A novel Salmonella Typhi-based immunotherapy promotes tumor killing via an antitumor Th1-type cellular immune response and neutrophil activation in a mouse model of breast cancer

Vaccine

Volumn 29, Issue 4, 2011, Pages 728-736

  Vendrell, Alejandrina ^a   Gravisaco, María J ^a,d   Pasetti, Marcela F ^b   Croci, Máximo ^c   Colombo, Lucas ^a   Rodríguez, Carla ^a   Mongini, Claudia ^a   Waldner, Claudia I ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b University of Maryland School of Medicine Center for Vaccine Development   (United States)

^c Instituto de Oncologia Angel H Roffo   (Argentina)

^d INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

Author keywords

Cancer immunotherapy; Salmonella Typhi; Tumor specific Th1 type response

Indexed keywords

GAMMA INTERFERON; TYPHOID VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CYTOKINE RESPONSE; DRUG EFFICACY; FEMALE; HISTOPATHOLOGY; LEUKOCYTE ACTIVATION; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SALMONELLA TYPHI; T CELL DEPLETION; TH1 CELL;

ADENOCARCINOMA; ANIMALS; BREAST NEOPLASMS; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; FEMALE; IMMUNITY, CELLULAR; IMMUNOTHERAPY; MICE; MICE, INBRED BALB C; NEOPLASM METASTASIS; NEUTROPHIL ACTIVATION; SALMONELLA TYPHI; SURVIVAL ANALYSIS; TH1 CELLS; TUMOR NECROSIS FACTOR-ALPHA; VACCINATION; VACCINES, ATTENUATED;

EID: 78650569511     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2010.11.017     Document Type: Article

References (42)

1. Rosenberg S.A., Yang J.C., Restifo N.P. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004, 10:909-915.
2. Marincola F.M., Wang E., Herlyn M., Seliger B., Ferrone S. Tumors as elusive targets of T-cell-based active immunotherapy. Trends Immunol 2003, 24:335-342.
3. Grover A., Kim G.J., Lizée G., Tschoi M., Wang G., Wunderlich J.R., et al. Intralymphatic dendritic cell vaccination induces tumor antigen-specific, skin-homing T lymphocytes. Clin Cancer Res 2006, 12:5801-5808.
4. Wilson M., Seymour R., Henderson B. Bacterial perturbation of cytokine networks. Infect Immun 1998, 66:2401-2409.
5. Avogadri F., Martinoli C., Petrovska L., Chiodoni C., Transidico P., Bronte V., et al. Cancer immunotherapy based on killing of Salmonella-infected tumor cells. Cancer Res 2005, 65:3920-3927.
6. Coley W.B. The treatment of inoperable malignant tumour with the toxins of erysipelas and Bacillus prodigiosus. Trans Am Surg Assoc 1894, 12:183-196.
7. Jain R.K., Forbes N.S. Can engineered bacteria help control cancer?. Proc Natl Acad Sci USA 2001, 98:14748-14750.
8. Pawelek J.M., Low K.B., Bermudes D. Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res 1997, 57:4537-4544.
9. Rosenberg S.A., Spiess P.J., Kleiner D.E. Antitumor effects in mice of the intravenous injection of attenuated Salmonella typhimurium. J Immunother 2002, 25:218-225.
10. Agorio C., Schreiber F., Sheppard M., Mastroeni P., Fernandez M., Martinez M.A., et al. Live attenuated Salmonella as a vector for oral cytokine gene therapy in melanoma. J Gene Med 2007, 9:416-423.
11. Al-Ramadi B.K., Fernandez-Cabezudo M.J., El-Hasasna H., Al-Salam S., Attoub S., Xu D., et al. Attenuated bacteria as effectors in cancer immunotherapy. Ann N Y Acad Sci 2008, 1138:351-357.
12. Nagakura C., Hayashi K., Zhao M., Yamauchi K., Yamamoto N., Tsuchiya H., et al. Efficacy of a genetically-modified Salmonella typhimurium in an orthotopic human pancreatic cancer in nude mice. Anticancer Res 2009, 29:1873-1878.
13. Zhao M., Geller J., Ma H., Yang M., Penman S., Hoffman R.M. Monotherapy with a tumor-targeting mutant of Salmonella typhimurium cures orthotopic metastatic mouse models of human prostate cancer. Proc Natl Acad Sci USA 2007, 104:10170-10174.
14. Zhao M., Yang M., Ma H., Li X., Tan X., Li S., et al. Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice. Cancer Res 2006, 66:7647-7652.
15. Germanier R., Fürer E. Isolation and characterization of galE mutant Ty21a of Salmonella typhi: a candidate strain for a live oral typhoid vaccine. J Infect Dis 1975, 131:553-558.
16. Wang J.Y., Pasetti M.F., Noriega F.R., Anderson R.J., Wasserman S.S., Galen J.E., et al. Construction, genotypic and phenotypic characterization and immunogenicity of attenuated DeltaguaBA Salmonella enterica serovar Typhi strain CVD 915. Infect Immun 2001, 69:4734-4741.
17. Urtreger A., Ladeda V., Puricelli L., Rivelli A., Vidal M.C., Sacerdote de Lustig E., et al. Modulation of fibronectin expression and proteolytic activity associated with the invasive and metastatic phenotype in two new murine mammary tumor cell lines. Int J Oncol 1997, 11:489-496.
18. Zimmermann V.S., Benigni F., Mondino A. Immune surveillance and anti-tumor immune responses: an anatomical perspective. Immunol Lett 2005, 98:1-8.
19. Ruybal P., Gravisaco M.J., Barcala V., Escalada A., Di Sciullo P., Waldner C., et al. Complete rejection of a T-cell lymphoma due to synergism of T-cell receptor costimulatory molecules, CD80, CD40L, and CD40. Vaccine 2008, 26:697-705.
20. Mongini C., Ruybal P., Gravisaco M.J., Croci M., Sánchez Lockhart M., Fabris V., et al. Characterization of the immunophenotype and the metastatic properties of a murine T-lymphoma cell line. Unexpected expression of cytoplasmatic CD4. In Vitro Cell Dev Biol Anim 2001, 37:499-504.
21. Liyanage U.K., Moore T.T., Joo H.G., Tanaka Y., Herrmann V., Doherty G., et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 2002, 169:2756-2761.
22. Terabe M., Berzofsky J.A. Immunoregulatory T cells in tumor immunity. Curr Opin Immunol 2004, 16:157-162.
23. Ikeda H., Chamoto K., Tsuji T., Suzuki Y., Wakita D., Takeshima T., et al. The critical role of type-1 innate and acquired immunity in tumor immunotherapy. Cancer Sci 2004, 95:697-703.
24. Kirby A.C., Yrlid U., Wick M.J. The innate immune response differs in primary and secondary Salmonella infection. J Immunol 2002, 169:4450-4459.
25. Low K.B., Ittensohn M., Le T., Platt J., Sodi S., Amoss M., et al. A mutant Salmonella with suppressed virulence and TNF alpha induction retain tumor-targeting in vivo. Nat Biotechnol 1999, 17:37-41.
26. Avogadri F., Mittal D., Saccheri F., Sarrafiore M., Ciocca M., Larghi P., et al. Intra-tumoral Salmonella typhimurium induces a systemic anti-tumor immune response that is directed by low-dose radiation to treat distal disease. Eur J Immunol 2008, 38:1937-1947.
27. Yoshimura T., Takahashi M. IFN-γ-mediated survival enables human neutrophils to produce MCP-1/CCL2 in response to activation by TLR ligands. J Immunol 2007, 179:1942-1949.
28. Di Carlo E., Forni G., Lollini P., Colombo M.P., Modesti A., Musiani P. The intriguing role of polymorphonuclear neutrophils in antitumor reactions. Blood 2001, 97:339-345.
29. Ethuin F., Gérard B., Benna J.E., Boutten A., Gougereot-Pocidalo M.A., Jacob L., et al. Human neutrophils produce interferon γ upon stimulation by IL-12. Lab Invest 2004, 84:1363-1371.
30. Rüegg C., Yilmaz A., Bieler G., Bamat J., Chaubert P., Lejeune F.J. Evidence for the involvement of endothelial cell integrin alphaVbeta3 in the disruption of the tumor vasculature induced by TNF and IFN-gamma. Nat Med 1998, 4:408-414.
31. Fransen L., Van der Heyden J., Ruysschaert R., Fiers W. Recombinant tumor necrosis factor: its effect and its synergism with interferon-gamma on a variety of normal and transformed human cell lines. Eur J Cancer Clin Oncol 1986, 22:419-426.
32. Barrat F.J., Cua D.J., Boonstra A., Richards D.F., Crain C., Savelkoul H.F., et al. In vitro generation of interleukin 10-producing regulatory CD4(+) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J Exp Med 2002, 195:603-616.
33. Malek T.R., Bayer A.L. Tolerance, not immunity, crucially depends on IL-2. Nat Rev Immunol 2004, 4:665-674.
34. Pasetti M.F., Anderson R.J., Noriega F.R., Levine M.M., Sztein M.B. Attenuated deltaguaBA Salmonella typhi vaccine strain CVD 915 as a live vector utilizing prokaryotic or eukaryotic expression systems to deliver foreign antigens and elicit immune responses. Clin Immunol 1999, 92:76-89.
35. Capozzo A.V., Cuberos L., Levine M.M., Pasetti M.F. Mucosally delivered Salmonella live vector vaccines elicit potent immune responses against a foreign antigen in neonatal mice born to naive and immune mothers. Infect Immun 2004, 72:4637-4646.
36. Sztein M.B., Wasserman S.S., Tacket C.O., Edelman R., Hone D., Lindberg A.A., et al. Cytokine production patterns and lymphoproliferative responses in volunteers orally immunized with attenuated vaccine strains of Salmonella Typhi. J Infect Dis 1994, 170:1508-1517.
37. Taams L.S., Palmer D.B., Akbar A.N., Robinson D.S., Brown Z., Hawrylowicz C.M. Regulatory T cells in human disease and their potential for therapeutic manipulation. Immunology 2006, 118:1-9.
38. Khong H.T., Restifo N.P. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat Immunol 2002, 3:999-1005.
39. Conroy H., Marshall N.A., Mills K.H. TLR ligand suppression or enhancement of Treg cells? A double-edged sword in immunity to tumors. Oncogene 2008, 27:168-180.
40. Lee C.H., Wu C.L., Shiau A.L. Toll-like receptor 4 mediates an antitumor host response induced by Salmonella choleraesuis. Clin Cancer Res 2008, 14:1905-1912.
41. Sfondrini L., Rossini A., Besusso D., Merlo A., Tagliabue E., Mènard S., et al. Antitumor activity of the TLR-5 ligand flagellin in mouse models of cancer. J Immunol 2006, 176:6624-6630.
42. Lysaght J., Jarnicki A.G., Mills K.H. Reciprocal effects of Th1 and Treg cell inducing pathogen-associated immunomodulatory molecules on anti-tumor immunity. Cancer Immunol Immunother 2007, 56:1367-1379.