Papillomavirus virus like particle-based therapeutic vaccine against human papillomavirus infection related diseases: Immunological problems and future directions

Cellular Immunology

Volumn 269, Issue 1, 2011, Pages 5-9

  Chen, Jiezhong ^a   Ni, Guoying ^a   Liu, Xiao Song ^a  

^a UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

Alum; Cervical intraepithelial neoplasia; Human papillomavirus; IL10; Therapeutic vaccine; Virus like particles

Indexed keywords

ALUMINUM POTASSIUM SULFATE; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; PAPILLOMAVIRUS VIRUS LIKE PARTICLE BASED WART VIRUS VACCINE; PHOSPHORYL LIPID A; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; WART VIRUS VACCINE;

ANTIBODY PRODUCTION; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG EFFICACY; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; LYMPHOCYTIC CHORIOMENINGITIS; NONHUMAN; PAPILLOMAVIRUS INFECTION; PAPILLOMAVIRUS VIRUS LIKE PARTICLE; PRIORITY JOURNAL; REVIEW; TH1 CELL; TH2 CELL; UTERINE CERVIX CANCER; VIRUS NEUTRALIZATION; VIRUS PARTICLE;

CHEMISTRY, PHARMACEUTICAL; FEMALE; HUMANS; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; VACCINES, VIRUS-LIKE PARTICLE;

ANIMALIA; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; PAPILLOMAVIRIDAE;

EID: 79955476377     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2011.03.003     Document Type: Review

References (65)

1. Stanley M. Prophylactic HPV vaccines: prospects for eliminating ano-genital cancer. Br. J. Cancer 2007, 96:1320-1323.
2. Clifford G.M., Smith J.S., Aguado T., Franceschi S. Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis. Br. J. Cancer 2003, 89:101-105.
3. Schiffman M., Castle P.E., Jeronimo J., Rodriguez A.C., Wacholder S. Human papillomavirus and cervical cancer. Lancet 2007, 370:890-907.
4. Schiller J.T., Castellsague X., Villa L.L., Hildesheim A. An update of prophylactic human papillomavirus L1 virus-like particle vaccine clinical trial results. Vaccine 2008, 26(Suppl. 10):K53-K61.
5. Zhou J., Sun X.Y., Stenzel D.J., Frazer I.H. Expression of vaccinia recombinant HPV 16 L1 and L2 ORF proteins in epithelial cells is sufficient for assembly of HPV virion-like particles. Virology 1991, 185:251-257.
6. Govan V.A., Williamson A.L. Rabbits immunised with recombinant BCG expressing the cottontail rabbit papillomavirus (CRPV) L2E7E2 genes induces regression of established papillomas. Virus Res. 2007, 127:43-48.
7. Kirnbauer R., Booy F., Cheng N., Lowy D.R., Schiller J.T. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc. Natl. Acad. Sci. USA 1992, 89:12180-12184.
8. Ismaili J., Rennesson J., Aksoy E., Vekemans J., Vincart B., Amraoui Z., Van Laethem F., Goldman M., Dubois P.M. Monophosphoryl lipid A activates both human dendritic cells and T cells. J. Immunol. 2002, 168:926-932.
9. Ruiz W., McClements W.L., Jansen K.U., Esser M.T. Kinetics and isotype profile of antibody responses in rhesus macaques induced following vaccination with HPV 6, 11, 16 and 18 L1-virus-like particles formulated with or without Merck aluminum adjuvant. J. Immune Based Ther. Vaccines 2005, 3:2.
10. Schwarz T.F., Leo O. Immune response to human papillomavirus after prophylactic vaccination with ASO4-adjuvanted HPV-16/18 vaccine: improving upon nature. Gynecol. Oncol. 2008, 110:S1-S10.
11. Parkin D.M. The global health burden of infection-associated cancers in the year 2002. Int. J. Cancer 2006, 118:3030-3044.
12. Trimble C.L., Frazer I.H. Development of therapeutic HPV vaccines. Lancet Oncol. 2009, 10:975-980.
13. Kenter G.G., Welters M.J., Valentijn A.R., Lowik M.J., Berends-van der Meer D.M., Vloon A.P., Essahsah F., Fathers L.M., Offringa R., Drijfhout J.W., Wafelman A.R., Oostendorp J., Fleuren G.J., van der Burg S.H., Melief C.J. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J. Med. 2009, 361:1838-1847.
14. Hildesheim A., Herrero R., Wacholder S., Rodriguez A.C., Solomon D., Bratti M.C., Schiller J.T., Gonzalez P., Dubin G., Porras C., Jimenez S.E., Lowy D.R. Effect of human papillomavirus 16/18 L1 viruslike particle vaccine among young women with preexisting infection: a randomized trial. JAMA 2007, 298:743-753.
15. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions, N. Engl. J. Med. 356 (2007) 1915-1927.
16. Villa L.L., Costa R.L., Petta C.A., Andrade R.P., Paavonen J., Iversen O.E., Olsson S.E., Hoye J., Steinwall M., Riis-Johannessen G., Andersson-Ellstrom A., Elfgren K., Krogh G., Lehtinen M., Malm C., Tamms G.M., Giacoletti K., Lupinacci L., Railkar R., Taddeo F.J., Bryan J., Esser M.T., Sings H.L., Saah A.J., Barr E. High sustained efficacy of a prophylactic quadrivalent human papillomavirus types 6/11/16/18 L1 virus-like particle vaccine through 5 years of follow-up. Br. J. Cancer 2006, 95:1459-1466.
17. Kaufmann A.M., Nieland J.D., Jochmus I., Baur S., Friese K., Gabelsberger J., Gieseking F., Gissmann L., Glasschroder B., Grubert T., Hillemanns P., Hopfl R., Ikenberg H., Schwarz J., Karrasch M., Knoll A., Kuppers V., Lechmann M., Lelle R.J., Meissner H., Muller R.T., Pawlita M., Petry K.U., Pilch H., Walek E., Schneider A. Vaccination trial with HPV16 L1E7 chimeric virus-like particles in women suffering from high grade cervical intraepithelial neoplasia (CIN 2/3). Int. J. Cancer 2007, 121:2794-2800.
18. Zhang L.F., Zhou J., Chen S., Cai L.L., Bao Q.Y., Zheng F.Y., Lu J.Q., Padmanabha J., Hengst K., Malcolm K., Frazer I.H. HPV6b virus like particles are potent immunogens without adjuvant in man. Vaccine 2000, 18:1051-1058.
19. Warrino D.E., Olson W.C., Scarrow M.I., D'Ambrosio-Brennan L.J., Guido R.S., Da Silva D.M., Kast W.M., Storkus W.J. Human papillomavirus L1L2-E7 virus-like particles partially mature human dendritic cells and elicit E7-specific T-helper responses from patients with cervical intraepithelial neoplasia or cervical cancer in vitro. Hum. Immunol. 2005, 66:762-772.
20. Liu X.S., Xu Y., Hardy L., Khammanivong V., Zhao W., Fernando G.J., Leggatt G.R., Frazer I.H. IL-10 mediates suppression of the CD8 T cell IFN-gamma response to a novel viral epitope in a primed host. J. Immunol. 2003, 171:4765-4772.
21. Kaufmann A.M., Nieland J., Schinz M., Nonn M., Gabelsberger J., Meissner H., Muller R.T., Jochmus I., Gissmann L., Schneider A., Durst M. HPV16 L1E7 chimeric virus-like particles induce specific HLA-restricted T cells in humans after in vitro vaccination. Int. J. Cancer 2001, 92:285-293.
22. Stanley M., Lowy D.R., Frazer I. Prophylactic HPV vaccines: underlying mechanisms. Vaccine 2006, 24(Suppl. 3). S3/106-S3/113 (Chapter 12).
23. Schwarz T.F. Clinical update of the AS04-adjuvanted human papillomavirus-16/18 cervical cancer vaccine,Cervarix. Adv. Ther. 2009, 26:983-998.
24. Coffman R.L., Sher A., Seder R.A. Vaccine adjuvants: putting innate immunity to work. Immunity 2010, 33:492-503.
25. HogenEsch H. Mechanisms of stimulation of the immune response by aluminum adjuvants. Vaccine 2002, 20(Suppl. 3):S34-S39.
26. Eisenbarth S.C., Colegio O.R., O'Connor W., Sutterwala F.S., Flavell R.A. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008, 453:1122-1126.
27. Liu X.S., Dyer J., Leggatt G.R., Fernando G.J., Zhong J., Thomas R., Frazer I.H. Overcoming original antigenic sin to generate new CD8 T cell IFN-gamma responses in an antigen-experienced host. J. Immunol. 2006, 177:2873-2879.
28. Leggatt G.R., Frazer I.H. HPV vaccines: the beginning of the end for cervical cancer. Curr. Opin. Immunol. 2007, 19:232-238.
29. van Scott M.R., Justice J.P., Bradfield J.F., Enright E., Sigounas A., Sur S. IL-10 reduces Th2 cytokine production and eosinophilia but augments airway reactivity in allergic mice. Am. J. Physiol. Lung Cell Mol. Physiol. 2000, 278:L667-L674.
30. Harris S.J., Woodrow S.A., Gearing A.J., Adams S.E., Kingsman A.J., Layton G.T. The effects of adjuvants on CTL induction by V3:Ty-virus-like particles (V3-VLPs) in mice. Vaccine 1996, 14:971-976.
31. den Haan J.M., Kraal G., Bevan M.J. Cutting edge: lipopolysaccharide induces IL-10-producing regulatory CD4+ T cells that suppress the CD8+ T cell response. J. Immunol. 2007, 178:5429-5433.
32. Liu X.S., Leerberg J., MacDonald K., Leggatt G.R., Frazer I.H. IFN-gamma promotes generation of IL-10 secreting CD4+ T cells that suppress generation of CD8 responses in an antigen-experienced host. J. Immunol. 2009, 183:51-58.
33. Breitburd F., Kirnbauer R., Hubbert N.L., Nonnenmacher B., Trin-Dinh-Desmarquet C., Orth G., Schiller J.T., Lowy D.R. Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J. Virol. 1995, 69:3959-3963.
34. Ghim S., Newsome J., Bell J., Sundberg J.P., Schlegel R., Jenson A.B. Spontaneously regressing oral papillomas induce systemic antibodies that neutralize canine oral papillomavirus. Exp. Mol. Pathol. 2000, 68:147-151.
35. Woo M.K., Hur S.J., Park S., Kim H.J. Study of cell-mediated response in mice by HPV16 L1 virus-like particles expressed in Saccharomyces cerevisiae. J. Microbiol. Biotechnol. 2007, 17:1738-1741.
36. Wheelock E.F. Interferon-like virus-inhibitor induced in human leukocytes by phytohemagglutinin. Science 1965, 149:310-311.
37. Wheelock E.F. Interferon-like virus-inhibitor induced in human leukocytes by phytohemagglutinin. Science 1965, 149:310-311.
38. Karupiah G., Fredrickson T.N., Holmes K.L., Khairallah L.H., Buller R.M. Importance of interferons in recovery from mousepox. J. Virol. 1993, 67:4214-4226.
39. Karupiah G., Xie Q.W., Buller R.M., Nathan C., Duarte C., MacMicking J.D. Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase. Science 1993, 261:1445-1448.
40. Sakala I.G., Chaudhri G., Buller R.M., Nuara A.A., Bai H., Chen N., Karupiah G. Poxvirus-encoded gamma interferon binding protein dampens the host immune response to infection. J. Virol. 2007, 81:3346-3353.
41. Um S.J., Rhyu J.W., Kim E.J., Jeon K.C., Hwang E.S., Park J.S. Abrogation of IRF-1 response by high-risk HPV E7 protein in vivo. Cancer Lett. 2002, 179:205-212.
42. Nelms K., Keegan A.D., Zamorano J., Ryan J.J., Paul W.E. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 1999, 17:701-738.
43. Lembo D., Donalisio M., De Andrea M., Cornaglia M., Scutera S., Musso T., Landolfo S. A cell-based high-throughput assay for screening inhibitors of human papillomavirus-16 long control region activity. FASEB J. 2006, 20:148-150.
44. Donalisio M., Cornaglia M., Landolfo S., Lembo D. TGF-beta1 and IL-4 downregulate human papillomavirus-16 oncogene expression but have differential effects on the malignant phenotype of cervical carcinoma cells. Virus Res. 2008, 132:253-256.
45. Ohlschlager P., Osen W., Dell K., Faath S., Garcea R.L., Jochmus I., Muller M., Pawlita M., Schafer K., Sehr P., Staib C., Sutter G., Gissmann L. Human papillomavirus type 16 L1 capsomeres induce L1-specific cytotoxic T lymphocytes and tumor regression in C57BL/6 mice. J. Virol. 2003, 77:4635-4645.
46. Peng S., Frazer I.H., Fernando G.J., Zhou J. Papillomavirus virus-like particles can deliver defined CTL epitopes to the MHC class I pathway. Virology 1998, 240:147-157.
47. Greenstone H.L., Nieland J.D., de Visser K.E., De Bruijn M.L., Kirnbauer R., Roden R.B., Lowy D.R., Kast W.M., Schiller J.T. Chimeric papillomavirus virus-like particles elicit antitumor immunity against the E7 oncoprotein in an HPV16 tumor model. Proc. Natl. Acad. Sci. USA 1998, 95:1800-1805.
48. Liu X.S., Abdul-Jabbar I., Qi Y.M., Frazer I.H., Zhou J. Mucosal immunisation with papillomavirus virus-like particles elicits systemic and mucosal immunity in mice. Virology 1998, 252:39-45.
49. Liu W.J., Liu X.S., Zhao K.N., Leggatt G.R., Frazer I.H. Papillomavirus virus-like particles for the delivery of multiple cytotoxic T cell epitopes. Virology 2000, 273:374-382.
50. Di Bonito P., Grasso F., Mochi S., Petrone L., Fanales-Belasio E., Mei A., Cesolini A., Laconi G., Conrad H., Bernhard H., Dembek C.J., Cosma A., Santini S.M., Lapenta C., Donati S., Muratori C., Giorgi C., Federico M. Anti-tumor CD8+ T cell immunity elicited by HIV-1-based virus-like particles incorporating HPV-16 E7 protein. Virology 2009, 395:45-55.
51. Woo W.P., Doan T., Herd K.A., Netter H.J., Tindle R.W. Hepatitis B surface antigen vector delivers protective cytotoxic T-lymphocyte responses to disease-relevant foreign epitopes. J. Virol. 2006, 80:3975-3984.
52. Rudolf M.P., Fausch S.C., Da Silva D.M., Kast W.M. Human dendritic cells are activated by chimeric human papillomavirus type-16 virus-like particles and induce epitope-specific human T cell responses in vitro. J. Immunol. 2001, 166:5917-5924.
53. Bellone S., El-Sahwi K., Cocco E., Casagrande F., Cargnelutti M., Palmieri M., Bignotti E., Romani C., Silasi D.A., Azodi M., Schwartz P.E., Rutherford T.J., Pecorelli S., Santin A.D. Human papillomavirus type 16 (HPV-16) virus-like particle L1-specific CD8+ cytotoxic T lymphocytes (CTLs) are equally effective as E7-specific CD8+ CTLs in killing autologous HPV-16-positive tumor cells in cervical cancer patients: implications for L1 dendritic cell-based therapeutic vaccines. J. Virol. 2009, 83:6779-6789.
54. Govan V.A., Rybicki E.P., Williamson A.L. Therapeutic immunisation of rabbits with cottontail rabbit papillomavirus (CRPV) virus-like particles (VLP) induces regression of established papillomas. Virol. J. 2008, 5:45.
55. Da Silva D.M., Pastrana D.V., Schiller J.T., Kast W.M. Effect of preexisting neutralizing antibodies on the anti-tumor immune response induced by chimeric human papillomavirus virus-like particle vaccines. Virology 2001, 290:350-360.
56. Yan M., Peng J., Jabbar I.A., Liu X., Filgueira L., Frazer I.H., Thomas R. Activation of dendritic cells by human papillomavirus-like particles through TLR4 and NF-kappaB-mediated signalling, moderated by TGF-beta. Immunol.Cell Biol. 2005, 83:83-91.
57. Cools N., Ponsaerts P., Van Tendeloo V.F., Berneman Z.N. Regulatory T cells and human disease. Clin. Dev. Immunol. 2007, 2007:89195.
58. Jankovic D., Kugler D.G., Sher A. IL-10 production by CD4+ effector T cells: a mechanism for self-regulation. Mucosal. Immunol. 2010, 3:239-246.
59. O'Garra A., Barrat F.J., Castro A.G., Vicari A., Hawrylowicz C. Strategies for use of IL-10 or its antagonists in human disease. Immunol. Rev. 2008, 223:114-131.
60. Brooks D.G., Lee A.M., Elsaesser H., McGavern D.B., Oldstone M.B. IL-10 blockade facilitates DNA vaccine-induced T cell responses and enhances clearance of persistent virus infection. J. Exp. Med. 2008, 205:533-541.
61. Brooks D.G., Trifilo M.J., Edelmann K.H., Teyton L., McGavern D.B., Oldstone M.B. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 2006, 12:1301-1309.
62. Ejrnaes M., Filippi C.M., Martinic M.M., Ling E.M., Togher L.M., Crotty S., von Herrath M.G. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 2006, 203:2461-2472.
63. Bai F., Town T., Qian F., Wang P., Kamanaka M., Connolly T.M., Gate D., Montgomery R.R., Flavell R.A., Fikrig E. IL-10 signaling blockade controls murine West Nile virus infection. PLoS Pathol. 2009, 5:e1000610.
64. Humphreys I.R., de Trez C., Kinkade A., Benedict C.A., Croft M., Ware C.F. Cytomegalovirus exploits IL-10-mediated immune regulation in the salivary glands. J. Exp. Med. 2007, 204:1217-1225.
65. Kobayashi A., Weinberg V., Darragh T., Smith-McCune K. Evolving immunosuppressive microenvironment during human cervical carcinogenesis. Mucosal. Immunol. 2008, 1:412-420.