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Genetic variants in microRNA and microRNA biogenesis pathway genes and breast cancer risk among women of African ancestry

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Abstract

MicroRNAs (miRNA) regulate breast biology by binding to specific RNA sequences, leading to RNA degradation and inhibition of translation of their target genes. While germline genetic variations may disrupt some of these interactions between miRNAs and their targets, studies assessing the relationship between genetic variations in the miRNA network and breast cancer risk are still limited, particularly among women of African ancestry. We systematically put together a list of 822 and 10,468 genetic variants among primary miRNA sequences and 38 genes in the miRNA biogenesis pathway, respectively; and examined their association with breast cancer risk in the ROOT consortium which includes women of African ancestry. Findings were replicated in an independent consortium. Logistic regression was used to estimate the odds ratio (OR) and 95 % confidence intervals (CI). For overall breast cancer risk, three single-nucleotide polymorphisms (SNPs) in miRNA biogenesis genes DROSHA rs78393591 (OR = 0.69, 95 % CI: 0.55–0.88, P = 0.003), ESR1 rs523736 (OR = 0.88, 95 % CI: 0.82–0.95, P = 3.99 × 10−4), and ZCCHC11 rs114101502 (OR = 1.33, 95 % CI: 1.11–1.59, P = 0.002), and one SNP in primary miRNA sequence (rs116159732 in miR-6826, OR = 0.74, 95 % CI: 0.63–0.89, P = 0.001) were found to have significant associations in both discovery and validation phases. In a subgroup analysis, two SNPs were associated with risk of estrogen receptor (ER)-negative breast cancer, and three SNPs were associated with risk of ER-positive breast cancer. Several variants in miRNA and miRNA biogenesis pathway genes were associated with breast cancer risk. Risk associations varied by ER status, suggesting potential new mechanisms in etiology.

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Acknowledgments

This work was supported by National Cancer Institute Grants R01-CA142996, P50-CA125183, and R01-CA89085.

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Authors and Affiliations

  1. Department of Medicine, University of Chicago, Chicago, IL, USA

    Frank Qian, Yonglan Zheng & Olufunmilayo I. Olopade

  2. Department of Preventive Medicine, Keck School of Medicine and Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, CA, USA

    Ye Feng, Sue A. Ingles & Christopher A. Haiman

  3. Department of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria

    Temidayo O. Ogundiran

  4. Center for Population and Reproductive Health, College of Medicine, University of Ibadan, Ibadan, Nigeria

    Oladosu Ojengbede

  5. Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University, Nashville, TN, USA

    Wei Zheng & William Blot

  6. Roswell Park Cancer Institute, Buffalo, NY, USA

    Christine B. Ambrosone

  7. Cancer Prevention Institute of California, Fremont, CA, USA

    Esther M. John

  8. Department of Health Research and Policy (Epidemiology) and Stanford Cancer Institute, Stanford University School of Medicine Stanford, Stanford, CA, USA

    Esther M. John

  9. Division of Cancer Etiology, Department of Population Science, Beckman Research Institute, City of Hope, Duarte, CA, USA

    Leslie Bernstein

  10. Sylvester Comprehensive Cancer Center and Department of Epidemiology and Public Health, University of Miami Miller School of Medicine, Miami, FL, USA

    Jennifer J. Hu

  11. Epidemiology and Biostatistics Program, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, DC, USA

    Regina G. Ziegler

  12. Department of Epidemiology, Gillings School of Global Public Health and Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, NC, USA

    Sarah Nyante

  13. Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA

    Elisa V. Bandera

  14. Department of Pathology, Keck School of Medicine and Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, CA, USA

    Michael F. Press

  15. Department of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Katherine L. Nathanson

  16. Chronic Disease Research Centre and Tropical Medicine Research Institute, University of the West Indies, Bridgetown, Barbados

    Anselm Hennis

  17. Department of Preventive Medicine, State University of New York at Stony Brook, Stony Brook, NY, USA

    Barbara Nemesure

  18. Laboratory of Human Carcinogenesis, National Cancer Institute, Bethesda, MD, USA

    Stefan Ambs

  19. Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA

    Laurence N. Kolonel

  20. Department of Public Health Sciences, University of Chicago, 5841 S. Maryland Ave., MC 2007, Chicago, IL, 60637, USA

    Dezheng Huo

Authors
  1. Frank Qian
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  2. Ye Feng
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  3. Yonglan Zheng
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  4. Temidayo O. Ogundiran
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  5. Oladosu Ojengbede
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  6. Wei Zheng
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  7. William Blot
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  8. Christine B. Ambrosone
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  9. Esther M. John
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  10. Leslie Bernstein
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  11. Jennifer J. Hu
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  12. Regina G. Ziegler
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  13. Sarah Nyante
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  14. Elisa V. Bandera
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  15. Sue A. Ingles
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  16. Michael F. Press
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  17. Katherine L. Nathanson
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  18. Anselm Hennis
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  19. Barbara Nemesure
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  20. Stefan Ambs
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  21. Laurence N. Kolonel
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  22. Olufunmilayo I. Olopade
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  23. Christopher A. Haiman
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  24. Dezheng Huo
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Corresponding author

Correspondence to Dezheng Huo.

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The authors declare no conflicts of interest.

This study is compliant with the ethical standards of human research. Written informed consent was obtained from all participants.

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Qian, F., Feng, Y., Zheng, Y. et al. Genetic variants in microRNA and microRNA biogenesis pathway genes and breast cancer risk among women of African ancestry. Hum Genet 135, 1145–1159 (2016). https://doi.org/10.1007/s00439-016-1707-1

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  • DOI: https://doi.org/10.1007/s00439-016-1707-1

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