A multimeric L2 vaccine for prevention of animal papillomavirus infections

Virology

Volumn 420, Issue 1, 2011, Pages 43-50

  Jagu, Subhashini ^a   Malandro, Nicole ^a   Kwak, Kihyuck ^a   Yuan, Hang ^c   Schlegel, Richard ^c   Palmer, Kenneth E ^d   Huh, Warner K ^e   Campo, M Saveria ^f   Roden, Richard B S ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d University of Louisville School of Medicine   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

L2; Papillomavirus; Sarcoid; Vaccination; Warts

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; CAPSID PROTEIN L1; L2 VACCINE; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BOVINE PAPILLOMAVIRUS TYPE 1; BOVINE PAPILLOMAVIRUS TYPE 4; CANINE ORAL PAPILLOMAVIRUS; CONTROLLED STUDY; FEMALE; GENE SEQUENCE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PAPILLOMAVIRUS INFECTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TREATMENT OUTCOME; VACCINATION; VIRUS IMMUNITY; VIRUS LIKE AGENT; VIRUS TRANSMISSION;

ANIMALS; ANTIBODIES, VIRAL; CAPSID PROTEINS; CATTLE; CATTLE DISEASES; CELL LINE; DOG DISEASES; DOGS; FEMALE; MICE; MICE, INBRED BALB C; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; VACCINATION;

ANIMALIA; BOS; BOVINAE; BOVINE PAPILLOMAVIRUS - 4; CANINE ORAL PAPILLOMAVIRUS; MUS; PAPILLOMAVIRIDAE;

EID: 80053386924     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.07.020     Document Type: Article

References (56)

1. Bell J.A., Sundberg J.P., Ghim S.J., Newsome J., Jenson A.B., Schlegel R. A formalin-inactivated vaccine protects against mucosal papillomavirus infection: a canine model. Pathobiology 1994, 62(4):194-198.
2. Bernard H.U., Burk R.D., Chen Z., van Doorslaer K., Hausen H., de Villiers E.M. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010, 401(1):70-79.
3. Bregman C.L., Hirth R.S., Sundberg J.P., Christensen E.F. Cutaneous neoplasms in dogs associated with canine oral papillomavirus vaccine. Vet. Pathol. 1987, 24(6):477-487.
4. 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(6):3959-3963.
5. Buck C.B., Pastrana D.V., Lowy D.R., Schiller J.T. Efficient intracellular assembly of papillomaviral vectors. J. Virol. 2004, 78(2):751-757.
6. Campo M.S. Papillomas and cancer in cattle. Cancer Surv. 1987, 6(1):39-54.
7. Campo M.S. Vaccination against papillomavirus in cattle. Curr. Top. Microbiol. Immunol. 1994, 186:255-266.
8. Campo M.S. Vaccination against papillomavirus in cattle. Clin. Dermatol. 1997, 15(2):275-283.
9. Campo M.S., Roden R.B. Papillomavirus prophylactic vaccines: established successes, new approaches. J. Virol. 2010, 84(3):1214-1220.
10. Campo M.S., O'Neil B.W., Grindlay G.J., Curtis F., Knowles G., Chandrachud L. A peptide encoding a B-cell epitope from the N-terminus of the capsid protein L2 of bovine papillomavirus-4 prevents disease. Virology 1997, 234(2):261-266.
11. Chackerian B., Lowy D.R., Schiller J.T. Conjugation of a self-antigen to papillomavirus-like particles allows for efficient induction of protective autoantibodies. J. Clin. Invest. 2001, 108(3):415-423.
12. Chandrachud L.M., Grindlay G.J., McGarvie G.M., O'Neil B.W., Wagner E.R., Jarrett W.F., Campo M.S. Vaccination of cattle with the N-terminus of L2 is necessary and sufficient for preventing infection by bovine papillomavirus-4. Virology 1995, 211(1):204-208.
13. Christensen N.D., Kreider J.W., Kan N.C., DiAngelo S.L. The open reading frame L2 of cottontail rabbit papillomavirus contains antibody-inducing neutralizing epitopes. Virology 1991, 181(2):572-579.
14. Christensen N.D., Reed C.A., Cladel N.M., Han R., Kreider J.W. Immunization with viruslike particles induces long-term protection of rabbits against challenge with cottontail rabbit papillomavirus. J. Virol. 1996, 70(2):960-965.
15. Davidson E.J., Boswell C.M., Sehr P., Pawlita M., Tomlinson A.E., McVey R.J., Dobson J., Roberts J.S., Hickling J., Kitchener H.C., Stern P.L. Immunological and clinical responses in women with vulval intraepithelial neoplasia vaccinated with a vaccinia virus encoding human papillomavirus 16/18 oncoproteins. Cancer Res. 2003, 63(18):6032-6041.
16. Day P.M., Gambhira R., Roden R.B., Lowy D.R., Schiller J.T. Mechanisms of human papillomavirus type 16 neutralization by l2 cross-neutralizing and l1 type-specific antibodies. J. Virol. 2008, 82(9):4638-4646.
17. Day P.M., Kines R.C., Thompson C.D., Jagu S., Roden R.B., Lowy D.R., Schiller J.T. In vivo mechanisms of vaccine-induced protection against HPV infection. Cell Host Microbe 2010, 8(3):260-270.
18. Dvoretzky I., Shober R., Chattopadhyay S.K., Lowy D.R. A quantitative in vitro focus assay for bovine papilloma virus. Virology 1980, 103(2):369-375.
19. Fiander A.N., Tristram A.J., Davidson E.J., Tomlinson A.E., Man S., Baldwin P.J., Sterling J.C., Kitchener H.C. Prime-boost vaccination strategy in women with high-grade, noncervical anogenital intraepithelial neoplasia: clinical results from a multicenter phase II trial. Int. J. Gynecol. Cancer 2006, 16(3):1075-1081.
20. Gambhira R., Jagu S., Karanam B., Gravitt P.E., Culp T.D., Christensen N.D., Roden R.B. Protection of rabbits against challenge with rabbit papillomaviruses by immunization with the N-terminus of HPV16 minor capsid antigen L2. J. Virol. 2007, 81(21):13927-13931.
21. Gambhira R., Karanam B., Jagu S., Roberts J.N., Buck C.B., Bossis I., Alphs H., Culp T., Christensen N.D., Roden R.B. A protective and broadly cross-neutralizing epitope of human papillomavirus L2. J. Virol. 2007, 81(24):13927-13931.
22. Gaukroger J.M., Chandrachud L.M., O'Neil B.W., Grindlay G.J., Knowles G., Campo M.S. Vaccination of cattle with bovine papillomavirus type 4 L2 elicits the production of virus-neutralizing antibodies. J. Gen. Virol. 1996, 77(Pt 7):1577-1583.
23. 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.
24. 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(7):743-753.
25. Jagu S., Karanam B., Gambhira R., Chivukula S.V., Chaganti R.J., Lowy D.R., Schiller J.T., Roden R.B. Concatenated multitype L2 fusion proteins as candidate prophylactic pan-human papillomavirus vaccines. J. Natl. Cancer Inst. 2009, 101(11):782-792.
26. Jarrett W.F., O'Neil B.W., Gaukroger J.M., Smith K.T., Laird H.M., Campo M.S. Studies on vaccination against papillomaviruses: the immunity after infection and vaccination with bovine papillomaviruses of different types. Vet. Rec. 1990, 126(19):473-475.
27. Jarrett W.F., Smith K.T., O'Neil B.W., Gaukroger J.M., Chandrachud L.M., Grindlay G.J., McGarvie G.M., Campo M.S. Studies on vaccination against papillomaviruses: prophylactic and therapeutic vaccination with recombinant structural proteins. Virology 1991, 184(1):33-42.
28. Kawana K., Yoshikawa H., Taketani Y., Yoshiike K., Kanda T. Common neutralization epitope in minor capsid protein L2 of human papillomavirus types 16 and 6. J. Virol. 1999, 73(7):6188-6190.
29. Kines R.C., Thompson C.D., Lowy D.R., Schiller J.T., Day P.M. The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(48):20458-20463.
30. Kirnbauer R., Chandrachud L.M., O'Neil B.W., Wagner E.R., Grindlay G.J., Armstrong A., McGarvie G.M., Schiller J.T., Lowy D.R., Campo M.S. Virus-like particles of bovine papillomavirus type 4 in prophylactic and therapeutic immunization. Virology 1996, 219(1):37-44.
31. Knowles G., Grindlay G.J., Campo M.S., Chandrachud L.M., O'Neil B.W. Linear B-cell epitopes in the N-terminus of L2 of bovine papillomavirus type 4. Res. Vet. Sci. 1997, 62(3):289-291.
32. Koller L.D., Olson C. Attempted transmission of warts from man, cattle, and horses and of deer fibroma, to selected hosts. J. Invest. Dermatol. 1972, 58(6):366-368.
33. Koutsky L.A., Ault K.A., Wheeler C.M., Brown D.R., Barr E., Alvarez F.B., Chiacchierini L.M., Jansen K.U. A controlled trial of a human papillomavirus type 16 vaccine. N. Engl. J. Med. 2002, 347(21):1645-1651.
34. Lin Y.L., Borenstein L.A., Selvakumar R., Ahmed R., Wettstein F.O. Effective vaccination against papilloma development by immunization with L1 or L2 structural protein of cottontail rabbit papillomavirus. Virology 1992, 187(2):612-619.
35. McGarvie G.M., Chandrachud L., Gaukroger J.M., Grindlay G.J., O'Neil B.W., Baird J.W., Wagner E.R., Jarrett W.F.H., Campo M.S. Vaccination of cattle with L2 protein prevents BPV-4 infection. Immunology of Human Papillomaviruses 1994, 283-290. Plenum Press, New York. M.A. Stanley (Ed.).
36. Munday J.S., Kiupel M. Papillomavirus-associated cutaneous neoplasia in mammals. Vet. Pathol. 2010, 47(2):254-264.
37. Munoz N., Bosch F.X., Castellsague X., Diaz M., de Sanjose S., Hammouda D., Shah K.V., Meijer C.J. Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int. J. Cancer 2004, 111(2):278-285.
38. Nasir L., Campo M.S. Bovine papillomaviruses: their role in the aetiology of cutaneous tumours of bovids and equids. Vet. Dermatol. 2008, 19(5):243-254.
39. Olson C., Luedke A.J., Brobst D.F. Induced immunity of skin, vagina, and urinary bladder to bovine papillomatosis. Cancer Res. 1962, 22:463-468.
40. Olson C., Robl M.G., Larson L.L. Cutaneous and penile bovine fibropapillomatosis and its control. J. Am. Vet. Med. Assoc. 1968, 153(9):1189-1194.
41. Parkin D.M., Bray F. Chapter 2: the burden of HPV-related cancers. Vaccine 2006, 24(Suppl. 3):S11-S25.
42. Pastrana D.V., Buck C.B., Pang Y.Y., Thompson C.D., Castle P.E., FitzGerald P.C., Kruger Kjaer S., Lowy D.R., Schiller J.T. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 2004, 321(2):205-216.
43. Pastrana D.V., Gambhira R., Buck C.B., Pang Y.Y., Thompson C.D., Culp T.D., Christensen N.D., Lowy D.R., Schiller J.T., Roden R.B. Cross-neutralization of cutaneous and mucosal papillomavirus types with anti-sera to the amino terminus of L2. Virology 2005, 337(2):365-372.
44. Pilacinski W.P., Glassman D.L., Glassman K.F., Reed D.E., Lum M.A., Marshall R.F., Muscoplat C.C., Faras A.J. Immunization against bovine papillomavirus infection. CIBA Found. Symp. 1986, 120:136-156.
45. Pinto L.A., Edwards J., Castle P.E., Harro C.D., Lowy D.R., Schiller J.T., Wallace D., Kopp W., Adelsberger J.W., Baseler M.W., Berzofsky J.A., Hildesheim A. Cellular immune responses to human papillomavirus (HPV)-16 L1 in healthy volunteers immunized with recombinant HPV-16 L1 virus-like particles. J. Infect. Dis. 2003, 188(2):327-338.
46. Pinto L.A., Viscidi R., Harro C.D., Kemp T.J., Garcia-Pineres A.J., Trivett M., Demuth F., Lowy D.R., Schiller J.T., Berzofsky J.A., Hildesheim A. Cellular immune responses to HPV-18, -31, and -53 in healthy volunteers immunized with recombinant HPV-16 L1 virus-like particles. Virology 2006, 353(2):451-462.
47. Richards R.M., Lowy D.R., Schiller J.T., Day P.M. Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(5):1522-1527.
48. Roberts J.N., Buck C.B., Thompson C.D., Kines R., Bernardo M., Choyke P.L., Lowy D.R., Schiller J.T. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat. Med. 2007, 13(7):857-861.
49. Roden R., Wu T.C. How will HPV vaccines affect cervical cancer?. Nat. Rev. Cancer 2006, 6(10):753-763.
50. Roden R.B., Yutzy W.H.t., Fallon R., Inglis S., Lowy D.R., Schiller J.T. Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology 2000, 270(2):254-257.
51. Schiller J.T., Day P.M., Kines R.C. Current understanding of the mechanism of HPV infection. Gynecol. Oncol. 2010, 118(1 Suppl.):S12-7.
52. Shafti-Keramat S., Schellenbacher C., Handisurya A., Christensen N., Reininger B., Brandt S., Kirnbauer R. Bovine papillomavirus type 1 (BPV1) and BPV2 are closely related serotypes. Virology 2009, 393(1):1-6.
53. Smyth L.J., Van Poelgeest M.I., Davidson E.J., Kwappenberg K.M., Burt D., Sehr P., Pawlita M., Man S., Hickling J.K., Fiander A.N., Tristram A., Kitchener H.C., Offringa R., Stern P.L., Van Der Burg S.H. Immunological responses in women with human papillomavirus type 16 (HPV-16)-associated anogenital intraepithelial neoplasia induced by heterologous prime-boost HPV-16 oncogene vaccination. Clin. Cancer Res. 2004, 10(9):2954-2961.
54. Suzich J.A., Ghim S.J., Palmer-Hill F.J., White W.I., Tamura J.K., Bell J.A., Newsome J.A., Jenson A.B., Schlegel R. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proc. Natl. Acad. Sci. U. S. A. 1995, 92(25):11553-11557.
55. Vandepapeliere P., Barrasso R., Meijer C.J., Walboomers J.M., Wettendorff M., Stanberry L.R., Lacey C.J. Randomized controlled trial of an adjuvanted human papillomavirus (HPV) type 6 L2E7 vaccine: infection of external anogenital warts with multiple HPV types and failure of therapeutic vaccination. J. Infect. Dis. 2005, 192(12):2099-2107.
56. 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(11-12):1051-1058.