alcohol dependence in Australian and Dutch populations. Twin Res Hum Genet 13:10-29.
19. Liu JZ, Tozzi F, Waterworth DM, Pillai SG, Muglia P, Middleton L, Berrettini W, Knouff CW, Yuan X, Waeber G, Vollenweider P, Preisig M, Wareham NJ, Zhao JH, Loos RJ, Barroso I, Khaw KT, Grundy S, Barter P, Mahley R, Kesaniemi A, McPherson R, Vincent JB, Strauss J, Kennedy JL, Farmer A, McGuffin P, Day R, Matthews K, Bakke P, Gulsvik A, Lucae S, Ising M, Brueckl T, Horstmann S, Wichmann HE, Rawal R, Dahmen N, Lamina C, Polasek O, Zgaga L, Huffman J, Campbell S, Kooner J, Chambers JC, Burnett MS, Devaney JM, Pichard AD, Kent KM, Satler L, Lindsay JM, Waksman R, Epstein S, Wilson JF, Wild SH, Campbell H, Vitart V, Reilly MP, Li M, Qu L, Wilensky R, Matthai W, Hakonarson HH, Rader DJ, Franke A, Wittig M, Schafer A, Uda M, Terracciano A, Xiao X, Busonero F, Scheet P, Schlessinger D, St Clair D, Rujescu D, Abecasis GR, Grabe HJ, Teumer A, Volzke H, Petersmann A, John U, Rudan I, Hayward C, Wright AF, Kolcic I, Wright BJ, Thompson JR, Balmforth AJ, Hall AS, Samani NJ, Anderson CA, Ahmad T, Mathew CG, Parkes M, Satsangi J, Caulfield M, Munroe PB, Farrall M, Dominiczak A, Worthington J, Thomson W, Eyre S, Barton A, Mooser V, Francks C, Marchini J (2010) Meta-analysis and imputation refines the association of 15q25 with smoking quantity. Nat Genet 42:436-440.
20. Plafker SM, Macara IG (2000) Importin-11, a nuclear import receptor for the ubiquitin-conjugating enzyme, UbcM2. EMBO J 19:5502-5513.
21. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904-909.
22. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559-575.
23. Ray R, Tyndale RF, Lerman C (2009) Nicotine dependence pharmacogenetics: role of genetic variation in nicotine-metabolizing enzymes. J Neurogenet 23:252-261.
24. Saccone SF, Hinrichs AL, Saccone NL, Chase GA, Konvicka K, Madden PA, Breslau N, Johnson EO, Hatsukami D, Pomerleau O, Swan GE, Goate AM, Rutter J, Bertelsen S, Fox L, Fugman D, Martin NG, Montgomery GW, Wang JC, Ballinger DG, Rice JP, Bierut LJ (2007) Cholinergic nicotinic receptor genes implicated in a nicotine dependence association study targeting 348 candidate genes with 3713 SNPs. Hum Mol Genet 16:36-49.
25. Schumann G, Coin LJ, Lourdusamy A, Charoen P, Berger KH, Stacey D, Desrivieres S, Aliev FA, Khan AA, Amin N, Aulchenko YS, Bakalkin G, Bakker SJ, Balkau B, Beulens JW, Bilbao A, de Boer RA, Beury D, Bots ML, Breetvelt EJ, Cauchi S, Cavalcanti-Proenca C, Chambers JC, Clarke TK, Dahmen N, de Geus EJ, Dick D, Ducci F, Easton A, Edenberg HJ, Esko T, Fernandez-Medarde A, Foroud T, Freimer NB, Girault JA, Grobbee DE, Guarrera S, Gudbjartsson DF, Hartikainen AL, Heath AC, Hesselbrock V, Hofman A, Hottenga JJ, Isohanni MK, Kaprio J, Khaw KT, Kuehnel B, Laitinen J, Lobbens S, Luan J, Mangino M, Maroteaux M, Matullo G, McCarthy MI, Mueller C, Navis G, Numans ME, Nunez A, Nyholt DR, Onland-Moret CN, Oostra BA, O'Reilly PF, Palkovits M, Penninx BW, Polidoro S, Pouta A, Prokopenko I, Ricceri F, Santos E, Smit JH, Soranzo N, Song K, Sovio U, Stumvoll M, Surakk I, Thorgeirsson TE, Thorsteinsdottir U, Troakes C, Tyrfingsson T, Tonjes A, Uiterwaal CS, Uitterlinden AG, van der Harst P, van der Schouw YT, Staehlin O, Vogelzangs N, Vollenweider P, Waeber G, Wareham NJ, Waterworth DM, Whitfield JB, Wichmann EH, Willemsen G, Witteman JC, Yuan X, Zhai G, Zhao JH, Zhang W, Martin NG, Metspalu A, Doering A, Scott J, Spector TD, Loos RJ, Boomsma DI, Mooser V, Peltonen L, Stefansson K, van Duijn CM, Vineis P, Sommer WH, Kooner JS, Spanagel R, Heberlein UA, Jarvelin MR, Elliott P (2011) Genome-wide association and genetic functional studies identify autism susceptibility candidate 2 gene (AUTS2) in the regulation of alcohol consumption. Proc Natl Acad Sci U S A 108:7119-7124.
26. Stranger BE, Forrest MS, Clark AG, Minichiello MJ, Deutsch S, Lyle R, Hunt S, Kahl B, Antonarakis SE, Tavare S, Deloukas P, Dermitzakis ET (2005) Genome-wide associations of gene expression variation in humans. PLoS Genet 1:e78.
27. Strobel A, Gutknecht L, Rothe C, Reif A, Mossner R, Zeng Y, Brocke B, Lesch KP (2003) Allelic variation in 5-HT1A receptor expression is associated with anxiety- and depression-related personality traits. J Neural Transm 110:1445-1453.
28. Substance Abuse and Mental Health Services Administration (SAMHSA) (2010) State Estimates of Substance Use from the 2007-2008 National Surveys on Drug Use and Health (Office of Applied Studies, NSDUH Series H-37, HHS Publication No. SMA 10-4472). SAMHSA, Rockville, MD.
29. Swan GE, Carmelli D, Cardon LR (1997) Heavy consumption of cigarettes, alcohol and coffee in male twins. J Stud Alcohol 58:182-190.
30. Thorgeirsson TE, Gudbjartsson DF, Surakka I, Vink JM, Amin N, Geller F, Sulem P, Rafnar T, Esko T, Walter S, Gieger C, Rawal R, Mangino M, Prokopenko I, Magi R, Keskitalo K, Gudjonsdottir IH, Gretarsdottir S, Stefansson H, Thompson JR, Aulchenko YS, Nelis M, Aben KK, den Heijer M, Dirksen A, Ashraf H, Soranzo N, Valdes AM, Steves C, Uitterlinden AG, Hofman A, Tonjes A, Kovacs P, Hottenga JJ, Willemsen G, Vogelzangs N, Doring A, Dahmen N, Nitz B, Pergadia ML, Saez B, De Diego V, Lezcano V, Garcia-Prats MD, Ripatti S, Perola M, Kettunen J, Hartikainen AL, Pouta A, Laitinen J, Isohanni M, Huei-Yi S, Allen M, Krestyaninova M, Hall AS, Jones GT, van Rij AM, Mueller T, Dieplinger B, Haltmayer M, Jonsson S, Matthiasson SE, Oskarsson H, Tyrfingsson T, Kiemeney LA, Mayordomo JI, Lindholt JS, Pedersen JH, Franklin WA, Wolf H, Montgomery GW, Heath AC, Martin NG, Madden PA, Giegling I, Rujescu D, Jarvelin MR, Salomaa V, Stumvoll M, Spector TD, Wichmann HE, Metspalu A, Samani NJ, Penninx BW, Oostra BA, Boomsma DI, Tiemeier H, van Duijn CM, Kaprio J, Gulcher JR, McCarthy MI, Peltonen L, Thorsteinsdottir U, Stefansson K (2010) Sequence variants at CHRNB3-CHRNA6 and CYP2A6 affect smoking behavior. Nat Genet 42:448-453.
31. Treutlein J, Cichon S, Ridinger M, Wodarz N, Soyka M, Zill P, Maier W, Moessner R, Gaebel W, Dahmen N, Fehr C, Scherbaum N, Steffens M, Ludwig KU, Frank J, Wichmann HE, Schreiber S, Dragano N, Sommer WH, Leonardi-Essmann F, Lourdusamy A, Gebicke-Haerter P, Wienker TF, Sullivan PF, Nothen MM, Kiefer F, Spanagel R, Mann K, Rietschel M (2009) Genome-wide association study of alcohol dependence. Arch Gen Psychiatry 66:773-784.
32. Wang KS, Liu X, Zhang Q, Pan Y, Aragam N, Zeng M (2011) A meta-analysis of two genome-wide association studies identifies 3 new loci for alcohol dependence. J Psychiatr Res 45:1419-1425.
33. Wojnar M, Brower KJ, Jakubczyk A, Zmigrodzka I, Burmeister M, Matsumoto H, Wozny E, Sliwerska E, Hegedus AM, Husar A, Slufarska A, Lipinski M, Zucker RA (2006) Influence of impulsivity, suicidality and serotonin genes on treatment outcomes in alcohol dependence. Psychiatr Pol 40:985-994.
34. Zhou FC, Zhao Q, Liu Y, Goodlett CR, Liang T, McClintick JN, Edenberg HJ, Li L (2011) Alteration of gene expression by alcohol exposure at early neurulation. BMC Genomics 12:124.
35. Zuo L, Zhang CK, Wang F, Li CS, Zhao H, Lu L, Zhang XY, Lu L, Zhang H, Zhang F, Krystal JH, Luo X (2011) A novel, functional and replicable risk gene region for alcohol dependence identified by genome-wide association study. PLoS ONE 6:e26726.
36. Zuo L, Zhang H, Malison RT, Li CS, Zhang XY, Wang F, Lu L, Lu L, Wang X, Krystal JH, Zhang F, Deng HW, Luo X (in press) Rare ADH variant constellations are specific for alcohol dependence. Alcohol Alcohol doi: 10.1093/alcalc/ags104 [Epub ahead of print].