A genome-wide association study identifies variants in KCNIP4 associated with ACE inhibitor-induced cough

Pharmacogenomics Journal

Volumn 16, Issue 3, 2016, Pages 231-237

  Mosley, J D ^a   Shaffer, C M ^a   Van Driest, S L ^a,b   Weeke, P E ^a,c   Wells, Q S ^a   Karnes, J H ^a   Velez Edwards, D R ^b   Wei, W Q ^b   Teixeira, P L ^b   Bastarache, L ^b   Crawford, D C ^d   Li, R ^e   Manolio, T A ^e   Bottinger, E P ^f   McCarty, C A ^g   Linneman, J G ^h   Brilliant, M H ^h   Pacheco, J A ⁱ   Thompson, W ⁱ   Chisholm, R L ⁱ   Jarvik, G P ^j   Crosslin, D R ^j   Carrell, D S ^k   Baldwin, E ^k   Ralston, J ^k   Larson, E B ^k   Grafton, J ^k   Scrol, A ^k   Jouni, H ^l   Kullo, I J ^l   Tromp, G ^m   Borthwick, K M ^m   Kuivaniemi, H ^m   Carey, D J ^m   Ritchie, M D ⁿ   Bradford, Y ⁿ   Verma, S S ⁿ   Chute, C G ^o   Veluchamy, A ^p   Siddiqui, M K ^p   Palmer, C N A ^p   Doney, A ^p   MahmoudPour, S H ^q   Maitland van der Zee, A H ^q   Morris, A D ^r   Denny, J C ^a,b   Roden, D M ^a   more..

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^g Essentia Institute of Rural Health   (United States)

^h MARSHFIELD CLINIC   (United States)

ⁱ NORTHWESTERN UNIVERSITY   (United States)

^j UNIVERSITY OF WASHINGTON   (United States)

^k GROUP HEALTH RESEARCH INSTITUTE   (United States)

^l MAYO CLINIC   (United States)

^m WEIS CENTER FOR RESEARCH   (United States)

ⁿ PENNSYLVANIA STATE UNIVERSITY   (United States)

^o JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^p UNIVERSITY OF DUNDEE   (United Kingdom)

^q UTRECHT UNIVERSITY   (Netherlands)

^r UNIVERSITY OF EDINBURGH   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; KCNIP4 PROTEIN, HUMAN; KV CHANNEL INTERACTING PROTEIN;

ADULT; AFRICAN; ARTICLE; CHROMOSOME 4; COHORT ANALYSIS; CONTROLLED STUDY; COUGHING; EUROPEAN; FEMALE; GENE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIABILITY; HUMAN; INTRON; KCNIP4 GENE; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; REPLICATION STUDY; SINGLE NUCLEOTIDE POLYMORPHISM; BIOLOGY; CASE CONTROL STUDY; CHEMICALLY INDUCED; ELECTRONIC HEALTH RECORD; ETHNOLOGY; GENETIC DATABASE; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MULTIVARIATE ANALYSIS; ODDS RATIO; PHENOTYPE; RISK ASSESSMENT; RISK FACTOR; SCOTLAND; STATISTICAL MODEL; UNITED STATES;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; CASE-CONTROL STUDIES; COMPUTATIONAL BIOLOGY; COUGH; DATABASES, GENETIC; ELECTRONIC HEALTH RECORDS; FEMALE; GENE FREQUENCY; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; KV CHANNEL-INTERACTING PROTEINS; LOGISTIC MODELS; MALE; MULTIVARIATE ANALYSIS; ODDS RATIO; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK ASSESSMENT; RISK FACTORS; SCOTLAND; UNITED STATES;

EID: 84970023347     PISSN: 1470269X     EISSN: 14731150     Source Type: Journal    
DOI: 10.1038/tpj.2015.51     Document Type: Article

References (54)

1. Zaman MA, Oparil S, Calhoun DA. Drugs targeting the renin-Angiotensinaldosterone system. Nat Rev Drug Discov 2002; 1: 621-636
2. Overlack A. ACE inhibitor-induced cough and bronchospasm. Incidence, mechanisms and management. Drug Saf 1996; 15: 72-78
3. Lee YJ, Tsai JC. Angiotensin-converting enzyme gene insertion/deletion, not bradykinin B2 receptor-58 T/C gene polymorphism, associated with angiotensin-converting enzyme inhibitor-related cough in Chinese female patients with non-insulin-dependent diabetes mellitus. Metab Clin Exp 2001; 50: 1346-1350
4. Woo KS, Nicholls MG. High prevalence of persistent cough with angiotensin converting enzyme inhibitors in Chinese. Br J Clin Pharmacol 1995; 40: 141-144
5. Wood R. Bronchospasm and cough as adverse reactions to the ACE inhibitors captopril, enalapril and lisinopril. A controlled retrospective cohort study. Br J Clin Pharmacol 1995; 39: 265-270
6. Bernstein KE, Ong FS, Blackwell W-LB, Shah KH, Giani JF, Gonzalez-Villalobos RA, et al. A modern understanding of the traditional and nontraditional biological functions of angiotensin-converting enzyme. Pharmacol Rev 2013; 65: 1-46
7. Fox AJ, Lalloo UG, Belvisi MG, Bernareggi M, Chung KF, Barnes PJ. Bradykinin-evoked sensitization of airway sensory nerves: a mechanism for ACE-inhibitor cough. Nat Med 1996; 2: 814-817
8. Furuya K, Yamaguchi E, Hirabayashi T, Itoh A, Hizawa N, Ohnuma N, et al. Angiotensin-I-converting enzyme gene polymorphism and susceptibility to cough. Lancet 1994; 343: 354
9. Mukae S, Itoh S, Aoki S, Iwata T, Nishio K, Sato R, et al. Association of polymorphisms of the renin-Angiotensin system and bradykinin B2 receptor with ACEinhibitor-related cough. J Hum Hypertens 2002; 16: 857-863
10. Woo SW, Bang S, Chung MW, Jin SK, Kim YS, Lee SH. Lack of association between ACE and bradykinin B2 receptor gene polymorphisms and ACE inhibitor-induced coughing in hypertensive Koreans. J Clin Pharm Ther 2009; 34: 561-567
11. Takahashi T, Yamaguchi E, Furuya K, Kawakami Y. The ACE gene polymorphism and cough threshold for capsaicin after cilazapril usage. Respir Med 2001; 95: 130-135
12. Li Y-F, Zhu X-M, Liu F, Xiao C-S, Bian Y-F, Li H, et al. Angiotensin-converting enzyme (ACE) gene insertion/deletion polymorphism and ACE inhibitor-related cough: a meta-Analysis. PLoS One 2012; 7: e37396
13. Grilo A, Sáez-Rosas MP, Santos-Morano J, Sánchez E, Moreno-Rey C, Real LM, et al. Identification of genetic factors associated with susceptibility to angiotensinconverting enzyme inhibitors-induced cough. Pharmacogenet Genomics 2011; 21: 10-17
14. Mas S, Gassò P, Alvarez S, Ortiz J, Sotoca JM, Francino A, et al. Pharmacogenetic predictors of angiotensin-converting enzyme inhibitor-induced cough: the role of ACE, ABO, and BDKRB2 genes. Pharmacogenet Genomics 2011; 21: 531-538
15. Mukae S, Aoki S, Itoh S, Iwata T, Ueda H, Katagiri T. Bradykinin B(2) receptor gene polymorphism is associated with angiotensin-converting enzyme inhibitorrelated cough. Hypertension 2000; 36: 127-131
16. Kim T-B, Oh S-Y, Park H-K, Jeon S-G, Chang Y-S, Lee K-Y, et al. Polymorphisms in the neurokinin-2 receptor gene are associated with angiotensin-converting enzyme inhibitor-induced cough. J Clin Pharm Ther 2009; 34: 457-464
17. Mahmoudpour SH, Leusink M, Putten L, van der, Terreehorst I, Asselbergs FW, de Boer A, et al. Pharmacogenetics of ACE inhibitor-induced angioedema and cough: a systematic review and meta-Analysis. Pharmacogenomics 2013; 14: 249-260
18. Zee RY, Rao VS, Paster RZ, Sweet CS, Lindpaintner K. Three candidate genes and angiotensin-converting enzyme inhibitor-related cough: a pharmacogenetic analysis. Hypertension 1998; 31: 925-928
19. Terao C, Bayoumi N, McKenzie CA, Zelenika D, Muro S, Mishima M, et al. Quantitative variation in plasma angiotensin-I converting enzyme activity shows allelic heterogeneity in the ABO blood group locus. Ann Hum Genet 2013; 77: 465-471
20. Luo J-Q, He F-Z, Luo Z-Y, Wen J-G, Wang L-Y, Sun N-L, et al. Rs495828 polymorphism of the ABO gene is a predictor of enalapril-induced cough in Chinese patients with essential hypertension. Pharmacogenet Genomics 2014; 24: 306-313
21. Gottesman O, Kuivaniemi H, Tromp G, Faucett WA, Li R, Manolio TA, et al. The Electronic Medical Records and Genomics (eMERGE) Network: past, present, and future. Genet Med 2013; 15: 761-771
22. Crawford DC, Crosslin DR, Tromp G, Kullo IJ, Kuivaniemi H, Hayes MG, et al. eMERGEing progress in genomics-The first seven years. Front Genet 2014; 5: 184
23. Bowton E, Field JR, Wang S, Schildcrout JS, Van Driest SL, Delaney JT, et al. Biobanks and electronic medical records: enabling cost-effective research. Sci Transl Med 2014; 6: 234cm3
24. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000; 155: 945-959
25. Dumitrescu L, Ritchie MD, Brown-Gentry K, Pulley JM, Basford M, Denny JC, et al. Assessing the accuracy of observer-reported ancestry in a biorepository linked to electronic medical records. Genet Med 2010; 12: 648-650
26. Kho AN, Pacheco JA, Peissig PL, Rasmussen L, Newton KM, Weston N, et al. Electronic medical records for genetic research: results of the eMERGE consortium. Sci Transl Med 2011; 3: 79re1
27. Israel RA. The International Classification of Disease. Two hundred years of development. Public Health Rep 1978; 93: 150-152
28. Liu M, Shah A, Jiang M, Peterson NB, Dai Q, Aldrich MC, et al. A study of transportability of an existing smoking status detection module across institutions. AMIA Annu Symp Proc 2012; 2012: 577-586
29. 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
30. Delaneau O, Zagury J-F, Marchini J. Improved whole-chromosome phasing for disease and population genetic studies. Nat Methods 2013; 10: 5-6
31. Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS Genet 2006; 2: e190
32. Zuvich RL, Armstrong LL, Bielinski SJ, Bradford Y, Carlson CS, Crawford DC, et al. Pitfalls of merging GWAS data: lessons learned in the eMERGE network and quality control procedures to maintain high data quality. Genet Epidemiol 2011; 35: 887-898
33. Verma SS, de Andrade M, Tromp G, Kuivaniemi H, Pugh E, Namjou B, et al. Imputation and quality control steps for combining multiple genome-wide datasets. Front Genet 2014; 5: 370
34. Mägi R, Morris AP. GWAMA: software for genome-wide association meta-Analysis. BMC Bioinformatics 2010; 11: 288
35. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007; 81: 559-575
36. 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
37. 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
38. Viechtbauer W. Conducting meta-Analyses in R with the metafor package. J Stat Softw 2010; 36: 1-48
39. GTEx Consortium. The Genotype-Tissue Expression (GTEx) project. Nat Genet 2013; 45: 580-585
40. Ward LD, Kellis M. HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res 2012; 40: D930-D934
41. Roden DM, Pulley JM, Basford MA, Bernard GR, Clayton EW, Balser JR, et al. Development of a large-scale de-identified DNA biobank to enable personalized medicine. Clin Pharmacol Ther 2008; 84: 362-369
42. Shibata R, Misonou H, Campomanes CR, Anderson AE, Schrader LA, Doliveira LC, et al. A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J Biol Chem 2003; 278: 36445-36454
43. Pruunsild P, Timmusk T. Structure, alternative splicing, and expression of the human and mouse KCNIP gene family. Genomics 2005; 86: 581-593
44. Massone S, Vassallo I, Castelnuovo M, Fiorino G, Gatta E, Robello M, et al. RNA polymerase III drives alternative splicing of the potassium channelinteracting protein contributing to brain complexity and neurodegeneration. J Cell Biol 2011; 193: 851-866
45. Xiong H, Kovacs I, Zhang Z. Differential distribution of KChIPs mRNAs in adult mouse brain. Brain Res Mol Brain Res 2004; 128: 103-111
46. Morohashi Y, Hatano N, Ohya S, Takikawa R, Watabiki T, Takasugi N, et al. Molecular cloning and characterization of CALP/KChIP4, a novel EF-hand protein interacting with presenilin 2 and voltage-gated potassium channel subunit Kv4. J Biol Chem 2002; 277: 14965-14975
47. Takahama K, Araki T, Fuchikami J, Kohjimoto Y, Miyata T. Studies on the magnitude and the mechanism of cough potentiation by angiotensin-converting enzyme inhibitors in guinea-pigs: involvement of bradykinin in the potentiation. J Pharm Pharmacol 1996; 48: 1027-1033
48. Himes BE, Sheppard K, Berndt A, Leme AS, Myers RA, Gignoux CR, et al. Integration of mouse and human genome-wide association data identifies KCNIP4 as an asthma gene. PLoS One 2013; 8: e56179
49. Wojczynski MK, Tiwari HK. Definition of phenotype. Adv Genet 2008; 60: 75-105
50. Rice JP, Saccone NL, Rasmussen E. Definition of the phenotype. Adv Genet 2001; 42: 69-76
51. Sinnott JA, Kraft P. Artifact due to differential error when cases and controls are imputed from different platforms. Hum Genet 2012; 131: 111-119
52. Johnson EO, Hancock DB, Levy JL, Gaddis NC, Saccone NL, Bierut LJ, et al. Imputation across genotyping arrays for genome-wide association studies: assessment of bias and a correction strategy. Hum Genet 2013; 132: 509-522
53. Smemo S, Tena JJ, Kim K-H, Gamazon ER, Sakabe NJ, Gómez-Marín C, et al. Obesity-Associated variants within FTO form long-range functional connections with IRX3. Nature 2014; 507: 371-375
54. Van den Boogaard M, Smemo S, Burnicka-Turek O, Arnolds DE, van de Werken HJG, Klous P, et al. A common genetic variant within SCN10A modulates cardiac SCN5A expression. J Clin Invest 2014; 124: 1844-1852