F: forward primer; R: reverse primer; PCR: polymerase chain reaction; Tm: melting temperature; HPV: human papillomavirus; EBV: Epstein-Barr virus; MMTV: mouse mammary tumor virus; SV40: Simian virus 40. M = A + C, R = A + G, W= A + T, Y = C + T
Declarations
Acknowledgments
Special acknowledgment for support of Faculty of Sciences and Techniques, Mohammedia, University Hassan II of Casablanca and Ministry of National Education, Vocational Training, Higher Education and Scientific Research in Morocco.
Author contributions
KAT: Conceptualization, Data curation, Methodology, Formal analysis, Software, Investigation, Project administration, Writing—original draft. AS: Writing—review & editing, Project administration. SAS: Visualization, Validation. KN: Investigation. MB: Resources. MME: Project administration, Supervision. All authors read and approved the submitted version.
Conflicts of interest
The authors declare that they have no conflicts of interest.
Ethical approval
The study protocol was approved by the Ethics Committee for Biomedical Research of the Faculty of Medicine and Pharmacy of Casablanca, Morocco (Reference 3/2018 on 30.04.2018).
Consent to participate
Free and informed consent was obtained from all patients involved in this research and the confidentiality of their personal information was well-respected according to ethical rules.
Consent to publication
Not applicable.
Availability of data and materials
The datasets generated and/or analyzed in the course of the present study are available from the corresponding author upon reasonable request.
Open Exploration maintains a neutral stance on jurisdictional claims in published institutional affiliations and maps. All opinions expressed in this article are the personal views of the author(s) and do not represent the stance of the editorial team or the publisher.
References
Horn J, Vatten LJ. Reproductive and hormonal risk factors of breast cancer: a historical perspective.Int J Womens Health. 2017;9:265–72. [DOI] [PubMed] [PMC]
Glenn WK, Heng B, Delprado W, Iacopetta B, Whitaker NJ, Lawson JS. Epstein-Barr virus, human papillomavirus and mouse mammary tumour virus as multiple viruses in breast cancer.PLoS One. 2012;7:e48788. [DOI] [PubMed] [PMC]
Wong M, Pagano JS, Schiller JT, Tevethia SS, Raab-Traub N, Gruber J. New associations of human papillomavirus, Simian virus 40, and Epstein-Barr virus with human cancer.J Natl Cancer Inst. 2002;94:1832–6. [DOI] [PubMed]
Naushad W, Surriya O, Sadia H. Prevalence of EBV, HPV and MMTV in Pakistani breast cancer patients: A possible etiological role of viruses in breast cancer.Infect Genet Evol. 2017;54:230–7. [DOI] [PubMed]
Doorslaer KV, Chen Z, Bernard H, Chan PKS, DeSalle R, Dillner J, et al. ICTV Virus Taxonomy Profile: Papillomaviridae.J Gen Virol. 2018;99:989–90. [DOI] [PubMed] [PMC]
Graham SV. The human papillomavirus replication cycle, and its links to cancer progression: a comprehensive review.Clin Sci (Lond). 2017;131:2201–21. [DOI] [PubMed]
Tadlaoui KA, Hassou N, Bennani B, Ennaji MM. Emergence of oncogenic high-risk human papillomavirus types and cervical cancer. In: Ennaji MM, editor. Emerging and Reemerging Viral Pathogens. Elsevier; 2020. pp.539–70. [DOI]
Tadlaoui KA, Ennaji MM. The molecular mechanism of novel oncogenes dysregulating signaling pathways associated with cervical carcinoma. In: Ennaji MM, editor. Immunological Implications and Molecular Diagnostics of Genitourinary Cancer. Elsevier; 2020. pp. 19–31. [DOI]
Belglaiaa E. Génotypage moléculaire des papillomavirus humains chez des femmes à risque de cancer du col de l'utérus: implication pour le dépistage et la prévention [dissertation]. Agadir: Université Ibn Zohr; 2015. French.
Omland T, Lie KA, Akre H, Sandlie LE, Jebsen P, Sandvik L, et al. Recurrent respiratory papillomatosis: HPV genotypes and risk of high-grade laryngeal neoplasia.PLoS One. 2014;9:e99114. [DOI] [PubMed] [PMC]
de Martel C, Plummer M, Vignat J, Franceschi S. Worldwide burden of cancer attributable to HPV by site, country and HPV type.Int J Cancer. 2017;141:664–70. [DOI] [PubMed] [PMC]
Serrano B, Brotons M, Bosch FX, Bruni L. Epidemiology and burden of HPV-related disease.Best Pract Res Clin Obstet Gynaecol. 2018;47:14–26. [DOI] [PubMed]
Lonardo AD, Venuti A, Marcante ML. Human papillomavirus in breast cancer.Breast Cancer Res Treat. 1992;21:95–100. [DOI] [PubMed]
Yasmeen A, Bismar TA, Kandouz M, Foulkes WD, Desprez P, Moustafa AA. E6/E7 of HPV type 16 promotes cell invasion and metastasis of human breast cancer cells.Cell Cycle. 2007;6:2038–42. [DOI] [PubMed]
Amarante MK, Watanabe MAE. The possible involvement of virus in breast cancer.J Cancer Res Clin Oncol. 2009;135:329–37. [DOI] [PubMed]
Akil N, Yasmeen A, Kassab A, Ghabreau L, Darnel AD, Moustafa AA. High-risk human papillomavirus infections in breast cancer in Syrian women and their association with Id-1 expression: a tissue microarray study.Br J Cancer. 2008;99:404–7. [DOI] [PubMed] [PMC]
Lawson JS, Günzburg WH, Whitaker NJ. Viruses and human breast cancer.Future Microbiol. 2006;1:33–51. [DOI] [PubMed]
Muhammad U, Yasir H, Mukhtiar A. Does Epstein–Barr Virus Participate in the Development of Breast Cancer? A Brief and Critical Review with Molecular Evidences.Biomedical and Biotechnology Research Journal (BBRJ). 2020;4:285–92. [DOI]
Horiuchi K, Mishima K, Ohsawa M, Aozasa K. Carcinoma of stomach and breast with lymphoid stroma: localisation of Epstein-Barr virus.J Clin Pathol. 1994;47:538–40. [DOI] [PubMed] [PMC]
Labrecque LG, Barnes DM, Fentiman IS, Griffin BE. Epstein-Barr virus in epithelial cell tumors: a breast cancer study.Cancer Res. 1995;55:39–45. [PubMed]
Fina F, Romain S, Ouafik L, Palmari J, Ayed FB, Benharkat S, et al. Frequency and genome load of Epstein-Barr virus in 509 breast cancers from different geographical areas.Br J Cancer. 2001;84:783–90. [DOI] [PubMed] [PMC]
Taneja P, Frazier DP, Kendig RD, Maglic D, Sugiyama T, Kai F, et al. MMTV mouse models and the diagnostic values of MMTV-like sequences in human breast cancer.Expert Rev Mol Diagn. 2009;9:423–40. [DOI] [PubMed] [PMC]
Melana SM, Nepomnaschy I, Sakalian M, Abbott A, Hasa J, Holland JF, et al. Characterization of viral particles isolated from primary cultures of human breast cancer cells.Cancer Res. 2007;67:8960–5. [DOI] [PubMed]
Lawson JS, Glenn WK, Salmons B, Ye Y, Heng B, Moody P, et al. Mouse mammary tumor virus-like sequences in human breast cancer.Cancer Res. 2010;70:3576–85. [DOI] [PubMed]
Stewart AFR, Chen H. Revisiting the MMTV Zoonotic Hypothesis to Account for Geographic Variation in Breast Cancer Incidence.Viruses. 2022;14:559. [DOI] [PubMed] [PMC]
Shang D, Zhou T, Zhuang X, Wu Y, Liu H, Tu Z. Molecular dissection on inhibition of Ras-induced cellular senescence by small t antigen of SV40.Cell Mol Life Sci. 2022;79:242. [DOI] [PubMed] [PMC]
Alibek K, Kakpenova A, Mussabekova A, Sypabekova M, Karatayeva N. Role of viruses in the development of breast cancer.Infect Agent Cancer. 2013;8:32. [DOI] [PubMed] [PMC]
Hachana M, Trimeche M, Ziadi S, Amara K, Korbi S. Evidence for a role of the Simian Virus 40 in human breast carcinomas.Breast Cancer Res Treat. 2009;113:43–58. [DOI] [PubMed]
Agha R, Abdall-Razak A, Crossley E, Dowlut N, Iosifidis C, Mathew G, et al.; STROCSS Group. STROCSS 2019 Guideline: Strengthening the reporting of cohort studies in surgery.Int J Surg. 2019;72:156–65. [DOI] [PubMed]
Saiki RK, Bugawan TL, Horn GT, Mullis KB, Erlich HA. Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes.Nature. 1986;324:163–6. [DOI] [PubMed]
Lee SH, Vigliotti VS, Vigliotti JS, Pappu S. Validation of human papillomavirus genotyping by signature DNA sequence analysis.BMC Clin Pathol. 2009;9:3. [DOI] [PubMed] [PMC]
van Baarle D, Hovenkamp E, Kersten MJ, Klein MR, Miedema F, van Oers MH. Direct Epstein-Barr virus (EBV) typing on peripheral blood mononuclear cells: no association between EBV type 2 infection or superinfection and the development of acquired immunodeficiency syndrome-related non-Hodgkin’s lymphoma.Blood. 1999;93:3949–55. [PubMed]
Pogo BG, Melana SM, Holland JF, Mandeli JF, Pilotti S, Casalini P, et al. Sequences homologous to the mouse mammary tumor virus env gene in human breast carcinoma correlate with overexpression of laminin receptor.Clin Cancer Res. 1999;5:2108–11. [PubMed]
Li R, Mannon RB, Kleiner D, Tsokos M, Bynum M, Kirk AD, et al. BK virus and SV40 co-infection in polyomavirus nephropathy.Transplantation. 2002;74:1497–504. [DOI] [PubMed]
ElAmrani A, Gheit T, Benhessou M, McKay-Chopin S, Attaleb M, Sahraoui S, et al. Prevalence of mucosal and cutaneous human papillomavirus in Moroccan breast cancer.Papillomavirus Res. 2018;5:150–5. [DOI] [PubMed] [PMC]
Wang T, Chang P, Wang L, Yao Q, Guo W, Chen J, et al. The role of human papillomavirus infection in breast cancer.Med Oncol. 2012;29:48–55. [DOI] [PubMed]
Lawson JS, Glenn WK, Salyakina D, Delprado W, Clay R, Antonsson A, et al. Human Papilloma Viruses and Breast Cancer.Front Oncol. 2015;5:277. [DOI] [PubMed] [PMC]
Ngamkham J, Karalak A, Chaiwerawattana A, Sornprom A, Thanasutthichai S, Sukarayodhin S, et al. Prevalence of Human Papillomavirus Infection in Breast Cancer Cells from Thai Women.Asian Pac J Cancer Prev. 2017;18:1839–45. [DOI] [PubMed] [PMC]
Khan NA, Castillo A, Koriyama C, Kijima Y, Umekita Y, Ohi Y, et al. Human papillomavirus detected in female breast carcinomas in Japan.Br J Cancer. 2008;99:408–14. [DOI] [PubMed] [PMC]
de Villiers EM, Sandstrom RE, Hausen Hz, Buck CE. Presence of papillomavirus sequences in condylomatous lesions of the mamillae and in invasive carcinoma of the breast.Breast Cancer Res. 2005;7:R1–11. [DOI] [PubMed] [PMC]
Hennig EM, Suo Z, Thoresen S, Holm R, Kvinnsland S, Nesland JM. Human papillomavirus 16 in breast cancer of women treated for high grade cervical intraepithelial neoplasia (CIN III).Breast Cancer Res Treat. 1999;53:121–35. [DOI] [PubMed]
Damin APS, Karam R, Zettler CG, Caleffi M, Alexandre COP. Evidence for an association of human papillomavirus and breast carcinomas.Breast Cancer Res Treat. 2004;84:131–7. [DOI] [PubMed]
Yu Y, Morimoto T, Sasa M, Okazaki K, Harada Y, Fujiwara T, et al. HPV33 DNA in premalignant and malignant breast lesions in Chinese and Japanese populations.Anticancer Res. 1999;19:5057–61. [PubMed]
Kan C, Iacopetta BJ, Lawson JS, Whitaker NJ. Identification of human papillomavirus DNA gene sequences in human breast cancer.Br J Cancer. 2005;93:946–8. [DOI] [PubMed] [PMC]
Fernandes A, Bianchi G, Feltri AP, Pérez M, Correnti M. Presence of human papillomavirus in breast cancer and its association with prognostic factors.Ecancermedicalscience. 2015;9:548. [DOI] [PubMed] [PMC]
Richardson AK, Currie MJ, Robinson BA, Morrin H, Phung Y, Pearson JF, et al. Cytomegalovirus and Epstein-Barr virus in breast cancer.PLoS One. 2015;10:e0118989. [DOI] [PubMed] [PMC]
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. [DOI] [PubMed] [PMC]
Gihbid A, Amrani AE, Mouh FZ, Gheit T, Benhessou M, Amrani M, et al. Prevalence of Polyomaviruses and Herpesviruses in Moroccan Breast Cancer.Pathogens. 2023;12:640. [DOI] [PubMed] [PMC]
Zhang W, Zhu G, Xu W, Zhang W, Wang H, Wang Y, et al. Association of PD-1/PD-L1 expression and Epstein--Barr virus infection in patients with invasive breast cancer.Diagn Pathol. 2022;17:61. [DOI] [PubMed] [PMC]
Slaoui M, Mzibri ME, Razine R, Qmichou Z, Attaleb M, Amrani M. Detection of MMTV-Like sequences in Moroccan breast cancer cases.Infect Agent Cancer. 2014;9:37. [DOI] [PubMed] [PMC]
Saif I, Bouziyane A, Mzibri ME, Kerroumi ME, Benhessou M, Ennaji MM. Prevalence of Human Papillomavirus and Mouse Mammary Tumor Virus Like DNAs in Tumors from Moroccan Breast Cancer Patients.Indian J Gynecol Oncolog. 2022;20:38. [DOI]
Amarante MK, de Sousa Pereira N, Vitiello GAF, Watanabe MAE. Involvement of a mouse mammary tumor virus (MMTV) homologue in human breast cancer: Evidence for, against and possible causes of controversies.Microb Pathog. 2019;130:283–94. [DOI] [PubMed]
Martini F, Mazzoni E, Corallini A, Taronna A, Querzoli P, Magri E, et al. Breast cancer and simian virus 40 infection.Epidemiology. 2013;24:464–5. [DOI] [PubMed]
Mazzanti CM, Hamad MA, Fanelli G, Scatena C, Zammarchi F, Zavaglia K, et al. A mouse mammary tumor virus env-like exogenous sequence is strictly related to progression of human sporadic breast carcinoma.Am J Pathol. 2011;179:2083–90. [DOI] [PubMed] [PMC]
Hu R, Dawood S, Holmes MD, Collins LC, Schnitt SJ, Cole K, et al. Androgen receptor expression and breast cancer survival in postmenopausal women.Clin Cancer Res. 2011;17:1867–74. [DOI] [PubMed] [PMC]
Kroupis C, Markou A, Vourlidis N, Dionyssiou-Asteriou A, Lianidou ES. Presence of high-risk human papillomavirus sequences in breast cancer tissues and association with histopathological characteristics.Clin Biochem. 2006;39:727–31. [DOI] [PubMed]
Kouloura A, Nicolaidou E, Misitzis I, Panotopoulou E, Kassiani T, Smyrniotis V, et al. HPV infection and breast cancer. Results of a microarray approach.Breast. 2018;40:165–9.Erratum in: Breast. 2018;41:136. [DOI] [PubMed]
Elagali AM, Suliman AA, Altayeb M, Dannoun AI, Parine NR, Sakr HI, et al. Human papillomavirus, gene mutation and estrogen and progesterone receptors in breast cancer: a cross-sectional study.Pan Afr Med J. 2021;38:43. [DOI] [PubMed] [PMC]
Gupta I, Ulamec M, Peric-Balja M, Ramic S, Moustafa AA, Vranic S, et al. Presence of high-risk HPVs, EBV, and MMTV in human triple-negative breast cancer.Hum Vaccin Immunother. 2021;17:4457–66. [DOI] [PubMed] [PMC]
Arbach H, Viglasky V, Lefeu F, Guinebretière J, Ramirez V, Bride N, et al. Epstein-Barr virus (EBV) genome and expression in breast cancer tissue: effect of EBV infection of breast cancer cells on resistance to paclitaxel (Taxol).J Virol. 2006;80:845–53. [DOI] [PubMed] [PMC]
Jubair L, Fallaha S, McMillan NAJ. Systemic Delivery of CRISPR/Cas9 Targeting HPV Oncogenes Is Effective at Eliminating Established Tumors.Mol Ther. 2019;27:2091–9. [DOI] [PubMed] [PMC]
Chen AC, Waterboer T, Keleher A, Morrison B, Jindal S, McMillan D, et al. Human papillomavirus in benign prostatic hyperplasia and prostatic adenocarcinoma patients.Pathol Oncol Res. 2011;17:613–7. [DOI] [PubMed]
Antonsson A, Spurr TP, Chen AC, Francis GD, McMillan NAJ, Saunders NA, et al. High prevalence of human papillomaviruses in fresh frozen breast cancer samples.J Med Virol. 2011;83:2157–63. [DOI] [PubMed]
Malki MI, Gupta I, Fernandes Q, Aboulkassim T, Yasmeen A, Vranic S, et al. Co-presence of Epstein-Barr virus and high-risk human papillomaviruses in Syrian colorectal cancer samples.Hum Vaccin Immunother. 2020;16:2403–7. [DOI] [PubMed] [PMC]
Cyprian FS, Al-Farsi HF, Vranic S, Akhtar S, Moustafa AA. Epstein-Barr Virus and Human Papillomaviruses Interactions and Their Roles in the Initiation of Epithelial-Mesenchymal Transition and Cancer Progression.Front Oncol. 2018;8:111. [DOI] [PubMed] [PMC]