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[Cancer Research 56, 21-26, January 1, 1996]
© 1996 American Association for Cancer Research
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Treatment of Established Tumors with a Novel Vaccine That Enhances Major Histocompatibility Class II Presentation of Tumor Antigen1

Ken-Yu Lin, Frank G. Guarnieri, Kevin F. Staveley-O'Carroll, Hyam I. Levitsky, J. Thomas August, Drew M. Pardoll and Tzyy-Choou Wu2

Departments of Pathology [K-Y. L., T-C. W.], Pharmacology and Molecular Science [F. G. G., J. T. A.], Surgery [K. F. S-O.], and Oncology [H. I. L., J. T. A., D. M. P.], The Johns Hopkins Medical Institutions, Baltimore, Maryland 21287-6417

Presentation of antigenic peptides by MHC class II molecules to CD4+ T cells is critical to the generation of antitumor immunity. In an attempt to enhance MHC class II antigen processing, we linked the sorting signals of the lysosome-associated membrane protein (LAMP-1) to the cytoplasmic/nuclear human papilloma virus (HPV-16) E7 antigen, creating a chimera (Sig/E7/LAMP-1). Previously, we found that expression of this chimera in vitro and in vivo with a recombinant vaccinia vector targeted E7 to endosomal and lysosomal compartments and enhanced MHC class II presentation to CD4+ T cells compared to vaccinia expressing wild-type E7. In the current study, we tested these recombinant vaccinia for in vivo protection against an E7+ tumor, TC-1, which was derived from primary epithelial cells of C57BL/6 mice cotransformed with HPV-16 E6 and E7 and c-Ha-ras oncogenes. All mice vaccinated with 1 x 107 plaque-forming units of wild-type E7-vaccinia showed progressive tumor growth when challenged with a tumorigenic dose of TC-1 tumor cells; in contrast, 80% of mice vaccinated with the chimeric Sig/E7/LAMP1 vaccinia remained tumor free 3 months after tumor injection. Furthermore, treatment with the Sig/E7/LAMP-1 vaccinia vaccine cured mice with small established TC-1 tumors, whereas the wild-type E7-vaccinia showed no effect on this established tumor burden. These findings point out the therapeutic limitations of recombinant vaccinia expressing unmodified tumor antigens. Further, they demonstrate that modifications that reroute a cytosolic tumor antigen to the endosomal/lysosomal compartment can profoundly improve the in vivo therapeutic potency of recombinant vaccines.

1 This work was supported by NIH Grants 5 PO1 34582-01 and P50 CA62924, and by a gift from Mr. and Mrs. Zandy Leaderman. F. G. G. was supported by the Gustavus and Louise Pfeiffer Research Foundation.

2 To whom requests for reprints should be addressed, at Department of Pathology, The Johns Hopkins Hospital, 600 North Wolfe Street, Baltimore, MD 21287. Phone: (410) 614-3899; Fax: (410) 614-3548.

Received 10/27/95. Accepted 11/22/95.




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S. Zwaveling, S. C. F. Mota, J. Nouta, M. Johnson, G. B. Lipford, R. Offringa, S. H. van der Burg, and C. J. M. Melief
Established Human Papillomavirus Type 16-Expressing Tumors Are Effectively Eradicated Following Vaccination with Long Peptides
J. Immunol., July 1, 2002; 169(1): 350 - 358.
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M. C. Wolkers, M. Toebes, M. Okabe, J. B. A. G. Haanen, and T. N. M. Schumacher
Optimizing the Efficacy of Epitope-Directed DNA Vaccination
J. Immunol., May 15, 2002; 168(10): 4998 - 5004.
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M. H. Manjili, R. Henderson, X.-Y. Wang, X. Chen, Y. Li, E. Repasky, L. Kazim, and J. R. Subjeck
Development of a Recombinant HSP110-HER-2/neu Vaccine Using the Chaperoning Properties of HSP110
Cancer Res., March 1, 2002; 62(6): 1737 - 1742.
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C.-F. Hung, L. He, J. Juang, T.-J. Lin, M. Ling, and T.-C. Wu
Improving DNA Vaccine Potency by Linking Marek's Disease Virus Type 1 VP22 to an Antigen
J. Virol., February 22, 2002; 76(6): 2676 - 2682.
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G. R. Gunn, A. Zubair, C. Peters, Z.-K. Pan, T.-C. Wu, and Y. Paterson
Two Listeria monocytogenes Vaccine Vectors That Express Different Molecular Forms of Human Papilloma Virus-16 (HPV-16) E7 Induce Qualitatively Different T Cell Immunity That Correlates with Their Ability to Induce Regression of Established Tumors Immortalized by HPV-16
J. Immunol., December 1, 2001; 167(11): 6471 - 6479.
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F. Rodriguez, S. Harkins, J. M. Redwine, J. M. de Pereda, and J. L. Whitton
CD4+ T Cells Induced by a DNA Vaccine: Immunological Consequences of Epitope-Specific Lysosomal Targeting
J. Virol., November 1, 2001; 75(21): 10421 - 10430.
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M. P. Velders, S. McElhiney, M. C. Cassetti, G. L. Eiben, T. Higgins, G. R. Kovacs, A. G. Elmishad, W. M. Kast, and L. R. Smith
Eradication of Established Tumors by Vaccination with Venezuelan Equine Encephalitis Virus Replicon Particles Delivering Human Papillomavirus 16 E7 RNA
Cancer Res., November 1, 2001; 61(21): 7861 - 7867.
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A. Lamikanra, Z.-K. Pan, S. N. Isaacs, T.-C. Wu, and Y. Paterson
Regression of Established Human Papillomavirus Type 16 (HPV-16) Immortalized Tumors In Vivo by Vaccinia Viruses Expressing Different Forms of HPV-16 E7 Correlates with Enhanced CD8+ T-Cell Responses That Home to the Tumor Site
J. Virol., October 15, 2001; 75(20): 9654 - 9664.
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 Proc. Natl. Acad. Sci. USAHome page
J. P. Medema, J. de Jong, L. T. C. Peltenburg, E. M. E. Verdegaal, A. Gorter, S. A. Bres, K. L. M. C. Franken, M. Hahne, J. P. Albar, C. J. M. Melief, et al.
Blockade of the granzyme B/perforin pathway through overexpression of the serine protease inhibitor PI-9/SPI-6 constitutes a mechanism for immune escape by tumors
PNAS, September 13, 2001; (2001) 201398198.
[Abstract] [Full Text] [PDF]

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R. W. Tindle, K. Herd, T. Doan, G. Bryson, G. R. Leggatt, P. Lambert, I. H. Frazer, and M. Street
Nonspecific Down-Regulation of CD8+ T-Cell Responses in Mice Expressing Human Papillomavirus Type 16 E7 Oncoprotein from the Keratin-14 Promoter
J. Virol., July 1, 2001; 75(13): 5985 - 5997.
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 Cancer Res.Home page
J. D. Heller, J. Kuo, T. C. Wu, W. M. Kast, and R. C. C. Huang
Tetra-O-methyl Nordihydroguaiaretic Acid Induces G2 Arrest in Mammalian Cells and Exhibits Tumoricidal Activity in Vivo
Cancer Res., July 1, 2001; 61(14): 5499 - 5504.
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W.-F. Cheng, C.-F. Hung, C.-Y. Chai, K.-F. Hsu, L. He, C. M. Rice, M. Ling, and T.-C. Wu
Enhancement of Sindbis Virus Self-Replicating RNA Vaccine Potency by Linkage of Mycobacterium tuberculosis Heat Shock Protein 70 Gene to an Antigen Gene
J. Immunol., May 15, 2001; 166(10): 6218 - 6226.
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 Cancer Res.Home page
C.-F. Hung, W.-F. Cheng, K.-F. Hsu, C.-Y. Chai, L. He, M. Ling, and T-C. Wu
Cancer Immunotherapy Using a DNA Vaccine Encoding the Translocation Domain of a Bacterial Toxin Linked to a Tumor Antigen
Cancer Res., May 1, 2001; 61(9): 3698 - 3703.
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C.-F. Hung, W.-F. Cheng, C.-Y. Chai, K.-F. Hsu, L. He, M. Ling, and T.-C. Wu
Improving Vaccine Potency Through Intercellular Spreading and Enhanced MHC Class I Presentation of Antigen
J. Immunol., May 1, 2001; 166(9): 5733 - 5740.
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C. Bonini, S. P. Lee, S. R. Riddell, and P. D. Greenberg
Targeting Antigen in Mature Dendritic Cells for Simultaneous Stimulation of CD4+ and CD8+ T Cells
J. Immunol., April 15, 2001; 166(8): 5250 - 5257.
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B. Wu, J.-M. Wu, A. Miagkov, R. N. Adams, H. I. Levitsky, and D. B. Drachman
Specific Immunotherapy by Genetically Engineered APCs: The ""Guided Missile"" Strategy
J. Immunol., April 1, 2001; 166(7): 4773 - 4779.
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W.-F. Cheng, C.-F. Hung, C.-Y. Chai, K.-F. Hsu, L. He, M. Ling, and T.-C. Wu
Enhancement of Sindbis Virus Self-Replicating RNA Vaccine Potency by Linkage of Herpes Simplex Virus Type 1 VP22 Protein to Antigen
J. Virol., March 1, 2001; 75(5): 2368 - 2376.
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 Cancer Res.Home page
C.-F. Hung, K.-F. Hsu, W.-F. Cheng, C.-Y. Chai, L. He, M. Ling, and T-C. Wu
Enhancement of DNA Vaccine Potency by Linkage of Antigen Gene to a Gene Encoding the Extracellular Domain of Fms-like Tyrosine Kinase 3-Ligand
Cancer Res., February 1, 2001; 61(3): 1080 - 1088.
[Abstract] [Full Text]

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 Cancer Res.Home page
J. van Bergen, M. Camps, R. Offringa, C. J. M. Melief, F. Ossendorp, and F. Koning
Superior Tumor Protection Induced by a Cellular Vaccine Carrying a Tumor-specific T Helper Epitope by Genetic Exchange of the Class II-associated Invariant Chain Peptide
Cancer Res., November 1, 2000; 60(22): 6427 - 6433.
[Abstract] [Full Text]

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D.-W. Liu, Y.-P. Tsao, C.-H. Hsieh, J.-T. Hsieh, J. T. Kung, C.-L. Chiang, S.-J. Huang, and S.-L. Chen
Induction of CD8 T Cells by Vaccination with Recombinant Adenovirus Expressing Human Papillomavirus Type 16 E5 Gene Reduces Tumor Growth
J. Virol., October 1, 2000; 74(19): 9083 - 9089.
[Abstract] [Full Text]

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 Cancer Res.Home page
M. P. M. Vierboom, S. Zwaveling, G. M. J. Bos, M. Ooms, G. M. Krietemeijer, C. J. M. Melief, and R. Offringa
High Steady-State Levels of p53 Are Not a Prerequisite for Tumor Eradication by Wild-Type p53-specific Cytotoxic T Lymphocytes
Cancer Res., October 1, 2000; 60(19): 5508 - 5513.
[Abstract] [Full Text]

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D.-W. Liu, Y.-P. Tsao, J. T. Kung, Y.-A. Ding, H.-K. Sytwu, X. Xiao, and S.-L. Chen
Recombinant Adeno-Associated Virus Expressing Human Papillomavirus Type 16 E7 Peptide DNA Fused with Heat Shock Protein DNA as a Potential Vaccine for Cervical Cancer
J. Virol., March 15, 2000; 74(6): 2888 - 2894.
[Abstract] [Full Text]

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 Cancer Res.Home page
C.-H. Chen, T.-L. Wang, C.-F. Hung, Y. Yang, R. A. Young, D. M. Pardoll, and T-C. Wu
Enhancement of DNA Vaccine Potency by Linkage of Antigen Gene to an HSP70 Gene
Cancer Res., February 1, 2000; 60(4): 1035 - 1042.
[Abstract] [Full Text]

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W. Shi, P. Bu, J. Liu, A. Polack, S. Fisher, and L. Qiao
Human Papillomavirus Type 16 E7 DNA Vaccine: Mutation in the Open Reading Frame of E7 Enhances Specific Cytotoxic T-Lymphocyte Induction and Antitumor Activity
J. Virol., September 1, 1999; 73(9): 7877 - 7881.
[Abstract] [Full Text]

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T. F. Greten and E. M. Jaffee
Cancer Vaccines
J. Clin. Oncol., March 1, 1999; 17(3): 1047 - 1047.
[Abstract] [Full Text] [PDF]

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P. Chaux, V. Vantomme, V. Stroobant, K. Thielemans, J. Corthals, R. Luiten, A. M.M. Eggermont, T. Boon, and P. van der Bruggen
Identification of MAGE-3 Epitopes Presented by HLA-DR Molecules to CD4+ T Lymphocytes
J. Exp. Med., March 1, 1999; 189(5): 767 - 778.
[Abstract] [Full Text] [PDF]

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G. J. P. Fernando, T. J. Stewart, R. W. Tindle, and I. H. Frazer
Th2-Type CD4+ Cells Neither Enhance nor Suppress Antitumor CTL Activity in a Mouse Tumor Model
J. Immunol., September 1, 1998; 161(5): 2421 - 2427.
[Abstract] [Full Text] [PDF]

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D. R. Lowy and J. T. Schiller
Papillomaviruses and Cervical Cancer: Pathogenesis and Vaccine Development
J Natl Cancer Inst Monographs, April 1, 1998; 1998(23): 27 - 30.
[Abstract] [Full Text]

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S. A. Thomson, S. R. Burrows, I. S. Misko, D. J. Moss, B. E. H. Coupar, and R. Khanna
Targeting a Polyepitope Protein Incorporating Multiple Class II-Restricted Viral Epitopes to the Secretory/Endocytic Pathway Facilitates Immune Recognition by CD4+ Cytotoxic T Lymphocytes: a Novel Approach to Vaccine Design
J. Virol., March 1, 1998; 72(3): 2246 - 2252.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
H. L. Greenstone, J. D. Nieland, K. E. de Visser, M. L. H. De Bruijn, R. Kirnbauer, R. B. S. Roden, D. R. Lowy, W. M. Kast, and J. T. Schiller
Chimeric papillomavirus virus-like particles elicit antitumor immunity against the E7 oncoprotein in an HPV16 tumor model
PNAS, February 17, 1998; 95(4): 1800 - 1805.
[Abstract] [Full Text] [PDF]

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T. Tuting, C. C. Wilson, D. M. Martin, Y. L. Kasamon, J. Rowles, D. I. Ma, C. L. Slingluff Jr., S. N. Wagner, P. van der Bruggen, J. Baar, et al.
Autologous Human Monocyte-Derived Dendritic Cells Genetically Modified to Express Melanoma Antigens Elicit Primary Cytotoxic T Cell Responses In Vitro: Enhancement by Cotransfection of Genes Encoding the Th1-Biasing Cytokines IL-12 and IFN-{alpha}
J. Immunol., February 1, 1998; 160(3): 1139 - 1147.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
S. Osanto
Vaccine Trials for the Clinician: Prospects for Tumor Antigens
Oncologist, October 1, 1997; 2(5): 284 - 299.
[Abstract] [Full Text] [PDF]

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A. L. Ruff, F. G. Guarnieri, K. Staveley-O'Carroll, R. F. Siliciano, and J. T. August
The Enhanced Immune Response to the HIV gp160/LAMP Chimeric Gene Product Targeted to the Lysosome Membrane Protein Trafficking Pathway
J. Biol. Chem., March 28, 1997; 272(13): 8671 - 8678.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J. P. Medema, J. de Jong, L. T. C. Peltenburg, E. M. E. Verdegaal, A. Gorter, S. A. Bres, K. L. M. C. Franken, M. Hahne, J. P. Albar, C. J. M. Melief, et al.
Blockade of the granzyme B/perforin pathway through overexpression of the serine protease inhibitor PI-9/SPI-6 constitutes a mechanism for immune escape by tumors
PNAS, September 25, 2001; 98(20): 11515 - 11520.
[Abstract] [Full Text] [PDF]


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