Nicotinic acetylcholine receptor β2 subunit gene implicated in a systems-based candidate gene study of smoking cessation

Human Molecular Genetics

Volumn 17, Issue 18, 2008, Pages 2834-2848

  Conti, David V ^a   Lee, Won ^a   Li, Dalin ^a   Liu, Jinghua ^a   Van den Berg, David ^a   Thomas, Paul D ^b   Bergen, Andrew W ^b   Swan, Gary E ^b   Tyndale, Rachel F ^c   Benowitz, Neal L ^d   Lerman, Caryn ^e  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b SRI INTERNATIONAL   (United States)

^c CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE 1; AMFEBUTAMONE; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; AROMATIC LEVO AMINO ACID DECARBOXYLASE; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID 1 RECEPTOR; CATECHOL METHYLTRANSFERASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLIN DEPENDENT KINASE 5; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE BETA MONOOXYGENASE; ERYTHROCYTE BAND 4.1 PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 16; MITOGEN ACTIVATED PROTEIN KINASE 1; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BETA2; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; PHOSPHORYLASE KINASE; PHOSPHORYLASE KINASE DELTA; PLACEBO; POLYPEPTIDE; SEROTONIN 1A RECEPTOR; SEROTONIN 1B RECEPTOR; TRYPTOPHAN 2,3 DIOXYGENASE;

3' UNTRANSLATED REGION; ADULT; ALLELE; ARTICLE; COMPUTER ANALYSIS; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HETEROZYGOTE; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RELAPSE; SINGLE NUCLEOTIDE POLYMORPHISM; SMOKING CESSATION; TOBACCO DEPENDENCE; TREND STUDY; WITHDRAWAL SYNDROME;

3' UNTRANSLATED REGIONS; ADULT; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; FOLLOW-UP STUDIES; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, NICOTINIC; RECURRENCE; SMOKING; SMOKING CESSATION; SUBSTANCE WITHDRAWAL SYNDROME; TOBACCO USE DISORDER;

NICOTIANA TABACUM;

EID: 50849143769     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn181     Document Type: Article

References (82)

1. Scholl, R.A. and Lerman, C. (2006) Current and emerging pharmacotherapies for treating tobacco dependence. Expert Opin. Emerg. Drugs, 11, 429-444.
2. Swan, G.E., Jack, L.M., Javitz, H.S., McAfee, T. and McClure, J.B. (2008) Predictors of 12-month outcome in smokers who received bupropion sustained-release for smoking cessation. CNS Drugs, 22, 239-256.
3. Swan, G.E., Javitz, H.S., Jack, L.M,, Curry, S.J. and McAfee, T. (2004) Heterogeneity in 12-month outcome among female and male smokers. Addiction, 99, 237-250.
4. Swan, G.E.,McAfee, T., Curry, S.J., Jack, L. M., Javitz, H., Dacey, S. and Bergman, K. (2003) Effectiveness of bupropion sustained release for smoking cessation in a health care setting: A randomized trial. Arch. Intern. Med., 163, 2337-2344.
5. Dale, L.C., Glover, E.D., Sachs, D.P., Schroeder, D.R., Offord, K.P., Croghan, I.T. and Hurt, R.D. (2001) Bupropion for smoking cessation: predictors of successful outcome. Chest, 119, 1357-1364.
6. Hurt, R.D., Sachs, D.P., Glover, E.D., Offord, K.P., Johnston, J.A., Dale, L.C., Khayrallah, M.A., Schroeder, D.R., Glover, P.N., Sullivan, C.R. et al. (1997) A comparison of sustained-release bupropion and placebo for smoking cessation. N. Engl. J. Med., 337, 1195-1202.
7. Benowitz, N.L. (2008) Clinical pharmacology of nicotine: Implications for understanding, preventing and treating tobacco addiction. Clin. Pharmacol. Ther., 83, 531-541.
8. Paterson, N.E., Balfour, D.J. and Markou, A. (2007). Chronic bupropion attenuated the anhedonic component of nicotine withdrawal in rats via inhihition of dopamine reuptake in the nucleus accumbens shell. Eur J. Neurosci., 25, 3099-3108.
9. Portugal, G.S. and Gould, T.J. (2007) Bupropion dose-dependently reverses nicotine withdrawal deficits, in contextual fear conditioning. Pharmacol. Biochem. Behav., 88, 179-187.
10. Lerman, C., Roth, D., Kaufmann, V., Audrain, J., Hawk, L., Liu, A., Niaura, R. and Epstein, L. (2002) Mediating mechanisms for the impact of bupropion in smoking cessation treatment. Drug-Alc. Depend., 67 219-223.
11. West, R., Baker, C.L., Cappelleri, J.C. and Bushmakin, A. G. (2008) Effect of varenicline and bupropion SR on craving, nicotine withdrawal symptoms, and rewarding effects of smoking during a quit attempt. Psychopharmacology (Berlin), 197, 371-377.
12. Gelernter, J., Yu, Y., Weiss, R., Brady, K., Panhuysen, C., Yang, B.Z., Kranzler, H.R. and Farrer, L. (2006) Haplotype spanning TTC12 and ANKK1, flanked by the DRD2 and NCAM1 loci, is strongly associated to nicotine dependence in two distinct American populations. Hum. Mol. Genet., 15, 3498-3507.
13. Huang, W., Payne, T.J., Ma, J.Z., Beuten, J., Dupont, R.T., Inohara, N. and Li, M.D. (2008) Significant association of ANKK1 and detection of a functional polymorphism with nicotine dependence in an African-American sample. Neuropsychopharmacology. Epub ahead of print 19 March, doi:10.1038/npp.2008.37.
14. Hutchison, K.E. Allen, D.L.; Filbey, F.M., Jepson, C., Lerman, C., Benowitz, N.L., Stitzel, J., Bryan, A., McGeary, J. and Haughey, H.M. (2007) CHRNA4 and tobacco dependence from gene regulation to treatment outcome. Arch. Gen. Psychiatry, 64, 1078-1086.
15. Saccone, S.F., Hinrichs, A.L., Saccone, N.L., Chase, G.A., Konvicka, K., Madden, P.A., Breslau, N., Johnson, E.O., Hatsukami, D., Pomerleau, O. et al. (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.
16. Zhang, H., Ye, Y., Wang, X., Gelernter, J., Ma, J.Z. and Li, M.D. (2006) DOPA decarboxylase gene is associated with nicotine dependence. Pharmacogenomics, 7, 1159-1166.
17. Berrettini, W.H., Wileyto, E.P., Epstein, L., Restine, S., Hawk, L., Shields, P., Niaura, R. and Lerman, C. (2007) Catechol-O methyltransferase (COMT) gene variants predict response to bupropion therapy for tobacco dependence. Biol. Psychiatry, 61, 111-118.
18. David, S.P., Strong, D.R., Munafo, M.R., Brown, R.A., Lloyd-Richardson, E.E., Wileyto, P.E., Evins, E.A., Shields, P.G., Lerman, C. and Niaura, R. (2007) Bupropion efficacy for smoking cessation is influenced by the DRD2 Taq1A polymorphism: Analysis of pooled data from two clinical trials. Nicotine. Tob. Res., 9, 1251-1257.
19. Heitjan, D.F., Guo, M., Ray, R., Wileyto, E.P., Epstein, L.H. and Lerman, C. (2007) Identification of pharmacogenetic markers in smoking cessation therapy. Am. J. Med. Genet. B Neuropsychiatr. Genet. Epub ahead of print 28 Dec, doi:10.1038/sj.tpj.6500492.
20. Lerman, C., Jepson, C., Wileyto, E.P., Epstein, L.H., Rukstalis, M., Patterson, F., Kaufmann, V., Restine, S., Hawk, L., Niaura, R. et al. (2006) 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, 31, 231-242.
21. Swan, G.E., Jack, L.M., Valdes, A.M., Ring, H.Z., Ton, C.C., Curry, S.J. and McAfee, T. (2007) Joint effect of dopaminergic genes on likelihood of smoking following treatment with bupropion SR. Health Psychol., 26, 361-368.
22. Swan, G.E., Valdes, A.M., Ring, H.Z., Khroyan, T.V., Jack, L.M., Ton, C.C., Curry, S.J. and McAfee, T. (2005) Dopamine receptor DRD2 genotype and smoking cessation outcome following treatment with bupropion SR. Pharmacogen. J., 5, 21-29.
23. Gotti, C., Moretti, M., Gaimarri, A., Zanardi, A., Clementi, F. and Zoli, M. (2007) Heterogeneity and complexity of native brain nicotinic receptors. Biochem. Pharmacol., 74, 1102-1111.
24. Hughes, J.R., Stead, L.F. and Lancaster, T. (2007) Antidepressants for smoking cessation. Cochrane Database Syst. Rev., CD000031.
25. Barrett, J.C., Fry, B., Maller, J. and Daly, M.J. (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265.
26. Mooney, M.E. and Sofuoglu, M. (2006) Bupropion for the treatment of nicotine withdrawal and craving. Expert. Rev. Neurother., 6, 965-981.
27. Cryan, J.F., Bruijnzeel, A.W., Skjei, K.L. and Markou, A. (2003) Bupropion enhances brain reward function and reverses the affective and somatic aspects of nicotine withdrawal in the rat. Psychopharmacology (Berlin), 168, 347-358.
28. Kenny, P.J. and Markou, A. (2006) Nicotine self-administration acutely activates brain reward systems and induces a long-lasting increase in reward sensitivity. Neuropsychopharmacology, 31, 1203-1211.
29. Kenny, P.J. and Markou, A. (2005) Conditioned nicotine withdrawal profoundly decreases the activity of brain reward systems. J. Neurosci., 25, 6208-6212.
30. Picciotto, M.R., Zoli, M., Rimondini, R., Lena, C., Marubio, L.M., Pich, E.M., Fuxe, K. and Changeux, J.P. (1998) Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature, 391, 173-177.
31. Brunzell, D.H., Chang, J.R., Schneider, B., Olausson, P., Taylor, J.R. and Picciotto, M.R. (2006) β2-Subunit containing nicotinic acetylcholine receptors are involved in nicotine-induced increases in conditioned reinforcement but not progressive ratio responding for food in C57BL/6 mice. Psychopharmacology (Berlin), 184, 328-338.
32. Walters, C.L., Brown, S., Changeux, J.P., Martin, B. and Damaj, M.I. (2006) The beta2 but not alpha7 subunit of the nicotinic acetylcholine receptor is required for nicotine-conditioned place preference in mice. Psychopharmacology (Berlin), 184, 339-344.
33. Portugal, G.S., Kenney, J.W. and Gould, T.J. (2008) Beta2 subunit containing acetylcholine receptors mediate nicotine withdrawal deficits in the acquisition of contextual fear conditioning. Neurobiol. Learn. Mem., 89, 106-113.
34. Wehner, J.M., Keller, J.J., Keller, A.B., Picciotto, M.R., Paylor, R., Booker, T.K., Beaudet, A., Heinemann, S.F. and Balogh, S.A. (2004) Role of neuronal nicotinic receptors in the effects of nicotine and ethanol on contextual fear conditioning. Neuroscience, 129, 11-24.
35. Brody, A.L. (2006) Functional brain imaging of tobacco use and dependence. J. Psychiatry Res., 40, 404-418.
36. Staley, J.K., Krishnan-Sarin, S., Cosgrove, K.P., Krantzler, E., Frohlich, E., Perry, E., Dubin, J.A., Estok, K., Brenner, E., Baldwin, R-M. et al. (2006) Human tobacco smokers in early abstinence have higher levels of beta2* nicotinic acetylcholine receptors than nonsmokers. J. Neurosci., 26, 8707-8714.
37. Ehringer, M.A., Clegg, H.V., Collins, A.C., Corley, R.P., Crowley, T., Hewitt, J.K., Hopfer, C.J., Krauter, K., Lessem, J., Rhee, S. R. et al. (2007) Association of the neuronal nicotinic receptor beta2 subunit gene (CHRNB2) with subjective responses to alcohol and nicotine. Am. J. Med. Genet. B Neuropsychiatir. Genet., 144, 596-604.
38. Li, M.D., Beuten, J., Ma, J.Z., Payne, T.J., Lou, X.Y., Garcia, V., Duenes, A.S., Crews, K.M. and Elston, R.C. (2005) Ethnic- and gender-specific association-of the nicotinic acetylcholine receptor alpha4 subunit gene (CHRNA4) with nicotine dependence. Hum. Mol. Genet., 14, 1211-1219.
39. Lueders, K.K., Hu, S., McHugh, L., Myakishev, M.V., Sirota, L.A. and Hamer, D.H. (2002) Genetic and functional analysis of single nucleotide polymorphisms in the beta2-neuronal nicotinic acetylcholine receptor gene (CHRNB2). Nicotine. Tob. Res., 4, 115-125.
40. Silverman, M.A., Neale, M.C., Sullivan, P.F., Harris-Kerr, C., Wormley, B,, Sadek, H., Ma, Y., Kendler, K.S. and Straub, R.E. (2000) Haplotypes of four novel single nucleotide polymorphisms in the nicotinic acetylcholine receptor beta2-subunit (CHRNB2) gene show no association with smoking initiation or nicotine dependence. Am. J. Med. Genet. 96, 646-653.
41. Lou, X.Y., Chen, G.B., Yan, L., Ma, J.Z., Zhu, J., Elston, R.C. and Li, M.D. (2007) A generalized combinatorial approach for detecting gene-by-gene and gene-by-environment interactions with application to nicotine dependence. Am. J. Hum. Genet., 80, 1125-1137.
42. Lessov-Schlaggar, C.N., Pergadia, M.L., Khroyan, T.V. and Swan, G.E. (2008) Genetics of nicotine dependence and pharmacotherapy. Biochemical. Pharm., 75, 178-195.
43. Amos, C.I., Wu, X., Broderick, P., Gorlov, I.P., Gu, J., Eisen, T., Dong, Q., Zhang, Q., Gu, X., Vijayakrishnan, J. et al. (2008) Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat. Genet., 40, 612-622.
44. Berrettini, W., Yuan, X., Tozzi, F., Song, K., Francks, C., Chilcoat, H., Waterworth, D., Muglia, P. and Mooser, V. (2008) Alpha-5/alpha-3 nicotinic receptor subunit alleles increase risk for heavy smoking. Mol. Psychitary, 13, 368-373.
45. Hung, R.J., McKay, J.D., Gaborieau, V., Boffetta, P., Hashibe, M., Zaridze, D., Mukeria, A., Szeszenia-Dabrowska, N., Lissowska, J., Rudnai, P. et al. (2008) A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature, 452, 633-637.
46. Thorgeirsson, T.E., Geller, F., Sulem, P., Rafnar, T., Wiste, A., Magnusson, K.P., Manolescu, A., Thorleifsson, G., Stefansson, H., Ingason, A. et al. (2008) A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature, 452, 638-642.
47. Thomas, D.C. and WittA, J.S. (2002) Point: Population stratification: a problem for case-control studies of candidate-gene associations? Cancer Epidemiol. Biol. Prev., 11, 505-512.
48. Wacholder, S., Rothman, N. and Caporaso, N. (2000) Population stratification in epidemiologic studies of common genetic variants and cancer: Quantification of bias. J. Natl. Cancer Inst., 92, 1151-1158.
49. Wacholder, S., Rothman, N. and Caporaso, N. (2002) Counterpoint: Bias from population stratification is not a major threat to the validity of conclusions from epidemiological studies of common polymorphisms and cancer. Cancer Epidemiol., Biol. Prev., 11, 513-520.
50. Hamada, M., Hendrick, J.P., Ryan, G.R., Kuroiwa, M., Higashi, H., Tanaka, M., Nairn, A.C., Greengard, P. and Nishi, A. (2005) Nicotine regulates DARPP-32 (dopamine- and cAMP-regulated phosphoprotein of 32 kDa) phosphorylation at multiple sites in neostriatal neurons. J. Pharmacol. Exp. Ther., 315, 872-878.
51. Lerer, E., Kanyas, K., Kami, O., Ebstein, R.-P. and Lerer, B. (2006) Why do young women smoke? II. Role of traumatic life experience, psychological characteristics and serotonergic genes. Mol. Psychiatry 11, 771-781.
52. Soderstrom, K., Qin, W., Williams, H., Taylor, D.A. and McMillen, B.A. (2007) Nicotine increases FosB expression within a subset of reward- and memory-related brain regions during both peri- and post-adolescence. Psychopharmacology (Berlin), 191, 891-897.
53. Sullivan, P.F., Neale, B.M., van den Oord, E., Miles, M.F., Neale, M.C., Bulik, C.M., Joyce, P.R., Straub, R.E. and Kendler, K.S. (2004) Candidate genes for nicotine dependence via linkage, epistasis, and bioinformatics. Am. J. Med. Genet. B Neuropsychiatr. Genet., 126, 23-36.
54. Huang, W., Ma, J.Z., Payne, T.J., Beuten, J., Dupont, R.T. and Li, M.D. (2008) Significant association of DRD1 with nicotine dependence. Hum. Genet., 123, 133-140.
55. Huang, W., Payne, T.J., Ma, J.Z. and Li, M.D. (2008) A functional polymorphism, rs6280, in DRD3 is significantly associated with nicotine dependence in European-American smokers. Am. J. Med. Genet. B Neuropsychiatr. Genet.
56. Li, M.D., Lou, X.Y., Chen, G., Ma, J.Z. and.Elston, R.C. (2008) Gene-gene interactions among CHRNA4, CHRNB2, BDNF, and NTRK2 in nicotine dependence. Biol. Psychiatry. Epub ahead of print 3 June, doi:10.1016/j.biopsych.2008.04.026.
57. Lohmueller, K.E., Pearce, C.L., Pike, M., Lander, E.S. and Hirschhom, J.N. (2003) Meta-analysis of genetic association studies supports a contribution of common variants to susceptibility to common disease. Nat. Genet., 33, 177-182.
58. Conti, D.V., Cortessis, V., Molitor, J. and Thomas, D.C. (2003) Bayesian modeling of complex metabolic pathways. Hum. Hered., 56, 83-93.
59. Conti, D.V., Lewinger, J.P., Swan, G.E., Tyndale, R.F., Benowitz, N.L. and Thomas, P.D. Using Ontolgies in Hierarchical Modeling of Genes and Exposures in Biologic Pathways. In National Cancer Institute. Phenotypes and Endophenotypes: Foundations for Genetic Studies of Nicotine use and Dependence, Tobacco Control Monograph No. 20. Bethesda, MD: U.S. Department of Health and Human Services, National Institutes of Health, National Cancer Institute, in press.
60. Thomas, C.E. and Ganji, G. (2006) Integration of genomic and metabonomic data in systems biology - are we 'there' yet? Curr. Opin. Drug Discov. Devel., 9, 92-100.
61. Thomas, D.C. (2005) The need for a systematic approach to complex pathways in molecular epidemiology. Cancer Epidemiol. Biol. Prev., 14, 557-559.
62. Kabbani, N., Woll, M.P., Levenson, R., Lindstrom, J.M. and Changeux, J.P. (2007) Intracellular complexes of the beta2 subunit of the nicotinic acetylcholine receptor in brain identified by proteomics. Proc. Natl Acad. Sci. USA, 104, 20570-20575.
63. Griffiths-Jones, S., Grocock, R.J., van Dongen, S., Bateman, A. and Enright, A.J. (2006) miRBase: MicroRNA sequences, targets and gene nomenclature. Nucleic Acids Res., 34, D140-D144.
64. Heatherton, T.F., Kozlowski, L.T., Frecker, R.C. and Fagerstrom, K.O. (1991) The Fagerstrom test for nicotine dependence: A revision of the Fagerstrom tolerance questionnaire. Br. J. Addict., 86. 1119-1127.
65. Brown, R., Burgess, E., Sales, S. and Whiteley, J. (1998) Reliability and validity of a smoking timeline follow-back interview. Psychol. Addictive. Behav., 12, 101-112.
66. Feycrabend, C. and Russell, M.A. (1990) A rapid gas-liquid chromatographic method for the determination of cotinine and nicotine in biological fluids. J. Pharm. Pharmacol., 42, 450-452.
67. SRNT Subcommittee on Biochemical Verification (2002) Biochemical verification of tobacco use and cessation. Nictotine. Tob. Res., 4, 149-159.
68. Smith, M.W., Patterson, N., Lautenberger, J.A., Truelove, A.L., McDonald, G.J., Waliszewska, A., Kessing, B.D., Malasky, M.J., Scafe, C., Le, E. et al. (2004) A high-density admixture map for disease gene discovery in african americans. Am. J. Hum. Genet., 74, 1001-1013.
69. Pritchard, J.K., Stephens, M. and Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
70. Pritchard, J.K.. Stephens, M., Rosenberg, N.A. and Donnelly, P. (2000) Association mapping in structured populations. Am. J. Hum. Genet., 67, 170-181.
71. Price, A.L., Patterson, N.J., Plenge, R.M., Weinblatt, M.E., Shadick, N.A. and Reich, D. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet., 38, 904-909.
72. Haiman, C.A., Stram, D.O., Pike, M.C., Kolonel, L.N:, Burtt, N.P., Altshuler, D., Hirschhom, J. and Henderson, B.E. (2003) A comprehensive haplotype analysis of CYP19 and breast cancer risk: The multiethnic cohort. Hum. Mol. Genet.. 12, 2679-2692.
73. Edlund, C.K, Lee, W.H., Li, D., Van Den Berg, D.J. and Conti, D.V. (2008) Snagger: A user-friendly program for incorporating additional information for tagSNP selection. BMC Bioinformat., 9, 174.
74. Thorisson, G.A., Smith, A.V., Krishnan, L. and Stein, L.D. (2005) The international HapMap project web site. Genome Res., 15, 1592-1593.
75. Chou, C.P., Li, Y., Unger, J.B., Xia, J., Sun, P., Guo, Q., Shakib, S., Gong, J., Xie. B., Liu, C. et al. (2006) A randomized intervention of smoking for adolescents in urban Wuhan, China. Prev. Med., 42, 280-285.
76. Cox, D.G. and Kraft, P. (2006) Quantification of the power of Hardy-Weinberg equilibrium testing to detect genotyping error. Hum. Hered., 61, 10-14.
77. Kang, S.J., Gordon, D. and Finch, S.J. (2004) What SNP genotyping errors are most costly for genetic association studies? Genet. Epidemiol. 26, 132-141.
78. Leal, S.M. (2005) Detection of genotyping errors and pseudo-SNPs via deviations from Hardy-Weinberg equilibrium. Genet. Epidemiol., 29, 204-214.
79. Zou, G.Y. and Donner, A. (2006) The merits of testing Hardy-Weinberg equilibrium in the analysis of unmatched case-control data: A cautionary note. Ann. Hum. Genet., 70, 923-933.
80. Kraft, P., Yen, Y.C., Stram, D.O., Morrison, J. and Gauderman, W.J. (2007) Exploiting gene-environment interaction to detect genetic associations. Hum. Hered., 63, 111-119.
81. R Development Core Team (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria.
82. Conneely, K.N. and Boehnke, M. (2007) So many correlated tests, so little time! Rapid adjustment of P-values for multiple correlated tests. Am. J. Hum. Genet., 81, 1158-1168.