Immune-mediated regression of established B16F10 melanoma by intratumoral injection of attenuated Toxoplasma gondii protects against rechallenge

Journal of Immunology

Volumn 190, Issue 1, 2013, Pages 469-478

  Baird, Jason R ^a   Byrne, Katelyn T ^a   Lizotte, Patrick H ^a   Toraya Brown, Seiko ^a   Scarlett, Uciane K ^a   Alexander, Matthew P ^a   Sheen, Mee Rie ^a   Fox, Barbara A ^a   Bzik, David J ^a   Bosenberg, Marcus ^b   Mullins, David W ^a,c   Turk, Mary Jo ^a,c   Fiering, Steven ^a,c  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NORRIS COTTON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON; INTERLEUKIN 12; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CANCER REGRESSION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; CUTANEOUS MELANOMA; CYTOKINE RELEASE; DRUG EFFICACY; HUMAN; HUMAN CELL; IMMUNOLOGICAL MEMORY; IN VIVO STUDY; MELANOMA B16F10; MONOTHERAPY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TOXOPLASMA GONDII; TRANSPLANTABLE SOLID TUMORS; TREATMENT OUTCOME; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CANCER VACCINES; CELL LINE, TUMOR; INJECTIONS, INTRADERMAL; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MICE, TRANSGENIC; NEOPLASM RECURRENCE, LOCAL; SKIN NEOPLASMS; TOXOPLASMA; TUMOR ESCAPE; VACCINES, ATTENUATED;

EID: 84871843085     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201209     Document Type: Article

References (39)

1. Coley, W. B. 1991. The treatment of malignant tumors by repeated inoculations of erysipelas: with a report of ten original cases: 1893. Clin. Orthop. Relat. Res. 262: 3-11.
2. Sylvester, R. J., A. P. van der Meuden, and D. L. Lamm. 2002. Intravesical bacillus Calmette-Guerin reduces the risk of progression in patients with superficial bladder cancer: a meta-analysis of the published results of randomized clinical trials. J. Urol. 168: 1964-1970.
3. Gravekamp, C., and Y. Paterson. 2010. Harnessing Listeria monocytogenes to target tumors. Cancer Biol. Ther. 9: 257-265.
4. Manuel, E. R., C. A. Blache, R. Paquette, T. I. Kaltcheva, H. Ishizaki, J. D. Ellenhorn, M. Hensel, L. Metelitsa, and D. J. Diamond. 2011. Enhancement of cancer vaccine therapy by systemic delivery of a tumor-targeting Salmonellabased STAT3 shRNA suppresses the growth of established melanoma tumors. Cancer Res. 71: 4183-4191.
5. Paterson, Y., P. D. Guirnalda, and L. M. Wood. 2010. Listeria and Salmonella bacterial vectors of tumor-associated antigens for cancer immunotherapy. Semin. Immunol. 22: 183-189.
6. Fox, B. A., and D. J. Bzik. 2002. De novo pyrimidine biosynthesis is required for virulence of Toxoplasma gondii. Nature 415: 926-929. (Pubitemid 34174756)
7. Gigley, J. P., B. A. Fox, and D. J. Bzik. 2009. Cell-mediated immunity to Toxoplasma gondii develops primarily by local Th1 host immune responses in the absence of parasite replication. J. Immunol. 182: 1069-1078.
8. Wang, J., S. Saffold, X. Cao, J. Krauss, and W. Chen. 1998. Eliciting T cell immunity against poorly immunogenic tumors by immunization with dendritic cell-tumor fusion vaccines. J. Immunol. 161: 5516-5524. (Pubitemid 28519115)
9. Amos, S. M., H. J. Pegram, J. A. Westwood, L. B. John, C. Devaud, C. J. Clarke, N. P. Restifo, M. J. Smyth, P. K. Darcy, and M. H. Kershaw. 2011. Adoptive immunotherapy combined with intratumoral TLR agonist delivery eradicates established melanoma in mice. Cancer Immunol. Immunother. 60: 671-683.
10. Klebanoff, C. A., L. Gattinoni, D. C. Palmer, P. Muranski, Y. Ji, C. S. Hinrichs, Z. A. Borman, S. P. Kerkar, C. D. Scott, S. E. Finkelstein, et al. 2011. Determinants of successful CD8+ T-cell adoptive immunotherapy for large established tumors in mice. Clin. Cancer Res. 17: 5343-5352.
11. Scarlett, U. K., M. R. Rutkowski, A. M. Rauwerdink, J. Fields, X. Escovar-Fadul, J. Baird, J. R. Cubillos-Ruiz, A. C. Jacobs, J. L. Gonzalez, J. B. Weaver, et al. 2012. Ovarian cancer progression is controlled by phenotypic changes in dendritic cells. J. Exp. Med. 209: 495-506.
12. Tenter, A. M., A. R. Heckeroth, and L. M. Weiss. 2000. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30: 1217-1258.
13. Zenner, L., A. Foulet, Y. Caudrelier, F. Darcy, B. Gosselin, A. Capron, and M. F. Cesbron-Delauw. 1999. Infection with Toxoplasma gondii RH and Prugniaud strains in mice, rats and nude rats: kinetics of infection in blood and tissues related to pathology in acute and chronic infection. Pathol. Res. Pract. 195: 475-485. (Pubitemid 29361383)
14. Shultz, L. D., B. L. Lyons, L. M. Burzenski, B. Gott, X. Chen, S. Chaleff, M. Kotb, S. D. Gillies, M. King, J. Mangada, et al. 2005. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174: 6477-6489. (Pubitemid 40663843)
15. Gross, U., W. A. Müller, S. Knapp, and J. Heesemann. 1991. Identification of a virulence-associated antigen of Toxoplasma gondii by use of a mouse monoclonal antibody. Infect. Immun. 59: 4511-4516.
16. Hunter, C. A., D. Yu, M. Gee, C. V. Ngo, C. Sevignani, M. Goldschmidt, T. V. Golovkina, S. Evans, W. F. Lee, and A. Thomas-Tikhonenko. 2001. Cutting edge: systemic inhibition of angiogenesis underlies resistance to tumors during acute toxoplasmosis. J. Immunol. 166: 5878-5881. (Pubitemid 32440710)
17. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259: 1739-1742. (Pubitemid 23114658)
18. Murphy, C. A., C. L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R. A. Kastelein, J. D. Sedgwick, and D. J. Cua. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198: 1951-1957. (Pubitemid 38032126)
19. Musha, H., H. Ohtani, T. Mizoi, M. Kinouchi, T. Nakayama, K. Shiiba, K. Miyagawa, H. Nagura, O. Yoshie, and I. Sasaki. 2005. Selective infiltration of CCR5(+)CXCR3(+) T lymphocytes in human colorectal carcinoma. Int. J. Cancer 116: 949-956. (Pubitemid 41209203)
20. LaRosa, D. F., J. S. Stumhofer, A. E. Gelman, A. H. Rahman, D. K. Taylor, C. A. Hunter, and L. A. Turka. 2008. T cell expression of MyD88 is required for resistance to Toxoplasma gondii. Proc. Natl. Acad. Sci. USA 105: 3855-3860. (Pubitemid 351723489)
21. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122. (Pubitemid 29359962)
22. Ibrahim, H. M., H. Bannai, X. Xuan, and Y. Nishikawa. 2009. Toxoplasma gondii cyclophilin 18-mediated production of nitric oxide induces Bradyzoite conversion in a CCR5-dependent manner. Infect. Immun. 77: 3686-3695.
23. Aliberti, J., J. G. Valenzuela, V. B. Carruthers, S. Hieny, J. Andersen, H. Charest, C. Reis e Sousa, A. Fairlamb, J. M. Ribeiro, and A. Sher. 2003. Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat. Immunol. 4: 485-490. (Pubitemid 36592442)
24. Sato, N., W. A. Kuziel, P. C. Melby, R. L. Reddick, V. Kostecki, W. Zhao, N. Maeda, S. K. Ahuja, and S. S. Ahuja. 1999. Defects in the generation of IFN-gamma are overcome to control infection with Leishmania donovani in CC chemokine receptor (CCR) 5-, macrophage inflammatory protein-1 alpha-, or CCR2-deficient mice. J. Immunol. 163: 5519-5525.
25. Dankort, D., D. P. Curley, R. A. Cartlidge, B. Nelson, A. N. Karnezis, W. E. Damsky, Jr., M. J. You, R. A. DePinho, M. McMahon, and M. Bosenberg.2009. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 41: 544-552.
26. Hellmann, K., and K. Burrage. 1969. Control of malignant metastases by ICRF 159. Nature 224: 273-275.
27. Yang, J. C. 2011. Melanoma vaccines. Cancer J. 17: 277-282.
28. Hibbs, J. B., Jr., L. H. Lambert, Jr., and J. S. Remington. 1971. Resistance to murine tumors conferred by chronic infection with intracellular protozoa, Toxoplasma gondii and Besnoitia jellisoni. J. Infect. Dis. 124: 587-592.
29. Motamedi, M., S. Arab, S. M. Moazzeni, M. Khamis Abadi, and J. Hadjati. 2009. Improvement of a dendritic cell-based therapeutic cancer vaccine with components of Toxoplasma gondii. Clin. Vaccine Immunol. 16: 1393-1398.
30. Seavey, M. M., P. C. Maciag, N. Al-Rawi, D. Sewell, and Y. Paterson. 2009. An anti-vascular endothelial growth factor receptor 2/fetal liver kinase-1 Listeria monocytogenes anti-angiogenesis cancer vaccine for the treatment of primary and metastatic Her-2/neu+ breast tumors in a mouse model. J. Immunol. 182: 5537-5546.
31. Seavey, M. M., Z. K. Pan, P. C. Maciag, A. Wallecha, S. Rivera, Y. Paterson, and V. Shahabi. 2009. A novel human Her-2/neu chimeric molecule expressed by Listeria monocytogenes can elicit potent HLA-A2 restricted CD8-positive T cell responses and impact the growth and spread of Her-2/neu-positive breast tumors. Clin. Cancer Res. 15: 924-932.
32. Sinnathamby, G., P. Lauer, J. Zerfass, B. Hanson, A. Karabudak, J. Krakover, A. A. Secord, T. M. Clay, M. A. Morse, T. W. Dubensky, Jr., et al. 2009. Priming and activation of human ovarian and breast cancer-specific CD8+ T cells by polyvalent Listeria monocytogenes-based vaccines. J. Immunother. 32: 856-869.
33. Dzierszinski, F., M. Pepper, J. S. Stumhofer, D. F. LaRosa, E. H. Wilson, L. A. Turka, S. K. Halonen, C. A. Hunter, and D. S. Roos. 2007. Presentation of Toxoplasma gondii antigens via the endogenous major histocompatibility complex class I pathway in nonprofessional and professional antigen-presenting cells. Infect. Immun. 75: 5200-5209. (Pubitemid 350041458)
34. Nordlund, J. J., J. M. Kirkwood, B. M. Forget, G. Milton, D. M. Albert, and A. B. Lerner. 1983. Vitiligo in patients with metastatic melanoma: a good prognostic sign. J. Am. Acad. Dermatol. 9: 689-696. (Pubitemid 14230566)
35. Bystryn, J. C., D. Rigel, R. J. Friedman, and A. Kopf. 1987. Prognostic significance of hypopigmentation in malignant melanoma. Arch. Dermatol. 123: 1053-1055. (Pubitemid 17134848)
36. Quaglino, P., F. Marenco, S. Osella-Abate, N. Cappello, M. Ortoncelli, B. Salomone, M. T. Fierro, P. Savoia, and M. G. Bernengo. 2010. Vitiligo is an independent favourable prognostic factor in stage III and IV metastatic melanoma patients: results from a single-institution hospital-based observational cohort study. Ann. Oncol. 21: 409-414.
37. Byrne, K. T., A. L. Côté, P. Zhang, S. M. Steinberg, Y. Guo, R. Allie, W. Zhang, M. S. Ernstoff, E. J. Usherwood, and M. J. Turk. 2011. Autoimmune melanocyte destruction is required for robust CD8+ memory T cell responses to mouse melanoma. J. Clin. Invest. 121: 1797-1809.
38. Levy, E. M., M. P. Roberti, and J. Mordoh. 2011. Natural killer cells in human cancer: from biological functions to clinical applications. J. Biomed. Biotechnol. 2011: 676198.
39. Mullins, I. M., C. L. Slingluff, J. K. Lee, C. F. Garbee, J. Shu, S. G. Anderson, M. E. Mayer, W. A. Knaus, and D. W. Mullins. 2004. CXC chemokine receptor 3 expression by activated CD8+ T cells is associated with survival in melanoma patients with stage III disease. Cancer Res. 64: 7697-7701. (Pubitemid 39446899)