Skip to main content

Advertisement

SpringerLink
Log in

Genetic variants in microRNAs and breast cancer risk in African American and European American women

  • Epidemiology
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are an integral part of the post-transcriptional machinery of gene expression and have been implicated in the carcinogenic cascade. Single nucleotide polymorphisms (SNPs) in miRNAs and risk of breast cancer have been evaluated in populations of European or Asian ancestry, but not among women of African ancestry. Here we examined 145 SNPs in six miRNA processing genes and in 78 miRNAs which target genes known to be important in breast cancer among 906 African American (AA) and 653 European American (EA) cases and controls enrolled in the Women’s Circle of Health Study. Allele frequencies of most SNPs (87 %) differed significantly by race. We found a number of SNPs in miRNAs and processing genes in association with breast cancer overall or stratified by estrogen receptor (ER) status. Several associations were significantly different by race, with none of the associations being significant in both races. Using a polygenic risk score to combine the effects of multiple SNPs, we found significant associations with the score in each subgroup analysis. For ER-positive cancer, each unit increment of the risk score was associated with a 51 % increased risk in AAs (OR = 1.51, 95 % CI = 1.30–1.74, p = 3.3 × 10−8) and a 73 % increased risk in EAs (OR = 1.73, 95 % CI = 1.45–2.06, p = 1.4 × 10−9). These data show, for the first time, that miRNA-related genetic variations may underlie the etiology of breast cancer in both populations of African and European ancestries. Future studies are needed to validate our findings and to explore the underlying mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Siegel R, Ward E, Brawley O, Jemal A (2011) Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 61(4):212–236. doi:10.3322/caac.20121

    Article  PubMed  Google Scholar 

  2. Gerend MA, Pai M (2008) Social determinants of Black-White disparities in breast cancer mortality: a review. Cancer Epidemiol Biomarkers Prev 17(11):2913–2923. doi:10.1158/1055-9965.EPI-07-0633

    Article  PubMed  Google Scholar 

  3. Ademuyiwa FO, Edge SB, Erwin DO, Orom H, Ambrosone CB, Underwood W III (2011) Breast cancer racial disparities: unanswered questions. Cancer Res 71(3):640–644. doi:10.1158/0008-5472.CAN-10-3021

    Article  PubMed  CAS  Google Scholar 

  4. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielsen TO, Moorman PG, Earp HS, Millikan RC (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295(21):2492–2502. doi:10.1001/jama.295.21.2492

    Article  PubMed  CAS  Google Scholar 

  5. Cunningham JE, Butler WM (2004) Racial disparities in female breast cancer in South Carolina: clinical evidence for a biological basis. Breast Cancer Res Treat 88(2):161–176. doi:10.1007/s10549-004-0592-9

    Article  PubMed  Google Scholar 

  6. Jemal A, Siegel R, Xu J (2010) Ward E Cancer statistics. CA Cancer J Clin 60(5):277–300. doi:10.3322/caac.20073

    Article  PubMed  Google Scholar 

  7. Lund MJ, Trivers KF, Porter PL, Coates RJ, Leyland-Jones B, Brawley OW, Flagg EW, O’Regan RM, Gabram SG, Eley JW (2009) Race and triple negative threats to breast cancer survival: a population-based study in Atlanta. GA. Breast Cancer Res Treat 113(2):357–370. doi:10.1007/s10549-008-9926-3

    Article  Google Scholar 

  8. Stead LA, Lash TL, Sobieraj JE, Chi DD, Westrup JL, Charlot M, Blanchard RA, Lee JC, King TC, Rosenberg CL (2009) Triple-negative breast cancers are increased in black women regardless of age or body mass index. Breast Cancer Res 11(2):R18. doi:10.1186/bcr2242

    Article  PubMed  Google Scholar 

  9. Menashe I, Anderson WF, Jatoi I, Rosenberg PS (2009) Underlying causes of the black-white racial disparity in breast cancer mortality: a population-based analysis. J Natl Cancer Inst 101(14):993–1000. doi:10.1093/jnci/djp176

    Article  PubMed  Google Scholar 

  10. Cheng AM, Byrom MW, Shelton J, Ford LP (2005) Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 33(4):1290–1297. doi:10.1093/nar/gki200

    Article  PubMed  CAS  Google Scholar 

  11. Berezikov E (2011) Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 12(12):846–860. doi:10.1038/nrg3079

    Article  PubMed  CAS  Google Scholar 

  12. Negrini M, Nicoloso MS, Calin GA (2009) MicroRNAs and cancer—new paradigms in molecular oncology. Curr Opin Cell Biol 21(3):470–479. doi:10.1016/j.ceb.2009.03.002

    Article  PubMed  CAS  Google Scholar 

  13. Blenkiron C, Goldstein LD, Thorne NP, Spiteri I, Chin SF, Dunning MJ, Barbosa-Morais NL, Teschendorff AE, Green AR, Ellis IO, Tavare S, Caldas C, Miska EA (2007) MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol 8(10):R214. doi:10.1186/gb-2007-8-10-r214

    Article  PubMed  Google Scholar 

  14. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Menard S, Palazzo JP, Rosenberg A, Musiani P, Volinia S, Nenci I, Calin GA, Querzoli P, Negrini M, Croce CM (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65(16):7065–7070. doi:10.1158/0008-5472.CAN-05-1783

    Article  PubMed  CAS  Google Scholar 

  15. Sempere LF, Christensen M, Silahtaroglu A, Bak M, Heath CV, Schwartz G, Wells W, Kauppinen S, Cole CN (2007) Altered MicroRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res 67(24):11612–11620. doi:10.1158/0008-5472.CAN-07-5019

    Article  PubMed  CAS  Google Scholar 

  16. Son JW, Kim YJ, Cho HM, Lee SY, Jang JS, Choi JE, Lee JU, Kang MG, Lee YM, Kwon SJ, Choi E, Na MJ, Park JY (2009) MicroRNA expression profiles in Korean non-small cell lung cancer. Tuberc Respir Dis 67(5):413

    Article  Google Scholar 

  17. Wang T, Zhang X, Obijuru L, Laser J, Aris V, Lee P, Mittal K, Soteropoulos P, Wei JJ (2007) A micro-RNA signature associated with race, tumor size, and target gene activity in human uterine leiomyomas. Genes Chromosomes Cancer 46(4):336–347. doi:10.1002/gcc.20415

    Article  PubMed  CAS  Google Scholar 

  18. Hu Z, Liang J, Wang Z, Tian T, Zhou X, Chen J, Miao R, Wang Y, Wang X, Shen H (2009) Common genetic variants in pre-microRNAs were associated with increased risk of breast cancer in Chinese women. Hum Mutat 30(1):79–84. doi:10.1002/humu.20837

    Article  PubMed  CAS  Google Scholar 

  19. Shen J, Ambrosone CB, DiCioccio RA, Odunsi K, Lele SB, Zhao H (2008) A functional polymorphism in the miR-146a gene and age of familial breast/ovarian cancer diagnosis. Carcinogenesis 29(10):1963–1966. doi:10.1093/carcin/bgn172

    Article  PubMed  CAS  Google Scholar 

  20. Shen J, Ambrosone CB, Zhao H (2009) Novel genetic variants in microRNA genes and familial breast cancer. Int J Cancer 124(5):1178–1182. doi:10.1002/ijc.24008

    Article  PubMed  CAS  Google Scholar 

  21. Wu M, Jolicoeur N, Li Z, Zhang L, Fortin Y, L’Abbe D, Yu Z, Shen SH (2008) Genetic variations of microRNAs in human cancer and their effects on the expression of miRNAs. Carcinogenesis 29(9):1710–1716. doi:10.1093/carcin/bgn073

    Article  PubMed  CAS  Google Scholar 

  22. Ambrosone CB, Ciupak GL, Bandera EV, Jandorf L, Bovbjerg DH, Zirpoli G, Pawlish K, Godbold J, Furberg H, Fatone A, Valdimarsdottir H, Yao S, Li Y, Hwang H, Davis W, Roberts M, Sucheston L, Demissie K, Amend KL, Tartter P, Reilly J, Pace BW, Rohan T, Sparano J, Raptis G, Castaldi M, Estabrook A, Feldman S, Weltz C, Kemeny M (2009) Conducting molecular epidemiological research in the age of HIPAA: a multi-institutional case–control study of breast cancer in African-American and European-American women. J Oncol 2009:871250. doi:10.1155/2009/871250

    Article  PubMed  Google Scholar 

  23. Bandera EV, Chandran U, Zirpoli G, McCann SE, Ciupak G, Ambrosone CB (2013) Rethinking sources of representative controls for the conduct of case–control studies in minority populations. BMC Med Res Methodol 13:71. doi:10.1186/1471-2288-13-71

    Article  PubMed  Google Scholar 

  24. Xu Z, Kaplan NL, Taylor JA (2007) TAGster: efficient selection of LD tag SNPs in single or multiple populations. Bioinformatics 23(23):3254–3255

    Article  PubMed  CAS  Google Scholar 

  25. Tsai HJ, Choudhry S, Naqvi M, Rodriguez-Cintron W, Burchard EG, Ziv E (2005) Comparison of three methods to estimate genetic ancestry and control for stratification in genetic association studies among admixed populations. Hum Genet 118(3–4):424–433. doi:10.1007/s00439-005-0067-z

    Article  PubMed  Google Scholar 

  26. Speliotes EK, Willer CJ, Berndt SI, Monda KL, Thorleifsson G, Jackson AU, Lango Allen H, Lindgren CM, Luan J, Magi R, Randall JC, Vedantam S, Winkler TW, Qi L, Workalemahu T, Heid IM, Steinthorsdottir V, Stringham HM, Weedon MN, Wheeler E, Wood AR, Ferreira T, Weyant RJ, Segre AV, Estrada K, Liang L, Nemesh J, Park JH, Gustafsson S, Kilpelainen TO, Yang J, Bouatia-Naji N, Esko T, Feitosa MF, Kutalik Z, Mangino M, Raychaudhuri S, Scherag A, Smith AV, Welch R, Zhao JH, Aben KK, Absher DM, Amin N, Dixon AL, Fisher E, Glazer NL, Goddard ME, Heard-Costa NL, Hoesel V, Hottenga JJ, Johansson A, Johnson T, Ketkar S, Lamina C, Li S, Moffatt MF, Myers RH, Narisu N, Perry JR, Peters MJ, Preuss M, Ripatti S, Rivadeneira F, Sandholt C, Scott LJ, Timpson NJ, Tyrer JP, van Wingerden S, Watanabe RM, White CC, Wiklund F, Barlassina C, Chasman DI, Cooper MN, Jansson JO, Lawrence RW, Pellikka N, Prokopenko I, Shi J, Thiering E, Alavere H, Alibrandi MT, Almgren P, Arnold AM, Aspelund T, Atwood LD, Balkau B, Balmforth AJ, Bennett AJ, Ben-Shlomo Y, Bergman RN, Bergmann S, Biebermann H, Blakemore AI, Boes T, Bonnycastle LL, Bornstein SR, Brown MJ, Buchanan TA, Busonero F, Campbell H, Cappuccio FP, Cavalcanti-Proenca C, Chen YD, Chen CM, Chines PS, Clarke R, Coin L, Connell J, Day IN, den Heijer M, Duan J, Ebrahim S, Elliott P, Elosua R, Eiriksdottir G, Erdos MR, Eriksson JG, Facheris MF, Felix SB, Fischer-Posovszky P, Folsom AR, Friedrich N, Freimer NB, Fu M, Gaget S, Gejman PV, Geus EJ, Gieger C, Gjesing AP, Goel A, Goyette P, Grallert H, Grassler J, Greenawalt DM, Groves CJ, Gudnason V, Guiducci C, Hartikainen AL, Hassanali N, Hall AS, Havulinna AS, Hayward C, Heath AC, Hengstenberg C, Hicks AA, Hinney A, Hofman A, Homuth G, Hui J, Igl W, Iribarren C, Isomaa B, Jacobs KB, Jarick I, Jewell E, John U, Jorgensen T, Jousilahti P, Jula A, Kaakinen M, Kajantie E, Kaplan LM, Kathiresan S, Kettunen J, Kinnunen L, Knowles JW, Kolcic I, Konig IR, Koskinen S, Kovacs P, Kuusisto J, Kraft P, Kvaloy K, Laitinen J, Lantieri O, Lanzani C, Launer LJ, Lecoeur C, Lehtimaki T, Lettre G, Liu J, Lokki ML, Lorentzon M, Luben RN, Ludwig B, Manunta P, Marek D, Marre M, Martin NG, McArdle WL, McCarthy A, McKnight B, Meitinger T, Melander O, Meyre D, Midthjell K, Montgomery GW, Morken MA, Morris AP, Mulic R, Ngwa JS, Nelis M, Neville MJ, Nyholt DR, O’Donnell CJ, O’Rahilly S, Ong KK, Oostra B, Pare G, Parker AN, Perola M, Pichler I, Pietilainen KH, Platou CG, Polasek O, Pouta A, Rafelt S, Raitakari O, Rayner NW, Ridderstrale M, Rief W, Ruokonen A, Robertson NR, Rzehak P, Salomaa V, Sanders AR, Sandhu MS, Sanna S, Saramies J, Savolainen MJ, Scherag S, Schipf S, Schreiber S, Schunkert H, Silander K, Sinisalo J, Siscovick DS, Smit JH, Soranzo N, Sovio U, Stephens J, Surakka I, Swift AJ, Tammesoo ML, Tardif JC, Teder-Laving M, Teslovich TM, Thompson JR, Thomson B, Tonjes A, Tuomi T, van Meurs JB, van Ommen GJ, Vatin V, Viikari J, Visvikis-Siest S, Vitart V, Vogel CI, Voight BF, Waite LL, Wallaschofski H, Walters GB, Widen E, Wiegand S, Wild SH, Willemsen G, Witte DR, Witteman JC, Xu J, Zhang Q, Zgaga L, Ziegler A, Zitting P, Beilby JP, Farooqi IS, Hebebrand J, Huikuri HV, James AL, Kahonen M, Levinson DF, Macciardi F, Nieminen MS, Ohlsson C, Palmer LJ, Ridker PM, Stumvoll M, Beckmann JS, Boeing H, Boerwinkle E, Boomsma DI, Caulfield MJ, Chanock SJ, Collins FS, Cupples LA, Smith GD, Erdmann J, Froguel P, Gronberg H, Gyllensten U, Hall P, Hansen T, Harris TB, Hattersley AT, Hayes RB, Heinrich J, Hu FB, Hveem K, Illig T, Jarvelin MR, Kaprio J, Karpe F, Khaw KT, Kiemeney LA, Krude H, Laakso M, Lawlor DA, Metspalu A, Munroe PB, Ouwehand WH, Pedersen O, Penninx BW, Peters A, Pramstaller PP, Quertermous T, Reinehr T, Rissanen A, Rudan I, Samani NJ, Schwarz PE, Shuldiner AR, Spector TD, Tuomilehto J, Uda M, Uitterlinden A, Valle TT, Wabitsch M, Waeber G, Wareham NJ, Watkins H, Wilson JF, Wright AF, Zillikens MC, Chatterjee N, McCarroll SA, Purcell S, Schadt EE, Visscher PM, Assimes TL, Borecki IB, Deloukas P, Fox CS, Groop LC, Haritunians T, Hunter DJ, Kaplan RC, Mohlke KL, O’Connell JR, Peltonen L, Schlessinger D, Strachan DP, van Duijn CM, Wichmann HE, Frayling TM, Thorsteinsdottir U, Abecasis GR, Barroso I, Boehnke M, Stefansson K, North KE, McCarthy MI, Hirschhorn JN, Ingelsson E, Loos RJ (2010) Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nat Genet 42(11):937–948. doi:10.1038/ng.686

    Article  PubMed  CAS  Google Scholar 

  27. Gao LB, Bai P, Pan XM, Jia J, Li LJ, Liang WB, Tang M, Zhang LS, Wei YG, Zhang L (2011) The association between two polymorphisms in pre-miRNAs and breast cancer risk: a meta-analysis. Breast Cancer Res Treat 125(2):571–574. doi:10.1007/s10549-010-0993-x

    Article  PubMed  Google Scholar 

  28. Hoffman AE, Zheng T, Yi C, Leaderer D, Weidhaas J, Slack F, Zhang Y, Paranjape T, Zhu Y (2009) microRNA miR-196a-2 and breast cancer: a genetic and epigenetic association study and functional analysis. Cancer Res 69(14):5970–5977. doi:10.1158/0008-5472.CAN-09-0236

    Article  PubMed  CAS  Google Scholar 

  29. Xu W, Xu J, Liu S, Chen B, Wang X, Li Y, Qian Y, Zhao W, Wu J (2011) Effects of common polymorphisms rs11614913 in miR-196a2 and rs2910164 in miR-146a on cancer susceptibility: a meta-analysis. PLoS ONE 6(5):e20471. doi:10.1371/journal.pone.0020471

    Article  PubMed  CAS  Google Scholar 

  30. Jedlinski DJ, Gabrovska PN, Weinstein SR, Smith RA, Griffiths LR (2011) Single nucleotide polymorphism in hsa-mir-196a-2 and breast cancer risk: a case control study. Twin Res Hum Genet 14(5):417–421. doi:10.1375/twin.14.5.417

    Article  PubMed  Google Scholar 

  31. Garcia AI, Cox DG, Barjhoux L, Verny-Pierre C, Barnes D, Antoniou AC, Stoppa-Lyonnet D, Sinilnikova OM, Mazoyer S (2011) The rs2910164:G>C SNP in the MIR146A gene is not associated with breast cancer risk in BRCA1 and BRCA2 mutation carriers. Hum Mutat 32(9):1004–1007. doi:10.1002/humu.21539

    Article  PubMed  CAS  Google Scholar 

  32. Catucci I, Yang R, Verderio P, Pizzamiglio S, Heesen L, Hemminki K, Sutter C, Wappenschmidt B, Dick M, Arnold N, Bugert P, Niederacher D, Meindl A, Schmutzler RK, Bartram CC, Ficarazzi F, Tizzoni L, Zaffaroni D, Manoukian S, Barile M, Pierotti MA, Radice P, Burwinkel B, Peterlongo P (2010) Evaluation of SNPs in miR-146a, miR196a2 and miR-499 as low-penetrance alleles in German and Italian familial breast cancer cases. Hum Mutat 31(1):E1052–E1057. doi:10.1002/humu.21141

    Article  PubMed  Google Scholar 

  33. Zhang L, Volinia S, Bonome T, Calin GA, Greshock J, Yang N, Liu CG, Giannakakis A, Alexiou P, Hasegawa K, Johnstone CN, Megraw MS, Adams S, Lassus H, Huang J, Kaur S, Liang S, Sethupathy P, Leminen A, Simossis VA, Sandaltzopoulos R, Naomoto Y, Katsaros D, Gimotty PA, DeMichele A, Huang Q, Butzow R, Rustgi AK, Weber BL, Birrer MJ, Hatzigeorgiou AG, Croce CM, Coukos G (2008) Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc Natl Acad Sci USA 105(19):7004–7009. doi:10.1073/pnas.0801615105

    Article  PubMed  CAS  Google Scholar 

  34. Lavon I, Zrihan D, Granit A, Einstein O, Fainstein N, Cohen MA, Zelikovitch B, Shoshan Y, Spektor S, Reubinoff BE, Felig Y, Gerlitz O, Ben-Hur T, Smith Y, Siegal T (2010) Gliomas display a microRNA expression profile reminiscent of neural precursor cells. Neuro-oncology 12(5):422–433. doi:10.1093/neuonc/nop061

    PubMed  CAS  Google Scholar 

  35. Toffanin S, Hoshida Y, Lachenmayer A, Villanueva A, Cabellos L, Minguez B, Savic R, Ward SC, Thung S, Chiang DY, Alsinet C, Tovar V, Roayaie S, Schwartz M, Bruix J, Waxman S, Friedman SL, Golub T, Mazzaferro V, Llovet JM (2011) MicroRNA-based classification of hepatocellular carcinoma and oncogenic role of miR-517a. Gastroenterology 140(5):1618.e16–1628.e16. doi:10.1053/j.gastro.2011.02.009

    Article  Google Scholar 

  36. Shen J, Wang D, Gregory SR, Medico L, Hu Q, Yan L, Odunsi K, Lele SB, Ambrosone CB, Liu S, Zhao H (2012) Evaluation of microRNA expression profiles and their associations with risk alleles in lymphoblastoid cell lines of familial ovarian cancer. Carcinogenesis 33(3):604–612. doi:10.1093/carcin/bgs008

    Article  PubMed  CAS  Google Scholar 

  37. Ganz PA, Land SR, Geyer CE Jr, Cecchini RS, Costantino JP, Pajon ER, Fehrenbacher L, Atkins JN, Polikoff JA, Vogel VG, Erban JK, Livingston RB, Perez EA, Mamounas EP, Wolmark N, Swain SM (2011) Menstrual history and quality-of-life outcomes in women with node-positive breast cancer treated with adjuvant therapy on the NSABP B-30 trial. J Clin Oncol 29(9):1110–1116. doi:10.1200/JCO.2010.29.7689

    Article  PubMed  Google Scholar 

  38. Zheng W, Cai Q, Signorello LB, Long J, Hargreaves MK, Deming SL, Li G, Li C, Cui Y, Blot WJ (2009) Evaluation of 11 breast cancer susceptibility loci in African-American women. Cancer Epidemiol Biomarkers Prev 18(10):2761–2764. doi:10.1158/1055-9965.EPI-09-0624

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the U.S. Army Medical Research and Material Command (USARMMC) (DAMD-17-01-1-0334 and W81XWH-08-1-0379), the National Cancer Institute (R01 CA100598, R01 CA136483 and R25 CA114101), the Breast Cancer Research Foundation and a gift from Philip L. Hubbell family. Samples were stored and managed by the RPCI DataBank and BioRepository (DBBR) and genotyping was performed in the RPCI Genomics Core Facility, both CCSG shared resources, supported by P30 CA016056-32. The New Jersey State Cancer Registry (NJSCR) is a participant in the Centers for Disease Control and Prevention’s National Program of Cancer Registries (NPCR) and is a National Cancer Institute SEER Expansion Registry. The NJSCR is supported by the Centers for Disease Control and Prevention under cooperative agreement 1U58DP00039311-01 awarded to the New Jersey Department of Health. The collection of State of New Jersey cancer incidence data is also supported by the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) Program under contract N01-PC-2010-00027 and the State of New Jersey. The funding agents played no role in design, in the collection, analysis, and interpretation of data, in the writing of the manuscript, or in the decision to submit the manuscript for publication. We are grateful to the women who participated in this study, and to colleagues, physicians, and clinical staff at participating hospitals in New York who facilitated identification and enrollment of cases into the study: Drs. Kandace Amend (i3 Drug Safety), Helena Furberg (Memorial Sloan-Kettering Cancer Center), Thomas Rohan and Joseph Sparano (Albert Einstein College of Medicine), Kitwaw Demissie (University of Medicine and Dentistry of New Jersey), Paul Tartter and Alison Estabrook (St. Luke’s Roosevelt Hospital), James Reilly (Kings County Hospital Center), Benjamin Pace, George Raptis and Christina Weltz (Mount Sinai School of Medicine), Maria Castaldi (Jacob Medical Center), Sheldon Feldman (New York-Presbyterian), and Margaret Kemeny (Queens Hospital Center).

Conflict of interest

Dr. Kelly Graham is an employee of Susan G. Komen Foundation for the Cure.

Author information

Authors and Affiliations

  1. Department of Cancer Prevention & Control, Roswell Park Cancer Institute, Buffalo, NY, USA

    Song Yao, Kelly Graham, Lara E. Sucheston Campbell, Gary Zirpoli, Michelle Roberts, Gregory Ciupak, Warren Davis & Christine B. Ambrosone

  2. Department of Epidemiology, M.D. Anderson Cancer Center, The University of Texas, Houston, TX, USA

    Jie Shen & Hua Zhao

  3. Department of Pharmacology & Therapeutics, Roswell Park Cancer Institute, Buffalo, NY, USA

    Prashant Singh

  4. Department of Pathology, Roswell Park Cancer Institute, Buffalo, NY, USA

    Helena Hwang & Thaer Khoury

  5. University of Pittsburgh Cancer Institute, University of Pittsburgh, Pittsburgh, PA, USA

    Dana H. Bovbjerg

  6. Department of Oncological Sciences, Mount Sinai School of Medicine, New York, NY, USA

    Lina Jandorf

  7. New Jersey State Cancer Registry, New Jersey Department of Health, Trenton, NJ, USA

    Karen S. Pawlish

  8. Rutgers Cancer Institute of New Jersey, Robert Wood Johnson Medical School, New Brunswick, NJ, USA

    Elisa V. Bandera

  9. Department of Biostatistics, Roswell Park Cancer Institute, Buffalo, NY, USA

    Song Liu

Authors
  1. Song Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kelly Graham
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jie Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lara E. Sucheston Campbell
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Prashant Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gary Zirpoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michelle Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gregory Ciupak
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Warren Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Helena Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Thaer Khoury
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Dana H. Bovbjerg
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Lina Jandorf
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Karen S. Pawlish
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Elisa V. Bandera
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Song Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Christine B. Ambrosone
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Hua Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Song Yao or Hua Zhao.

Additional information

Song Yao and Kelly Graham contributed equally to the work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 194 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yao, S., Graham, K., Shen, J. et al. Genetic variants in microRNAs and breast cancer risk in African American and European American women. Breast Cancer Res Treat 141, 447–459 (2013). https://doi.org/10.1007/s10549-013-2698-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-013-2698-4

Keywords

Search

Navigation