Recombinant HPV16 E7 assembled into particles induces an immune response and specific tumour protection administered without adjuvant in an animal model

Journal of Translational Medicine

Volumn 9, Issue , 2011, Pages

  Petrone, Linda ^a   Ammendolia, Maria G ^a   Cesolini, Armando ^a   Caimi, Stefano ^a   Superti, Fabiana ^a   Giorgi, Colomba ^a   Di Bonito, Paola ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLUTATHIONE TRANSFERASE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; OLIGOMER; PROTEIN E7; RECOMBINANT PROTEIN; ZINC ION; IMMUNOLOGICAL ADJUVANT; ONCOGENE PROTEIN E7, HUMAN PAPILLOMAVIRUS TYPE 16;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CANCER IMMUNIZATION; CANCER INHIBITION; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG DETERMINATION; DRUG MECHANISM; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSPOT ASSAY; ESCHERICHIA COLI; FEMALE; HUMAN PAPILLOMAVIRUS TYPE 16; HUMORAL IMMUNITY; IMMUNE RESPONSE; LYMPHOCYTE PROLIFERATION; MASS SPECTROMETRY; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PARTICLE SIZE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; TH1 CELL; TH2 CELL; TUMOR CELL; TUMOR IMMUNITY; WESTERN BLOTTING; ANIMAL; ANTIBODY PRODUCTION; C57BL MOUSE; CHEMISTRY; DISEASE MODEL; IMMUNITY; IMMUNOLOGY; NEOPLASM; ULTRASTRUCTURE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODY FORMATION; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; IMMUNITY; IMMUNITY, CELLULAR; MICE; MICE, INBRED C57BL; NEOPLASMS; PAPILLOMAVIRUS E7 PROTEINS; RECOMBINANT PROTEINS;

EID: 79955973570     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-9-69     Document Type: Article

References (47)

1. Zur Hausen H. Papillomavirus infections: A Major Cause of Human Cancer. Infections Causing Human Cancer 2006, 145-243. Weinheim: WILEY-VCH Verlag GmbH & Co. KGaA, Harald zur Hausen.
2. Wise-Draper TM, Wells SI. Papillomavirus E6 and E7 proteins and their cellular targets. Frontiers in Bioscience 2008, 13:1003-1017. 10.2741/2739, 17981607.
3. McLaughlin-Drubin ME, Münger K. The human papillomavirus E7 oncoprotein. Virology 2009, 384:335-344. 10.1016/j.virol.2008.10.006, 2661820, 19007963.
4. Ghittoni R, Accardi R, Hasan U, Gheit T, Sylla B, Tommasino M. The biological properties of E6 and E7 oncoproteins from human papillomaviruses. Virus Genes 2009, 40:1-13.
5. Alonso LG, Smal C, Garcia-Alai MM, Chemes L, Salame M, de Prat-Gay G. Chaperone holdase activity of human papillomavirus E7 oncoprotein. Biochemistry 2006, 45:657-667. 10.1021/bi0522549, 16411741.
6. Coulie PG, Weynants P, Lehmann F, Herman J, Brichard V, Wölfel T, Van Pel A, De Plaen E, Brasseur F, Boon T. Genes coding for tumor antigens recognized by human cytolytic T lymphocytes. J Immunother Emphasis Tumor Immunol 1993, 14:104-109.
7. Hellner K, Münger K. Human Papillomaviruses As Therapeutic Targets in Human Cancer. J Clin Oncol 2011, Published online ahead of print on Jan 10 at., http://jco.ascopubs.org/content/29/13/1785.full?sid=23bbb452-d962-4f56-acaa-4a40c9093c56
8. Su JH, Wu A, Scotney E, Ma B, Monie A, Hung CF, Wu TC. Immunotherapy for cervical cancer: Research status and clinical potential. BioDrugs 2010, 24:109-129. 10.2165/11532810-000000000-00000, 2913436, 20199126.
9. van der Burg SH, Melief CJ. Therapeutic vaccination against human papillomavirus induced malignancies. Curr Opin Immunol 2011, 23:1-6. 10.1016/j.coi.2010.12.001, 21185707.
10. Barbosa MS, Lowy DR, Schiller JT. Papillomavirus polypeptides E6 and E7 are zinc-binding proteins. J Virol 1989, 63:1404-1407. 247840, 2536841.
11. McIntyre MC, Frattini MG, Grossmon S, Laimons LA. Human papillomavirus type 18 E7 protein requires intact Cys-X-X-Cys motifs for zinc binding, dimerization, and transformation but not for Rb binding. J Virol 1993, 67:3142-3150. 237652, 8497045.
12. Pahel G, Aulabaugh A, Short SA, Barnes JA, Painter GR, Ray P, Phelps WC. Structural and functional characterization of the HPV16 E7 protein expressed in bacteria. J Biol Chem 1993, 68:26018-26025.
13. Alonso LG, Garcia-Alai MM, Nadra AD, Lapena AN, Almeida FL, Gualfetti P, de Prat-Gay G. High-risk (HPV16) human papillomavirus E7 oncoprotein is highly stable and extended, with conformational transitions that could explain its multiple cellular binding partners. Biochemistry 2002, 41:10510-10518. 10.1021/bi025579n, 12173938.
14. Patrick DR, Zhang K, Defeo-Jones D, Vuocolo GR, Maigetter RZ, Sardana MK, Oliff A, Heimbrook DC. Characterization of functional HPV-16 E7 protein produced in Escherichia coli. J Biol Chem 1992, 267:6910-6915.
15. Sato H, Watanabe S, Furuno A, Yoshiike K. Human papillomavirus type 16 E7 protein expressed in Escherichia coli and monkey COS-1 cells: immunofluorescence detection of the nuclear E7 protein. Virology 1989, 170:311-315. 10.1016/0042-6822(89)90386-3, 2541550.
16. Tommasino M, Contorni M, Scarlato V, Bugnoli M, Maundrell K, Cavalieri F. Synthesis, phosphorylation, and nuclear localization of human papillomavirus E7 protein in Schizosaccharomyces pombe. Gene 1990, 93:265-270. 10.1016/0378-1119(90)90234-I, 2172091.
17. Carter JJ, Yaegashi N, Jenison SA, Galloway DA. Expression of human papillomavirus proteins in yeast Saccharomyces cerevisiae. Virology 1991, 182:513-521. 10.1016/0042-6822(91)90592-Y, 1850917.
18. Patrick DR, Zhang K, Defeo-Jones D, Vuocolo GR, Maigetter RZ, Sardana MK, Oliff A, Heimbrook DC. Characterization of functional HPV-16 E7 protein produced in Escherichia coli. J Biol Chem 1992, 267:6910-6915.
19. Park DS, Selvey LA, Kelsall SR, Frazer IH. Human papillomavirus type 16 E6, E7 and L1 and type 18 E7 proteins produced by recombinant baculoviruses. J Virol Methods 1993, 45:303-318. 10.1016/0166-0934(93)90115-8, 8106603.
20. Chinami M, Sasaki S, Hachiya N, Yuge K, Ohsugi T, Maeda H, Shingu M. Functional oligomerization of purified human papillomavirus types 16 and 6b E7 proteins expressed in Escherichia coli. J Gen Virol 1994, 75:277-281. 10.1099/0022-1317-75-2-277, 8113748.
21. Clemens KE, Brent R, Gyuris J, Münger K. Dimerization of the human papillomavirus E7 oncoprotein in vivo. Virology 1995, 214:289-293. 10.1006/viro.1995.9926, 8525630.
22. Zwerschke W, Joswig S, Jansen-Dürr P. Identification of domains required for transcriptional activation and protein dimerization in the human papillomavirus type-16 E7 protein. Oncogene 1996, 12:213-220.
23. Clements A, Johnston K, Mazzarelli JM, Ricciardi RP, Marmorstein R. Oligomerization properties of the viral oncoproteins adenovirus E1A and human papillomavirus E7 and their complexes with the retinoblastoma protein. Biochemistry 2000, 39:16033-16045. 10.1021/bi002111g, 11123931.
24. Mirecka EA, Rudolph R, Hey T. Expression and purification of His-tagged HPV16 E7 protein active in pRb binding. Protein Expr Purif 2006, 48:281-291.
25. Franconi R, Di Bonito P, Dibello F, Accardi L, Muller A, Cirilli A, Simeone P, Donà G, Venuti A, Giorgi C. Plant-derived human papillomavirus 16 E7 oncoprotein induces immune response and specific tumor protection. Cancer Research 2002, 62:3654-3658.
26. Massa S, Simeone P, Muller A, Benvenuto E, Venuti A, Franconi R. Antitumor activity of DNA vaccines based on the human papillomavirus-16 E7 protein genetically fused to a plant virus coat protein. Hum Gene Ther 2008, 19:354-364. 10.1089/hum.2007.122, 18439124.
27. Alonso LG, García-Alai MM, Smal C, Centeno JM, Iacono R, Castaño E, Gualfetti P, de Prat-Gay G. The HPV16 E7 viral oncoprotein self-assembles into defined spherical oligomers. Biochemistry 2004, 43:3310-3317. 10.1021/bi036037o, 15035602.
28. Di Lonardo A, Marcante ML, Poggiali F, Venuti A. HPV 16 E7 antibody levels in cervical cancer patients: before and after treatment. J Med Virol 1998, 54:192-195. 10.1002/(SICI)1096-9071(199803)54:3<192::AID-JMV9>3.0.CO;2-0, 9515768.
29. Waterboer T, Sehr P, Michael KM, Franceschi S, Nieland JD, Joos TO, Templin MF, Pawlita M. Multiplex human papillomavirus serology based on in situ-purified glutathione S-transferase fusion proteins. Clin Chem 2005, 51:1845-1853. 10.1373/clinchem.2005.052381, 16099939.
30. Di Bonito P, Grasso F, Mochi S, Accardi L, Donà MG, Branca M, Costa S, Mariani L, Agarossi A, Ciotti M, Syrjänen K, Giorgi C. Serum antibody response to Human papillomavirus (HPV) infections detected by a novel ELISA technique based on denatured recombinant HPV16 L1, L2, E4, E6 and E7 proteins. Infect Agent Cancer 2006, 8:1-6.
31. Ferguson M, Heath A, Johnes S, Pagliusi S, Dillner J. Results of the first WHO international collaborative study on the standardization of the detection of antibodies to human papillomaviruses. Int J Cancer 2006, 118:1508-1514. 10.1002/ijc.21515, 16184553.
32. Lin KY, Guarnieri FG, Staveley-O'Carroll KF, Levitsky HI, August JT, Pardoll DM, Wu TC. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res 1996, 56:21-26.
33. Ramachandra L, Simmons D, Harding CV. MHC molecules and microbial antigen processing in phagosomes. Curr Opin Immunol 2009, 21:98-104. 10.1016/j.coi.2009.01.001, 19217269.
34. Di Bonito P, Grasso F, Mangino G, Massa S, Illiano E, Franconi R, Fanales-Belasio E, Falchi M, Affabris E, Giorgi C. Immunomodulatory activity of a plant extract containing human papillomavirus 16-E7 protein in human monocyte-derived dendritic cells. Int J Immunopathol Pharmacol 2009, 22:967-978.
35. Di Bonito P, Grasso F, Mochi S, Petrone L, Fanales-Belasio E, Mei A, Cesolini A, Laconi G, Conrad H, Bernhard H, Dembek CJ, Cosma A, Santini SM, 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. 10.1016/j.virol.2009.09.012, 19800648.
36. Bauer S, Heeg K, Wagner H, Lipford GB. Identification of H-2Kb binding and immunogenic peptides from human papilloma virus tumour antigens E6 and E7. Scand J Immunol 1995, 42:317-323. 10.1111/j.1365-3083.1995.tb03662.x, 7660065.
37. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 2008, 8:34-47. 10.1038/nri2206, 18064051.
38. John E, Laskow TC, Buchser WJ, Pitt BR, Basse PH, Butterfield LH, Kalinski P, Lotze MT. Zinc in innate and adaptive tumor immunity. J Transl Med 2010, 8:118. 10.1186/1479-5876-8-118, 3002329, 21087493.
39. Nandedkar TD. Nanovaccines: recent developments in vaccination. J Biosci 2009, 34:995-1003. 10.1007/s12038-009-0114-3, 20093753.
40. Oyewumi MO, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Rev Vaccines 2010, 9:1095-1107. 10.1586/erv.10.89, 20822351.
41. Dantur K, Alonso L, Castaño E, Morelli L, Centeno-Crowley JM, Vighi S, de Prat-Gay G. Cytosolic accumulation of HPV16 E7 oligomers supports different transformation routes for the prototypic viral oncoprotein: the amyloid-cancer connection. Int J Cancer 2009, 125:1902-1911. 10.1002/ijc.24579, 19598264.
42. Valdovinos-Torres H, Orozco-Morales M, Pedroza-Saavedra A, Padilla-Noriega L, Esquivel-Guadarrama F, Gutierrez-Xicotencatl L. Different Isoforms of HPV-16 E7 Protein are Present in Cytoplasm and Nucleus. Open Virol J 2008, 2:15-23. 10.2174/1874357900802010015, 2678815, 19440460.
43. Knapp AA, McManus PM, Bockstall K, Moroianu J. Identification of the nuclear localization and export signals of high risk HPV16 E7 oncoprotein. Virology 2009, 383:60-68. 10.1016/j.virol.2008.09.037, 2646614, 18996550.
44. Nestle FO, Di Meglio P, Qin JZ, Nickoloff BJ. Skin immune sentinels in health and disease. Nat Rev Immunol 2009, 8:679-691.
45. Schädlich L, Senger T, Kirschning CJ, Müller M, Gissmann L. Refining HPV 16 L1 purification from E. coli: reducing endotoxin contaminations and their impact on immunogenicity. Vaccine 2009, 27:1511-1522. 10.1016/j.vaccine.2009.01.014, 19174177.
46. Bian T, Wang Y, Lu Z, Ye Z, Zhao L, Ren J, Zhang H, Ruan L, Tian H. Human papillomavirus type 16 L1E7 chimeric capsomeres have prophylactic and therapeutic efficacy against papillomavirus in mice. Mol Cancer Ther 2008, 7:1329-1335. 10.1158/1535-7163.MCT-07-2015, 18483320.
47. Rubio I, Bolchi A, Moretto N, Canali E, Gissmann L, Tommasino M. Potent anti-HPV immune responses induced by tandem repeats of the HPV16 L2 (20-38) peptide displayed on bacterial thioredoxin. Vaccine 2009, 27:1949-1956. 10.1016/j.vaccine.2009.01.102, 19368776.