Immunization with an HPV-16 L1-based chimeric virus-like particle containing HPV-16 E6 and E7 epitopes elicits long-lasting prophylactic and therapeutic efficacy in an HPV-16 tumor mice model

Archives of Virology

Volumn 159, Issue 2, 2014, Pages 291-305

  Monroy García, Alberto ^a,b   Gómez Lim, Miguel Angel ^c   Weiss Steider, Benny ^b   Hernández Montes, Jorge ^b   Huerta Yepez, Sara ^d   Rangel Santiago, Jesús F ^d   Santiago Osorio, Edelmiro ^e   Mora García, María de Lourdes ^b  

^a INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

^d HOSPITAL INFANTIL DE MÉXICO FEDERICO GÓMEZ   (Mexico)

^e UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; EPITOPE; HYBRID PROTEIN; L1 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; NEUTRALIZING ANTIBODY; ONCOGENE PROTEIN E7, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN; PROTEIN E7; RECOMBINANT VACCINE; REPRESSOR PROTEIN; VIRUS ANTIBODY; VIRUS LIKE PARTICLE VACCINE; WART VIRUS VACCINE;

ANIMAL; ARTICLE; BLOOD; C57BL MOUSE; CARCINOMA; DISEASE MODEL; FEMALE; GENETICS; IMMUNOLOGY; MOUSE; PAPILLOMAVIRUS INFECTION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CAPSID PROTEINS; CARCINOMA; DISEASE MODELS, ANIMAL; EPITOPES, T-LYMPHOCYTE; FEMALE; MICE; MICE, INBRED C57BL; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; VACCINES, SYNTHETIC; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84895073283     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-013-1819-z     Document Type: Article

References (61)

1. Bosch FX, Lorincz A, Muñoz N, Meijer CJ, Shah KV (2002) The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 55: 244-265.
2. Females United to Unilaterally Reduce Endo-Ectocervical Disease (FUTURE) II Study Group (2007) Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 356: 1915-1927.
3. Joura EA, Leodolter S, Hernandez-Avila M, Wheeler CM, Perez G, Koutsky LA, Garland SM, Harper DM, Tang GW, Ferris DG, Steben M, Jones RW, Bryan J, Taddeo FJ, Bautista OM, Esser MT, Sings HL, Nelson M, Boslego JW, Sattler C, Barr E, Paavonen J (2007) Efficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11, 16, and 18) L1 virus-like-particle vaccine against high grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet 369: 1693-1702.
4. Joura EA, Kjaer SK, Wheeler CM, Sigurdsson K, Iversen OE, Hernandez-Avila M, Perez G, Brown DR, Koutsky LA, Tay EH, García P, Ault KA, Garland SM, Leodolter S, Olsson SE, Tang GW, Ferris DG, Paavonen J, Lehtinen M, Steben M, Bosch X, Dillner J, Kurman RJ, Majewski S, Muñoz N, Myers ER, Villa LL, Taddeo FJ, Roberts C, Tadesse A, Bryan J, Lupinacci LC, Giacoletti KE, Lu S, Vuocolo S, Hesley TM, Haupt RM, Barr E (2008) HPV antibody levels and clinical efficacy following administration of a prophylactic quadrivalent HPV vaccine. Vaccine 26: 6844-6851.
5. McKeage K, Romanowski B (2011) AS04-adjuvanted human papillomavirus (HPV) types 16 and 18 vaccine (Cervarix®): a review of its use in the prevention of premalignant cervical lesions and cervical cancer causally related to certain oncogenic HPV types. Drugs 71: 465-488.
6. Kemp TJ, Hildesheim A, Safaeian M, Dauner JG, Pan Y, Porras C, Schiller JT, Lowy DR, Herrero R, Pinto LA (2011) HPV16/18 L1 VLP vaccine induces cross-neutralizing antibodies that may mediate cross-protection. Vaccine 29: 2011-2014.
7. Moody CA, Laimins LA (2010) Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 10: 550-560.
8. Galloway DA, Mc Dugall JK (1996) The disruption of cell cycle checkpoints by papillomavirus oncoproteins contributes to anogenital neoplasia. Semin Cancer Biol 7: 309-315.
9. Feltkamp MC, Smits HL, Vierboom MP, Minnaar RP, de Jongh BM, Drijfhout JW, ter Schegget J, Melief CJ, Kast WM (1993) Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur J Immunol 23: 2242-2249.
10. Kadish AS, Romney SL, Ledwidge R, Tindle R, Fernando GJ, Zee SY, van Ranst MA, Burk RD (1994) Cell-mediated immune responses to E7 peptides of human papillomavirus (HPV) type 16 are dependent on the HPV type infecting the cervix whereas serological reactivity is not type-specific. J Gen Virol 75: 2277-2284.
11. Greenstone HL, Nieland JD, de Visser KE, De Bruijn ML, Kirnbauer R, Roden RB, Lowy DR, Kast WM, Schiller JT (1998) Chimeric papillomavirus virus-like particles elicit antitumor immunity against the E7 oncoprotein in an HPV16 tumor model. Proc Natl Acad Sci USA 95: 1800-1805.
12. Schäfer K, Müller M, Faath S, Henn A, Osen W, Zentgraf H, Benner A, Gissmann L, Jochmus I (1999) Immune response to human papillomavirus 16 L1E7 chimeric virus-like particles: induction of cytotoxic T cells and specific tumor protection. Int J Cancer 81: 881-888.
13. Bian T, Wang Y, Lu Z, Ye Z, Zhao L, Ren J, Zhang H, Ruan L, Tian H (2008) Human papillomavirus type 16 L1E7 chimeric capsomeres have prophylactic and therapeutic efficacy against papillomavirus in mice. Mol Cancer Ther 7: 1329-1335.
14. Sharma C, Dey B, Wahiduzzaman M, Singh N (2012) Human papillomavirus 16 L1-E7 chimeric virus like particles show prophylactic and therapeutic efficacy in murine model of cervical cancer. Vaccine 30: 5417-5424.
15. Peng S, Frazer IH, Fernando GJ, Zhou J (1998) Papillomavirus virus-like particles can deliver defined CTL epitopes to the MHC class I pathway. Virology 240: 147-157.
16. Liu WJ, Liu XS, Zhao KN, Leggatt GR, Frazer IH (2000) Papillomavirus virus-like particles for the delivery of multiple cytotoxic T cell epitopes. Virology 273: 374-382.
17. Gomez Lim MA (2007) Transgenic plants in therapeutically valuable protein production. Transgenic Plant J 1: 256-266.
18. Šmídková M, Holá M, Brouzdová J, Angelis KJ (2012) Plant production of vaccine against HPV. In: Broeck DV (ed) A new perspectives, human papillomavirus and related diseases-from bench to bedside-a clinical perspective. INTECH, Croatia, pp 147-217.
19. Biemelt S, Sonnewald U, Galmbacher P, Willmitzer L, Muller M (2003) Production of human papillomavirus type 16 virus-like particles in transgenic plants. J Virol 77: 9211-9212.
20. Kohl T, Hitzeroth I, Christensen N, Rybicki E (2007) Expression of HPV-11 L1 protein in transgenic Arabidopsis thaliana and Nicotiana tabacum. BMC Biotechnol 7: 56.
21. Warzecha H, Mason HS, Lane C, Tryggvesson A, Rybicki EP, Williamson AL, Clements JD, Rose RC (2003) Oral immunogenicity of human papillomavirus-like particles expressed in potato. J Virol 77: 8702-8711.
22. Paz de la Rosa G, Monroy-García A, Mora-García ML, Hernández-Montes J, Weiss-Steider B, Gómez-Lim MA (2009) An HPV16 L1-based chimeric human papilloma virus-like particles containing astring of epitopes produced in plants is able to elicit humoral and cytotoxic T-cell activity in mice. Virol J 6: 2.
23. Ressing ME, Sette A, Brandt RM, Ruppert J, Wentworth PA, Hartman M, Oseroff C, Grey HM, Melief CJ (1995) Human CTL epitopes encoded by human papillomavirus type 16 E6 and E7 identified through in vivo and in vitro immunogenicity studies of HLA-A*0201-binding peptides. J Immunol 154: 5934-5943.
24. Kadish AS, Timmins P, Wang Y, Ho GY, Burk RD, Ketz J, He W, Romney SL, Johnson A, Angeletti R, Abadi M (2002) Regression of cervical intraepithelial neoplasia and loss of human papillomavirus (HPV) infection is associated with cell-mediated immune responses to an HPV type 16 E7 peptide. Cancer Epidemiol Biomarkers Prev 11: 483-488.
25. Khammanivong V, Liu XS, Liu WJ, Rodda SJ, Leggatt GR, Tndle RW, Frazer IH, Fernando GJ (2003) Paucity of functional CTL epitopes in the E7 oncoprotein of cervical cancer associated human papillomavirus type 16. Immunol Cell Biol 81: 1-7.
26. Monroy-García A, Hernández-Montes J, Mora-García ML (2007) Identification of epitopes from L1, E6, and E7 proteins of the HPV-16 and 18 types and its implication for diagnosis and treatment of cervical carcinoma. In: Manual Moderno, UNAM, PUIS (eds) Advances in cancer research at UNAM (Universidad Nacional Autónoma de México). UNAM, Mexico, pp 1-32.
27. Monroy-García A, Gómez-Lim MA, Weiss-Steider B, la Rosa GP, Hernández-Montes J, Pérez-Saldaña K, Tapia-Guerrero YS, Toledo-Guzmán ME, Santiago-Osorio E, Sanchez-Peña HI, Mora-García Mde L (2011) A novel HPV 16 L1-based chimeric virus-like particle containing E6 and E7 seroreactive epitopes permits highly specific detection of antibodies in patients with CIN 1 and HPV-16 infection. Virol J 8: 59.
28. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
29. Roden RB, Hubbert NL, Kirnbauer R, Breitburd F, Lowy DR, Schiller JT (1995) Papillomavirus L1 capsids agglutinate mouse erythrocytes through a proteinaceous receptor. J Virol 69: 5147-5151.
30. Lin KY, Guarnieri FG, Staveley-O'Carroll KF, Levitsky HI, August JT, Pardoll DM, Wu TC (1996) Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res 56: 21-26.
31. Attia MA, Weiss DW (1966) Immunology of spontaneous mammary carcinomas in mice V. Acquired tumor resistance and enhancement in strain A mice infected with mammary tumor virus. Cancer Res 26: 1787-1800.
32. Huerta S, Heinzerling JH, Anguiano-Hernandez YM, Huerta-Yepez S, Lin J, Chen D, Bonavida B, Livingston EH (2007) Modification of gene products involved in resistance to apoptosis in metastatic colon cancer cells: roles of Fas, Apaf-1, NFkappaB, IAPs, Smac/DIABLO, and AIF. J Surg Res 142: 184-194.
33. Huerta S, Srivatsan ES, Venkatesan N, Peters J, Moatamed F, Renner S, Livingston EH (2001) Alternative mRNA splicing in colon cancer causes loss of expression of neural cell adhesion molecule. Surgery 130: 834-843.
34. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT (1992) Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci USA 89: 12180-12184.
35. Ochi H, Kondo K, Matsumoto K, Oki A, Yasugi T, Furuta R, Hirai Y, Yoshikawa H, Kanda T (2008) Neutralizing antibodies against human papillomavirus types 16, 18, 31, 52, and 58 in serum samples from women in Japan with low-grade cervical intraepithelial neoplasia. Clin Vaccine Immunol 15: 1536-1540.
36. Nakagawa M, Viscidi R, Deshmukh I, Costa MD, Palefsky JM, Farhat S, Moscicki AB (2002) Time course of humoral and cell-mediated immune responses to human papillomavirus type 16 in infected women. Clin Diagn Lab Immunol 9: 877-882.
37. Malik ZA, Hailpern SM, Burk RD (2009) Persistent antibodies to HPV virus-like particles following natural infection are protective against subsequent cervicovaginal infection with related and unrelated HPV. Viral Immunol 22: 445-449.
38. Wick DA, Webb JR (2011) A novel, broad spectrum therapeutic HPV vaccine targeting the E7 proteins of HPV16, 18, 31, 45 and 52 that elicits potent E7-specific CD8T cell immunity and regression of large, established, E7-expressing TC-1 tumors. Vaccine 29: 7857-7866.
39. Barrios K, Celis E (2012) TriVax-HPV: an improved peptide-based therapeutic vaccination strategy against human papillomavirus-induced cancers. Cancer Immunol Immunother 61: 1307-1317.
40. FUTURE I/II Study Group, Dillner J, Kjaer SK, Wheeler CM, Sigurdsson K, Iversen OE, Hernandez-Avila M, Perez G, Brown DR, Koutsky LA, Tay EH, García P, Ault KA, Garland SM, Leodolter S, Olsson SE, Tang GW, Ferris DG, Paavonen J, Lehtinen M, Steben M, Bosch FX, Joura EA, Majewski S, Muñoz N, Myers ER, Villa LL, Taddeo FJ, Roberts C, Tadesse A, Bryan JT, Maansson R, Lu S, Vuocolo S, Hesley TM, Barr E, Haupt R (2010) Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial. BMJ 341: c3493.
41. Stanley M (2010) HPV-immune response to infection and vaccination. Infect Agents Cancer 5: 19.
42. Schiller JT, Castellsagué X, Garland SM (2012) A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine 30S: F123-F138.
43. Jemal A, Simard EP, Dorell C, Noone A-M, Markowitz LE, Kohler B, Eheman C, Saraiya M, Bandi P, Saslow D, Cronin KA, Watson M, Mark Schiffman S, Henley J, Schymura MJ, Anderson RN, Yankey D, Edwards BK (2013) Annual report to the nation on the status of cancer, 1975-2009, featuring the burden and trends in human papillomavirus (HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst 105: 175-201.
44. Kuck D, Leder C, Kern A, Müller M, Piuko K, Gissmann L, Kleinschmidt JA (2006) Efficiency of HPV 16 L1/E7 DNA immunization: influence of cellular localization and capsid assembly. Vaccine 24: 2952-2965.
45. Zhang T, Xu Y, Qiao L, Wang Y, Wu X, Fan D, Peng Q, Xu X (2010) Trivalent human papillomavirus (HPV) VLP vaccine covering HPV type 58 can elicit high level of humoral immunity but also induce immune interference among component types. Vaccine 28: 3479-3487.
46. Combita AL, Bravo MM, Touze A, Orozco O, Coursaget P (2002) Serologic response to human oncogenic papillomavirus types 16, 18, 31, 33, 39, 58 and 59 virus-like particles in Colombian women with invasive cervical cancer. Int J Cancer 97: 796-803.
47. Combita AL, Touze A, Bousarghin L, Christensen ND, Coursaget P (2002) Identification of two cross-neutralizing linear epitopes within the L1 major capsid protein of human papillomaviruses. J Virol 76: 6480-6486.
48. Jenkins D (2008) A review of cross-protection against oncogenic HPV by an HPV-16/18 AS04-adjuvanted cervical cancer vaccine: importance of virological and clinical endpoints and implications for mass vaccination in cervical cancer prevention. Gynecol Oncol 110: S18-S25.
49. Paavonen J, Naud P, Salmerón J, Wheeler CM, Chow SN, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR, Hedrick J, Jaisamrarn U, Limson G, Garland S, Szarewski A, Romanowski B, Aoki FY, Schwarz TF, Poppe WA, Bosch FX, Jenkins D, Hardt K, Zahaf T, Descamps D, Struyf F, Lehtinen M, Dubin G, HPV PATRICIA Study Group (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.
50. Smith JF, Brownlow M, Brown M, Kowalski R, Esser MT, Ruiz W, Barr E, Brown DR, Bryan JT (2007) Antibodies from women immunized with Gardasil cross neutralize HPV 45 pseudovirions. Hum Vaccine 3: 109-115.
51. Kaufmann AM, Nieland J, Schinz M, Nonn M, Gabelsberger J, Meissner H, Müller RT, Jochmus I, Gissmann L, Schneider A, Dürst M (2001) HPV16 L1E7 chimeric virus-like particles induce specific HLA-restricted T cells in humans after in vitro vaccination. Int J Cancer 92: 285-293.
52. Rudolf MP, Fausch SC, Da Silva DM, Kast WM (2001) 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 166: 5917-5924.
53. Fausch SC, Da Silva DM, Kast WM (2003) Differential uptake and cross-presentation of human papillomavirus virus-like particles by dendritic cells and Langerhans cells. Cancer Res 63: 3478-3482.
54. Bellone S, El-Sahwi K, Cocco E, Casagrande F, Cargnelutti M, Palmieri M, Bignotti E, Romani C, Silasi DA, Azodi M, Schwartz PE, Rutherford TJ, Pecorelli S, Santin AD (2009) 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 83: 6779-6789.
55. Da Silva DM, Fausch SC, Verbeek JS, Kast WM (2007) Uptake of human papillomavirus virus-like particles by dendritic cells is mediated by Fcgamma receptors and contributes to acquisition of T cell immunity. J Immunol 178: 7587-7597.
56. Amigorena S, Bonnerot C (1999) Fc receptor signaling and trafficking: a connection for antigen processing. Immunol Rev 172: 279-284.
57. Rodriguez A, Regnault A, Kleijmeer M, Ricciardi-Castagnoli P, Amigorena S (1999) Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat Cell Biol 1: 362-368.
58. Regnault A, Lankar D, Lacabanne V, Rodriguez A, Thery C, Rescigno M, Saito T, Verbeek S, Bonnerot C, Ricciardi-Castagnoli P, Amigorena S (1999) Fc receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J Exp Med 189: 371-380.
59. De Jong JM, Schuurhuis DH, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Ossendorp F, Toes RE, Verbeek JS (2006) Murine Fc receptors for IgG are redundant in facilitating presentation of immune complex derived antigen to CD8 T cells in vivo. Mol Immunol 43: 2045-2050.
60. Da Silva DM, Velders MP, Nieland JD, Schiller JT, Nickoloff BJ, Kast WM (2001) Physical interaction of human papillomavirus virus-like particles with immune cells. Int Immunol 13: 633-641.
61. Fausch SC, Da Silva DM, Kast WM (2005) Heterologous papillomavirus virus-like particles and human papillomavirus virus-like particle immune complexes activate human Langerhans cells. Vaccine 23: 1720-1729.