Human papillomavirus in head and neck squamous cell carcinoma: Are some head and neck cancers a sexually transmitted disease?

Current Opinion in Oncology

Volumn 11, Issue 3, 1999, Pages 191-199

  Gillison, Maura L ^a,b   Koch, Wayne M ^a,c   Shah, Keerti V ^b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE;

ALCOHOL CONSUMPTION; HEAD AND NECK CANCER; HUMAN; PRIORITY JOURNAL; REVIEW; SEXUALLY TRANSMITTED DISEASE; SQUAMOUS CELL CARCINOMA; TOBACCO; TUMOR DIFFERENTIATION; UTERINE CERVIX CANCER; WALDEYER RING; WART VIRUS;

CARCINOMA, SQUAMOUS CELL; DNA, VIRAL; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; MALE; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; RISK FACTORS; SEXUALLY TRANSMITTED DISEASES; TUMOR VIRUS INFECTIONS; UTERINE CERVICAL NEOPLASMS;

EID: 0032918220     PISSN: 10408746     EISSN: None     Source Type: Journal    
DOI: 10.1097/00001622-199905000-00010     Document Type: Review

References (110)

1. Landis S, Murray T, Bolden S, Wingo P: Cancer statistics, 1998. CA Cancer J Clin 1998, 48:6-29.
2. La Vecchia C, Tavani A, Franceschi S, Levi F, Corrao G, Negri E: Epidemiology and prevention of oral cancer. Oral Oncol 1997, 33:302-312.
3. La Vecchia C, Luccini F, Negri E, Boyle P, Levi F: Trends in cancer mortality, 1955-1989: Asia, Africa and Oceania. Eur J Cancer 1993, 29A:2168-2211.
4. Franceschi S, Talamini R, Barra S: Smoking and drinking in relation to cancers of the oral cavity, pharynx, larynx and esophagus in Northern Italy. Cancer Res 1990, 50:6502-6507.
5. Munoz N, Cardis E, Teuchmann S: Comparative epidemiological aspects of ano-genital cancers. In: Papillomaviruses in Human Pathology. Recent Progress in Epidermoid Precancers, vol. 78. Edited by Monsonego J. New York: Raven Press; 1990:1-12.
6. Bjorge T, Hennig E, Skare G, Soreide O, Thoresen S: Second primary cancers in patients with carcinoma in situ of the uterine cervix. Int J Cancer 1995, 62:29-33.
7. Rabkin C, Biggar R, Melbye M, Curtis R: Second primary cancers following anal and cervical carcinoma: evidence of shared etiologic factors. Am J Epidemiol 1992, 136:54-58.
8. Boice J, Day N, Andersen A, Briton L, Brown R, Choi N, et al.: Second cancers following radiation treatment for cervical cancer. An international collaboration among cancer registries. J Natl Cancer Inst 1985, 74:955-975.
9. zur Hausen H: Papillomavirus infections - a major cause of human cancers. Biochim Biophys Acta 1996, 1288:F55-F78.
10. Walboomers J, De Roda Husman A, Van Den Brule J, Snijders P, Meijer C: Detection of genital human papillomavirus infections: critical review of methods and prevalence studies in relation to cervical cancer. In: Human Papillomaviruses and Cervical Cancer: Biology and Immunology. Edited by Stern P, Stanley M. Oxford: Oxford University Press; 1994:41-71.
11. Ostwald C, Muller P, Barten M, Rutsatz K, Sonnenburg M, Milde-Langosch K, Loning T: Human papillomavirus DNA in oral squamous cell carcinomas and normal mucosa. J Oral Pathol Med 1994, 23:220-225.
12. Franceschi S, Munoz N, Bosch X, Snijders P, Walboomers J: Human papillomavirus and cancers of the upper aerodigestive tract: a review of epidemiological and experimental evidence. Cancer Epidemiol Biomarkers Prev 1996, 5:567-575.
13. Lawton G, Thomas S, Schonrock J, Monsour F, Frazer I: Human papillomavirus in normal oral mucosa: a comparison of methods for sample collection. J Oral Pathol Med 1992, 21:265-269.
14. Syrjanen S, Syrjanen K, Happonen R, Lamberg M: In situ DNA hybridization analysis of human papillomavirus sequences in benign oral mucosal lesions. Arch Dermatol Res 1987, 279:543-549.
15. Mounts P, Shah K, Kashima H: Viral etiology of juvenile and adult onset squamous papilloma of the larynx. Proc Natl Acad Sci USA 1982, 79:5425-5429.
16. Caruana S, Zwiebel N, Cocker R, McCormick S, Eberle R, Lazarus P: p53 alteration and human papillomavirus infection in paranasal sinus cancer. Cancer 1997, 79:1320-1328.
17. Galloway T, Soper G, Elsen G: Carcinoma of the larynx after irradiation for papilloma. Arch Otolaryngol 1960, 72:289-294.
18. McKaig R, Baric R, Olshan A: Human papillomavirus and head and neck cancer: epidemiology and molecular biology. Head Neck 1998, 20:250-265.
19. Van Rensburg E, Engelbracht S, Van Heerden W, Raubennheimer EJ, Schoub B: Human papillomavirus DNA in oral squamous cell carcinomas from an African population sample. Anticancer Res 1996, 16:969-974.
20. Chang F, Syrjanen S, Nuutinen J, Karja J, Syrjanen K: Detection of human papillomavirus (HPV) DNA in oral squamous cell carcinomas by in situ hybridization and polymerase chain reaction. Arch Dermatol Res 1990, 282:493-497.
21. Balaram P, Nalinakumari K, Abraham E, Balan A, Hareendran N, Bernard H-U, Chan S-Y: Human papillomavirus in 91 oral cancers from Indian betel quid chewers-high prevalence and multiplicity of infections. Int J Cancer 1995, 61:450-454.
22. Chang K, Chang C, Lai K, Chou M, Choo K: High prevalence of human papillomavirus infection and possible association with betel quid chewing and smoking in oral epidermoid carcinomas in Taiwan. J Med Virol 1989, 28:57-61.
23. Paz I, Cook N, Odom-Maryon T, Xie Y, Wilczynski S: Human papillomavirus (HPV) in head and neck cancer. An association of HPV 16 with squamous cell carcinoma of Waldeyer's tonsillar ring. Cancer 1997, 79:595-604.
24. Fouret P, Martin F, Flahault A, Lacau Saint-Guily J: Human papillomavirus infection in the malignant and premalignant head and neck epithelium. Diagn Mol Pathol 1995, 4:122-127.
25. Lie E, Karlsen F, Holm R: Presence of human papillomavirus in squamous cell laryngeal carcinomas. A study of thirty-nine cases using polymerase chain reaction and in situ hybridization. Acta Otolaryngol 1996, 116:900-905.
26. Brandwein MS, Nuovo G, Biller H: Analysis of prevalence of human papillomavirus in laryngeal carcinomas. Study of 40 cases using polymerase chain reaction and consensus primers. Ann Otol Rhinol Laryngol 1993, 102:309-313.
27. Kasperbauer J, O'Halloran G, Espy M, Smith T, Lewis J: Polymerase chain reaction identification of human papillomavirus DNA in verrucous carcinoma of the larynx. Laryngoscope 1993, 103:416-420.
28. Perez-Ayala M, Ruiz-Cabeelo R, Esteban F, Concha A, Redondo M, Oliva M, Cabrera T, Garrido F: Presence of HPV 16 sequences in laryngeal carcinomas. Int J Cancer 1990, 46:8-11.
29. Brandsma J, Abramson A: Association of papillomavirus with cancers of the head and neck. Arch Otolaryngol Head Neck Surg 1989, 115:621-625.
30. Fouret P, Monceaux G, Teman S, Lacourreye L, Lacau St Guily J: Human papillomavirus in head and neck squamous cell carcinomas in nonsmokers. Arch Otolaryngol Head Neck Surg 1997, 123:513-516.
31. Schwartz S, Daling J, Doody D, Wipf G, Carter J, Madeleine M, et al.: Oral cancer risk in relation to sexual history and evidence of human papillomavirus infection. J Natl Cancer Inst 1998, 90:1626-1636. The authors provide the most thorough evaluation of risk factor exposures (including sexual behaviors, HPV infection, alcohol, and tobacco) and HNSCC development available to date.
32. Steinberg B, DiLorenzo T: A possible role for human papillomaviruses in head and neck cancer. Cancer Metastasis Rev 1996, 15:91-112.
33. Niedobitek G, Pitteroff S, Herbst H, Shepard P, Finn T, Anagnostopoulos I, Stein H: Detection of human papillomavirus type 16 DNA in carcinomas of the palatine tonsil. J Clin Pathol 1990, 43:918-921.
34. Snijders P, Cromme F, Van Den Brule A, Schrijnemakers H, Snow G, Meijer C, Walboomers J: Prevalence and expression of human papillomavirus in tonsillar carcinomas, indicating a possible viral etiology. Int J Cancer 1992, 51:845-850.
35. IARC: IARC Monograph on the Evaluation of Carcinogenic Risks to Humans. In Human Papillomaviruses, vol. 64. Lyon, France: International Agency for Research on Cancer; 1995.
36. Snijders P, Scholes A, Hart C, Jones A, Vaughan E, Woolgar J, et al.: Prevalence of mucosotropic human papillomaviruses in squamous-cell carcinomas of the head and neck. Int J Cancer 1996, 66:464-469.
37. Steenbergen R, Hermsen M, Walboomers J, Joenje H, Arwert F, Meijer C, Snijders P: Integrated human papillomavirus type 16 and loss of heterozygosity at 11q22 and 18q21 in an oral carcinoma and its derivative cell line. Cancer Res 1995, 55:5465-5471.
38. Kahn T, Turazza E, Ojeda R, Bercovich A, Stremlau A, Lichter P, et al.: Integration of human papillomavirus type 6a DNA in a tonsillar carcinoma: chromosomal localization and nucleotide sequence of the genomic target region. Cancer Res 1994, 54:1305-1312.
39. Snijders P, Meijer C, van den Brule A, Schrijnemakers H, Snow G, Walboomers J: Human papillomavirus (HPV) type 16 and 33 E6/E7 region transcripts in tonsillar carcinomas can originate from integrated and episomal HPV DNA. J Gen Virol 1992, 73:2059-2066.
40. Fouret P, Dabit D, Sibony M, Alili D, Commo F, Saint-Guily J, Callard P: Expression of p53 protein related to the presence of human papillomavirus infection in precancer lesions of the larynx. Am J Pathol 1995, 146:599-604.
41. Miller C, White D: Human papillomavirus expression in oral mucosa, premalignant conditions, and squamous cell carcinoma. A retrospective review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996, 82:57-68.
42. Wilczynski S, Lin B, Xie Y, Paz B: Detection of human papillomavirus DNA and oncoprotein overexpression are associated with distinct morphological patterns of tonsillar squamous cell carcinoma. Am J Pathol 1998, 152:145-156.
43. Andl T, Kahn T, Pfuhl A, Nicola T, Erber R, Conradt C, et al.: Etiological involvement of oncogenic human papillomavirus in tonsillar squamous cell carcinomas lacking retinoblastoma cell cycle control. Cancer Res 1998, 58:5-13.
44. Brandwein M, Zeitlin J, Nuovo G, MacConell P, Bodian C, Urken M, Biller H: HPV detection using "hot start" polymerase chain reaction in patients with oral cancer: a clinicopathologic study of 64 patients. Mod Pathol 1994, 7:720-727.
45. Trimble C, Hildesheim A, Briton L, Shah K, Kurman R: Heterogeneous etiology of squamous cell carcinoma of the vulva. Obstet Gynecol 1996, 87:59-64.
46. Kurman R, Toki T, Schiffman M: Basaloid and warty carcinomas of the vulva: distinctive types of squamous cell carcinoma frequently associated with human papillomavirus. J Surg Pathol 1993, 17:133-145.
47. Watanabe S, Ogura H, Fukushima K, Yabe Y: Comparison of Virapap filter hybridization with polymerase chain reaction and Southern blot hybridization methods for detection of human papillomavirus in tonsillar and pharyngeal cancers. Eur Arch Otorhinolaryngol 1993, 250:115-119.
48. Maden C, Beckman A, Thomas D, McKnight B, Sherman K, Ashley R, et al.: Human papillomaviruses, herpes simplex viruses, and the risk of oral cancer in men. Am J Epidemiol 1992, 135:1093-1102.
49. Smith E, Hoffman H, Summersgill K, Kirchner H, Turek L, Haugen T: Human papillomavirus and risk of oral cancer. Laryngoscope 1998, 108:1098-1103.
50. Watts D, Koutsky L, Holmes K, Goldman D, Kuypers J, Kiviat N, Gallway D: Low risk of perinatal transmission of human papillomavirus: results from a prospective cohort study. Am J Obstet Gynecol 1998, 178:365-373.
51. Koch A, Hansen S, Nielsen N, Palefsky J, Melbye M: HPV detection in children prior to sexual debut. Int J Cancer 1997, 73:621-624.
52. Kellokoski J, Syrjanen S, Syrjanen K, Yliskoski M: Oral mucosal changes in women with genital HPV infection. J Oral Pathol Med 1990, 19:142-148.
53. Kellokoski J, Syrjanen S, Chang F, Yliskoski M, Syrjanen K: Southern blot hybridization and PCR detection of oral human papillomavirus (HPV) infections in women with genital HPV infections. J Oral Pathol Med 1992, 21:459-464.
54. Premoli-De-Percoco G, Ramirez J, Galindo I: Correlation between HPV types associated with oral squamous cell carcinoma and cervicovaginal cytology. An in situ hybridization study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998, 86:77-81.
55. Ho G, Bierman R, Beardsley L, Chang C, Burk R: Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998, 338:423-428.
56. McIndoe W, McLean M, Jones R: The invasive potential of carcinoma in situ of the cervix. Obstet Gynecol 1984, 64:451-458.
57. Kottmeier H: Evolution et traitment des epitheliomas. Rev Fran Gynechol d'Obstet 1961, 56:821-826.
58. Shah K, Viscidi R, Alberg A, Helzlsouer K, Comslock G: Antibodies to human papillomavirus 16 and subsequent in situ or invasive cancer of the cervix. Cancer Epidemiol Biomarkers Prev 1997, 6:233-237.
59. Bosch F, Manos M, Munoz N, Sherman M, Jansen A, Peto J, et al., Group IBSoCCIS: Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. J Natl Cancer Inst 1995, 87:796-803.
60. Galloway D, McDougall J: The disruption of cell cycle checkpoints by papillomavirus oncoprofeins contributes to anogenital neoplasia. Semin Cancer Biol 1996, 7:309-315.
61. McDougall J: Immortalization and transformation of human cells by human papillomavirus. Curr Top Microbiol Immunol 1994, 186:101-119.
62. Woodworth C, Cheng S, Simpson S, Hamsacher L, Chow L, Broker T, DiPaulo J: Recombinant retroviruses encoding human papillomavirus type 18 E6 and E7 genes stimulate and delay differentiation of human keratinocytes early after infection. Oncogene 1992, 7:619-626.
63. Havre P, Yuan J, Hedrick L, Cho K, Glazer P: p53 inactivation by HPV 16 E6 results in increased mutagenesis in human cells. Cancer Res 1995, 55:4420-4424.
64. Liu X, Han S, Baluda M, Park N: HPV-16 oncogenes E6 and E7 are mutagenic in normal human oral keratinocytes. Oncogene 1997, 14:2347-2353.
65. White A, Livanos E, Tlsty T: Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev 1994, 8:666-677.
66. Hashida T, Yasumoto S: Induction of chromosomal abnormalities in mouse and human keratinocytes by the human papillomavirus type 16 E7 oncogene. J Gen Virol 1991, 72:1569-1577.
67. Schwartz E, Freese U, Gissman L, Mayer W, Roggenbuck B, Stremlau A, zur Hausen H: Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985, 314:111-114.
68. Crook T, Morgenstern J, Crawford L, Banks L: Continued expression of HPV-16 E7 protein is required for maintenance of the transformed phenotype of cells co-transformed by HPV-16 plus EJ-ras. EMBO J 1989, 8:513-519.
69. Rapp L, Chen J: The papillomavirus E6 proteins. Biochim Biophys Acta 1998, 1378:F1-F19.
70. Huibregtse J, Beaudenon S: Mechanism of HPV E6 proteins in cellular transformation. Semin Cancer Biol 1996, 7:317-326.
71. Jones D, Munger K: Interactions of the human papillomavirus E7 protein with cell cycle regulators. Semin Cancer Biol 1996, 7:327-337.
72. Scheffner M, Huibregtse J, Vierstra R, Howley P: The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993, 75:495-505.
73. Werness B, Levine A, Howley P: Association of human papillomavirus types 16 and 18 E6 protein with p53. Science 1990, 248:76-79.
74. Kessis T, Slebos R, Nelson W, Kastan M, Plunkett B, Han S, et al.: Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc Natl Acad Sci U S A 1993, 90:3988-3992.
75. Kubbutat M, KH V: New HPV E6 binding proteins: dangerous liaisons? Trends Microbiol 1998, 6:5-7.
76. Klingelhutz A, Foster S, McDougall J: Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 1996, 380:79-81.
77. Groos-Mesilaty S, Reinstein E, Bercovich B, Tobias K, Schwartz A, Kahana C, Ciechanover A: Basal and human papillomavirus E6 oncoprotein-induced degradation of Myc proteins by the ubiquitin pathway. Proc Natl Acad Sci U S A 1998, 95:8058-8063.
78. Munger K, Werness B, Dyson N, Phelps W, Harlow E, Howley P: Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J 1989, 8:4099-4105.
79. Lee J, Russo A, Pavletich N: Structure of the retinoblastoma tumor-suppressor pocket domain bound to a peptide from HPV E7. Nature 1998, 391:859-865. The crystal structure of the HPV-16 E7 peptide with the pRb pocket domain could conceivably lead to development of "small molecules" capable of targeting this interaction for therapeutic purposes.
80. Nevins J: E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 1992, 258:424-429.
81. Jones D, Munger K: Analysis of the p53-mediated G1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J Virol 1997, 71:2905-2912.
82. Demers G, Foster S, Halbert C, Gallway D: Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7. Proc Natl Acad Sci U S A 1994, 91:4382-4386.
83. Slebos R, Lee M, Plunkett B, Kessis T, Williams B, Jacks T, Hedrick L, Kastan M, Cho K: p53-dependent G1 arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoprotein. Proc Natl Acad Sci U S A 1994, 91:5320-5324.
84. El-Diery W, Tokino T, Velculescu V, Levy D, Parsons R, Trent J, Lin D, Mercer W, Kinzler K, Vogelstien B: WAF1, a potential mediator of p53 tumor suppression. Cell 1993, 75:817-825.
85. Funk J, Waga S, Harry J, Espling E, Stillman B, Galloway D: Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 oncoprotein. Genes Dev 1997, 11:2090-2100.
86. Jones D, Alani R, Munger K: The human papillomavirus E7 oncoprotein can uncouple cellular differentiation and proliferation in human keratinocytes by abrogating p21 -mediated inhibition of cdk2. Genes Dev 1997, 11:2101-2111.
87. Sidransky D: Molecular genetics of head and neck cancer. Curr Opin Oncol 1995, 7:229-233.
88. Nawroz H, Riet V, Hruban R, Koch W, Ruppert J, Sidransky D: Allelotype of head and neck squamous cell carcinoma. Cancer Res 1994, 54:1152-1155.
89. Ah-See K, Cooke T, Pickford I, Soutar D, Balmain A: An allelotype of squamous carcinoma of the head and neck using microsatellite markers. Cancer Res 1994, 54:1617-1621.
90. Bockmuhl U, Wolf G, Schmidt S, Schwendel A, Jahnke V, Dielel M, Petersen I: Genomic alterations associated with malignancy in head and neck cancer. Head Neck 1998, 20:145-151.
91. Liggett W, Sidransky D: Role of p16 tumor suppressor gene in cancer. J Clin Oncol 1998, 16:1197-1206.
92. Denissenko M, Pao A, Tang M, Pfeifer G: Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in p53. Science 1996, 274:430-432.
93. Brennan J, Boyle J, Koch W, Goodman S, Hruban R, Eby Y, et al.: Association between cigarette smoking and mutation of p53 gene in squamous-cell carcinoma of the head and neck. N Engl J Med 1995, 332:712-717.
94. Salam M, Rockett J, Morris A: The prevalence of different human papillomavirus types and p53 mutations in laryngeal carcinomas: is there a reciprocal relationship? Eur J Surg Oncol 1995, 21:290-296.
95. Chiba I, Shindoh M, Yasuda M, Yamazaki Y, Amemiya A, Sato Y, et al.: Mutations in the p53 gene and human papillomavirus infection as significant prognostic factors in squamous cell carcinomas of the oral cavity. Oncogens 1996, 12:1663-1668.
96. Snijders P, Steenbergen R, Top B, Scott S, Meijer C, Walboorners JMM: Analysis of p53 status in tonsillar carcinomas associated with human papillomavirus. J Gen Virol 1994, 75:2769-2775.
97. Scholes A, Lilogou T, Snijders P, Hart C, Jones A, Woolgar J, et al.: p53 mutations in relation to human papillomavirus type 16 infection in squamous cell carcinomas of the head and neck. Int J Cancer 1997, 71:796-799.
98. Brachman D, Graves D, Vokes E, Beckett M, Haraf D, Montag A, et al.: Occurrence of p53 gene deletions and human papilloma virus infection in human head and neck cancer. Cancer Res 1992, 52:4832-4836.
99. Crook T, Ludwig R, Marston N, Willkomm D, Vousden K: Sensitivity of p53 lysine mutants to ubiquitin-directed degradation targeted by human papillomavirus E6. Virology 1996, 217:285-292.
100. Gardiol D, Banks L: Comparison of human papillomavirus type 18 (HPV-18) E6-mediated degradation of p53 in vitro and in vivo reveals significant differences based on p53 structure and cell type but little difference with respect to mutants of HPV-18 E6. J Gen Virol 1998, 79:1963-1970.
101. Storey A, Thomas M, Kalita A, Harwood C, Gardiol D, Mantovani F, et al.: Role of p53 polymorphism in the development of human papillomavirus-associated cancer. Nature 1998, 303:229-234. Storey et al. suggested that common p53 polymorphisms in the population could affect individual risk for development of HPV-associated cancers. Unconfirmed by two subsequent reports (Rosenthal et al., Lancet 1998, 352:871-872 and Minaguchi et al., Cancer Res 1998, 58:4585-4586), this paper has stimulated much research, discussion, and controversy.
102. Rosenthal A, Ryan A, Al-Jehani R, Storey A, Harwood C, Jacobs I: p53 codon 72 polymorphism and risk of cervical cancer in UK. Lancet 1998, 352:871-872.
103. Minaguchi T, Kanamori Y, Matsushima M, Yoshikawa H, Tekatani Y, Nakamura Y: No evidence of correlation between polymorphism at codon 72 of p53 and risk of cervical cancer in Japanese patients with human papillomavirus 16/18. Cancer Res 1998, 58:4585-4586.
104. Magal S, Jackman A, Pei X, Schlegel R, Sherman L: Induction of apoptosis in human keratinocytes containing mutated p54 alleles and its inhibition by both the E6 and E7 oncoproteins. Int J Cancer 1998, 75:96-104.
105. Song S, Gulliver G, Lambert P: Human papillomavirus type 16 E6 and E7 oncogenes abrogate radiation-induced DNA damage responses in vivo through p53-dependent and p53-independent pathways. Proc Natl Acad Sci U S A 1998, 95:2290-2295. This paper provides evidence that HPVs can disrupt cellular control of the cell cycle by as yet undetermined mechanisms. Further research could not only provide insight into HPV-mediated tumorigenesis, but also identify other cellular genes important in control of cell cycle regulation, DNA repair, and induction of apoptosis.
106. Ho G, Kadish A, Burk R, Basu J, Palan P, Mikhail M, Romney S: HPV 16 and cigarette smoking as risk factors for high-grade cervical intra-epithelial neoplasia. Int J Cancer 1998, 78:281-285.
107. Prokopczyk B, Cox J, Hoffman D, Waggoner S: Identification of tobacco-specific carcinogen in the cervical mucus of smokers and nonsmokers. J Natl Cancer Inst 1997, 89:868-873.
108. Park N, Gujuluva C, Baek J, Cherrick H, Shin K, Min B: Combined oral carcinogenicity of HPV-16 and benzo(a)pyrene: an in vitro multistep carcinogenesis model. Oncogene 1995, 10:2145-2153.
109. Shin K, Tannyhill R, Liu X, Park N: Oncogenic transformation of HPV-immortalized human keratinocytes is associated with the genetic instability of cells. Oncogene 1996, 12:1089-1096.
110. Gerrett L, Perez-Reyes N, Smith P, McDougall J: Interaction of HPV-18 and nitrosomethylurea in the induction of squamous cell carcinoma. Carcinogenesis 1993, 14:329-332.