Immunologic Control of Papillomavirus Type 1

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While most patients clear human papillomavirus (HPV) infection, some develop persistent papillomas, especially if immunocompromised. Likewise, we find a fraction of outbred SKH-1 mice challenged with Mus musculus papillomavirus type 1 (MusPV1/MmuPV1) develop persistent papillomas, whereas most SKH-1 mice, as seen for the inbred C57BL/6 and BALB/c strains, clear the infection. Viral clearance requires both CD4+ and CD8+ T cells, and depletion of either subset permits persistent but subclinical infection. In C57BL/6 mice, CD8+ T cell epitopes were mapped to MusPV1 E6 and E7; however the CD8+ T cell response to E6 dominated and correlated with spontaneous regression. A MusPV1 E6-specific CD8+ T cell line was developed by vaccination and culture in vitro, and its systemic administration once was sufficient to effect papilloma clearance in an immunodeficient mouse. Our observations in inbred and outbred mice challenged with MusPV1 suggest promise for immunotherapy to treat HPV-associated disease.

Vyšlo v časopise: Immunologic Control of Papillomavirus Type 1. PLoS Pathog 11(10): e32767. doi:10.1371/journal.ppat.1005243
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005243

Souhrn

Zdroje

1. zur Hausen H (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2: 342–350. 12044010

2. Bzhalava D, Guan P, Franceschi S, Dillner J, Clifford G (2013) A systematic review of the prevalence of mucosal and cutaneous human papillomavirus types. Virology 445: 224–231. doi: 10.1016/j.virol.2013.07.015 23928291

3. de Villiers EM (2013) Cross-roads in the classification of papillomaviruses. Virology 445: 2–10. doi: 10.1016/j.virol.2013.04.023 23683837

4. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H (2004) Classification of papillomaviruses. Virology 324: 17–27. 15183049

5. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, et al. (2009) A review of human carcinogens—Part B: biological agents. Lancet Oncol 10: 321–322. 19350698

6. Walboomers JMM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, et al. (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. Journal of Pathology 189: 12–19. 10451482

7. Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, et al. (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. New England Journal of Medicine 348: 518–527. 12571259

8. D'Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, et al. (2007) Case-control study of human papillomavirus and oropharyngeal cancer. New England Journal of Medicine 356: 1944–1956. 17494927

9. Quint KD, Genders RE, de Koning MN, Borgogna C, Gariglio M, et al. (2015) Human Beta-papillomavirus infection and keratinocyte carcinomas. Journal of Pathology 235: 342–354. doi: 10.1002/path.4425 25131163

10. Bruggink SC, Eekhof JA, Egberts PF, van Blijswijk SC, Assendelft WJ, et al. (2013) Natural course of cutaneous warts among primary schoolchildren: a prospective cohort study. Ann Fam Med 11: 437–441. doi: 10.1370/afm.1508 24019275

11. Massimi P, Thomas M, Bouvard V, Ruberto I, Campo MS, et al. (2008) Comparative transforming potential of different human papillomaviruses associated with non-melanoma skin cancer. Virology 371: 374–379. 17997466

12. de Villiers EM, Ruhland A, Sekaric P (1999) Human papillomaviruses in non-melanoma skin cancer. Semin Cancer Biol 9: 413–422. 10712888

13. Vajdic CM, van Leeuwen MT (2009) What types of cancers are associated with immune suppression in HIV? Lessons from solid organ transplant recipients. Current Opinion in Hiv and Aids 4: 35–41. 19343829

14. Clifford G, Fronceschi S (2007) Immunity, infection, and cancer. Lancet 370: 6–7. 17617251

15. Dugue PA, Rebolj M, Garred P, Lynge E (2013) Immunosuppression and risk of cervical cancer. Expert Rev Anticancer Ther 13: 29–42. doi: 10.1586/era.12.159 23259425

16. Villa LL, Perez G, Kjaer SK, Paavonen J, Lehtinen M, et al. (2007) Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. New England Journal of Medicine 356: 1915–1927. 17494925

17. Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, et al. (2007) Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. New England Journal of Medicine 356: 1928–1943. 17494926

18. Paavonen J, Jenkins D, Bosch FX, Naud P, Salmeron J, et al. (2007) Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet 369: 2161–2170. 17602732

19. Paovonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, et al. (2009) Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 374: 301–314. doi: 10.1016/S0140-6736(09)61248-4 19586656

20. Joura EA, Giuliano AR, Iversen OE, Bouchard C, Mao C, et al. (2015) A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med 372: 711–723. doi: 10.1056/NEJMoa1405044 25693011

21. Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD (1998) Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338: 423–428. 9459645

22. Koutsky L (1997) Epidemiology of genital human papillomavirus infection. Am J Med 102: 3–8. 9217656

23. Schiller JT, Castellsague X, Villa LL, Hildesheim A (2008) An update of prophylactic human papillomavirus L1 virus-like particle vaccine clinical trial results. Vaccine 26 Suppl 10: K53–61. doi: 10.1016/j.vaccine.2008.06.002 18847557

24. Evander M, Edlund K, Gustafsson A, Jonsson M, Karlsson R, et al. (1995) Human papillomavirus infection is transient in young women: a population-based cohort study. J Infect Dis 171: 1026–1030. 7706782

25. Helmerhorst TJ, Meijer CJ (2002) Cervical cancer should be considered as a rare complication of oncogenic HPV infection rather than a STD. Int J Gynecol Cancer 12: 235–236. 12060443

26. Chen HC, Schiffman M, Lin CY, Pan MH, You SL, et al. (2011) Persistence of type-specific human papillomavirus infection and increased long-term risk of cervical cancer. J Natl Cancer Inst 103: 1387–1396. doi: 10.1093/jnci/djr283 21900119

27. Castle PE, Rodriguez AC, Burk RD, Herrero R, Wacholder S, et al. (2011) Long-term persistence of prevalently detected human papillomavirus infections in the absence of detectable cervical precancer and cancer. J Infect Dis 203: 814–822. doi: 10.1093/infdis/jiq116 21343148

28. Frazer IH, Leggatt GR, Mattarollo SR (2011) Prevention and Treatment of Papillomavirus-Related Cancers Through Immunization. Annual Review of Immunology, Vol 29 29: 111–138. doi: 10.1146/annurev-immunol-031210-101308 21166538

29. Wang JW, Hung CF, Huh WK, Trimble CL, Roden RB (2014) Immunoprevention of human papillomavirus-associated malignancies. Cancer Prev Res (Phila).

30. Ingle A, Ghim S, Joh J, Chepkoech I, Bennett Jenson A, et al. (2011) Novel laboratory mouse papillomavirus (MusPV) infection. Veterinary Pathology 48: 500–505. doi: 10.1177/0300985810377186 20685915

31. Cladel NM, Budgeon LR, Cooper TK, Balogh KK, Hu J, et al. (2013) Secondary infections, expanded tissue tropism, and evidence for malignant potential in immunocompromised mice infected with Mus musculus papillomavirus 1 DNA and virus. J Virol 87: 9391–9395. doi: 10.1128/JVI.00777-13 23785210

32. Handisurya A, Day PM, Thompson CD, Bonelli M, Lowy DR, et al. (2014) Strain-specific properties and T cells regulate the susceptibility to papilloma induction by Mus musculus papillomavirus 1. PLoS Pathog 10: e1004314. doi: 10.1371/journal.ppat.1004314 25121947

33. Handisurya A, Day PM, Thompson CD, Buck CB, Pang YY, et al. (2013) Characterization of Mus musculus papillomavirus 1 infection in situ reveals an unusual pattern of late gene expression and capsid protein localization. J Virol 87: 13214–13225. doi: 10.1128/JVI.02162-13 24067981

34. Maglennon GA, McIntosh PB, Doorbar J (2014) Immunosuppression facilitates the reactivation of latent papillomavirus infections. J Virol 88: 710–716. doi: 10.1128/JVI.02589-13 24173230

35. Maglennon GA, McIntosh P, Doorbar J (2011) Persistence of viral DNA in the epithelial basal layer suggests a model for papillomavirus latency following immune regression. Virology 414: 153–163. doi: 10.1016/j.virol.2011.03.019 21492895

36. Lin KY, Guarnieri FG, StaveleyOCarroll KF, Levitsky HI, August JT, et al. (1996) Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res 56: 21–26. 8548765

37. Peng S, Ji H, Trimble C, He L, Tsai YC, et al. (2004) Development of a DNA vaccine targeting human papillomavirus type 16 oncoprotein E6. J Virol 78: 8468–8476. 15280455

38. Peng S, Tomson TT, Trimble C, He L, Hung CF, et al. (2006) A combination of DNA vaccines targeting human papillomavirus type 16 E6 and E7 generates potent antitumor effects. Gene Ther 13: 257–265. 16177818

39. Akgul B, Cooke JC, Storey A (2006) HPV-associated skin disease. Journal of Pathology 208: 165–175. 16362995

40. Gravitt PE (2011) The known unknowns of HPV natural history. J Clin Invest 121: 4593–4599. doi: 10.1172/JCI57149 22133884

41. Nicholls PK, Klaunberg BA, Moore RA, Santos EB, Parry NR, et al. (1999) Naturally occurring, nonregressing canine oral papillomavirus infection: host immunity, virus characterization, and experimental infection. Virology 265: 365–374. 10600607

42. Breitburd F, Salmon J, Orth G (1997) The rabbit viral skin papillomas and carcinomas: a model for the immunogenetics of HPV-associated carcinogenesis. Clin Dermatol 15: 237–247. 9167908

43. Han R, Breitburd F, Marche PN, Orth G (1992) Linkage of regression and malignant conversion of rabbit viral papillomas to MHC class II genes. Nature 356: 66–68. 1347151

44. van der Burg SH, Palefsky JM (2009) Human Immunodeficiency Virus and Human Papilloma Virus—why HPV-induced lesions do not spontaneously resolve and why therapeutic vaccination can be successful. J Transl Med 7: 108. doi: 10.1186/1479-5876-7-108 20021658

45. Hu J, Cladel NM, Pickel MD, Christensen ND (2002) Amino acid residues in the carboxy-terminal region of cottontail rabbit papillomavirus E6 influence spontaneous regression of cutaneous papillomas. J Virol 76: 11801–11808. 12414922

46. Vinzon SE, Braspenning-Wesch I, Muller M, Geissler EK, Nindl I, et al. (2014) Protective Vaccination against Papillomavirus-Induced Skin Tumors under Immunocompetent and Immunosuppressive Conditions: A Preclinical Study Using a Natural Outbred Animal Model. PLoS Pathog 10. doi: 10.1371/journal.ppat.1003924 24586150

47. Ghim S, Newsome J, Bell J, Sundberg JP, Schlegel R, et al. (2000) Spontaneously regressing oral papillomas induce systemic antibodies that neutralize canine oral papillomavirus. Exp Mol Pathol 68: 147–151. 10816383

48. Cheng WF, Hung CF, Chai CY, Hsu KF, He L, et al. (2001) Tumor-specific immunity and antiangiogenesis generated by a DNA vaccine encoding calreticulin linked to a tumor antigen. J Clin Invest 108: 669–678. 11544272

49. Steele JC, Mann CH, Rookes S, Rollason T, Murphy D, et al. (2005) T cell responses to human papillomavirus type 16 among women with different grades of cervical neoplasia. Br J Cancer 93: 248–259. 15986031

50. Peh WL, Middleton K, Christensen N, Nicholls P, Egawa K, et al. (2002) Life cycle heterogeneity in animal models of human papillomavirus-associated disease. J Virol 76: 10401–10416. 12239317

51. Woo YL, van den Hende M, Sterling JC, Coleman N, Crawford RA, et al. (2010) A prospective study on the natural course of low-grade squamous intraepithelial lesions and the presence of HPV16 E2-, E6- and E7-specific T cell responses. Int J Cancer 126: 133–141. doi: 10.1002/ijc.24804 19645010

52. Stevanovic S, Draper LM, Langhan MM, Campbell TE, Kwong ML, et al. (2015) Complete Regression of Metastatic Cervical Cancer After Treatment With Human Papillomavirus-Targeted Tumor-Infiltrating T Cells. J Clin Oncol. doi: 10.1200/JCO.2014.58.9093 25823737

53. Wang JW, Jagu S, Kwak K, Wang C, Peng S, et al. (2014) Preparation and properties of a papillomavirus infectious intermediate and its utility for neutralization studies. Virology 449: 304–316. doi: 10.1016/j.virol.2013.10.038 24418565

54. Kim D, Gambhira R, Karanam B, Monie A, Hung CF, et al. (2008) Generation and characterization of a preventive and therapeutic HPV DNA vaccine. Vaccine 26: 351–360. 18096279