Strain-Specific Properties and T Cells Regulate the Susceptibility to Papilloma Induction by Mus musculus Papillomavirus 1

PLoS Pathogens

Volumn 10, Issue 8, 2014, Pages

  Handisurya, Alessandra ^a   Day, Patricia M ^a   Thompson, Cynthia D ^a   Bonelli, Michael ^b,c   Lowy, Douglas R ^a   Schiller, John T ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN L1; CYCLOSPORIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE DOSAGE; GENE EXPRESSION REGULATION; IMMUNOCOMPETENCE; MOUSE; MUS MUSCULUS; NONHUMAN; PAPILLOMA; PAPILLOMATOSIS; PAPILLOMAVIRIDAE; PROTEIN EXPRESSION; SKIN INFECTION; T CELL DEPLETION; T LYMPHOCYTE; VIRUS CARCINOGENESIS; VIRUS REPLICATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; DISEASE PREDISPOSITION; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; KNOCKOUT MOUSE; PAPILLOMAVIRUS INFECTION; SENSITIVE TO CARCINOGENESIS MOUSE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE SUSCEPTIBILITY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICE, INBRED C57BL; MICE, INBRED SENCAR; MICE, KNOCKOUT; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS;

EID: 84941789100     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004314     Document Type: Article

References (53)

1. Howley PM, Schiller JT, Lowy DR (2013) Papillomaviruses. In: Knipe DM, Howley PM, editors. Fields Virology. Philadelphia, PA: Lippincott Williams & Wilkins. pp. 1662–1703.
2. Parsons RJ, Kidd JG, (1942) Oral Papillomatosis of Rabbits: a Virus Disease. J Exp Med 77: 233–250.
3. Nindl I, Gottschling M, Stockfleth E, (2007) Human papillomaviruses and non-melanoma skin cancer: basic virology and clinical manifestations. Dis Markers 23: 247–259.
4. Morison WL, (1975) Viral warts, herpes simplex and herpes zoster in patients with secondary immune deficiencies and neoplasms. Br J Dermatol 92: 625–630.
5. Campo MS, (2003) Papillomavirus and disease in humans and animals. Vet Comp Oncol 1: 3–14.
6. Ingle A, Ghim S, Joh J, Chepkoech I, Bennett Jenson A, et al. (2011) Novel laboratory mouse papillomavirus (MusPV1) infection. Vet Pathol 48: 500–505.
7. Joh J, Jenson AB, Proctor M, Ingle A, Silva KA, et al. (2012) Molecular diagnosis of a laboratory mouse papillomavirus (MusPV1). Exp Mol Pathol 93: 416–421.
8. 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 (MmuPV1) DNA and virus. J Virol 87: 9391–9395.
9. Handisurya A, Day PM, Thompson CD, Buck CB, Pang Y-YS, et al. (2013) Characterization of Mus musculus Papillomavirus 1 (MusPV1) Infection In Situ Reveals an Unusual Pattern of Late Gene Expression and Capsid Protein Localization. J Virol 87: 13214–13225.
10. Abel EL, Angel JM, Kiguchi K, DiGiovanni J, (2009) Multi-stage chemical carcinogenesis in mouse skin: fundamentals and applications. Nat Protoc 4: 1350–1362.
11. Hennings H, Devor D, Wenk ML, Slaga TJ, Former B, et al. (1981) Comparison of two-stage epidermal carcinogenesis initiated by 7,12-dimethylbenz(a)anthracene or N-methyl-N′-nitro-N-nitrosoguanidine in newborn and adult SENCAR and BALB/c mice. Cancer Res 41: 773–779.
12. Hennings H, Glick AB, Lowry DT, Krsmanovic LS, Sly LM, et al. (1993) FVB/N mice: an inbred strain sensitive to the chemical induction of squamous cell carcinomas in the skin. Carcinogenesis 14: 2353–2358.
13. Handisurya A, Day PM, Thompson CD, Buck CB, Kwak K, et al. (2012) Murine skin and vaginal mucosa are similarly susceptible to infection by pseudovirions of different papillomavirus classifications and species. Virology 433: 385–394.
14. Hamawy MM, (2003) Molecular actions of calcineurin inhibitors. Drug News Perspect 16: 277–282.
15. Holländer GA, Bierer BE, Burakoff SJ, (1994) Molecular and biological actions of cyclosporin A and FK506 on T cell development and function. Transfus Sci 15: 207–220.
16. 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.
17. Maglennon GA, McIntosh PB, Doorbar J, (2014) Immunosuppression facilitates the reactivation of latent papillomavirus infections. J Virol 88: 710–716.
18. White WI, Wilson SD, Bonnez W, Rose RC, Koenig S, et al. (1998) In vitro infection and type-restricted antibody-mediated neutralization of authentic human papillomavirus type 16. J Virol 72: 959–964.
19. Ozbun MA, (2002) Human papillomavirus type 31b infection of human keratinocytes and the onset of early transcription. J Virol 76: 11291–11300.
20. 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
21. Coleman N, Birley HD, Renton AM, Hanna NF, Ryait BK, et al. (1994) Immunological events in regressing genital warts. Am J Clin Pathol 102: 768–774.
22. Trimble CL, Clark RA, Thoburn C, Hanson NC, Tassellom J, et al. (2010) Human papillomavirus 16-associated cervical intraepithelial neoplasia in humans excludes CD8 T cells from dysplastic epithelium. J Immunol 185: 7107–7114.
23. Woo YL, Sterling J, Damay I, Coleman N, Crawford R, et al. (2008) Characterising the local immune responses in cervical intraepithelial neoplasia: a cross-sectional and longitudinal analysis. BJOG 115: 1616–1622.
24. Knowles G, O'Neil BW, Campo MS, (1996) Phenotypical characterization of lymphocytes infiltrating regressing papillomas. J Virol 70: 8451–8458.
25. Nicholls PK, Moore PF, Anderson DM, Moore RA, Parry NR, et al. (2001) Regression of canine oral papillomas is associated with infiltration of CD4+ and CD8+ lymphocytes. Virology 283: 31–39.
26. Wilgenburg BJ, Budgeon LR, Lang CM, Griffith JW, Christensen ND, (2005) Characterization of immune responses during regression of rabbit oral papillomavirus infections. Comp Med 55: 431–439.
27. Selvakumar R, Schmitt A, Iftner T, Ahmed R, Wettstein FO, (1997) Regression of papillomas induced by cottontail rabbit papillomavirus is associated with infiltration of CD8+ cells and persistence of viral DNA after regression. J Virol 71: 5540–5548.
28. Williams MA, Bevan MJ, (2007) Effector and memory CTL differentiation. Annu Rev Immunol 25: 171–192.
29. Wherry EJ, Ahmed R, (2004) Memory CD8 T-cell differentiation during viral infection. J Virol 78: 5535–5545.
30. Whitmire JK, (2011) Induction and function of virus-specific CD4+ T cell responses. Virology 411: 216–228.
31. Buller RM, Holmes KL, Hügin A, Frederickson TN, Morse HC, 3rd (1987) Induction of cytotoxic T-cell responses in vivo in the absence of CD4 helper cells. Nature 328: 77–79.
32. Ruedl C, Kopf M, Bachmann MF, (1999) CD8(+) T cells mediate CD40-independent maturation of dendritic cells in vivo. J Exp Med 189: 1875–1884.
33. Yauch LE, Prestwood TR, May MM, Morar MM, Zellweger RM, et al. (2010) CD4+ T cells are not required for the induction of dengue virus-specific CD8+ T cell or antibody responses but contribute to protection after vaccination. J Immunol 185: 5405–5416.
34. Hamilton SE, Tvinnereim AR, Harty JT, (2001) Listeria monocytogenes infection overcomes the requirement for CD40 ligand in exogenous antigen presentation to CD8(+) T cells. J Immunol 167: 5603–5609.
35. Nakanishi Y, Lu B, Gerard C, Iwasaki A, (2009) CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature 462: 510–513.
36. Bennett SR, Carbone FR, Karamalis F, Flavell RA, Miller JF, et al. (1998) Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393: 478–480.
37. Hernandez MG, Shen L, Rock KL, (2007) CD40-CD40 ligand interaction between dendritic cells and CD8T cells is needed to stimulate maximal T cell responses in the absence of CD4 T cell help. J Immunol 178: 2844–2852.
38. Johnson S, Zhan Y, Sutherland RM, Mount AM, Bedoui S, et al. (2009) Selected Toll-like receptor ligands and viruses promote helper-independent cytotoxic T cell priming by upregulating CD40L on dendritic cells. Immunity 30: 218–227.
39. Combe CL, Curiel TJ, Moretto MM, Khan IA, (2005) NK cells help to induce CD8(+)-T-cell immunity against Toxoplasma gondii in the absence of CD4(+) T cells. Infect Immun 73: 4913–4921.
40. Swain SL, McKinstry KK, Strutt TM, (2012) Expanding roles for CD4+ T cells in immunity to viruses. Nat Rev Immunol 12: 136–148.
41. Soghoian DZ, Streeck H, (2010) Cytolytic CD4(+) T cells in viral immunity. Expert Rev Vaccines 9: 1453–1463.
42. Sant AJ, McMichael A, (2012) Revealing the role of CD4(+) T cells in viral immunity. J Exp Med 209: 1391–1395.
43. Jellison ER, Kim SK, Welsh RM, (2005) Cutting edge: MHC class II-restricted killing in vivo during viral infection. J Immunol 174: 614–618.
44. Gaspari AA, Jenkins MK, Katz SI, (1988) Class II MHC-bearing keratinocytes induce antigen-specific unresponsiveness in hapten-specific Th1 clones. J Immunol 141: 2216–2220.
45. Yusuf N, Nasti TH, Katiyar SK, Jacobs MK, Seibert MD, et al. (2008) Antagonistic roles of CD4+ and CD8+ T-cells in 7,12-dimethylbenz(a)anthracene cutaneous carcinogenesis. Cancer Res 68: 3924–3930.
46. Roberts SJ, Ng BY, Filler RB, Lewis J, Glusac EJ, et al. (2007) Characterizing tumor-promoting T cells in chemically induced cutaneous carcinogenesis. Proc Natl Acad Sci U S A 104: 6770–6775.
47. Boxman IL, Berkhout RJ, Mulder LH, Wolkers MC, Bouwes Bavinck JN, et al. (1997) Detection of human papillomavirus DNA in plucked hairs from renal transplant recipients and healthy volunteers. J Invest Dermatol 108: 712–715.
48. Antonsson A, Erfurt C, Hazard K, Holmgren V, Simon M, et al. (2003) Prevalence and type spectrum of human papillomaviruses in healthy skin samples collected in three continents. J Gen Virol 84: 1881–1886.
49. Meyer T, Arndt R, Nindl I, Ulrich C, Christophers E, et al. (2003) Association of human papillomavirus infections with cutaneous tumors in immunosuppressed patients. Transpl Int 16: 146–153.
50. Harwood CA, Surentheran T, McGregor JM, Spink PJ, Leigh IM, et al. (2000) Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals. J Med Virol 61: 289–297.
51. Weissenborn S, Neale RE, Waterboer T, Abeni D, Bavinck JN, et al. (2012) Beta-papillomavirus DNA loads in hair follicles of immunocompetent people and organ transplant recipients. Med Microbiol Immunol 201: 117–25.
52. Buck CB, Thompson CD, (2007) Production of papillomavirus-based gene transfer vectors. Curr Protoc Cell Biol 37: 1–19.
53. Blüml S, Bonelli M, Niederreiter B, Puchner A, Mayr G, et al. (2011) Essential role of microRNA-155 in the pathogenesis of autoimmune arthritis in mice. Arthritis Rheum 63: 1281–1288.