Differential methylation between ethnic sub-groups reflects the effect of genetic ancestry and environmental exposures

eLife

Volumn 6, Issue , 2017, Pages

  Galanter, Joshua M ^a,b   Gignoux, Christopher R ^c   Oh, Sam S ^a,b   Torgerson, Dara ^b   Pino Yanes, Maria ^d,e   Thakur, Neeta ^a   Eng, Celeste ^a   Hu, Donglei ^a   Huntsman, Scott ^a   Farber, Harold J ^f   Avila, Pedro C ^g   Brigino Buenaventura, Emerita ^h   Lenoir, Michael A ⁱ   Meade, Kelly ^j   Serebrisky, Denise ^k   Rodríguez Cintrón, William ^l   Kumar, Rajesh ^g   Rodríguez Santana, Jose R ^m   Seibold, Max A ⁿ   Borrell, Luisa N ^o   Burchard, Esteban G ^a,b   Zaitlen, Noah ^a   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY   (United States)

^d HOSPITAL UNIVERSITARIO NUESTRA SEÑORA DE CANDELARIA   (Spain)

^e INSTITUTO DE SALUD CARLOS III   (Spain)

^f BAYLOR COLLEGE OF MEDICINE   (United States)

^g NORTHWESTERN UNIVERSITY   (United States)

^h KAISER PERMANENTE   (United States)

ⁱ Bay Area Pediatrics   (United States)

^j CHILDREN S HOSPITAL OAKLAND   (United States)

^k JACOBI MEDICAL CENTER   (United States)

^l Veterans Caribbean Health Care System   (United States)

^m Centro de Neumología Pediátrica   (United States)

ⁿ DEPARTMENT OF MEDICINE   (United States)

^o CITY UNIVERSITY OF NEW YORK   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; DNA STRUCTURE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; ETHNIC GROUP; ETHNICITY; FEMALE; GENOTYPE; HISPANIC; HUMAN; MAJOR CLINICAL STUDY; MATERNAL SMOKING; METHYLATION; PREGNANCY; DNA METHYLATION; GENETIC EPIGENESIS;

DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; ETHNIC GROUPS; HISPANIC AMERICANS; HUMANS;

EID: 85009516978     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.20532     Document Type: Article

References (60)

1. Alexander DH, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research 19:1655–1664. doi: 10.1101/gr.094052.109, PMID: 19648217
2. Baran Y, Pasaniuc B, Sankararaman S, Torgerson DG, Gignoux C, Eng C, Rodriguez-Cintron W, Chapela R, Ford JG, Avila PC, Rodriguez-Santana J, Burchard EG, Halperin E. 2012. Fast and accurate inference of local ancestry in Latino populations. Bioinformatics 28:1359–1367. doi: 10.1093/bioinformatics/bts144, PMID: 22495753
3. Barfield RT, Almli LM, Kilaru V, Smith AK, Mercer KB, Duncan R, Klengel T, Mehta D, Binder EB, Epstein MP, Ressler KJ, Conneely KN. 2014. Accounting for population stratification in DNA methylation studies. Genetic Epidemiology 38:231–241. doi: 10.1002/gepi.21789, PMID: 24478250
4. Barr RG, Avilés-Santa L, Davis SM, Aldrich TK, Gonzalez F, Henderson AG, Kaplan RC, LaVange L, Liu K, Loredo JS, Mendes ES, Ni A, Ries A, Salathe M, Smith LJ. 2016. Pulmonary disease and age at immigration among hispanics. results from the hispanic community health study study of latinos. American Journal of Respiratory and Critical Care Medicine 193:386–395. doi: 10.1164/rccm.201506-1211OC, PMID: 26451874
5. Bell CG, Finer S, Lindgren CM, Wilson GA, Rakyan VK, Teschendorff AE, Akan P, Stupka E, Down TA, Prokopenko I, Morison IM, Mill J, Pidsley R, Deloukas P, Frayling TM, Hattersley AT, McCarthy MI, Beck S, Hitman GA, International Type 2 Diabetes 1q Consortium. 2010. Integrated genetic and epigenetic analysis identifies haplotype-specific methylation in the FTO type 2 diabetes and obesity susceptibility locus. PloS One 5:e14040. doi: 10.1371/journal.pone.0014040, PMID: 21124985
6. Bell JT, Pai AA, Pickrell JK, Gaffney DJ, Pique-Regi R, Degner JF, Gilad Y, Pritchard JK. 2011. DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biology 12:R10. doi: 10.1186/gb-2011-12-1-r10, PMID: 21251332
7. Borghol N, Suderman M, McArdle W, Racine A, Hallett M, Pembrey M, Hertzman C, Power C, Szyf M. 2012. Associations with early-life socio-economic position in adult DNA methylation. International Journal of Epidemiology 41:62–74. doi: 10.1093/ije/dyr147, PMID: 22422449
8. Borrell LN. 2005. Racial identity among Hispanics: implications for health and well-being. American Journal of Public Health 95:379–381. doi: 10.2105/AJPH.2004.058172, PMID: 15727961
9. Bryc K, Velez C, Karafet T, Moreno-Estrada A, Reynolds A, Auton A, Hammer M, Bustamante CD, Ostrer H. 2010. Colloquium paper: genome-wide patterns of population structure and admixture among Hispanic/Latino populations. PNAS 107 Suppl 2:8954–8961. doi: 10.1073/pnas.0914618107, PMID: 20445096
10. Burchard EG, Ziv E, Coyle N, Gomez SL, Tang H, Karter AJ, Mountain JL, Pérez-Stable EJ, Sheppard D, Risch N. 2003. The importance of race and ethnic background in biomedical research and clinical practice. New England Journal of Medicine 348:1170–1175. doi: 10.1056/NEJMsb025007, PMID: 12646676
11. Chambers JC, Loh M, Lehne B, Drong A, Kriebel J, Motta V, Wahl S, Elliott HR, Rota F, Scott WR, Zhang W, Tan ST, Campanella G, Chadeau-Hyam M, Yengo L, Richmond RC, Adamowicz-Brice M, Afzal U, Bozaoglu K, Mok ZY, et al. 2015. Epigenome-wide association of DNA methylation markers in peripheral blood from Indian Asians and Europeans with incident type 2 diabetes: a nested case-control study. The Lancet Diabetes & Endocrinology 3:526–534. doi: 10.1016/S2213-8587(15)00127-8, PMID: 26095709
12. Chen W, Boutaoui N, Brehm JM, Han YY, Schmitz C, Cressley A, Acosta-Pérez E, Alvarez M, Colón-Semidey A, Baccarelli AA, Weeks DE, Kolls JK, Canino G, Celedón JC. 2013. ADCYAP1R1 and asthma in Puerto Rican children. American Journal of Respiratory and Critical Care Medicine 187:584–588. doi: 10.1164/rccm.201210-1789OC, PMID: 23328528
13. Cooper RS, Kaufman JS, Ward R. 2003. Race and genomics. New England Journal of Medicine 348:1166–1170. doi: 10.1056/NEJMsb022863, PMID: 12646675
14. Du P, Zhang X, Huang CC, Jafari N, Kibbe WA, Hou L, Lin SM. 2010. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics 11:587. doi: 10.1186/1471-2105-11-587, PMID: 21118553
15. Evans GW, Kantrowitz E. 2002. Socioeconomic status and health: the potential role of environmental risk exposure. Annual Review of Public Health 23:303–331. doi: 10.1146/annurev.publhealth.23.112001.112349, PMID: 11910065
16. Feil R, Fraga MF. 2012. Epigenetics and the environment: emerging patterns and implications. Nature Reviews Genetics 13:97–109. doi: 10.1038/nrg3142, PMID: 22215131
17. Florez JC, Price AL, Campbell D, Riba L, Parra MV, Yu F, Duque C, Saxena R, Gallego N, Tello-Ruiz M, Franco L, Rodríguez-Torres M, Villegas A, Bedoya G, Aguilar-Salinas CA, Tusié-Luna MT, Ruiz-Linares A. 2011. Strong Association of Socioeconomic Status and Genetic Ancestry in Latinos: Implications for Admixture Studies of Type 2 Diabetes. Racial Identities, Genetic Ancestry, and Health in South America:137–153. doi: 10.1057/9781137001702_7
18. Galanter JM, Fernandez-Lopez JC, Gignoux CR, Barnholtz-Sloan J, Fernandez-Rozadilla C, Via M, Hidalgo-Miranda A, Contreras AV, Figueroa LU, Raska P, Jimenez-Sanchez G, Zolezzi IS, Torres M, Ponte CR, Ruiz Y, Salas A, Nguyen E, Eng C, Borjas L, Zabala W, et al. 2012. Development of a panel of genome-wide ancestry informative markers to study admixture throughout the Americas. PLoS Genetics 8:e1002554. doi: 10.1371/journal.pgen.1002554, PMID: 22412386
19. Galanter JM, Gignoux CR, Torgerson DG, Roth LA, Eng C, Oh SS, Nguyen EA, Drake KA, Huntsman S, Hu D, Sen S, Davis A, Farber HJ, Avila PC, Brigino-Buenaventura E, LeNoir MA, Meade K, Serebrisky D, Borrell LN, Rodríguez-Cintrón W, et al. 2014. Genome-wide association study and admixture mapping identify different asthma-associated loci in Latinos: the Genes-environments & Admixture in Latino Americans study. Journal of Allergy and Clinical Immunology 134:295–305. doi: 10.1016/j.jaci.2013.08.055, PMID: 24406073
20. González Burchard E, Borrell LN, Choudhry S, Naqvi M, Tsai HJ, Rodriguez-Santana JR, Chapela R, Rogers SD, Mei R, Rodriguez-Cintron W, Arena JF, Kittles R, Perez-Stable EJ, Ziv E, Risch N. 2005. Latino populations: a unique opportunity for the study of race, genetics, and social environment in epidemiological research. American Journal of Public Health 95:2161–2168. doi: 10.2105/AJPH.2005.068668, PMID: 16257940
21. Grafodatskaya D, Choufani S, Ferreira JC, Butcher DT, Lou Y, Zhao C, Scherer SW, Weksberg R. 2010. EBV transformation and cell culturing destabilizes DNA methylation in human lymphoblastoid cell lines. Genomics 95:73–83. doi: 10.1016/j.ygeno.2009.12.001, PMID: 20005943
22. Hankinson JL, Odencrantz JR, Fedan KB. 1999. Spirometric reference values from a sample of the general U.S. population. American Journal of Respiratory and Critical Care Medicine 159:179–187. doi: 10.1164/ajrccm.159.1.9712108, PMID: 9872837
23. Hernandez RD, Kelley JL, Elyashiv E, Melton SC, Auton A, McVean G, Sella G, Przeworski M, 1000 Genomes Project. 2011. Classic selective sweeps were rare in recent human evolution. Science 331:920–924. doi: 10.1126/science.1198878, PMID: 21330547
24. Ho SM, Johnson A, Tarapore P, Janakiram V, Zhang X, Leung YK. 2012. Environmental epigenetics and its implication on disease risk and health outcomes. ILAR Journal 53:289–305. doi: 10.1093/ilar.53.3-4.289, PMID: 23744968
25. Hoffmann TJ, Zhan Y, Kvale MN, Hesselson SE, Gollub J, Iribarren C, Lu Y, Mei G, Purdy MM, Quesenberry C, Rowell S, Shapero MH, Smethurst D, Somkin CP, Van den Eeden SK, Walter L, Webster T, Whitmer RA, Finn A, Schaefer C, et al. 2011. Design and coverage of high throughput genotyping arrays optimized for individuals of East Asian, African American, and Latino race/ethnicity using imputation and a novel hybrid SNP selection algorithm. Genomics 98:422–430. doi: 10.1016/j.ygeno.2011.08.007, PMID: 21903159
26. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, Wiencke JK, Kelsey KT. 2012. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 13:86. doi: 10.1186/1471-2105-13-86, PMID: 22568884
27. Jiang R, Jones MJ, Sava F, Kobor MS, Carlsten C. 2014. Short-term diesel exhaust inhalation in a controlled human crossover study is associated with changes in DNA methylation of circulating mononuclear cells in asthmatics. Particle and Fibre Toxicology 11:71. doi: 10.1186/s12989-014-0071-3, PMID: 25487561
28. Joubert BR, Felix JF, Yousefi P, Bakulski KM, Just AC, Breton C, Reese SE, Markunas CA, Richmond RC, Xu CJ, Küpers LK, Oh SS, Hoyo C, Gruzieva O, Söderhall C, Salas LA, Baïz N, Zhang H, Lepeule J, Ruiz C, et al. 2016. DNA Methylation in Newborns and Maternal Smoking in Pregnancy: Genome-wide Consortium Meta-analysis. The American Journal of Human Genetics 98:680–696. doi: 10.1016/j.ajhg.2016.02.019, PMID: 27040690
29. Joubert BR, Håberg SE, Nilsen RM, Wang X, Vollset SE, Murphy SK, Huang Z, Hoyo C, Midttun Ø, Cupul-Uicab LA, Ueland PM, Wu MC, Nystad W, Bell DA, Peddada SD, London SJ. 2012. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environmental Health Perspectives 120:1425–1431. doi: 10.1289/ehp.1205412, PMID: 22851337
30. Kato N, Loh M, Takeuchi F, Verweij N, Wang X, Zhang W, Kelly TN, Saleheen D, Lehne B, Mateo Leach I, Drong AW, Abbott J, Wahl S, Tan ST, Scott WR, Campanella G, Chadeau-Hyam M, Afzal U, Ahluwalia TS, Bonder MJ, et al. 2015. Trans-ancestry genome-wide association study identifies 12 genetic loci influencing blood pressure and implicates a role for DNA methylation. Nature Genetics 47:1282–1293. doi: 10.1038/ng.3405, PMID: 26390057
31. Kulis M, Esteller M. 2010. DNA methylation and cancer. Advances in Genetics 70:27–56. doi: 10.1016/B978-0-12-380866-0.60002-2, PMID: 20920744
32. Kumar R, Seibold MA, Aldrich MC, Williams LK, Reiner AP, Colangelo L, Galanter J, Gignoux C, Hu D, Sen S, Choudhry S, Peterson EL, Rodriguez-Santana J, Rodriguez-Cintron W, Nalls MA, Leak TS, O’Meara E, Meibohm B, Kritchevsky SB, Li R, et al. 2010. Genetic ancestry in lung-function predictions. New England Journal of Medicine 363:321–330. doi: 10.1056/NEJMoa0907897, PMID: 20647190
33. Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE, Kobor MS. 2012. Factors underlying variable DNA methylation in a human community cohort. PNAS 109 Suppl 2:17253–17260. doi: 10.1073/pnas.1121249109, PMID: 23045638
34. Lardenoije R, Iatrou A, Kenis G, Kompotis K, Steinbusch HW, Mastroeni D, Coleman P, Lemere CA, Hof PR, van den Hove DL, Rutten BP. 2015. The epigenetics of aging and neurodegeneration. Progress in Neurobiology 131:21–64. doi: 10.1016/j.pneurobio.2015.05.002, PMID: 26072273
35. Leng S, Liu Y, Thomas CL, Gauderman WJ, Picchi MA, Bruse SE, Zhang X, Flores KG, Van Den Berg D, Stidley CA, Gilliland FD, Belinsky SA. 2013. Native American ancestry affects the risk for gene methylation in the lungs of Hispanic smokers from New Mexico. American Journal of Respiratory and Critical Care Medicine 188:1110–1116. doi: 10.1164/rccm.201305-0925OC, PMID: 24032348
36. Liu Y, Aryee MJ, Padyukov L, Fallin MD, Hesselberg E, Runarsson A, Reinius L, Acevedo N, Taub M, Ronninger M, Shchetynsky K, Scheynius A, Kere J, Alfredsson L, Klareskog L, Ekström TJ, Feinberg AP. 2013. Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis. Nature Biotechnology 31:142–147. doi: 10.1038/nbt.2487, PMID: 23334450
37. Michels KB, Binder AM, Dedeurwaerder S, Epstein CB, Greally JM, Gut I, Houseman EA, Izzi B, Kelsey KT, Meissner A, Milosavljevic A, Siegmund KD, Bock C, Irizarry RA. 2013. Recommendations for the design and analysis of epigenome-wide association studies. Nature Methods 10:949–955. doi: 10.1038/nmeth.2632, PMID: 24076989
38. Moreno-Estrada A, Gignoux CR, Fernández-López JC, Zakharia F, Sikora M, Contreras AV, Acuña-Alonzo V, Sandoval K, Eng C, Romero-Hidalgo S, Ortiz-Tello P, Robles V, Kenny EE, Nuño-Arana I, Barquera-Lozano R, Macín-Pérez G, Granados-Arriola J, Huntsman S, Galanter JM, Via M, et al. 2014. Human genetics. The genetics of Mexico recapitulates Native American substructure and affects biomedical traits. Science 344:1280–1285. doi: 10.1126/science.1251688, PMID: 24926019
39. Nalls MA, Wilson JG, Patterson NJ, Tandon A, Zmuda JM, Huntsman S, Garcia M, Hu D, Li R, Beamer BA, Patel KV, Akylbekova EL, Files JC, Hardy CL, Buxbaum SG, Taylor HA, Reich D, Harris TB, Ziv E. 2008. Admixture mapping of white cell count: genetic locus responsible for lower white blood cell count in the Health ABC and Jackson Heart studies. The American Journal of Human Genetics 82:81–87. doi: 10.1016/j.ajhg.2007.09.003, PMID: 18179887
40. Nguyen AB, Moser R, Chou WY. 2014. Race and health profiles in the United States: an examination of the social gradient through the 2009 CHIS adult survey. Public Health 128:1076–1086. doi: 10.1016/j.puhe.2014.10.003, PMID: 25457801
41. Nishimura KK, Galanter JM, Roth LA, Oh SS, Thakur N, Nguyen EA, Thyne S, Farber HJ, Serebrisky D, Kumar R, Brigino-Buenaventura E, Davis A, LeNoir MA, Meade K, Rodriguez-Cintron W, Avila PC, Borrell LN, Bibbins-Domingo K, Rodriguez-Santana JR, Sen Ś, et al. 2013. Early-life air pollution and asthma risk in minority children. The GALA II and SAGE II studies. American Journal of Respiratory and Critical Care Medicine 188: 309–318. doi: 10.1164/rccm.201302-0264OC, PMID: 23750510
42. Oh SS, Tcheurekdjian H, Roth LA, Nguyen EA, Sen S, Galanter JM, Davis A, Farber HJ, Gilliland FD, Kumar R, Avila PC, Brigino-Buenaventura E, Chapela R, Ford JG, LeNoir MA, Lurmann F, Meade K, Serebrisky D, Thyne S, Rodriguez-Cintron W, et al. 2012. Effect of secondhand smoke on asthma control among black and Latino children. Journal of Allergy and Clinical Immunology 129:1478–1483. doi: 10.1016/j.jaci.2012.03.017, PMID: 22552109
43. Patterson N, Price AL, Reich D. 2006. Population structure and eigenanalysis. PLoS Genetics 2:e190. doi: 10.1371/journal.pgen.0020190, PMID: 17194218
44. Phimister EG. 2003. Medicine and the racial divide. New England Journal of Medicine 348:1081–1082. doi: 10.1056/NEJMp030028, PMID: 12646663
45. Quanjer PH, Stanojevic S, Cole TJ, Baur X, Hall GL, Culver BH, Enright PL, Hankinson JL, Ip MS, Zheng J, Stocks J, ERS Global Lung Function Initiative. 2012. Multi-ethnic reference values for spirometry for the 3-95-yr age range: the global lung function 2012 equations. European Respiratory Journal 40:1324–1343. doi: 10.1183/09031936.00080312, PMID: 22743675
46. R Core Team. 2016. R: a language and environment for statistical computing. http://www.R-project.org/.
47. Rahmani E, Zaitlen N, Baran Y, Eng C, Hu D, Galanter J, Oh S, Burchard EG, Eskin E, Zou J, Halperin E. 2016. Sparse PCA corrects for cell type heterogeneity in epigenome-wide association studies. Nature Methods 13: 443–445. doi: 10.1038/nmeth.3809, PMID: 27018579
48. Ressler KJ, Mercer KB, Bradley B, Jovanovic T, Mahan A, Kerley K, Norrholm SD, Kilaru V, Smith AK, Myers AJ, Ramirez M, Engel A, Hammack SE, Toufexis D, Braas KM, Binder EB, May V. 2011. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 470:492–497. doi: 10.1038/nature09856, PMID: 21350482
49. Risch N, Burchard E, Ziv E, Tang H. 2002. Categorization of humans in biomedical research: genes, race and disease. Genome Biology 3:comment2007. PMID: 12184798
50. Rosenberg NA, Huang L, Jewett EM, Szpiech ZA, Jankovic I, Boehnke M. 2010. Genome-wide association studies in diverse populations. Nature Reviews Genetics 11:356–366. doi: 10.1038/nrg2760, PMID: 20395969
51. Smith ZD, Meissner A. 2013. DNA methylation: roles in mammalian development. Nature Reviews Genetics 14: 204–220. doi: 10.1038/nrg3354, PMID: 23400093
52. Tang H, Choudhry S, Mei R, Morgan M, Rodriguez-Cintron W, Burchard EG, Risch NJ. 2007. Recent genetic selection in the ancestral admixture of Puerto Ricans. The American Journal of Human Genetics 81:626–633. doi: 10.1086/520769, PMID: 17701908
53. Thakur N, Oh SS, Nguyen EA, Martin M, Roth LA, Galanter J, Gignoux CR, Eng C, Davis A, Meade K, LeNoir MA, Avila PC, Farber HJ, Serebrisky D, Brigino-Buenaventura E, Rodriguez-Cintron W, Kumar R, Williams LK, Bibbins-Domingo K, Thyne S, et al. 2013. Socioeconomic status and childhood asthma in urban minority youths. The GALA II and SAGE II studies. American Journal of Respiratory and Critical Care Medicine 188:1202–1209. doi: 10.1164/rccm.201306-1016OC, PMID: 24050698
54. Tingley D, Yamamoto T, Hirose K, Keele L, Imai K. 2014. mediation: R package for causal mediation analysis. Journal of Statistical Software 59. doi: 10.18637/jss.v059.i05
55. Udali S, Guarini P, Moruzzi S, Choi SW, Friso S. 2013. Cardiovascular epigenetics: from DNA methylation to microRNAs. Molecular Aspects of Medicine 34:883–901. doi: 10.1016/j.mam.2012.08.001, PMID: 22981780
56. Udler MS, Nadkarni GN, Belbin G, Lotay V, Wyatt C, Gottesman O, Bottinger EP, Kenny EE, Peter I. 2015. Effect of Genetic African Ancestry on eGFR and Kidney Disease. Journal of the American Society of Nephrology 26: 1682–1692. doi: 10.1681/ASN.2014050474, PMID: 25349204
57. van der Knaap LJ, Riese H, Hudziak JJ, Verbiest MM, Verhulst FC, Oldehinkel AJ, van Oort FV. 2014. Glucocorticoid receptor gene (NR3C1) methylation following stressful events between birth and adolescence. The TRAILS study. Translational Psychiatry 4:e381. doi: 10.1038/tp.2014.22, PMID: 24713862
58. Vidal AC, Benjamin Neelon SE, Liu Y, Tuli AM, Fuemmeler BF, Hoyo C, Murtha AP, Huang Z, Schildkraut J, Overcash F, Kurtzberg J, Jirtle RL, Iversen ES, Murphy SK. 2014. Maternal stress, preterm birth, and DNA methylation at imprint regulatory sequences in humans. Genetics & Epigenetics 6:37–44. doi: 10.4137/GEG.S18067, PMID: 25512713
59. Yudell M, Roberts D, DeSalle R, Tishkoff S. 2016. Science and society. Taking race out of human genetics. Science 351:564–565. doi: 10.1126/science.aac4951, PMID: 26912690
60. Ziv E, John EM, Choudhry S, Kho J, Lorizio W, Perez-Stable EJ, Burchard EG. 2006. Genetic ancestry and risk factors for breast cancer among Latinas in the San Francisco Bay Area. Cancer Epidemiology Biomarkers & Prevention 15:1878–1885. doi: 10.1158/1055-9965.EPI-06-0092, PMID: 17035394