Gender-stratified gene and gene-treatment interactions in smoking cessation

Pharmacogenomics Journal

Volumn 12, Issue 6, 2012, Pages 521-532

  Lee, W ^a   Bergen, A W ^b   Swan, G E ^b   Li, D ^a   Liu, J ^a   Thomas, P ^a   Tyndale, R F ^c   Benowitz, N L ^d   Lerman, C ^e   Conti, D V ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b SRI INTERNATIONAL   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

genetic association studies; heterogeneity; smoking cessation

Indexed keywords

AMFEBUTAMONE; CANNABINOID 1 RECEPTOR; ERYTHROCYTE BAND 4.1 PROTEIN; NICOTINE; NICOTINE DERIVATIVE; PLACEBO;

ADULT; ARTICLE; CNR1 GENE; EPB41 GENE; FEMALE; FOLLOW UP; GENE; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENE THERAPY; GENETIC ANALYSIS; GENETIC VARIABILITY; HUMAN; MAJOR CLINICAL STUDY; MALE; NICOTINE REPLACEMENT THERAPY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REWARD; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SMOKING CESSATION; TOBACCO DEPENDENCE; TRANSDERMAL PATCH; TREATMENT DURATION; TREATMENT RESPONSE;

ADULT; CYTOSKELETAL PROTEINS; FEMALE; HUMANS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RECEPTOR, CANNABINOID, CB1; SEX CHARACTERISTICS; SMOKING CESSATION;

EID: 84870058743     PISSN: 1470269X     EISSN: 14731150     Source Type: Journal    
DOI: 10.1038/tpj.2011.30     Document Type: Article

References (75)

1. Benowitz NL. Nicotine addiction. N Engl J Med 2010; 362: 2295-2303.
2. Hogg RC, Bertrand D. Neuroscience. What genes tell us about nicotine addiction. Science 2004; 306: 983-985.
3. Zbikowski SM, Swan GE, McClure JB. Cigarette smoking and nicotine dependence. Med Clin North Am 2004; 88: 1453-1465, x.
4. Berrettini WH, Lerman CE. Pharmacotherapy and pharmacogenetics of nicotine dependence. Am J Psychiatry 2005; 162: 1441-1451.
5. Ray R, Schnoll RA, Lerman C. Nicotine dependence: biology, behavior, and treatment. Annu Rev Med 2009; 60: 247-260.
6. Russell MA, Feyerabend C, Cole PV. Plasma nicotine levels after cigarette smoking and chewing nicotine gum. Br Med J 1976; 1: 1043-1046.
7. Russell MA, Wilson C, Taylor C, Baker CD. Smoking habits of men and women. Br Med J 1980; 281: 17-20.
8. Russell MA, Jarvis M, Iyer R, Feyerabend C. Relation of nicotine yield of cigarettes to blood nicotine concentrations in smokers. Br Med J 1980; 280: 972-976.
9. Hogle JM, Curtin JJ. Sex differences in negative affective response during nicotine withdrawal. Psychophysiology 2006; 43: 344-356.
10. Schnoll RA, Patterson F. Sex heterogeneity in pharmacogenetic smoking cessation clinical trials. Drug Alcohol Depend 2009; 104(Suppl 1): S94-S99.
11. Burgess DJ, Fu SS, Noorbaloochi S, Clothier BA, Ricards J, Widome R et al. Employment, gender, and smoking cessation outcomes in lowincome smokers using nicotine replacement therapy. Nicotine Tob Res 2009; 11: 1439-1447.
12. Perkins KA, Jacobs L, Sanders M, Caggiula AR. Sex differences in the subjective and reinforcing effects of cigarette nicotine dose. Psychopharmacology (Berl) 2002; 163: 194-201.
13. Pogun S, Yararbas G. Sex differences in nicotine action. Handb Exp Pharmacol 2009; 192): 261-291.
14. Munafo MR, Shields AE, Berrettini WH, Patterson F, Lerman C. Pharmacogenetics and nicotine addiction treatment. Pharmacogenomics 2005; 6: 211-223.
15. Perkins KA, Scott J. Sex differences in long-term smoking cessation rates due to nicotine patch. Nicotine Tob Res 2008; 10: 1245-1250.
16. Benowitz NL, Lessov-Schlaggar CN, Swan GE, Jacob 3rd P. Female sex and oral contraceptive use accelerate nicotine metabolism. Clin Pharmacol Ther 2006; 79: 480-488.
17. Higashi E, Fukami T, Itoh M, Kyo S, Inoue M, Yokoi T et al. Human CYP2A6 is induced by estrogen via estrogen receptor. Drug Metab Dispos 2007; 35: 1935-1941.
18. Harrington WR, Sengupta S, Katzenellenbogen BS. Estrogen regulation of the glucuronidation enzyme UGT2B15 in estrogen receptor-positive breast cancer cells. Endocrinology 2006; 147: 3843-3850.
19. Benowitz NL, Hukkanen J, Jacob 3rd P. Nicotine chemistry, metabolism, kinetics and biomarkers. Handb Exp Pharmacol 2009; 192): 29-60.
20. Hatchell PC, Collins AC. Influences of genotype and sex on behavioral tolerance to nicotine in mice. Pharmacol Biochem Behav 1977; 6: 25-30.
21. Isiegas C, Mague SD, Blendy JA. Sex differences in response to nicotine in C57Bl/6:129SvEv mice. Nicotine Tob Res 2009; 11: 851-858.
22. Lajtha A, Sershen H. Nicotine: alcohol reward interactions. Neurochem Res 2010; 35: 1248-1258.
23. Damaj MI. Influence of gender and sex hormones on nicotine acute pharmacological effects in mice. J Pharmacol Exp Ther 2001; 296: 132-140.
24. Conti DV, Lee W, Li D, Liu J, Van Den Berg D, Thomas PD et al. Nicotinic acetylcholine receptor beta2 subunit gene implicated in a systemsbased candidate gene study of smoking cessation. Hum Mol Genet 2008; 17: 2834-2848.
25. Lerman C, Jepson C, Wileyto EP, Epstein LH, Rukstalis M, Patterson F et al. Role of functional genetic variation in the dopamine D2 receptor (DRD2) in response to bupropion and nicotine replacement therapy for tobacco dependence: results of two randomized clinical trials. Neuropsychopharmacology 2006; 31: 231-242.
26. Lee AM, Jepson C, Hoffmann E, Epstein L, Hawk LW, Lerman C et al. CYP2B6 genotype alters abstinence rates in a bupropion smoking cessation trial. Biol Psychiatry 2007; 62: 635-641.
27. Strasser AA, Malaiyandi V, Hoffmann E, Tyndale RF, Lerman C. An association of CYP2A6 genotype and smoking topography. Nicotine Tob Res 2007; 9: 511-518.
28. Malaiyandi V, Goodz SD, Sellers EM, Tyndale RF. CYP2A6 genotype, phenotype, and the use of nicotine metabolites as biomarkers during ad libitum smoking. Cancer Epidemiol Biomarkers Prev 2006; 15: 1812-1819.
29. Yamanaka H, Nakajima M, Fukami T, Sakai H, Nakamura A, Katoh M et al. CYP2A6 AND CYP2B6 are involved in nornicotine formation from nicotine in humans: interindividual differences in these contributions. Drug Metab Dispos 2005; 33: 1811-1818.
30. Lerman C, Tyndale R, Patterson F, Wileyto EP, Shields PG, Pinto A et al. Nicotine metabolite ratio predicts efficacy of transdermal nicotine for smoking cessation. Clin Pharmacol Ther 2006; 79: 600-608.
31. Patterson F, Schnoll RA, Wileyto EP, Pinto A, Epstein LH, Shields PG et al. Toward personalized therapy for smoking cessation: a randomized placebo-controlled trial of bupropion. Clin Pharmacol Ther 2008; 84: 320-325.
32. Lerman C, Shields PG, Wileyto EP, Audrain J, Hawk Jr LH, Pinto A et al. Effects of dopamine transporter and receptor polymorphisms on smoking cessation in a bupropion clinical trial. Health Psychol 2003; 22: 541-548.
33. Bergen AW, Conti DV, Van Den Berg D, Lee W, Liu J, Li D et al. Dopamine genes and nicotine dependence in treatment-seeking and community smokers. Neuropsychopharmacology 2009; 34: 2252-2264.
34. Feyerabend C, Russell MA. A rapid gas-liquid chromatographic method for the determination of cotinine and nicotine in biological fluids. J Pharm Pharmacol 1990; 42: 450-452.
35. Edlund CK, Lee WH, Li D, Van Den Berg DJ, Conti DV. Snagger: a userfriendly program for incorporating additional information for tagSNP selection. BMC Bioinform 2008; 9: 174.
36. Thorisson GA, Smith AV, Krishnan L, Stein LD. The International HapMap Project Web site. Genome Res 2005; 15: 1592-1593.
37. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P. Association mapping in structured populations. Am J Hum Genet 2000; 67: 170-181.
38. Durbin RM, Abecasis GR, Altshuler DL, Auton A, Brooks LD, Gibbs RA et al. A map of human genome variation from population-scale sequencing. Nature 2010; 467: 1061-1073.
39. Howie BN, Donnelly P, Marchini J. A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet 2009; 5: e1000529.
40. Marchini J, Howie B, Myers S, McVean G, Donnelly P. A new multipoint method for genome-wide association studies by imputation of genotypes. Nat Genet 2007; 39: 906-913.
41. Pruim RJ, Welch RP, Sanna S, Teslovich TM, Chines PS, Gliedt TP et al. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 2010; 26: 2336-2337.
42. Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO. The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom tolerance questionnaire. Br J Addict 1991; 86: 1119-1127.
43. R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria, 2010.
44. Conneely KN, Boehnke M. So many correlated tests, so little time! Rapid adjustment of P values for multiple correlated tests. Am J Hum Genet 2007; 81: 1158-1168.
45. Li D. Multiple degree of freedom P-value adjustment using correlation of score statistics, 2010. Personal communication.
46. Perkins KA, Lerman C, Grottenthaler A, Ciccocioppo MM, Milanak M, Conklin CA et al. Dopamine and opioid gene variants are associated with increased smoking reward and reinforcement owing to negative mood. Behav Pharmacol 2008; 19: 641-649.
47. Keskitalo K, Broms U, Heliovaara M, Ripatti S, Surakka I, Perola M et al. Association of serum cotinine level with a cluster of three nicotinic acetylcholine receptor genes (CHRNA3/CHRNA5/CHRNB4) on chromosome 15. Hum Mol Genet 2009; 18: 4007-4012.
48. Amos CI, Gorlov IP, Dong Q, Wu X, Zhang H, Lu EY et al. Nicotinic acetylcholine receptor region on chromosome 15q25 and lung cancer risk among African Americans: a case-control study. J Natl Cancer Inst 2010; 102: 1199-1205.
49. Le Marchand L, Derby KS, Murphy SE, Hecht SS, Hatsukami D, Carmella SG et al. Smokers with the CHRNA lung cancer-associated variants are exposed to higher levels of nicotine equivalents and a carcinogenic tobacco-specific nitrosamine. Cancer Res 2008; 68: 9137-9140.
50. Lee AM, Jepson C, Shields PG, Benowitz N, Lerman C, Tyndale RF. CYP2B6 genotype does not alter nicotine metabolism, plasma levels, or abstinence with nicotine replacement therapy. Cancer Epidemiol Biomarkers Prev 2007; 16: 1312-1314.
51. Han BG, Nunomura W, Takakuwa Y, Mohandas N, Jap BK. Protein 4.1R core domain structure and insights into regulation of cytoskeletal organization. Nat Struct Biol 2000; 7: 871-875.
52. Shiffer KA, Goodman SR. Protein 4.1: its association with the human erythrocyte membrane. Proc Natl Acad Sci USA 1984; 81: 4404-4408.
53. Tran YK, Bogler O, Gorse KM, Wieland I, Green MR, Newsham IF. A novel member of the NF2/ERM/4.1 superfamily with growth suppressing properties in lung cancer. Cancer Res 1999; 59: 35-43.
54. Scott C, Keating L, Bellamy M, Baines AJ. Protein 4.1 in forebrain postsynaptic density preparations: enrichment of 4.1 gene products and detection of 4.1R binding proteins. Eur J Biochem 2001; 268: 1084-1094.
55. Binda AV, Kabbani N, Lin R, Levenson R. D2 and D3 dopamine receptor cell surface localization mediated by interaction with protein 4.1N. Mol Pharmacol 2002; 62: 507-513.
56. Gelernter J, Gueorguieva R, Kranzler HR, Zhang H, Cramer J, Rosenheck R et al. Opioid receptor gene (OPRM1, OPRK1, and OPRD1) variants and response to naltrexone treatment for alcohol dependence: results from the VA Cooperative Study. Alcohol Clin Exp Res 2007; 31: 555-563.
57. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005; 21: 263-265.
58. Zhang PW, Ishiguro H, Ohtsuki T, Hess J, Carillo F, Walther D et al. Human cannabinoid receptor 1: 5' exons, candidate regulatory regions, polymorphisms, haplotypes and association with polysubstance abuse. Mol Psychiatry 2004; 9: 916-931.
59. De Vries TJ, Schoffelmeer AN. Cannabinoid CB1 receptors control conditioned drug seeking. Trends Pharmacol Sci 2005; 26: 420-426.
60. Forget B, Hamon M, Thiebot MH. Cannabinoid CB1 receptors are involved in motivational effects of nicotine in rats. Psychopharmacology (Berl) 2005; 181: 722-734.
61. Tanda G, Goldberg SR. Cannabinoids: reward, dependence, and underlying neurochemical mechanisms-a review of recent preclinical data. Psychopharmacology (Berl) 2003; 169: 115-134.
62. Mascia MS, Obinu MC, Ledent C, Parmentier M, Bohme GA, Imperato A et al. Lack of morphine-induced dopamine release in the nucleus accumbens of cannabinoid CB(1) receptor knockout mice. Eur J Pharmacol 1999; 383: R1-R2.
63. Chen X, Williamson VS, An SS, Hettema JM, Aggen SH, Neale MC et al. Cannabinoid receptor 1 gene association with nicotine dependence. Arch Gen Psychiatry 2008; 65: 816-824.
64. Lerman C, Kaufmann V, Rukstalis M, Patterson F, Perkins K, Audrain-McGovern J et al. Individualizing nicotine replacement therapy for the treatment of tobacco dependence: a randomized trial. Ann Intern Med 2004; 140: 426-433.
65. Robinson JD, Cinciripini PM, Tiffany ST, Carter BL, Lam CY, Wetter DW. Gender differences in affective response to acute nicotine administration and deprivation. Addict Behav 2007; 32: 543-561.
66. Baker TB, Weiss RB, Bolt D, von Niederhausern A, Fiore MC, Dunn DM et al. Human neuronal acetylcholine receptor A5-A3-B4 haplotypes are associated with multiple nicotine dependence phenotypes. Nicotine Tob Res 2009; 11: 785-796.
67. Marubio LM, Gardier AM, Durier S, David D, Klink R, Arroyo-Jimenez MM et al. Effects of nicotine in the dopaminergic system of mice lacking the alpha4 subunit of neuronal nicotinic acetylcholine receptors. Eur J Neurosci 2003; 17: 1329-1337.
68. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM et al. Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 1998; 391: 173-177.
69. Saccone SF, Hinrichs AL, Saccone NL, Chase GA, Konvicka K, Madden PA et al. Cholinergic nicotinic receptor genes implicated in a nicotine dependence association study targeting 348 candidate genes with 3713 SNPs. Hum Mol Genet 2007; 16: 36-49.
70. Wada T, Naito M, Kenmochi H, Tsuneki H, Sasaoka T. Chronic nicotine exposure enhances insulin-induced mitogenic signaling via up-regulation of alpha7 nicotinic receptors in isolated rat aortic smooth muscle cells. Endocrinology 2007; 148: 790-799.
71. Chen RJ, Ho YS, Guo HR, Wang YJ. Long-term nicotine exposureinduced chemoresistance is mediated by activation of Stat3 and downregulation of ERK1/2 via nAChR and beta-adrenoceptors in human bladder cancer cells. Toxicol Sci 2010; 115: 118-130.
72. Saccone NL, Saccone SF, Hinrichs AL, Stitzel JA, Duan W, Pergadia ML et al. Multiple distinct risk loci for nicotine dependence identified by dense coverage of the complete family of nicotinic receptor subunit (CHRN) genes. Am J Med Genet B XNeuropsychiatr Genet 2009; 150B: 453-466.
73. Amos CI, Wu X, Broderick P, Gorlov IP, Gu J, Eisen T et al. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat Genet 2008; 40: 616-622.
74. Gago-Dominguez M, Jiang X, Conti DV, Castelao JE, Stern MC, Cortessis VK et al. Genetic variations on chromosomes 5p15 and 15q25 and bladder cancer risk: findings from the Los Angeles-Shanghai bladder case-control study. Carcinogenesis 2011; 32: 197-202.
75. Hung RJ, McKay JD, Gaborieau V, Boffetta P, Hashibe M, Zaridze D et al. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 2008; 452: 633-637.