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. 1991 Jul;4(3):270–285. doi: 10.1128/cmr.4.3.270

Pathobiology of papillomavirus-related cervical diseases: prospects for immunodiagnosis.

C P Crum 1, S Barber 1, J K Roche 1
PMCID: PMC358199  PMID: 1653642

Abstract

In recent years, the relationship between human papillomaviruses (HPV) and genital neoplasia has been explored intensively, and a molecular basis for the role of HPV in the genesis of these diseases has been convincingly demonstrated. These findings have provided justification for efforts to apply this molecular information to the early detection and possible prevention of HPV-related neoplasia. The technology of detecting viral nucleic acids in genital fluids brought with it initial hopes that it would serve to identify women at risk for having or developing precancers or cancers of the cervix. Subsequent studies, however, have demonstrated limitations of the technology for predicting future disease. Recently, molecular immunology has complemented these prior efforts, with the intent to identify serological indices of exposure to HPV and perhaps delineate individuals at risk. The molecular basis for this approach, its limitations, and future prospects for immunodiagnosis are the subject of this review.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abramson A. L., Steinberg B. M., Winkler B. Laryngeal papillomatosis: clinical, histopathologic and molecular studies. Laryngoscope. 1987 Jun;97(6):678–685. doi: 10.1288/00005537-198706000-00005. [DOI] [PubMed] [Google Scholar]
  2. Beckmann A. M., Daling J. R., Sherman K. J., Maden C., Miller B. A., Coates R. J., Kiviat N. B., Myerson D., Weiss N. S., Hislop T. G. Human papillomavirus infection and anal cancer. Int J Cancer. 1989 Jun 15;43(6):1042–1049. doi: 10.1002/ijc.2910430615. [DOI] [PubMed] [Google Scholar]
  3. Boshart M., Gissmann L., Ikenberg H., Kleinheinz A., Scheurlen W., zur Hausen H. A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. EMBO J. 1984 May;3(5):1151–1157. doi: 10.1002/j.1460-2075.1984.tb01944.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cason J., Patel D., Naylor J., Lunney D., Shepherd P. S., Best J. M., McCance D. J. Identification of immunogenic regions of the major coat protein of human papillomavirus type 16 that contain type-restricted epitopes. J Gen Virol. 1989 Nov;70(Pt 11):2973–2987. doi: 10.1099/0022-1317-70-11-2973. [DOI] [PubMed] [Google Scholar]
  5. Cauda R., Tyring S. K., Grossi C. E., Tilden A. B., Hatch K. D., Sams W. M., Jr, Baron S., Whitley R. J. Patients with condyloma acuminatum exhibit decreased interleukin-2 and interferon gamma production and depressed natural killer activity. J Clin Immunol. 1987 Jul;7(4):304–311. doi: 10.1007/BF00915552. [DOI] [PubMed] [Google Scholar]
  6. Chardonnet Y., Viac J., Staquet M. J., Thivolet J. Cell-mediated immunity to human papillomavirus. Clin Dermatol. 1985 Oct-Dec;3(4):156–164. doi: 10.1016/0738-081x(85)90060-4. [DOI] [PubMed] [Google Scholar]
  7. Chen E. Y., Howley P. M., Levinson A. D., Seeburg P. H. The primary structure and genetic organization of the bovine papillomavirus type 1 genome. Nature. 1982 Oct 7;299(5883):529–534. doi: 10.1038/299529a0. [DOI] [PubMed] [Google Scholar]
  8. Chen S. L., Mounts P. Transforming activity of E5a protein of human papillomavirus type 6 in NIH 3T3 and C127 cells. J Virol. 1990 Jul;64(7):3226–3233. doi: 10.1128/jvi.64.7.3226-3233.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Christensen N. D., Kreider J. W. Antibody-mediated neutralization in vivo of infectious papillomaviruses. J Virol. 1990 Jul;64(7):3151–3156. doi: 10.1128/jvi.64.7.3151-3156.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Christensen N. D., Kreider J. W., Cladel N. M., Galloway D. A. Immunological cross-reactivity to laboratory-produced HPV-11 virions of polysera raised against bacterially derived fusion proteins and synthetic peptides of HPV-6b and HPV-16 capsid proteins. Virology. 1990 Mar;175(1):1–9. doi: 10.1016/0042-6822(90)90180-y. [DOI] [PubMed] [Google Scholar]
  11. Crum C. P., Barber S., Symbula M., Snyder K., Saleh A. M., Roche J. K. Coexpression of the human papillomavirus type 16 E4 and L1 open reading frames in early cervical neoplasia. Virology. 1990 Sep;178(1):238–246. doi: 10.1016/0042-6822(90)90399-c. [DOI] [PubMed] [Google Scholar]
  12. Crum C. P., Egawa K., Barron B., Fenoglio C. M., Levine R. U., Richart R. M. Human papilloma virus infection (condyloma) of the cervix and cervical intraepithelial neoplasia: a histopathologic and statistical analysis. Gynecol Oncol. 1983 Feb;15(1):88–94. doi: 10.1016/0090-8258(83)90120-8. [DOI] [PubMed] [Google Scholar]
  13. Crum C. P., Mitao M., Levine R. U., Silverstein S. Cervical papillomaviruses segregate within morphologically distinct precancerous lesions. J Virol. 1985 Jun;54(3):675–681. doi: 10.1128/jvi.54.3.675-681.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Crum C. P., Nuovo G., Friedman D., Silverstein S. J. Accumulation of RNA homologous to human papillomavirus type 16 open reading frames in genital precancers. J Virol. 1988 Jan;62(1):84–90. doi: 10.1128/jvi.62.1.84-90.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Crum C. P., Symbula M., Ward B. E. Topography of early HPV 16 transcription in high-grade genital precancers. Am J Pathol. 1989 Jun;134(6):1183–1188. [PMC free article] [PubMed] [Google Scholar]
  16. DiMaio D., Guralski D., Schiller J. T. Translation of open reading frame E5 of bovine papillomavirus is required for its transforming activity. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1797–1801. doi: 10.1073/pnas.83.6.1797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dillner J., Dillner L., Robb J., Willems J., Jones I., Lancaster W., Smith R., Lerner R. A synthetic peptide defines a serologic IgA response to a human papillomavirus-encoded nuclear antigen expressed in virus-carrying cervical neoplasia. Proc Natl Acad Sci U S A. 1989 May;86(10):3838–3841. doi: 10.1073/pnas.86.10.3838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dillner J., Dillner L., Utter G., Eklund C., Rotola A., Costa S., DiLuca D. Mapping of linear epitopes of human papillomavirus type 16: the L1 and L2 open reading frames. Int J Cancer. 1990 Mar 15;45(3):529–535. doi: 10.1002/ijc.2910450326. [DOI] [PubMed] [Google Scholar]
  19. Dillner J. Mapping of linear epitopes of human papillomavirus type 16: the E1, E2, E4, E5, E6 and E7 open reading frames. Int J Cancer. 1990 Oct 15;46(4):703–711. doi: 10.1002/ijc.2910460426. [DOI] [PubMed] [Google Scholar]
  20. Dillner L., Bekassy Z., Jonsson N., Moreno-Lopez J., Blomberg J. Detection of IgA antibodies against human papillomavirus in cervical secretions from patients with cervical intraepithelial neoplasia. Int J Cancer. 1989 Jan 15;43(1):36–40. doi: 10.1002/ijc.2910430109. [DOI] [PubMed] [Google Scholar]
  21. Doorbar J., Campbell D., Grand R. J., Gallimore P. H. Identification of the human papilloma virus-1a E4 gene products. EMBO J. 1986 Feb;5(2):355–362. doi: 10.1002/j.1460-2075.1986.tb04219.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Doorbar J., Coneron I., Gallimore P. H. Sequence divergence yet conserved physical characteristics among the E4 proteins of cutaneous human papillomaviruses. Virology. 1989 Sep;172(1):51–62. doi: 10.1016/0042-6822(89)90106-2. [DOI] [PubMed] [Google Scholar]
  23. Dunn J. E., Jr, Crocker D. W., Rube I. F., Erickson C. C., Coleman S. A. Cervical cancer occurrence in Memphis and Shelby County, Tennessee, during 25 years of its cervical cytology screening program. Am J Obstet Gynecol. 1984 Dec 1;150(7):861–864. doi: 10.1016/0002-9378(84)90463-0. [DOI] [PubMed] [Google Scholar]
  24. Dyson N., Howley P. M., Münger K., Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science. 1989 Feb 17;243(4893):934–937. doi: 10.1126/science.2537532. [DOI] [PubMed] [Google Scholar]
  25. Dürst M., Gissmann L., Ikenberg H., zur Hausen H. A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3812–3815. doi: 10.1073/pnas.80.12.3812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Eriksen K. Treatment of the common wart by induced allergic inflammation. Dermatologica. 1980;160(3):161–166. doi: 10.1159/000250490. [DOI] [PubMed] [Google Scholar]
  27. Ferenczy A., Mitao M., Nagai N., Silverstein S. J., Crum C. P. Latent papillomavirus and recurring genital warts. N Engl J Med. 1985 Sep 26;313(13):784–788. doi: 10.1056/NEJM198509263131304. [DOI] [PubMed] [Google Scholar]
  28. Firzlaff J. M., Kiviat N. B., Beckmann A. M., Jenison S. A., Galloway D. A. Detection of human papillomavirus capsid antigens in various squamous epithelial lesions using antibodies directed against the L1 and L2 open reading frames. Virology. 1988 Jun;164(2):467–477. doi: 10.1016/0042-6822(88)90561-2. [DOI] [PubMed] [Google Scholar]
  29. Franquemont D. W., Ward B. E., Andersen W. A., Crum C. P. Prediction of 'high-risk' cervical papillomavirus infection by biopsy morphology. Am J Clin Pathol. 1989 Nov;92(5):577–582. doi: 10.1093/ajcp/92.5.577. [DOI] [PubMed] [Google Scholar]
  30. Fu Y. S., Braun L., Shah K. V., Lawrence W. D., Robboy S. J. Histologic, nuclear DNA, and human papillomavirus studies of cervical condylomas. Cancer. 1983 Nov 1;52(9):1705–1711. doi: 10.1002/1097-0142(19831101)52:9<1705::aid-cncr2820520926>3.0.co;2-d. [DOI] [PubMed] [Google Scholar]
  31. Fu Y. S., Huang I., Beaudenon S., Ionesco M., Barrasso R., de Brux J., Orth G. Correlative study of human papillomavirus DNA, histopathology and morphometry in cervical condyloma and intraepithelial neoplasia. Int J Gynecol Pathol. 1988;7(4):297–307. doi: 10.1097/00004347-198812000-00001. [DOI] [PubMed] [Google Scholar]
  32. Genner J. Verrucae vulgares. II. Demonstration of a complement fixation reaction. Acta Derm Venereol. 1971;51(5):365–373. [PubMed] [Google Scholar]
  33. Gissmann L., deVilliers E. M., zur Hausen H. Analysis of human genital warts (condylomata acuminata) and other genital tumors for human papillomavirus type 6 DNA. Int J Cancer. 1982 Feb 15;29(2):143–146. doi: 10.1002/ijc.2910290205. [DOI] [PubMed] [Google Scholar]
  34. Head J. R., Billingham R. E. Concerning the immunology of the uterus. Am J Reprod Immunol Microbiol. 1986 Mar;10(3):76–81. [PubMed] [Google Scholar]
  35. Hildesheim A., Reeves W. C., Brinton L. A., Lavery C., Brenes M., De La Guardia M. E., Godoy J., Rawls W. E. Association of oral contraceptive use and human papillomaviruses in invasive cervical cancers. Int J Cancer. 1990 May 15;45(5):860–864. doi: 10.1002/ijc.2910450513. [DOI] [PubMed] [Google Scholar]
  36. Höpfl R., Sandbichler M., Sepp N., Heim K., Müller-Holzner E., Wartusch B., Dapunt O., Jochmus-Kudielka I., ter Meulen J., Gissmann L. Skin test for HPV type 16 proteins in cervical intraepithelial neoplasia. Lancet. 1991 Feb 9;337(8737):373–374. doi: 10.1016/0140-6736(91)91014-l. [DOI] [PubMed] [Google Scholar]
  37. Jenison S. A., Firzlaff J. M., Langenberg A., Galloway D. A. Identification of immunoreactive antigens of human papillomavirus type 6b by using Escherichia coli-expressed fusion proteins. J Virol. 1988 Jun;62(6):2115–2123. doi: 10.1128/jvi.62.6.2115-2123.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Jenison S. A., Yu X. P., Valentine J. M., Galloway D. A. Human antibodies react with an epitope of the human papillomavirus type 6b L1 open reading frame which is distinct from the type-common epitope. J Virol. 1989 Feb;63(2):809–818. doi: 10.1128/jvi.63.2.809-818.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Jenison S. A., Yu X. P., Valentine J. M., Koutsky L. A., Christiansen A. E., Beckmann A. M., Galloway D. A. Evidence of prevalent genital-type human papillomavirus infections in adults and children. J Infect Dis. 1990 Jul;162(1):60–69. doi: 10.1093/infdis/162.1.60. [DOI] [PubMed] [Google Scholar]
  40. Jenson A. B., Rosenthal J. D., Olson C., Pass F., Lancaster W. D., Shah K. Immunologic relatedness of papillomaviruses from different species. J Natl Cancer Inst. 1980 Mar;64(3):495–500. [PubMed] [Google Scholar]
  41. Jochmus-Kudielka I., Schneider A., Braun R., Kimmig R., Koldovsky U., Schneweis K. E., Seedorf K., Gissmann L. Antibodies against the human papillomavirus type 16 early proteins in human sera: correlation of anti-E7 reactivity with cervical cancer. J Natl Cancer Inst. 1989 Nov 15;81(22):1698–1704. doi: 10.1093/jnci/81.22.1698. [DOI] [PubMed] [Google Scholar]
  42. KOSS L. G., DURFEE G. R. Unusual patterns of squamous epithelium of the uterine cervix: cytologic and pathologic study of koilocytotic atypia. Ann N Y Acad Sci. 1956 Mar 30;63(6):1245–1261. doi: 10.1111/j.1749-6632.1956.tb32134.x. [DOI] [PubMed] [Google Scholar]
  43. Kessler I. I. Human cervical cancer as a venereal disease. Cancer Res. 1976 Feb;36(2 Pt 2):783–791. [PubMed] [Google Scholar]
  44. Kienzler J. L. Humoral immunity to human papillomaviruses. Clin Dermatol. 1985 Oct-Dec;3(4):144–155. doi: 10.1016/0738-081x(85)90059-8. [DOI] [PubMed] [Google Scholar]
  45. Kiviat N. B., Koutsky L. A., Paavonen J. A., Galloway D. A., Critchlow C. W., Beckmann A. M., McDougall J. K., Peterson M. L., Stevens C. E., Lipinski C. M. Prevalence of genital papillomavirus infection among women attending a college student health clinic or a sexually transmitted disease clinic. J Infect Dis. 1989 Feb;159(2):293–302. doi: 10.1093/infdis/159.2.293. [DOI] [PubMed] [Google Scholar]
  46. Kjaer S. K., Engholm G., Teisen C., Haugaard B. J., Lynge E., Christensen R. B., Møller K. A., Jensen H., Poll P., Vestergaard B. F. Risk factors for cervical human papillomavirus and herpes simplex virus infections in Greenland and Denmark: a population-based study. Am J Epidemiol. 1990 Apr;131(4):669–682. doi: 10.1093/oxfordjournals.aje.a115551. [DOI] [PubMed] [Google Scholar]
  47. Kjaer S. K., Teisen C., Haugaard B. J., Lynge E., Christensen R. B., Møller K. A., Jensen H., Poll P., Vestergaard B. F., de Villiers E. M. Risk factors for cervical cancer in Greenland and Denmark: a population-based cross-sectional study. Int J Cancer. 1989 Jul 15;44(1):40–47. doi: 10.1002/ijc.2910440108. [DOI] [PubMed] [Google Scholar]
  48. Kjaer S. K., de Villiers E. M., Haugaard B. J., Christensen R. B., Teisen C., Møller K. A., Poll P., Jensen H., Vestergaard B. F., Lynge E. Human papillomavirus, herpes simplex virus and cervical cancer incidence in Greenland and Denmark. A population-based cross-sectional study. Int J Cancer. 1988 Apr 15;41(4):518–524. doi: 10.1002/ijc.2910410408. [DOI] [PubMed] [Google Scholar]
  49. Komly C. A., Breitburd F., Croissant O., Streeck R. E. The L2 open reading frame of human papillomavirus type 1a encodes a minor structural protein carrying type-specific antigens. J Virol. 1986 Nov;60(2):813–816. doi: 10.1128/jvi.60.2.813-816.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Koutsky L. A., Galloway D. A., Holmes K. K. Epidemiology of genital human papillomavirus infection. Epidemiol Rev. 1988;10:122–163. doi: 10.1093/oxfordjournals.epirev.a036020. [DOI] [PubMed] [Google Scholar]
  51. Kreider J. W., Howett M. K., Stoler M. H., Zaino R. J., Welsh P. Susceptibility of various human tissues to transformation in vivo with human papillomavirus type 11. Int J Cancer. 1987 Apr 15;39(4):459–465. doi: 10.1002/ijc.2910390409. [DOI] [PubMed] [Google Scholar]
  52. Kreider J. W., Howett M. K., Wolfe S. A., Bartlett G. L., Zaino R. J., Sedlacek T., Mortel R. Morphological transformation in vivo of human uterine cervix with papillomavirus from condylomata acuminata. Nature. 1985 Oct 17;317(6038):639–641. doi: 10.1038/317639a0. [DOI] [PubMed] [Google Scholar]
  53. Kurman R. J., Schiffman M. H., Lancaster W. D., Reid R., Jenson A. B., Temple G. F., Lorincz A. T. Analysis of individual human papillomavirus types in cervical neoplasia: a possible role for type 18 in rapid progression. Am J Obstet Gynecol. 1988 Aug;159(2):293–296. doi: 10.1016/s0002-9378(88)80070-x. [DOI] [PubMed] [Google Scholar]
  54. Kurman R. J., Shah K. H., Lancaster W. D., Jenson A. B. Immunoperoxidase localization of papillomavirus antigens in cervical dysplasia and vulvar condylomas. Am J Obstet Gynecol. 1981 Aug 15;140(8):931–935. doi: 10.1016/0002-9378(81)90087-9. [DOI] [PubMed] [Google Scholar]
  55. Laver W. G., Air G. M., Webster R. G., Smith-Gill S. J. Epitopes on protein antigens: misconceptions and realities. Cell. 1990 May 18;61(4):553–556. doi: 10.1016/0092-8674(90)90464-p. [DOI] [PubMed] [Google Scholar]
  56. Lorincz A. T., Schiffman M. H., Jaffurs W. J., Marlow J., Quinn A. P., Temple G. F. Temporal associations of human papillomavirus infection with cervical cytologic abnormalities. Am J Obstet Gynecol. 1990 Mar;162(3):645–651. doi: 10.1016/0002-9378(90)90974-c. [DOI] [PubMed] [Google Scholar]
  57. Lowy D. R., Dvoretzky I., Shober R., Law M. F., Engel L., Howley P. M. In vitro tumorigenic transformation by a defined sub-genomic fragment of bovine papilloma virus DNA. Nature. 1980 Sep 4;287(5777):72–74. doi: 10.1038/287072a0. [DOI] [PubMed] [Google Scholar]
  58. Lusky M., Botchan M. R. Genetic analysis of bovine papillomavirus type 1 trans-acting replication factors. J Virol. 1985 Mar;53(3):955–965. doi: 10.1128/jvi.53.3.955-965.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Lörincz A. T., Temple G. F., Patterson J. A., Jenson A. B., Kurman R. J., Lancaster W. D. Correlation of cellular atypia and human papillomavirus deoxyribonucleic acid sequences in exfoliated cells of the uterine cervix. Obstet Gynecol. 1986 Oct;68(4):508–512. [PubMed] [Google Scholar]
  60. Macnab J. C., Walkinshaw S. A., Cordiner J. W., Clements J. B. Human papillomavirus in clinically and histologically normal tissue of patients with genital cancer. N Engl J Med. 1986 Oct 23;315(17):1052–1058. doi: 10.1056/NEJM198610233151703. [DOI] [PubMed] [Google Scholar]
  61. Matthews R. S., Shirodaria P. V. Study of regressing warts by immunofluorescence. Lancet. 1973 Mar 31;1(7805):689–691. doi: 10.1016/s0140-6736(73)91478-5. [DOI] [PubMed] [Google Scholar]
  62. McDonnell J. M., Mayr A. J., Martin W. J. DNA of human papillomavirus type 16 in dysplastic and malignant lesions of the conjunctiva and cornea. N Engl J Med. 1989 Jun 1;320(22):1442–1446. doi: 10.1056/NEJM198906013202202. [DOI] [PubMed] [Google Scholar]
  63. Mcmillan S. A., Haire M. Smooth muscle antibody in patients with warts. Clin Exp Immunol. 1975 Aug;21(2):339–344. [PMC free article] [PubMed] [Google Scholar]
  64. Meisels A., Fortin R. Condylomatous lesions of the cervix and vagina. I. Cytologic patterns. Acta Cytol. 1976 Nov-Dec;20(6):505–509. [PubMed] [Google Scholar]
  65. Mitao M., Nagai N., Levine R. U., Silverstein S. J., Crum C. P. Human papillomavirus type 16 infection: a morphological spectrum with evidence for late gene expression. Int J Gynecol Pathol. 1986;5(4):287–296. [PubMed] [Google Scholar]
  66. Morison W. L. Cell-mediated immune responses in patients with warts. Br J Dermatol. 1975 Nov;93(5):553–556. doi: 10.1111/j.1365-2133.1975.tb02248.x. [DOI] [PubMed] [Google Scholar]
  67. Morris H. H., Gatter K. C., Sykes G., Casemore V., Mason D. Y. Langerhans' cells in human cervical epithelium: effects of wart virus infection and intraepithelial neoplasia. Br J Obstet Gynaecol. 1983 May;90(5):412–420. doi: 10.1111/j.1471-0528.1983.tb08936.x. [DOI] [PubMed] [Google Scholar]
  68. Moy R. L., Eliezri Y. D., Nuovo G. J., Zitelli J. A., Bennett R. G., Silverstein S. Human papillomavirus type 16 DNA in periungual squamous cell carcinomas. JAMA. 1989 May 12;261(18):2669–2673. [PubMed] [Google Scholar]
  69. Neary K., Horwitz B. H., DiMaio D. Mutational analysis of open reading frame E4 of bovine papillomavirus type 1. J Virol. 1987 Apr;61(4):1248–1252. doi: 10.1128/jvi.61.4.1248-1252.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Neill S. M., Lessana-Leibowitch M., Pelisse M., Moyal-Barracco M. Lichen sclerosus, invasive squamous cell carcinoma, and human papillomavirus. Am J Obstet Gynecol. 1990 Jun;162(6):1633–1634. doi: 10.1016/0002-9378(90)90942-z. [DOI] [PubMed] [Google Scholar]
  71. Nuovo G. J. Correlation of histology with human papillomavirus DNA detection in the female genital tract. Gynecol Oncol. 1988 Sep;31(1):176–183. doi: 10.1016/0090-8258(88)90290-9. [DOI] [PubMed] [Google Scholar]
  72. Nuovo G. J., Pedemonte B. M. Human papillomavirus types and recurrent cervical warts. JAMA. 1990 Mar 2;263(9):1223–1226. [PubMed] [Google Scholar]
  73. Papay F., Wood B., Coulson M. Squamous cell papilloma at the tracheoesophageal puncture stoma. Arch Otolaryngol Head Neck Surg. 1988 May;114(5):564–566. doi: 10.1001/archotol.1988.01860170094027. [DOI] [PubMed] [Google Scholar]
  74. Phelps W. C., Yee C. L., Münger K., Howley P. M. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell. 1988 May 20;53(4):539–547. doi: 10.1016/0092-8674(88)90570-3. [DOI] [PubMed] [Google Scholar]
  75. Purola E., Savia E. Cytology of gynecologic condyloma acuminatum. Acta Cytol. 1977 Jan-Feb;21(1):26–31. [PubMed] [Google Scholar]
  76. Reeves W. C., Arosemena J. R., Garcia M., de Lao S. L., Cuevas M., Quiroz E., Caussy D., Rawls W. E. Genital human papillomavirus infection in Panama City prostitutes. J Infect Dis. 1989 Oct;160(4):599–603. doi: 10.1093/infdis/160.4.599. [DOI] [PubMed] [Google Scholar]
  77. Reid R., Greenberg M., Jenson A. B., Husain M., Willett J., Daoud Y., Temple G., Stanhope C. R., Sherman A. I., Phibbs G. D. Sexually transmitted papillomaviral infections. I. The anatomic distribution and pathologic grade of neoplastic lesions associated with different viral types. Am J Obstet Gynecol. 1987 Jan;156(1):212–222. doi: 10.1016/0002-9378(87)90241-9. [DOI] [PubMed] [Google Scholar]
  78. Reid R., Laverty C. R., Coppleson M., Isarangkul W., Hills E. Noncondylomatous cervical wart virus infection. Obstet Gynecol. 1980 Apr;55(4):476–483. [PubMed] [Google Scholar]
  79. Richart R. M. Cervical intraepithelial neoplasia. Pathol Annu. 1973;8:301–328. [PubMed] [Google Scholar]
  80. Richart R. M., Townsend D. E., Crisp W., DePetrillo A., Ferenczy A., Johnson G., Lickrish G., Roy M., Villa Santa U. An analysis of "long-term" follow-up results in patients with cervical intraepithelial neoplasia treated by cryotherapy. Am J Obstet Gynecol. 1980 Aug 1;137(7):823–826. doi: 10.1016/0002-9378(80)90892-3. [DOI] [PubMed] [Google Scholar]
  81. Ritter D. B., Kadish A. S., Vermund S. H., Romney S. L., Villari D., Burk R. D. Detection of human papillomavirus deoxyribonucleic acid in exfoliated cervicovaginal cells as a predictor of cervical neoplasia in a high-risk population. Am J Obstet Gynecol. 1988 Dec;159(6):1517–1525. doi: 10.1016/0002-9378(88)90587-x. [DOI] [PubMed] [Google Scholar]
  82. Rotkin I. D. Epidemiology of cancer of the cervix. 3. Sexual characteristics of a cervical cancer population. Am J Public Health Nations Health. 1967 May;57(5):815–829. doi: 10.2105/ajph.57.5.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Rowson K. E., Mahy B. W. Human papova (wart) virus. Bacteriol Rev. 1967 Jun;31(2):110–131. doi: 10.1128/br.31.2.110-131.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Samuel M., Shirodaria P. V., McMillan S. A. Incidence of virus-specific antibodies and autoantibodies in sera of patients with warts. Clin Exp Dermatol. 1976 Sep;1(3):269–274. doi: 10.1111/j.1365-2230.1976.tb01429.x. [DOI] [PubMed] [Google Scholar]
  85. Sato H., Watanabe S., Furuno A., Yoshiike K. Human papillomavirus type 16 E7 protein expressed in Escherichia coli and monkey COS-1 cells: immunofluorescence detection of the nuclear E7 protein. Virology. 1989 May;170(1):311–315. doi: 10.1016/0042-6822(89)90386-3. [DOI] [PubMed] [Google Scholar]
  86. Schneider-Gädicke A., Kaul S., Schwarz E., Gausepohl H., Frank R., Bastert G. Identification of the human papillomavirus type 18 E6 and E6 proteins in nuclear protein fractions from human cervical carcinoma cells grown in the nude mouse or in vitro. Cancer Res. 1988 Jun 1;48(11):2969–2974. [PubMed] [Google Scholar]
  87. Seedorf K., Krämmer G., Dürst M., Suhai S., Röwekamp W. G. Human papillomavirus type 16 DNA sequence. Virology. 1985 Aug;145(1):181–185. doi: 10.1016/0042-6822(85)90214-4. [DOI] [PubMed] [Google Scholar]
  88. Seedorf K., Oltersdorf T., Krämmer G., Röwekamp W. Identification of early proteins of the human papilloma viruses type 16 (HPV 16) and type 18 (HPV 18) in cervical carcinoma cells. EMBO J. 1987 Jan;6(1):139–144. doi: 10.1002/j.1460-2075.1987.tb04731.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Sekine H., Fuse A., Inaba N., Takamizawa H., Simizu B. Detection of the human papillomavirus 6b E2 gene product in genital condyloma and laryngeal papilloma tissues. Virology. 1989 May;170(1):92–98. doi: 10.1016/0042-6822(89)90355-3. [DOI] [PubMed] [Google Scholar]
  90. Shah K. H., Lewis M. G., Jenson A. B., Kurman R. J., Lancaster W. D. Papillomavirus and cervical dysplasia. Lancet. 1980 Nov 29;2(8205):1190–1190. doi: 10.1016/s0140-6736(80)92617-3. [DOI] [PubMed] [Google Scholar]
  91. Shevchuk M. M., Richart R. M. DNA content of condyloma acuminatum. Cancer. 1982 Feb 1;49(3):489–492. doi: 10.1002/1097-0142(19820201)49:3<489::aid-cncr2820490316>3.0.co;2-u. [DOI] [PubMed] [Google Scholar]
  92. Smotkin D., Berek J. S., Fu Y. S., Hacker N. F., Major F. J., Wettstein F. O. Human papillomavirus deoxyribonucleic acid in adenocarcinoma and adenosquamous carcinoma of the uterine cervix. Obstet Gynecol. 1986 Aug;68(2):241–244. [PubMed] [Google Scholar]
  93. Smotkin D., Wettstein F. O. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4680–4684. doi: 10.1073/pnas.83.13.4680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Spalholz B. A., Yang Y. C., Howley P. M. Transactivation of a bovine papilloma virus transcriptional regulatory element by the E2 gene product. Cell. 1985 Aug;42(1):183–191. doi: 10.1016/s0092-8674(85)80114-8. [DOI] [PubMed] [Google Scholar]
  95. Steinberg B. M., Topp W. C., Schneider P. S., Abramson A. L. Laryngeal papillomavirus infection during clinical remission. N Engl J Med. 1983 May 26;308(21):1261–1264. doi: 10.1056/NEJM198305263082104. [DOI] [PubMed] [Google Scholar]
  96. Stoler M. H., Wolinsky S. M., Whitbeck A., Broker T. R., Chow L. T. Differentiation-linked human papillomavirus types 6 and 11 transcription in genital condylomata revealed by in situ hybridization with message-specific RNA probes. Virology. 1989 Sep;172(1):331–340. doi: 10.1016/0042-6822(89)90135-9. [DOI] [PubMed] [Google Scholar]
  97. Syrjänen K. J. Immunocompetent cells in uterine cervical lesions of human papillomavirus origin. Gynecol Obstet Invest. 1983;16(6):327–340. doi: 10.1159/000299290. [DOI] [PubMed] [Google Scholar]
  98. Tanese N., Roth M., Goff S. P. Expression of enzymatically active reverse transcriptase in Escherichia coli. Proc Natl Acad Sci U S A. 1985 Aug;82(15):4944–4948. doi: 10.1073/pnas.82.15.4944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Tindle R. W., Smith J. A., Geysen H. M., Selvey L. A., Frazer I. H. Identification of B epitopes in human papillomavirus type 16 E7 open reading frame protein. J Gen Virol. 1990 Jun;71(Pt 6):1347–1354. doi: 10.1099/0022-1317-71-6-1347. [DOI] [PubMed] [Google Scholar]
  100. Tomita Y., Shirasawa H., Sekine H., Simizu B. Expression of the human papillomavirus type 6b L2 open reading frame in Escherichia coli: L2-beta-galactosidase fusion proteins and their antigenic properties. Virology. 1987 May;158(1):8–14. doi: 10.1016/0042-6822(87)90231-5. [DOI] [PubMed] [Google Scholar]
  101. Ward B. E., Burkett B., Petersen C., Nuckols M. L., Brennan C., Birch L. M., Crum C. P. Cytologic correlates of cervical papillomavirus infection. Int J Gynecol Pathol. 1990;9(4):297–305. doi: 10.1097/00004347-199010000-00001. [DOI] [PubMed] [Google Scholar]
  102. Werness B. A., Levine A. J., Howley P. M. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science. 1990 Apr 6;248(4951):76–79. doi: 10.1126/science.2157286. [DOI] [PubMed] [Google Scholar]
  103. Wilbanks G. D., Richart R. M., Terner J. Y. DNA content of cervical intraepithelial neoplasia studied by two-wavelength Feulgen cytophotometry. Am J Obstet Gynecol. 1967 Jul 15;98(6):792–799. doi: 10.1016/0002-9378(67)90195-0. [DOI] [PubMed] [Google Scholar]
  104. Winkler B., Capo V., Reumann W., Ma A., La Porta R., Reilly S., Green P. M., Richart R. M., Crum C. P. Human papillomavirus infection of the esophagus. A clinicopathologic study with demonstration of papillomavirus antigen by the immunoperoxidase technique. Cancer. 1985 Jan 1;55(1):149–155. doi: 10.1002/1097-0142(19850101)55:1<149::aid-cncr2820550123>3.0.co;2-9. [DOI] [PubMed] [Google Scholar]
  105. de Villiers E. M., Gissmann L., zur Hausen H. Molecular cloning of viral DNA from human genital warts. J Virol. 1981 Dec;40(3):932–935. doi: 10.1128/jvi.40.3.932-935.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. de Villiers E. M., Weidauer H., Otto H., zur Hausen H. Papillomavirus DNA in human tongue carcinomas. Int J Cancer. 1985 Nov 15;36(5):575–578. doi: 10.1002/ijc.2910360510. [DOI] [PubMed] [Google Scholar]

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