Ménage à trois: An evolutionary interplay between human papillomavirus, a tumor, and a woman

Trends in Microbiology

Volumn 22, Issue 6, 2014, Pages 345-353

  Shulzhenko, Natalia ^a   Lyng, Heidi ^b   Sanson, Gerdine F ^c   Morgun, Andrey ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c FEDERAL UNIVERSITY OF MATO GROSSO   (Brazil)

Author keywords

Cervical cancer; Driver genes; Gene expression; Genomic aberrations; Human papillomavirus; Immune response; Network analysis

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; DENDRITIC CELL LYSOSOME ASSOCIATED MEMBRANE PROTEIN; DOUBLE STRANDED DNA; INTERFERON REGULATORY FACTOR 7; STAT1 PROTEIN; WART VIRUS VACCINE;

CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOME ABERRATION; COST EFFECTIVENESS ANALYSIS; CYTOSKELETON; DNA SYNTHESIS; GENE CONTROL; GENE EXPRESSION REGULATION; GENE REPLICATION; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNE RESPONSE; IMMUNOGENETICS; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTION; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION; UTERINE CERVIX CANCER; VIRION; ALPHAPAPILLOMAVIRUS; BIOLOGICAL MODEL; FEMALE; GENE REGULATORY NETWORK; HOST PATHOGEN INTERACTION; HUMAN GENOME; PATHOLOGY; PHYSIOLOGY; UTERINE CERVIX TUMOR; VIROLOGY;

HUMAN PAPILLOMAVIRUS;

ALPHAPAPILLOMAVIRUS; CARCINOGENESIS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; GENOME, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; UTERINE CERVICAL NEOPLASMS;

EID: 84901587807     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2014.02.009     Document Type: Review

References (98)

1. Forouzanfar M.H., et al. Breast and cervical cancer in 187 countries between 1980 and 2010: a systematic analysis. Lancet 2011, 378:1461-1484.
2. Clayton J. Clinical approval: trials of an anticancer jab. Nature 2012, 488:S4-S6.
3. Crow J.M. HPV: the global burden. Nature 2012, 488:S2-S3.
4. Sanderson K. Vaccination: a durable design. Nature 2012, 488:S7.
5. Vargas-Parada L. Pathology: three questions. Nature 2012, 488:S14-S15.
6. Zur Hausen H. Q&A: on the case. Interview by Michelle Grayson. Nature 2012, 488:S16.
7. Bernard H.U., et al. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010, 401:70-79.
8. Doorbar J., et al. The biology and life-cycle of human papillomaviruses. Vaccine 2012, 30(Suppl. 5):F55-F70.
9. Chen E.Y., et al. The primary structure and genetic organization of the bovine papillomavirus type 1 genome. Nature 1982, 299:529-534.
10. Danos O., et al. Human papillomavirus 1a complete DNA sequence: a novel type of genome organization among papovaviridae. EMBO J. 1982, 1:231-236.
11. Johansson C., Schwartz S. Regulation of human papillomavirus gene expression by splicing and polyadenylation. Nat. Rev. Microbiol. 2013, 11:239-251.
12. Steger G., Corbach S. Dose-dependent regulation of the early promoter of human papillomavirus type 18 by the viral E2 protein. J. Virol. 1997, 71:50-58.
13. Hummel M., et al. Differentiation-induced and constitutive transcription of human papillomavirus type 31b in cell lines containing viral episomes. J. Virol. 1992, 66:6070-6080.
14. Cheng S., et al. Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes. Genes Dev. 1995, 9:2335-2349.
15. Martin C.M., O'Leary J.J. Histology of cervical intraepithelial neoplasia and the role of biomarkers. Best Pract. Res. Clin. Obstet. Gynaecol. 2011, 25:605-615.
16. Bodily J., Laimins L.A. Persistence of human papillomavirus infection: keys to malignant progression. Trends Microbiol. 2011, 19:33-39.
17. Dillon S., et al. Resolution of cervical dysplasia is associated with T-cell proliferative responses to human papillomavirus type 16 E2. J. Gen. Virol. 2007, 88:803-813.
18. Nakagawa M., et al. Persistence of human papillomavirus type 16 infection is associated with lack of cytotoxic T lymphocyte response to the E6 antigens. J. Infect. Dis. 2000, 182:595-598.
19. Jeon S., Lambert P.F. Integration of human papillomavirus type 16 DNA into the human genome leads to increased stability of E6 and E7 mRNAs: implications for cervical carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:1654-1658.
20. Jeon S., et al. Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. J. Virol. 1995, 69:2989-2997.
21. Pett M., Coleman N. Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis?. J. Pathol. 2007, 212:356-367.
22. You J. Papillomavirus interaction with cellular chromatin. Biochim. Biophys. Acta 2010, 1799:192-199.
23. Melsheimer P., et al. DNA aneuploidy and integration of human papillomavirus type 16 e6/e7 oncogenes in intraepithelial neoplasia and invasive squamous cell carcinoma of the cervix uteri. Clin. Cancer Res. 2004, 10:3059-3063.
24. Romanczuk H., Howley P.M. Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:3159-3163.
25. Choo K.B., et al. Integration of human papillomavirus type 16 into cellular DNA of cervical carcinoma: preferential deletion of the E2 gene and invariable retention of the long control region and the E6/E7 open reading frames. Virology 1987, 161:259-261.
26. Bechtold V., et al. Human papillomavirus type 16 E2 protein has no effect on transcription from episomal viral DNA. J. Virol. 2003, 77:2021-2028.
27. Goodwin E.C., DiMaio D. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:12513-12518.
28. Hwang E.S., et al. Inhibition of cervical carcinoma cell line proliferation by the introduction of a bovine papillomavirus regulatory gene. J. Virol. 1993, 67:3720-3729.
29. Cricca M., et al. Viral DNA load, physical status and E2/E6 ratio as markers to grade HPV16 positive women for high-grade cervical lesions. Gynecol. Oncol. 2007, 106:549-557.
30. Cullen A.P., et al. Analysis of the physical state of different human papillomavirus DNAs in intraepithelial and invasive cervical neoplasm. J. Virol. 1991, 65:606-612.
31. Das B.C., et al. Analysis by polymerase chain reaction of the physical state of human papillomavirus type 16 DNA in cervical preneoplastic and neoplastic lesions. J. Gen. Virol. 1992, 73(Pt 9):2327-2336.
32. Hudelist G., et al. Physical state and expression of HPV DNA in benign and dysplastic cervical tissue: different levels of viral integration are correlated with lesion grade. Gynecol. Oncol. 2004, 92:873-880.
33. Kalantari M., et al. Physical state of HPV16 and chromosomal mapping of the integrated form in cervical carcinomas. Diagn. Mol. Pathol. 2001, 10:46-54.
34. Klaes R., et al. Detection of high-risk cervical intraepithelial neoplasia and cervical cancer by amplification of transcripts derived from integrated papillomavirus oncogenes. Cancer Res. 1999, 59:6132-6136.
35. Theelen W., et al. Human papillomavirus multiplex ligation-dependent probe amplification assay for the assessment of viral load, integration, and gain of telomerase-related genes in cervical malignancies. Hum. Pathol. 2013, 44:2410-2418.
36. Tonon S.A., et al. Physical status of the E2 human papilloma virus 16 viral gene in cervical preneoplastic and neoplastic lesions. J. Clin. Virol. 2001, 21:129-134.
37. Pett M.R., et al. Acquisition of high-level chromosomal instability is associated with integration of human papillomavirus type 16 in cervical keratinocytes. Cancer Res. 2004, 64:1359-1368.
38. Wentzensen N., et al. Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Res. 2004, 64:3878-3884.
39. Akagi K., et al. Genome-wide analysis of HPV integration in human cancers reveals recurrent, focal genomic instability. Genome Res. 2013, 24:185-199.
40. Ojesina A.I., et al. Landscape of genomic alterations in cervical carcinomas. Nature 2013, 506:371-375.
41. Thomas L.K., et al. Chromosomal gains and losses in human papillomavirus-associated neoplasia of the lower genital tract - a systematic review and meta-analysis. Eur. J. Cancer 2014, 50:85-98.
42. Lando M., et al. Gene dosage, expression, and ontology analysis identifies driver genes in the carcinogenesis and chemoradioresistance of cervical cancer. PLoS Genet. 2009, 5:e1000719.
43. Khan M.J., et al. The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of type-specific HPV testing in clinical practice. J. Natl. Cancer Inst. 2005, 97:1072-1079.
44. Mine K.L., et al. Gene network reconstruction reveals cell cycle and antiviral genes as major drivers of cervical cancer. Nat. Commun. 2013, 4:1806.
45. Perez-Diez A., et al. Microarrays for cancer diagnosis and classification. Adv. Exp. Med. Biol. 2007, 593:74-85.
46. Halle C., et al. Hypoxia-induced gene expression in chemoradioresistant cervical cancer revealed by dynamic contrast-enhanced MRI. Cancer Res. 2012, 72:5285-5295.
47. Harima Y., et al. Prediction of outcome of advanced cervical cancer to thermoradiotherapy according to expression profiles of 35 genes selected by cDNA microarray analysis. Int. J. Radiat. Oncol. Biol. Phys. 2004, 60:237-248.
48. Kitahara O., et al. Classification of sensitivity or resistance of cervical cancers to ionizing radiation according to expression profiles of 62 genes selected by cDNA microarray analysis. Neoplasia 2002, 4:295-303.
49. Lando M., et al. Identification of eight candidate target genes of the recurrent 3p12-p14 loss in cervical cancer by integrative genomic profiling. J. Pathol. 2013, 230:59-69.
50. Lyng H., et al. Gene expressions and copy numbers associated with metastatic phenotypes of uterine cervical cancer. BMC Genomics 2006, 7:268.
51. Sopov I., et al. Detection of cancer-related gene expression profiles in severe cervical neoplasia. Int. J. Cancer 2004, 112:33-43.
52. Kaczkowski B., et al. A decade of global mRNA and miRNA profiling of HPV-positive cell lines and clinical specimens. Open Virol. J. 2012, 6:216-231.
53. Koch M., Wiese M. Gene expression signatures of angiocidin and darapladib treatment connect to therapy options in cervical cancer. J. Cancer Res. Clin. Oncol. 2013, 139:259-267.
54. Rajkumar T., et al. Identification and validation of genes involved in cervical tumourigenesis. BMC Cancer 2011, 11:80.
55. Pe'er D., Hacohen N. Principles and strategies for developing network models in cancer. Cell 2011, 144:864-873.
56. Shulzhenko N., et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat. Med. 2011, 17:1585-1593.
57. Skinner J., et al. Construct and compare gene coexpression networks with DAPfinder and DAPview. BMC Bioinformatics 2011, 12:286.
58. Crosbie E.J., et al. Human papillomavirus and cervical cancer. Lancet 2013, 382:889-899.
59. Patel S., Chiplunkar S. Host immune responses to cervical cancer. Curr. Opin. Obstet. Gynecol. 2009, 21:54-59.
60. Pett M.R., et al. Selection of cervical keratinocytes containing integrated HPV16 associates with episome loss and an endogenous antiviral response. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3822-3827.
61. Herdman M.T., et al. Interferon-beta treatment of cervical keratinocytes naturally infected with human papillomavirus 16 episomes promotes rapid reduction in episome numbers and emergence of latent integrants. Carcinogenesis 2006, 27:2341-2353.
62. Chang Y.E., et al. Long-term effect of interferon on keratinocytes that maintain human papillomavirus type 31. J. Virol. 2002, 76:8864-8874.
63. Kaczkowski B., et al. Integrative analyses reveal novel strategies in HPV11, -16 and -45 early infection. Scientific Rep. 2012, 2:515.
64. Arai M., et al. The knockdown of endogenous replication factor C4 decreases the growth and enhances the chemosensitivity of hepatocellular carcinoma cells. Liver Int. 2009, 29:55-62.
65. Hong S., et al. Suppression of STAT-1 expression by human papillomaviruses is necessary for differentiation-dependent genome amplification and plasmid maintenance. J. Virol. 2011, 85:9486-9494.
66. Taylor M.W., et al. Changes in gene expression during pegylated interferon and ribavirin therapy of chronic hepatitis C virus distinguish responders from nonresponders to antiviral therapy. J. Virol. 2007, 81:3391-3401.
67. Kanao H., et al. Overexpression of LAMP3/TSC403/DC-LAMP promotes metastasis in uterine cervical cancer. Cancer Res. 2005, 65:8640-8645.
68. Rathinam V.A., et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 2010, 11:395-402.
69. Cheung T.H., et al. Dysregulated microRNAs in the pathogenesis and progression of cervical neoplasm. Cell Cycle 2012, 11:2876-2884.
70. Lee J.W., et al. Altered MicroRNA expression in cervical carcinomas. Clin. Cancer Res. 2008, 14:2535-2542.
71. Wang X., et al. Aberrant expression of oncogenic and tumor-suppressive microRNAs in cervical cancer is required for cancer cell growth. PLoS ONE 2008, 3:e2557.
72. Wilting S.M., et al. Altered microRNA expression associated with chromosomal changes contributes to cervical carcinogenesis. Oncogene 2013, 32:106-116.
73. Xie H., et al. miR-205 expression promotes cell proliferation and migration of human cervical cancer cells. PLoS ONE 2012, 7:e46990.
74. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
75. Pinto A.P., Crum C.P. Natural history of cervical neoplasia: defining progression and its consequence. Clin. Obstet. Gynecol. 2000, 43:352-362.
76. Vinokurova S., et al. Type-dependent integration frequency of human papillomavirus genomes in cervical lesions. Cancer Res. 2008, 68:307-313.
77. Das P., et al. HPV genotyping and site of viral integration in cervical cancers in Indian women. PLoS ONE 2012, 7:e41012.
78. Gray E., et al. In vitro progression of human papillomavirus 16 episome-associated cervical neoplasia displays fundamental similarities to integrant-associated carcinogenesis. Cancer Res. 2010, 70:4081-4091.
79. Guzman V.B., et al. New approach reveals CD28 and IFNG gene interaction in the susceptibility to cervical cancer. Hum. Mol. Genet. 2008, 17:1838-1844.
80. Ivansson E.L., et al. Interaction of immunological genes on chromosome 2q33 and IFNG in susceptibility to cervical cancer. Gynecol. Oncol. 2010, 116:544-548.
81. Ponten J., Guo Z. Precancer of the human cervix. Cancer Surv. 1998, 32:201-229.
82. Pachman D.R., et al. Randomized clinical trial of imiquimod: an adjunct to treating cervical dysplasia. Am. J. Obstet. Gynecol. 2012, 206. 42.e1-42.e7.
83. Roy S., et al. Defective dendritic cell generation from monocytes is a potential reason for poor therapeutic efficacy of interferon alpha2b (IFNalpha2b) in cervical cancer. Transl. Res. 2011, 158:200-213.
84. Boveri T. Über mehrpolige mitosen als mittel zur analyse des zellkerns. Verhandlungen der physicalisch-medizinischen Gesselschaft zu Würzburg 1902, 35:67-90.
85. Pennisi E. Microbiology. Gut bacteria lend a molecular hand to viruses. Science 2011, 334:168.
86. Arthur J.C., et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012, 338:120-123.
87. Iida N., et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 2013, 342:967-970.
88. Lee J.E., et al. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS ONE 2013, 8:e63514.
89. Chesson H.W., et al. Estimates of the annual direct medical costs of the prevention and treatment of disease associated with human papillomavirus in the United States. Vaccine 2012, 30:6016-6019.
90. Klussmann J.P., et al. Genetic signatures of HPV-related and unrelated oropharyngeal carcinoma and their prognostic implications. Clin. Cancer Res. 2009, 15:1779-1786.
91. Levin N.A., et al. Identification of novel regions of altered DNA copy number in small cell lung tumors. Genes Chromosomes Cancer 1995, 13:175-185.
92. Stanley M. Pathology and epidemiology of HPV infection in females. Gynecol. Oncol. 2010, 117:S5-S10.
93. Hafner N., et al. Integration of the HPV16 genome does not invariably result in high levels of viral oncogene transcripts. Oncogene 2008, 27:1610-1617.
94. Higgins G.D., et al. Transcription patterns of human papillomavirus type 16 in genital intraepithelial neoplasia: evidence for promoter usage within the E7 open reading frame during epithelial differentiation. J. Gen. Virol. 1992, 73(Pt 8):2047-2057.
95. Maitland N.J., et al. Expression patterns of the human papillomavirus type 16 transcription factor E2 in low- and high-grade cervical intraepithelial neoplasia. J. Pathol. 1998, 186:275-280.
96. Sotlar K., et al. Detection of high-risk human papillomavirus E6 and E7 oncogene transcripts in cervical scrapes by nested RT-polymerase chain reaction. J. Med. Virol. 2004, 74:107-116.
97. Xue Y., et al. HPV16 E2 is an immediate early marker of viral infection, preceding E7 expression in precursor structures of cervical carcinoma. Cancer Res. 2010, 70:5316-5325.
98. Bierkens M., et al. Chromosomal profiles of high-grade cervical intraepithelial neoplasia relate to duration of preceding high-risk human papillomavirus infection. Int. J. Cancer 2012, 131:E579-E585.