XWAS: A Software Toolset for Genetic Data Analysis and Association Studies of the X Chromosome

Journal of Heredity

Volumn 106, Issue 5, 2015, Pages 666-671

  Gao, Feng ^a,d   Chang, Diana ^a,b   Biddanda, Arjun ^a   Ma, Li ^a,c   Guo, Yingjie ^a   Zhou, Zilu ^a   Keinan, Alon ^a,b  

^a Program on Infrastructure Policy   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d HARBIN INSTITUTE OF TECHNOLOGY   (China)

Author keywords

Chromosome X; complex diseases; genetic association study; GWAS; sexual dimorphism; software

Indexed keywords

ARTICLE; AUTOIMMUNE DISEASE; BIOINFORMATICS; CORONARY ARTERY DISEASE; DATA ANALYSIS SOFTWARE; EFFECT SIZE; FEMALE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC RISK; HETEROZYGOTE; HOMOZYGOTE; HUMAN; MALE; PRIORITY JOURNAL; QUALITY CONTROL PROCEDURES; QUANTITATIVE GENETICS; RISK ASSESSMENT; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTOLIC BLOOD PRESSURE; X CHROMOSOME; X CHROMOSOME INACTIVATION; X CHROMOSOME LINKED DISORDER; GENETICS; GENOME-WIDE ASSOCIATION STUDY; PHENOTYPE; PROCEDURES; SOFTWARE;

CHROMOSOMES, HUMAN, X; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SOFTWARE; X CHROMOSOME INACTIVATION;

EID: 84941615863     PISSN: 00221503     EISSN: 14657333     Source Type: Journal    
DOI: 10.1093/jhered/esv059     Document Type: Article

References (66)

1. Abdou AG, Maraee AH, Reyad W. 2013. Immunohistochemical expression of heat shock protein 70 in vitiligo. Ann Diagn Pathol. 17:245-249.
2. Ahmeti KB, Ajroud-Driss S, Al-Chalabi A, Andersen PM, Armstrong J, Birve A, Blauw HM, Brown RH, Bruijn L, Chen W, et al. 2013. Age of onset of amyotrophic lateral sclerosis is modulated by a locus on 1p34.1. Neurobiol Aging. 34:357.e7-357.e19.
3. Ahn R, Ding YC, Murray J, Fasano A, Green PH, Neuhausen SL, Garner C. 2012. Association analysis of the extended MHC region in celiac disease implicates multiple independent susceptibility loci. PLoS One. 7:e36926.
4. Arbiza L, Gottipati S, Siepel A, Keinan A. 2014. Contrasting X-linked and autosomal diversity across 14 human populations. Am J Hum Genet. 94:827-844.
5. Baranzini SE, Wang J, Gibson RA, Galwey N, Naegelin Y, Barkhof F, Radue EW, Lindberg RL, Uitdehaag BM, Johnson MR, et al. 2009. Genome-wide association analysis of susceptibility and clinical phenotype in multiple sclerosis. Hum Mol Genet. 18:767-778.
6. Birlea SA, Jin Y, Bennett DC, Herbstman DM, Wallace MR, McCormack WT, Kemp EH, Gawkrodger DJ, Weetman AP, Picardo M, et al. 2011. Comprehensive association analysis of candidate genes for generalized vitiligo supports XBP1, FOXP3, and TSLP. J Invest Dermatol. 131:371-381.
7. Bowie LJ, Reddy PL, Beck KR. 1997. Alpha thalassemia and its impact on other clinical conditions. Clin Lab Med. 17:97-108.
8. Brown MB, Forsythe AB. 1974. Robust tests for equality of variances. J Am Stat Assoc. 69:364-367.
9. Carrel L, Willard HF. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature. 434:400-404.
10. Chang D, Gao F, Slavney A, Ma L, Waldman YY, Sams AJ, Billing-Ross P, Madar A, Spritz R, Keinan A. 2014. Accounting for eXentricities: analysis of the X chromosome in GWAS reveals X-linked genes implicated in autoimmune diseases. PLoS One. 9:e113684.
11. Clayton D. 2008. Testing for association on the X chromosome. Biostatistics. 9:593-600.
12. Clayton DG. 2009. Sex chromosomes and genetic association studies. Genome Med. 1:110.
13. Cotton AM, Lam L, Affleck JG, Wilson IM, Penaherrera MS, McFadden DE, Kobor MS, Lam WL, Robinson WP, Brown CJ. 2011. Chromosome-wide DNA methylation analysis predicts human tissue-specific X inactivation. Hum Genet. 130:187-201.
14. Cronin S, Berger S, Ding J, Schymick JC, Washecka N, Hernandez DG, Greenway MJ, Bradley DG, Traynor BJ, Hardiman O. 2008. A genome-wide association study of sporadic ALS in a homogenous Irish population. Hum Mol Genet. 17:768-774.
15. Disteche CM. 2012. Dosage compensation of the sex chromosomes. Annu Rev Genet. 46:537-560.
16. Duerr RH, Taylor KD, Brant SR, Rioux JD, Silverberg MS, Daly MJ, Steinhart AH, Abraham C, Regueiro M, Griffiths A, et al. 2006. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science. 314:1461-1463.
17. Emery LS, Felsenstein J, Akey JM. 2010. Estimators of the human effective sex ratio detect sex biases on different timescales. Am J Hum Genet. 87:848-856.
18. Evans DM, Spencer CC, Pointon JJ, Su Z, Harvey D, Kochan G, Oppermann U, Dilthey A, Pirinen M, Stone MA, et al. 2011. Interaction between ERAP1 and HLA-B27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nat Genet. 43:761-767.
19. Fisher RA. 1925. Statistical methods for research workers. Edinburgh (UK): Oliver and Boyd.
20. Gilks WP, Abbott JK, Morrow EH. 2014. Sex differences in disease genetics: evidence, evolution, and detection. Trends Genet. 30:453-463.
21. Hammer MF, Mendez FL, Cox MP, Woerner AE, Wall JD. 2008. Sex-biased evolutionary forces shape genomic patterns of human diversity. PLoS Genet. 4:e1000202.
22. Hammer MF, Woerner AE, Mendez FL, Watkins JC, Cox MP, Wall JD. 2010. The ratio of human X chromosome to autosome diversity is positively correlated with genetic distance from genes. Nat Genet. 42:830-831.
23. Howie B, Fuchsberger C, Stephens M, Marchini J, Abecasis GR. 2012. Fast and accurate genotype imputation in genome-wide association studies through pre-phasing. Nat Genet. 44:955-959.
24. Huynh KD, Fischle W, Verdin E, Bardwell VJ. 2000. BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev. 14:1810-1823.
25. International Multiple Sclerosis Genetics Consortium, Wellcome Trust Case Control Consortium, Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, Dilthey A, Su Z, et al. 2011. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature. 476:214-219.
26. Jiang B, Zhang X, Zuo Y, Kang G. 2011. A powerful truncated tail strength method for testing multiple null hypotheses in one dataset. J Theor Biol. 277:67-73.
27. Jin X, Chen YP, Chen SH, Xiang Z. 2013. Association between Helicobacter Pylori infection and ulcerative colitis-a case control study from China. Int J Med Sci. 10:1479-1484.
28. Jin Y, Birlea SA, Fain PR, Ferrara TM, Ben S, Riccardi SL, Cole JB, Gowan K, Holland PJ, Bennett DC, et al. 2012. Genome-wide association analyses identify 13 new susceptibility loci for generalized vitiligo. Nat Genet. 44:676-680.
29. Jin Y, Birlea SA, Fain PR, Gowan K, Riccardi SL, Holland PJ, Mailloux CM, Sufit AJ, Hutton SM, Amadi-Myers A, et al. 2010. Variant of TYR and autoimmunity susceptibility loci in generalized vitiligo. N Engl J Med. 362:1686-1697.
30. Ju T, Cummings RD. 2005. Protein glycosylation: chaperone mutation in Tn syndrome. Nature. 437:1252.
31. Keinan A, Reich D. 2010. Can a sex-biased human demography account for the reduced effective population size of chromosome X in non-Africans Mol Biol Evol. 27:2312-2321.
32. Korn JM, Kuruvilla FG, McCarroll SA, Wysoker A, Nemesh J, Cawley S, Hubbell E, Veitch J, Collins PJ, Darvishi K, et al. 2008. Integrated genotype calling and association analysis of SNPs, common copy number polymorphisms and rare CNVs. Nat Genet. 40:1253-1260.
33. Laaksovirta H, Peuralinna T, Schymick JC, Scholz SW, Lai SL, Myllykangas L, Sulkava R, Jansson L, Hernandez DG, Gibbs JR, et al. 2010. Chromosome 9p21 in amyotrophic lateral sclerosis in Finland: a genome-wide association study. Lancet Neurol. 9:978-985.
34. Lambert CA, Connelly CF, Madeoy J, Qiu R, Olson MV, Akey JM. 2010. Highly punctuated patterns of population structure on the X chromosome and implications for African evolutionary history. Am J Hum Genet. 86:34-44.
35. Lerner DJ, Kannel WB. 1986. Patterns of coronary heart disease morbidity and mortality in the sexes: a 26-year follow-up of the Framingham population. Am Heart J. 111:383-390.
36. Liu JZ, McRae AF, Nyholt DR, Medland SE, Wray NR, Brown KM, Hayward NK, Montgomery GW, Visscher PM, et al. 2010. A versatile gene-based test for genome-wide association studies. Am J Hum Genet. 87:139-145.
37. Lohmueller KE, Degenhardt JD, Keinan A. 2010. Sex-averaged recombination and mutation rates on the X chromosome: a comment on Labuda et al. Am J Hum Genet. 86:978-980; author reply 980-981.
38. Loley C, Ziegler A, Konig IR. 2011. Association tests for X-chromosomal markers-a comparison of different test statistics. Hum Hered. 71:23-36.
39. Luther J, Dave M, Higgins PD, Kao JY. 2010. Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Inflamm Bowel Dis. 16:1077-1084.
40. Ma L, Clark AG, Keinan A. 2013. Gene-based testing of interactions in association studies of quantitative traits. PLoS Genet. 9:e1003321.
41. Ma L, Hoffman G, Keinan A. 2015. X-inactivation informs variance-based testing for X-linked association of a quantitative trait. BMC Genomics. 16:241.
42. Mailman MD, Feolo M, Jin Y, Kimura M, Tryka K, Bagoutdinov R, Hao L, Kiang A, Paschall J, Phan L, et al. 2007. The NCBI dbGaP database of genotypes and phenotypes. Nat Genet. 39:1181-1186.
43. Matanoski G, Tao X, Almon L, Adade AA, Davies-Cole JO. 2006. Demographics and tumor characteristics of colorectal cancers in the United States, 1998-2001. Cancer. 107(5 Suppl):1112-1120.
44. Mosenson JA, Eby JM, Hernandez C, Le Poole IC. 2013. A central role for inducible heat-shock protein 70 in autoimmune vitiligo. Exp Dermatol. 22:566-569.
45. Mosenson JA, Zloza A, Klarquist J, Barfuss AJ, Guevara-Patino JA, Poole IC. 2012. HSP70i is a critical component of the immune response leading to vitiligo. Pigment Cell Melanoma Res. 25:88-98.
46. Muscat JE, Richie JP Jr, Thompson S, Wynder EL. 1996. Gender differences in smoking and risk for oral cancer. Cancer Res. 56:5192-5197.
47. Nair RP, Duffin KC, Helms C, Ding J, Stuart PE, Goldgar D, Gudjonsson JE, Li Y, Tejasvi T, Feng BJ, et al. 2009. Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat Genet. 41:199-204.
48. Ober C, Loisel DA, Gilad Y. 2008. Sex-specific genetic architecture of human disease. Nat Rev Genet. 9:911-922.
49. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. 2006. Principal components analysis corrects for stratification in genomewide association studies. Nat Genet. 38:904-909.
50. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, De Bakker PI, Daly MJ, et al. 2007. PLINK: a tool set for wholegenome association and population-based linkage analyses. Am J Hum Genet. 81:559-575.
51. Qi L, Cornelis MC, Kraft P, Stanya KJ, Linda Kao WH, Pankow JS, Dupuis J, Florez JC, Fox CS, Pare G, et al. 2010. Genetic variants at 2q24 are associated with susceptibility to type 2 diabetes. Hum Mol Genet. 19:2706-2715.
52. Stouffer SA. 1949. The American soldier. Princeton (NJ): Princeton University Press
53. The Wellcome Trust Case Control Consortium. 2007. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature. 447:661-678.
54. Thornton T, Zhang Q, Cai X, Ober C, McPeek MS. 2012. XM: association testing on the X-chromosome in case-control samples with related individuals. Genet Epidemiol. 36:438-450.
55. Tryka KA, Hao L, Sturcke A, Jin Y, Wang ZY, Ziyabari L, Lee M, Popova N, Sharopova N, Kimura M, et al. 2014. NCBI's database of genotypes and phenotypes: dbGaP. Nucleic Acids Res. 42(Database issue):D975-D979.
56. Tukiainen T, Pirinen M, Sarin AP, Ladenvall C, Kettunen J, Lehtimaki T, Lokki ML, Perola M, Sinisalo J, Vlachopoulou E, et al. 2014. Chromosome X-wide association study identifies Loci for fasting insulin and height and evidence for incomplete dosage compensation. PLoS Genet. 10:e1004127.
57. UK IBD Genetics Consortium, Barrett JC, Lee JC, Lees CW, Prescott NJ, Anderson CA, Phillips A, Wesley E, Parnell K, et al. 2009. Genome-wide association study of ulcerative colitis identifies three new susceptibility loci, including the HNF4A region. Nat Genet. 41:1330-1334.
58. Voskuhl R. 2011. Sex differences in autoimmune diseases. Biol Sex Differ. 2:1.
59. Welter D, Macarthur J, Morales J, Burdett T, Hall P, Junkins H, Klemm A, Flicek P, Manolio T, Hindorff L, et al. 2014. The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic Acids Res. 42(Database issue):D1001-D1006.
60. Willer CJ, Li Y, Abecasis GR. 2010. METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics. 26:2190-2191.
61. Williams OD. 1989. The Atherosclerosis Risk in Communities (Aric) Study-design and objectives. Am J Epidemiol. 129:687-702.
62. Wilson MA, Makova KD. 2009. Genomic analyses of sex chromosome evolution. Annu Rev Genomics Hum Genet. 10:333-354.
63. Wise AL, Gyi L, Manolio TA. 2013. eXclusion: toward integrating the X chromosome in genome-wide association analyses. Am J Hum Genet. 92:643-647.
64. Zaitlen N, Pasaniuc B, Patterson N, Pollack S, Voight B, Groop L, Altshuler D, Henderson BE, Kolonel LN, Le Marchand L, et al. 2012. Analysis of case-control association studies with known risk variants. Bioinformatics. 28:1729-1737.
65. Zaykin DV, Zhivotovsky LA, Westfall PH, Weir BS. 2002. Truncated product method for combining P-values. Genet Epidemiol. 22:170-185.
66. Zheng G, Joo J, Zhang C, Geller NL. 2007. Testing association for markers on the X chromosome. Genet Epidemiol. 31:834-843.