图书馆订阅: Guest
Begell Digital Portal Begell 数字图书馆 电子图书 期刊 参考文献及会议录 研究收集
肿瘤形成评论综述™
SJR: 0.631 SNIP: 0.503 CiteScore™: 2

ISSN 打印: 0893-9675
ISSN 在线: 2162-6448

肿瘤形成评论综述™

DOI: 10.1615/CritRevOncog.2020033071
pages 403-413

Role of Epstein-Barr Virus and Human Papillomavirus Coinfection in Oral and Anogenital Carcinogenesis: Potential Tumorigenic Pathways

Marcos Antonio Pereira de Lima
School of Medicine, Federal University of Cariri, UFCA, Barbalha, Ceará, Brazil
Ilara Parente Pinheiro Teodoro
School of Medicine, Federal University of Cariri, UFCA, Barbalha, Ceará, Brazil
Cláudio Gleidiston Lima da Silva
School of Medicine, Federal University of Cariri, UFCA, Barbalha, Ceará, Brazil
Marcos Venício Alves Lima
Ceará Cancer Institute, ICC, Fortaleza, Ceará, Brazil

ABSTRACT

Epstein-Barr virus (EBV) and human papillomavirus (HPV) have been implicated in 38% of all virus-related cancers. Over the past three decades, both have been detected in anogenital and head-and-neck squamous cell carcinomas (HNSCC), with evidence of involvement in tumor genesis and progression. Very little has been published on HPV/EBV coinfection. In this chapter, we review the literature on the role of these viruses in oral carcinoma and draw parallels with other HNSCCs and anogenital carcinomas, with emphasis on their interplay and potential signaling pathways. EBV infection seems to create an environment that favors HPV latency, supporting the claim that EBV is a cofactor in HPV-related carcinomas. In turn, under certain circumstances, HPV appears to be able to induce EBV to switch to the latent or replicative state. The main viral oncogenes expressed in these malignancies are EBNA1, EBNA2, LMP1, EBERs, and the high-risk HPV oncogenes E6 and E7. The most well-documented human proteins involved are p53, pRb, p16INK4a, p19ARF, Myc, E-cadherin, β-catenin, EGFR, MLH1, and COX-2. These proteins are directly associated not only with viral products but also with one another in the development of malignancy. Knowledge of the molecular machinery behind carcinomas coinfected with HPV and EBV may help understand how these viruses trigger carcinogenesis and subsidize the development of new biomarkers of tumor aggressiveness and prognosis, alternative surrogate virus markers, and possible therapeutic targets.

REFERENCES

  1. Shi Y, Peng SL, Yang LF, Chen X, Tao YG, Cao Y. Co-infection of Epstein-Barr virus and human papillomavirus in human tumorigenesis. Chin J Cancer. 2016;35:16.

  2. Zur Hausen H. The search for infectious causes of human cancers: where and why. Virology. 2009;392(1):1-10.

  3. de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, For man D, Plummer M. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012;13(6):607-15.

  4. Chen X, Kost J, Sulovari A, Wong N, Liang WS, Cao J, Li D. A virome-wide clonal integration analysis platform for discovering cancer viral etiology. Genome Res. 2019;29(5):819-30.

  5. Mesri EA, Feitelson MA, Munger K. Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe. 2014;15(3):266-82.

  6. Al Moustafa AE, Chen D, Ghabreau L, Akil N. Association between human papillomavirus and Epstein-Barr virus infections in human oral carcinogenesis. Med Hypotheses. 2009;73(2):184-6.

  7. Guidry JT, Myers JE, Bienkowska-Haba M, Songock WK, Ma X, Shi M, Nathan CO, Bodily JM, Sapp MJ, Scott RS. Inhibition of Epstein-Barr virus replication in human papillomavirus-immortalized keratinocytes. J Virol. 2019;93(2).

  8. Tsuchiya S. Diagnosis of Epstein-Barr virus-associated diseases. Crit Rev Oncol Hematol. 2002;44(3):227-38.

  9. Epstein MA, Achong BG, Barr YM. Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet. 1964;1(7335):702-3.

  10. Makielski KR, Lee D, Lorenz LD, Nawandar DM, Chiu YF, Kenney SC, Lamber PF. Human papillomavirus promotes Epstein-Barr virus maintenance and lytic reactivation in immortalized oral keratinocytes. Virology. 2016;495:52-62.

  11. Guidry JT, Scott RS. The interaction between human papillomavirus and other viruses. Virus Res. 2017;231:139-47.

  12. Vranic S, Cyprian FS, Akhtar S, Al Moustafa AE. The role of Epstein-Barr virus in cervical cancer: a brief update. Front Oncol. 2018;8:113.

  13. Cai Q, Cai J, Fang Y, Young KH. Epstein-Barr virus-positive natural killer/T-cell lymphoma. Front Oncol. 2019;9:386.

  14. World Health Organization. Epstein-Barr virus and Kaposi's sarcoma herpesvirus/human herpesvirus 8. In: IARC monographs on the evaluation of carcinogenic risks to humans, no. 70. Lyon, France: International Agency for Research on Cancer (IARC); 1997.

  15. de Lima M, Teodoro I, de Galiza L, Maia Filho P, Marques F, Pinheiro Junior R, Macedo G, Facundo HT, Silva C, Lima MV. Association between Epstein-Barr virus and oral carcinoma: a systematic review with meta-analysis. Crit Rev Oncogen. 2019;24(4):349-369.

  16. Guidry JT, Birdwell CE, Scott RS. Epstein-Barr virus in the pathogenesis of oral cancers. Oral Dis. 2018; 24(4):497-508.

  17. de Lima MAP, Neto PJN, Lima LPM, Gon^alves Junior J, Teixeira Junior AG, Teodoro IPP, Facundo HT, da Silva CG, Lima MV. Association between Epstein-Barr virus (EBV) and cervical carcinoma: a meta-analysis. Gynecol Oncol. 2018;148(2):317-28.

  18. Deng Z, Uehara T, Maeda H, Hasegawa M, Matayoshi S, Kiyuna A, Agena S, Pan X, Zhang C, Yamashita Y, Xie M. Epstein-Barr virus and human papillomavirus infections and genotype distribution in head and neck cancers. PLoS One. 2014;9(11):e113702.

  19. Afonso LA, Moyses N, Alves G, Ornellas AA, Passos MR, Oliveira LD, Cavalcanti SM. Prevalence of human papillomavirus and Epstein-Barr virus DNA in penile cancer cases from Brazil. Mem Inst Oswaldo Cruz. 2012;107(1):18-23.

  20. Al Moustafa AE, Al-Antary N, Aboulkassim T, Akil N, Batist G, Yasmeen A. Co-prevalence of Epstein-Barr virus and high-risk human papillomaviruses in Syrian women with breast cancer. Hum Vaccin Immunother. 2016; 12(7):1936-9.

  21. Al Moustafa AE, Cyprian FS, Al-Antary N, Yasmeen A. High-risk human papillomaviruses and Epstein-Barr virus presence and crosstalk in human oral carcinogenesis. In: Al Moustafa AE, editor. Development of oral cancer: risk factors and prevention strategies. Switzerland: Springer; 2017. p.83-94.

  22. Khenchouche A, Sadouki N, Boudriche A, Houali K, Graba A, Ooka T, Bouguermouh A. Human papillomavirus and Epstein-Barr virus co-infection in cervical carcinoma in Algerian women. Virol J. 2013;10:340.

  23. Aromseree S, Pientong C, Swangphon P, Chaiwongkot A, Patarapadungkit N, Kleebkaow P, Tungsiriwattana T, Kongyingyoes B, Vendrig T, Middeldorp JM, Ekalaksananan T. Possible contributing role of Epstein-Barr virus (EBV) as a cofactor in human papillomavirus (HPV)-associated cervical carcinogenesis. J Clin Virol. 2015;73:70-6.

  24. Sixbey JW, Lemon SM, Pagano JS. A second site for Epstein-Barr virus shedding: the uterine cervix. Lancet. 1986;2(8516):1122-4.

  25. Naher H, Gissmann L, Freese UK, Petzoldt D, Helfrich S. Subclinical Epstein-Barr virus infection of both the male and female genital tract-indication for sexual transmission. J Invest Dermatol. 1992;98(5):791-3.

  26. Sixbey JW, Nedrud JG, Raab-Traub N, Hanes RA, Pagano JS. Epstein-Barr virus replication in oropharyngeal epithelial cells. N Engl J Med. 1984;310(19):1225-30.

  27. Szostek S, Zawilinska B, Kopec J, Kosz-Vnenchak M. Herpesviruses as possible cofactors in HPV-16-related oncogenesis. Acta Biochim Pol. 2009;56(2):337-42.

  28. Kahla S, Oueslati S, Achour M, Kochbati L, Chanoufi MB, Maalej M, Oueslati R. Correlation between ebv co-infection and HPV16 genome integrity in Tunisian cervical cancer patients. Braz J Microbiol. 2012;43(2):744-53.

  29. Jiang R, Ekshyyan O, Moore-Medlin T, Rong X, Nathan S, Gu X, Abreo F, Rosenthal EL, Shi M, Guidry JT, Scott RS. Association between human papilloma virus/Epstein-Barr virus coinfection and oral carcinogenesis. J Oral Pathol Med. 2015;44(1):28-36.

  30. Birdwell CE, Queen KJ, Kilgore PC, Rollyson P, Trutschl M, Cvek U, Scott RS. Genome-wide DNA methylation as an epigenetic consequence of Epstein-Barr virus infection of immortalized keratinocytes. J Virol. 2014;88 (19):11442-58.

  31. McCormick TM, Canedo NH, Furtado YL, Silveira FA, de Lima RJ, Rosman AD, Almeida Filho GL, da C Carvalho MD. Association between human papillomavirus and Epstein-Barr virus DNA and gene promoter methylation of RB1 and CDH1 in the cervical lesions: a transversal study. Diagn Pathol. 2015;10:59.

  32. Szkaradkiewicz A, Wal M, Kuch A, Pieta P. Human papillomavirus (HPV) and Epstein-Barr virus (EBV) cervical infections in women with normal and abnormal cytology. Pol J Microbiol. 2004;53(2):95-9.

  33. Prayitno A. Cervical cancer with human papilloma virus and Epstein Barr virus positive. J Carcinog. 2006;5:13.

  34. Murata T, Tsurumi T. Switching of EBV cycles between latent and lytic states. Rev Med Virol. 2014;24(3):142-53.

  35. Birdwell CE, Prasai K, Dykes S, Jia Y, Munroe TGC, Bienkowska-Haba M, Scott RS. Epstein-Barr virus stably confers an invasive phenotype to epithelial cells through reprogramming of the WNT pathway. Oncotarget. 2018;9(12):10417-35.

  36. Cruz I, Van den Brule AJ, Steenbergen RD, Snijders PJ, Meijer CJ, Walboomers JM, Snow GB, Van der Waal I. Prevalence of Epstein-Barr virus in oral squamous cell carcinomas, premalignant lesions and normal mucosa-a study using the polymerase chain reaction. Oral Oncol. 1997;33(3):182-8.

  37. Ambinder RF. Gammaherpesviruses and "Hit-and-Run" oncogenesis. Am J Pathol. 2000;156(1):1-3.

  38. Horiuchi K, Mishima K, Ichijima K, Sugimura M, Ishida T, Kirita T. Epstein-Barr virus in the proliferative diseases of squamous epithelium in the oral cavity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1995;79(1):57-63.

  39. Tsuhako K, Nakazato I, Miyagi J, Iwamasa T, Arasaki A, Hiratsuka H, Sunakawa H, Kohama G, Abo T. Comparaive study of oral squamous cell carcinoma in Okinawa, Southern Japan and Sapporo in Hokkaido, Northern Japan; with special reference to human papillomavirus and Epstein-Barr virus infection. J Oral Pathol Med. 2000;29(2):70-9.

  40. O'Leary JJ, Landers RJ, Crowley M, Healy I, Kealy WF, Hogan J, Cullinane C, Kelehan P, Doyle CT. Genotypic mapping of HPV and assessment of EBV prevalence in endocervical lesions. J Clin Pathol. 1997;50Q1):904-10.

  41. Hilton DA, Brown LJ, Pringle JH, Nandha H. Absence of Epstein-Barr virus in carcinoma of the cervix. Cancer. 1993;72(6):1946-8.

  42. Shoji Y, Saegusa M, Takano Y, Hashimura M, Okayasu I. Detection of the Epstein-Barr virus genome in cervical neoplasia is closely related to the degree of infiltrating lymphoid cells: a polymerase chain reaction and in situ hybridization approach. Pathol Int. 1997;47(8):507-11.

  43. Turunen A, Rautava J, Grenman R, Syrjanen K, Syrjanen S. Epstein-Barr virus (EBV)-encoded small RNAs (EBERs) associated with poor prognosis of head and neck carcinomas. Oncotarget. 2017;8(16):27328-38.

  44. Cruz I, Van Den Brule AJ, Brink AA, Snijders PJ, Walboomers JM, Van Der Waal I, Meijer CJ. No direct role for Epstein-Barr virus in oral carcinogenesis: a study at the DNA, RNA and protein levels. Int J Cancer. 2000;86(3):356-61.

  45. Gonzalez-Moles MA, Gutierrez J, Rodriguez MJ, Ruiz-Avila I, Rodriguez-Archilla A. Epstein-Barr virus latent membrane protein-1 (LMP-1) expression in oral squamous cell carcinoma. Laryngoscope. 2002;112(3):482-7.

  46. Shimakage M, Horii K, Tempaku A, Kakudo K, Shirasaka T, Sasagawa T. Association of Epstein-Barr virus with oral cancers. Hum Pathol. 2002;33(6):608-14.

  47. Aromseree S, Middeldorp JM, Pientong C, van Eijndhoven M, Ramayanti O, Lougheed SM, Pegtel DM, Steenbergen RD, Ekalaksananan T. High levels of EBV-encoded RNA 1 (EBER1) trigger interferon and inflammation-related genes in keratinocytes expressing HPV16 E6/E7. PLoS One. 2017;12(1):e0169290.

  48. Ekalaksananan T, Wongjampa W, Phusingha P, Chuerduangphui J, Vatanasapt P, Promthet S, Patarapadungkit N, Pientong C. Comprehensive data of P53 R282 gene mutation with human papillomaviruses (HPV)-associated oral squamous cell carcinoma (OSCC). Pathol Oncol Res. 2019:1-9.

  49. Eze N, Lo YC, Burtness B. Biomarker driven treatment of head and neck squamous cell cancer. Cancers Head Neck. 2017;2:6.

  50. Hubert P, Caberg JH, Gilles C, Bousarghin L, Franzen-Detrooz E, Boniver J, Delvenne P. E-cadherin-dependent adhesion of dendritic and Langerhans cells to keratinocytes is defective in cervical human papillomavirus-associated (pre)neoplastic lesions. J Pathol. 2005;206(3):346-55.

  51. Caberg JH, Hubert PM, Begon DY, Herfs MF, Roncarati PJ, Boniver J, Delvenne P. Silencing of E7 oncogene restores functional E-cadherin expression in human papillomavirus 16-transformed keratinocytes. Carcinogenesis. 2008;29(7):1441-7.

  52. Hebner CM, Laimins LA. Human papillomaviruses: basic mechanisms of pathogenesis and oncogenicity. Rev Med Virol. 2006;16(2):83-97.

  53. Todd R, Hinds PW, Munger K, Rustgi AK, Opitz OG, Suliman Y, Wong DT. Cell cycle dysregulation in oral cancer. Crit Rev Oral Biol Med. 2002;13(1):51-61.

  54. Canepa ET, Scassa ME, Ceruti JM, Marazita MC, Carcagno AL, Sirkin PF, Ogara MF. INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life. 2007;59(7):419-26.

  55. Muller H, Helin K. The E2F transcription factors: key regulators of cell proliferation. Biochim Biophys Acta. 2000;1470(1):M1-12.

  56. Broccolo F, Ciccarese G, Rossi A, Anselmi L, Drago F, Toniolo A. Human papillomavirus (HPV) and Epstein-Barr virus (EBV) in keratinizing versus non-keratinizing squamous cell carcinoma of the oropharynx. Infect Agent Cancer. 2018;13:32.

  57. Bindra RS, Glazer PM. Co-repression of mismatch repair gene expression by hypoxia in cancer cells: role of the Myc/Max network. Cancer Lett. 2007;252(1):93-103.

  58. Laurson J, Khan S, Chung R, Cross K, Raj K. Epigenetic repression of E-cadherin by human papillomavirus 16 E7 protein. Carcinogenesis. 2010;31(5):918-26.

  59. van Roy F, Berx G. The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci. 2008;65(23):3756-88.

  60. Cyprian FS, Al-Farsi HF, Vranic S, Akhtar S, Al Moustafa AE. Epstein-Barr virus and human papillomaviruses inter-actions and their roles in the initiation of epithelial-mesenchymal transition and cancer progression. Front Oncol. 2018;8:111.

  61. Burassakarn A, Pientong C, Sunthamala N, Chuerduangphui J, Vatanasapt P, Patarapadungkit N, Kongyingyoes B, Ekalaksananan T. Aberrant gene promoter methylation of E-cadherin, p16 INK4a, p14 ARF, and MGMT in Epstein-Barr virus-associated oral squamous cell carcinomas. Med Oncol. 2017;34(7):128.

  62. Kim SH, Oh JM, No JH, Bang YJ, Juhnn YS, Song YS. Involvement of NF-kappaB and AP-1 in COX-2 upregulation by human papillomavirus 16 E5 oncoprotein. Carcinogenesis. 2009;30(5):753-7.

  63. Subbaramaiah K, Dannenberg AJ. Cyclooxygenase-2 transcription is regulated by human papillomavirus 16 E6 and E7 oncoproteins: evidence of a corepressor/coactivator exchange. Cancer Res. 2007;67(8):3976-85.

  64. Gunasekharan VK, Li Y, Andrade J, Laimins LA. Post-transcriptional regulation ofKLF4 by high-risk human papillomaviruses is necessary for the differentiation-dependent viral life cycle. PLoS Pathog. 2016;12(7):e1005747.

  65. Budhy TI. Molecular grading of oral squamous cell carcinomas infected with EBV. Asian Pac J Cancer Prev. 2018;19(7):1793-6.

  66. Frappier L. Viral disruption of promyelocytic leukemia (PML) nuclear bodies by hijacking host PML regulators. Virulence. 2011;2(1):58-62.

  67. Wilson JB, Manet E, Gruffat H, Busson P, Blondel M, Fahraeus R. EBNA1: oncogenic activity, immune evasion and biochemical functions provide targets for novel therapeutic strategies against Epstein-Barr virus-associated cancers. Cancers (Basel). 2018;10(4):E109.

  68. Frappier L. Contributions of Epstein-Barr nuclear antigen 1 (EBNA1) to cell immortalization and survival. Viruses. 2012;4(9):1537-47.

  69. Milian E, Prats E, Cairo JJ, Godia F, Vives J. BHRF1 exerts an antiapoptotic effect and cell cycle arrest via Bcl-2 in murine hybridomas. J Biotechnol. 2015;209:58-67.

  70. Young LS, Dawson CW, Eliopoulos AG. The expression and function of Epstein-Barr virus encoded latent genes. Mol Pathol. 2000;53(5):238-47.

  71. Murray PG, Young LS. Epstein-Barr virus infection: basis of malignancy and potential for therapy. Expert Rev Mol Med. 2001;3(28):1-20.

  72. Dolcetti R, Masucci MG. Epstein-Barr virus: induction and control of cell transformation. J Cell Physiol. 2003;196(2):207-18.

  73. Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene. 2005;24(17):2899-908.

  74. de Moraes E, Dar NA, de Moura Gallo CV, Hainaut P. Cross-talks between cyclooxygenase-2 and tumor suppressor protein p53: balancing life and death during inflammatory stress and carcinogenesis. Int J Cancer. 2007;121(5):929-37.

  75. Yang X, He Z, Xin B, Cao L. LMP1 of Epstein-Barr virus suppresses cellular senescence associated with the inhibition of p16INK4a expression. Oncogene. 2000; 19(16):2002-13.

  76. Rocco JW, Sidransky D. p16(MTS-1/CDKN2/INK4a) in cancer progression. Exp Cell Res. 2001;264(1):42-55.

  77. Al-Thawadi H, Ghabreau L, Aboulkassim T, Yasmeen A, Vranic S, Batist G, Moustafa A. Co-incidence of Epstein-Barr virus and high-risk human papillomaviruses in cervical cancer of Syrian women. Front Oncol. 2018;8:250.

  78. Ren Q, Zuo T, Lu H. Malignant transformation of a human oral squamous cell carcinoma cell strain OSC-19 by EBV encoded small RNAs. Lin Chuang Er Bi Yan Hou Ke Za Zhi. 2004;18(11):675-7 (in Chinese).

  79. Cao S, Wylie KM, Wyczalkowski MA, Karpova A, Ley J, Sun S, Mashl RJ, Liang WW, Wang X, Johnson K, DiPersio JF. Dynamic host immune response in virus-associated cancers. Commun Biol. 2019;2:109.

  80. Amati B, Alevizopoulos K, Vlach J. Myc and the cell cycle. Front Biosci. 1998;3:d250-68.

  81. Elend M, Eilers M. Cell growth: downstream of Mycto grow or to cycle? Curr Biol. 1999;9(24):R936-8.

  82. MacPartlin M, Homer E, Robinson H, McCormick CJ, Crouch DH, Durant ST, Matheson EC, Hall AG, Gillespie DA, Brown R. Interactions of the DNA mismatch repair proteins MLH1 and MSH2 with c-MYC and MAX. Oncogene. 2003;22(6):819-25.

  83. Yang JY, Zong CS, Xia W, Wei Y, Ali-Seyed M, Li Z, Broglio K, Berry DA, Hung MC. MDM2 promotes cell motility and invasiveness by regulating E-cadherin degradation. Mol Cell Biol. 2006;26(19):7269-82.

  84. Benoit V, de Moraes E, Dar NA, Taranchon E, Bours V, Hautefeuille A, Taniere P, Chariot A, Scoazec JY, de Moura Gallo CV, Merville MP. Transcriptional activation of cyclooxygenase-2 by tumor suppressor p53 requires nuclear factor-kappaB. Oncogene. 2006;25(42):5708-18.

  85. Dohadwala M, Yang SC, Luo J, Sharma S, Batra RK, Huang M, Lin Y, Goodglick L, Krysan K, Fishbein MC, Hong L. Cyclooxygenase-2-dependent regulation of E-cadherin: prostaglandin E2 induces transcriptional repressors ZEB1 and Snail in non-small cell lung cancer. Cancer Res. 2006 May 15;66(10):5338-45.

  86. Liu X, Lazenby AJ, Siegal GP. Signal transduction crosstalk during colorectal tumorigenesis. Adv Anat Pathol. 2006;13(5):270-74.

  87. Schmalhofer O, Brabletz S, Brabletz T. E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev. 2009;28(1-2):151-66.

  88. Saito T, Oda Y, Kawaguchi K, Takahira T, Yamamoto H, Sakamoto A, Tamiya S, Iwamoto Y, Tsuneyoshi M. Possible association between tumor-suppressor gene mutations and hMSH2/hMLH1 inactivation in alveolar soft part sarcoma. Hum Pathol. 2003;34(9):841-49.

  89. Karnes WE. Implications of low COX-2 expression in colorectal neoplasms with defective DNA mismatch repair. J Cell Biochem Suppl. 2000;34:23-7.

  90. Castiglia D, Bernardini S, Alvino E, Pagani E, De Luca N, Falcinelli S, Pacchiarotti A, Bonmassar E, Zambruno G, D'Atri S. Concomitant activation of Wnt pathway and loss of mismatch repair function in human melanoma. Genes Chromo Cancer. 2008;47(7):614-24.