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Can Bovine Leukemia Virus Be Related to Human Breast Cancer? A Review of the Evidence

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Journal of Mammary Gland Biology and Neoplasia Aims and scope Submit manuscript

Abstract

The incidence of breast cancer is continuously increasing worldwide, as influenced by many factors that act synergistically. In the last decade there was an increasing interest in the possible viral etiology of human breast cancer. Since then, many viruses have been associated with this disease (murine mammary tumor virus, MMTV; Epstein-Barr virus, EBV; and human papillomavirus, HPV). Recently, BLV has been identified in human breast cancers giving rise to the hypothesis that it could be one of the causative agents of this condition. BLV is a retrovirus distributed worldwide that affects cattle, causing lymphosarcoma in a small proportion of infected animals. Because of its similarity with human retroviruses like HTLV and HIV, BLV was assumed to also be involved in tumor emergence. Based on this assumption, studies were focused on the possible role of BLV in human breast cancer development. We present a compilation of the current knowledge on the subject and some prospective analysis that is required to fully end this controversy.

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Abbreviations

BRCA:

Breast cancer 1

CDH 1:

Caderin 1

PTEN:

Phosphatase and tensin homolog

STK11:

Serine/threonine kinase 11

TP53:

Tumor promoter 53

References

  1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127(12):2893–917.

    Article  PubMed  CAS  Google Scholar 

  2. Tao Z, Shi A, Lu C, Song T, Zhang Z, Zhao J. Breast Cancer: epidemiology and etiology. Cell Biochem Biophys. 2015;72(2):333–8.

    Article  PubMed  CAS  Google Scholar 

  3. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.

    Article  PubMed  CAS  Google Scholar 

  4. American Cancer Society. Cancer facts & figures 2017. Atlanta: American Cancer Society; 2017.

    Google Scholar 

  5. Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Dicker D, Pain A, et al. The global burden of cancer 2013. JAMA Oncol. 2015;1(4):505–27.

    Article  PubMed Central  Google Scholar 

  6. Kamińska M, Ciszewski T, Łopacka-Szatan K, Miotła P, Starosławska E. Breast cancer risk factors. Prz Menopauzalny. 2015;14(3):196–202.

    PubMed  PubMed Central  Google Scholar 

  7. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics. CA Cancer J Clin. 2015;65(2):87–108.

    Article  PubMed  Google Scholar 

  8. Campeau PM, Foulkes WD, Tischkowitz MD. Hereditary breast cancer: new genetic developments, new therapeutic avenues. Hum Genet. 2008;124(1):31–42.

    Article  PubMed  CAS  Google Scholar 

  9. Kuchenbaecker KB, Hopper JL, Barnes DR, Phillips KA, Mooij TM, Roos-Blom MJ, et al. Risks of breast, ovarian, and contralateral breast cancer for BRCA1 and BRCA2 mutation carriers. JAMA. 2017;317(23):2402–16.

    Article  PubMed  CAS  Google Scholar 

  10. Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer. 2006;118:3030–44.

    Article  PubMed  CAS  Google Scholar 

  11. Sarid R, Gao SJ. Viruses and human cancer: from detection to causality. Cancer Lett. 2011;305(2):218–27.

    Article  PubMed  CAS  Google Scholar 

  12. Di Lonardo A, Venuti A, Marcante ML. Human papillomavirus in breast cancer. Breast Cancer Res Treat. 1992;21(2):95–100.

    Article  PubMed  Google Scholar 

  13. Wang Y, Holland JF, Bleiweiss IJ, Melana S, Liu X, Pelisson I, et al. Detection of mammary tumor virus env gene-like sequences in human breast cancer. Cancer Res. 1995;55(22):5173–9.

    PubMed  CAS  Google Scholar 

  14. Ochoa Cruz A, Uribe A, Gutiérrez M. Estudio del potencial zoonótico del virus de la leucosis bovina y su presencia en casos de cáncer de seno. Univ Sci. 2006;11(2):31–40.

    Google Scholar 

  15. Buehring GC, Shen HM, Jensen HM, Choi KY, Sun D, Nuovo G. Bovine leukemia virus DNA in human breast tissue. Emerg Infect Dis. 2014;20(5):772–82.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Aida Y, Murakami H, Takahashi M, Takeshima SN. Mechanisms of pathogenesis induced by bovine leukemia virus as a model for human T-cell leukemia virus. Front Microbiol. 2013;4:328.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Panei CJ, Takeshima S, Omori T, Nunoya T, Davis WC, Ishizaki H, et al. Estimation of bovine leukemia virus (BLV) proviral load harbored by lymphocyte subpopulations in BLV-infected cattle at the subclinical stage of enzootic bovine leucosis using BLV-CoCoMo-qPCR. BMC Vet Res. 2013;9:95.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Gillet N, Florins A, Boxus M, Burteau C, Nigro A, Vandermeers F, et al. Mechanisms of leukemogenesis induced by bovine leukemia virus: prospects for novel anti-retroviral therapies in human. Retrovirology. 2007;4:18.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Rodríguez SM, Florins A, Gillet N, de Brogniez A, Sánchez-Alcaraz MT, Boxus M, et al. Preventive and therapeutic strategies for bovine leukemia virus: lessons for HTLV. Viruses. 2011;3:1210–48.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hopkins SG, Di Giacomo RF. Natural transmission of bovine leukemia virus in dairy and beef cattle. Vet Clin North Am Food Anim Pract. 1997;13(1):107–28.

    Article  PubMed  CAS  Google Scholar 

  21. Lassauzet ML, Thurmond MC, Johnson WO, Stevens F, Picanso JP. Factors associated with transmission of bovine leukemia virus by contact in cows on a California dairy. Am J Epidemiol. 1991;133(2):164–76.

    Article  PubMed  CAS  Google Scholar 

  22. Gutiérrez G, Lomonaco M, Alvarez I, Fernandez F, Trono K. Characterization of colostrum from dams of BLV endemic dairy herds. Vet Microbiol. 2015;177(3–4):366–9.

    Article  PubMed  Google Scholar 

  23. Van Der Maaten MJ, Miller JM, Schmerr MJF. Effect of colostral antibody on bovine leukemia virus infection of neonatal calves. Am J Vet Res. 1981;42:1498–500.

    Google Scholar 

  24. Van der Maaten MJ, Miller JM, Schmerr MJ. In utero transmission of bovine leukemia virus. Am J Vet Res. 1981 Jun;42(6):1052–4.

    PubMed  Google Scholar 

  25. Lewinski MK, Bushman FD. Retroviral DNA integration--mechanism and consequences. Adv Genet. 2005;55:147–81.

    PubMed  CAS  Google Scholar 

  26. Murakami H, Yamada T, Suzuki M, Nakahara Y, Suzuki K, Sentsui H. Bovine leukemia virus integration site selection in cattle that develop leukemia. Virus Res. 2011;156(1–2):107–12.

    Article  PubMed  CAS  Google Scholar 

  27. Florins A, Gillet N, Asquith B, Boxus M, Burteau C, Twizere JC, et al. Cell dynamics and immune response to BLV infection: a unifying model. Front Biosci. 2007;12:1520–31.

    Article  PubMed  CAS  Google Scholar 

  28. Buehring GC, Philpott SM, Choi KY. Humans have antibodies reactive with Bovine leukemia virus. AIDS Res Hum Retrovir. 2003;19(12):1105–13.

    Article  PubMed  CAS  Google Scholar 

  29. Sommerfelt MA. Retrovirus receptors. J Gen Virol. 1999;80:3049–64.

    Article  PubMed  CAS  Google Scholar 

  30. Manel N, Kim FJ, Kinet S, Taylor N, Sitbon M, Battini JL. The ubiquitous glucose transporter GLUT-1 is a receptor for HTLV. Cell. 2003;115(4):449–59.

    Article  PubMed  CAS  Google Scholar 

  31. Suzuki T, Matsubara Y, Kitani H, Iked H. Evaluation of the d subunit of bovine adaptor protein complex 3 as a receptor for bovine leukaemia virus. J Gen Virol. 2003;84:1309–16.

    Article  PubMed  CAS  Google Scholar 

  32. Robinson MS, Bonifacino JS. Adaptor-related proteins. Curr Opin Cell Biol. 2001;4:444–53.

    Article  Google Scholar 

  33. Graves DC, Ferrer JF. In vitro transmission and propagation of the bovine leukemia virus in monolayer cell cultures. Cancer Res. 1976;36:4152–9.

    PubMed  CAS  Google Scholar 

  34. Olaya-Galán NN, Corredor-Figueroa AP, Guzmán-Garzón TC, Ríos-Hernandez KS, Salas-Cárdenas SP, Patarroyo MA, et al. Bovine leukaemia virus DNA in fresh milk and raw beef for human consumption. Epidemiol Infect. 2017;145:3125–30.

    Article  PubMed  CAS  Google Scholar 

  35. Buehring GC, Shen HM, Jensen HM, Jin DL, Hudes M, Block G. Exposure to bovine leukemia virus is associated with breast cancer: a case-control study. PLoS One. 2015;10(9):e0134304.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Gross C, Thoma-Kress AK. Molecular mechanisms of HTLV-1: cell-to-cell transmission. Viruses. 2016;8(3):74.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans: Human papillomaviruses. IARC monographs on the evaluation of carcinogenic risks to humans/World Health Organization, International Agency for Research on Cancer . 2007, 90:1–636.

  38. Carneiro-Proietti ABF, Amaranto-Damasio MS, Leal-Horiguchi CF, Bastos RHC, Seabra-Freitas G, Borowiak DR, et al. Mother-to-child transmission of human T-cell lymphotropic viruses-1/2: what we know, and what are the gaps in understanding and preventing this route of infection. J Pediatric Infect Dis Soc. 2014;3(Suppl 1):S24–9.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Miyasaka T, Oguma K, Sentsui H. Distribution and characteristics of bovine leukemia virus integration sites in the host genome at three different clinical stages of infection. Arch Virol. 2015;160:39–46.

    Article  PubMed  CAS  Google Scholar 

  40. Takahashi M, Tajima S, Okada K, Davis WC, Aida Y. Involvement of bovine leukemia virus in induction and inhibition of apoptosis. Microbes Infect. 2004;7:19–28.

    Article  PubMed  CAS  Google Scholar 

  41. Twizere JC, Kruys V, Lefèbvre L, Vanderplasschen A, Collete D, Debacq C, et al. Interaction of retroviral tax oncoproteins with tristetraprolin and regulation of tumor necrosis factor-alpha expression. J Natl Cancer Inst. 2003;95(24):1846–59.

    Article  PubMed  CAS  Google Scholar 

  42. Ahmadi Ghezeldasht S, Shirdel A, Assarehzadegan MA, Hassannia T, Rahimi H, Miri R, et al. Lymphotropic virus type I (HTLV-I) oncogenesis: molecular aspects of virus and host interactions in pathogenesis of adult T cell leukemia/lymphoma (ATL). Iran J Basic Med Sci. 2013;16:179–95.

    PubMed  PubMed Central  Google Scholar 

  43. Buehring GC, Kramme PM, Schultz RD. Evidence for bovine leukemia virus in the mammary epithelial cells of infected cows. Lab Investig. 1994;71:359–65.

    PubMed  CAS  Google Scholar 

  44. Yoshinaka YK. Bovine leukemia virus protease: pirufication, chemical analysis, and in vitro processing of gag precursos polyproteins. J Virol. 1986;57:826–32.

    PubMed  PubMed Central  CAS  Google Scholar 

  45. Mesa G, Ulloa JC, Uribe AM, Gutierrez MF. Bovine leukemia virus gene segment detected in human breast tissue. Open J Med Microbiol 2013; 3: (1)84–90.

  46. Buehring GC, Shen H, Schwartz DA, Lawson JS. Bovine leukemia virus linked to breast cancer in Australian women and identified before breast cancer development. PLoS One. 2017;12(6):e0179367.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Zhang R, Jiang J, Sun W, Zhang J, Huang K, Gu X, et al. Lack of association between bovine leukemia virus and breast cancer in Chinese patients. Breast Cancer Res. 2016;18:101.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Buehring GC. Response to “lack of association between bovine leukemia virus and breast cancer in Chinese patients”. Breast Cancer Res. 2017;19:24.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Choi KY, Liu RB, Buehring GC. Relative sensitivity and specificity of agar gel immunodiffusion, enzyme immunosorbent assay, and immunoblotting for detection of anti-bovine leukemia virus antibodies in cattle. J Virol Methods. 2002;104:33–9.

    Article  PubMed  CAS  Google Scholar 

  50. Gillet N, Willems L. Whole genome sequencing of 51 breast cancers reveals that tumors are devoid of bovine leukemia virus DNA. Retrovirology. 2016;13:75.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Baltzell KA, Shen HM, Krishnamurty S, Sison JD, Nuovo GJ, Buehring GC. Bovine leukemia virus linked to breast cancer but not coinfection with human papillomavirus: case-control study of women in Texas. Cancer. 2018;124(7):1342–9.

    Article  PubMed  Google Scholar 

  52. Frie MC, Coussensa PM. Bovine leukemia virus: a major silent threat to proper immune responses in cattle. Vet Immunol Immunopathol. 2015;163(3–4):103–14.

    Article  PubMed  CAS  Google Scholar 

  53. Schiller JT, Lowy DR. Virus infection and human cancer: an overview. Recent Results Cancer Res. 2014;193:1–10.

    Article  PubMed  CAS  Google Scholar 

  54. Chen CJ, Hsu W, Yang H, Lee M, Chen H, Chien Y, et al. Epidemiology of virus infection and human cancer. Recent Results Cancer Res. 2014;193:11–32.

    Article  PubMed  Google Scholar 

  55. Hill AB. The environment and disease: association or causation? Proc R Soc Med. 1965;58:295–300.

    PubMed  PubMed Central  CAS  Google Scholar 

  56. He Y, Yang X, Xia J, Zhao L, Yang Y. Consumption of meat and dairy products in China: a review. Proc Nutr Soc. 2016;75:385–91.

    Article  PubMed  Google Scholar 

  57. Lawson JS, Salmons B, Glenn WK. Oncogenic viruses and breast cancer: mouse mammary tumor virus (MMTV), bovine leukemia virus (BLV), human papilloma virus (HPV), and Epstein - Barr virus (EBV). Front Oncol. 2018;8:1.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Lawson JS, Salmons B, Gunzburg WH. Commentary regarding Gannon et al. “viral infections and breast cancer e A current perspective”. Cancer Lett. 2018;424:117e118.

    Article  CAS  Google Scholar 

  59. Vinner L, Mourier T, Friis-Nielsen J, Gniadecki R, Dybkaer K, Rosenberg J, et al. Investigation of human cancers for retrovirus by low-stringency target enrichment and high-throughput sequencing. Sci Rep. 2015;5:13201.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Read SA, Douglas MW. Virus induced inflammation and cancer development. Cancer Lett. 2014;345(2):174–81.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratorio de Virología, Facultad de Cs. Veterinarias-UNCPBA, CIVETAN-CONICET, CICPBA, Campus Universitario, Paraje Arroyo Seco s/n, 7000, Tandil, Argentina

    Lucia Martinez Cuesta, Pamela Anahi Lendez, Maria Victoria Nieto Farias, Guillermina Laura Dolcini & Maria Carolina Ceriani

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  1. Lucia Martinez Cuesta
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  2. Pamela Anahi Lendez
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  3. Maria Victoria Nieto Farias
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  4. Guillermina Laura Dolcini
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  5. Maria Carolina Ceriani
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Correspondence to Maria Carolina Ceriani.

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Martinez Cuesta, L., Lendez, P.A., Nieto Farias, M.V. et al. Can Bovine Leukemia Virus Be Related to Human Breast Cancer? A Review of the Evidence. J Mammary Gland Biol Neoplasia 23, 101–107 (2018). https://doi.org/10.1007/s10911-018-9397-z

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  • DOI: https://doi.org/10.1007/s10911-018-9397-z

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