Bacteria-induced gap junctions in tumors favor antigen cross-presentation and antitumor immunity

Science Translational Medicine

Volumn 2, Issue 44, 2010, Pages

  Saccheri, Fabiana ^a   Pozzi, Chiara ^a   Avogadri, Francesca ^b   Barozzi, Sara ^a   Faretta, Mario ^a   Fusi, Paola ^c   Rescigno, Maria ^a  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; TUMOR ANTIGEN; FLUORESCENT DYE; GAMMA INTERFERON; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL KILLING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; FEMALE; GAP JUNCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MELANOMA CELL; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; T LYMPHOCYTE ACTIVATION; TUMOR GROWTH; TUMOR IMMUNITY; UPREGULATION; ANIMAL; ANTIGEN PRESENTATION; C57BL MOUSE; CELL JUNCTION; IMMUNOLOGY; LYMPH NODE; MELANOMA; METABOLISM; PATHOLOGY; SALMONELLA;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CONNEXIN 43; CROSS-PRIMING; DENDRITIC CELLS; FEMALE; FLUORESCENT DYES; GAP JUNCTIONS; HUMANS; INTERFERON-GAMMA; LYMPH NODES; MELANOMA; MICE; MICE, INBRED C57BL; PHAGOCYTOSIS; RNA, SMALL INTERFERING; SALMONELLA; SALMONELLA INFECTIONS;

EID: 77955626169     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3000739     Document Type: Article

References (39)

1. R. M. Steinman, J. Banchereau, Taking dendritic cells into medicine. Nature 449, 419-426 (2007).
2. P. van der Bruggen, B. J. Van den Eynde, Processing and presentation of tumor antigens and vaccination strategies. Curr. Opin. Immunol. 18, 98-104 (2006).
3. A. Paschen, S. Eichmuller, D. Schadendorf, Identification of tumor antigens and T-cell epitopes, and its clinical application. Cancer Immunol. Immunother. 53, 196-203 (2004).
4. L. Chapatte, M. Ayyoub, S. Morel, A. L. Peitrequin, N. Lévy, C. Servis, B. J. Van den Eynde, D. Valmori, F. Lévy, Processing of tumor-associated antigen by the proteasomes of dendritic cells controls in vivo T-cell responses. Cancer Res. 66, 5461-5468 (2006).
5. B. J. Nicholson, Gap junctions - from cell to molecule. J. Cell Sci. 116, 4479-4481 (2003).
6. G. Meşe, G. Richard, T. W. White, Gap junctions: Basic structure and function. J. Invest. Dermatol. 127, 2516-2524 (2007).
7. J. Neijssen, B. Pang, J. Neefjes, Gap junction-mediated intercellular communication in the immune system. Prog. Biophys. Mol. Biol. 94, 207-218 (2007).
8. T. J. King, J. S. Bertram, Connexins as targets for cancer chemoprevention and chemotherapy. Biochim. Biophys. Acta 1719, 146-160 (2005).
9. M. Mesnil, S. Crespin, J. L. Avanzo, M. L. Zaidan-Dagli, Defective gap junctional intercellular communication in the carcinogenic process. Biochim. Biophys. Acta 1719, 125-145 (2005).
10. T. Bopp, C. Becker, M. Klein, S. Klein-Hessling, A. Palmetshofer, E. Serfling, V. Heib, M. Becker, J. Kubach, S. Schmitt, S. Stoll, H. Schild, M. S. Staege, M. Stassen, H. Jonuleit, E. Schmitt, Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. J. Exp. Med. 204, 1303-1310 (2007).
11. E. Oviedo-Orta, W. Howard Evans, Gap junctions and connexin-mediated communication in the immune system. Biochim. Biophys. Acta 1662, 102-112 (2004).
12. H. Matsue, J. Yao, K. Matsue, A. Nagasaka, H. Sugiyama, R. Aoki, M. Kitamura, S. Shimada, Gap junction-mediated intercellular communication between dendritic cells (DCs) is required for effective activation of DCs. J. Immunol. 176, 181-190 (2006).
13. J. Neijssen, C. Herberts, J. W. Drijfhout, E. Reits, L. Janssen, J. Neefjes, Cross-presentation by intercellular peptide transfer through gap junctions. Nature 434, 83-88 (2005).
14. B. Pang, J. Neijssen, X. Qiao, L. Janssen, H. Janssen, C. Lippuner, J. Neefjes, Direct antigen presentation and gap junction mediated cross-presentation during apoptosis. J. Immunol. 183, 1083-1090 (2009).
15. H. Benlalam, A. Jalil, M. Hasmim, B. Pang, R. Tamouza, M. Mitterrand, Y. Godet, N. Lamerant, C. Robert, M. F. Avril, J. Neefjes, T. Tursz, F. Mami-Chouaib, C. Kieda, S. Chouaib, Gap junction communication between autologous endothelial and tumor cells induce cross-recognition and elimination by specific CTL. J. Immunol. 182, 2654-2664 (2009).
16. D. Bermudes, L. M. Zheng, I. C. King, Live bacteria as anticancer agents and tumor-selective protein delivery vectors. Curr. Opin. Drug Discov. Devel. 5, 194-199 (2002).
17. J. M. Pawelek, K. B. Low, D. Bermudes, Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res. 57, 4537-4544 (1997).
18. M. Loeffler, G. Le'Negrate, M. Krajewska, J. C. Reed, IL-18-producing Salmonella inhibit tumor growth. Cancer Gene Ther. 15, 787-794 (2008).
19. M. Loeffler, G. Le'Negrate, M. Krajewska, J. C. Reed, Salmonella typhimurium engineered to produce CCL21 inhibit tumor growth. Cancer Immunol. Immunother. 58, 769-775 (2009).
20. J. Fensterle, B. Bergmann, C. L. Yone, C. Hotz, S. R. Meyer, S. Spreng, W. Goebel, U. R. Rapp, I. Gentschev, Cancer immunotherapy based on recombinant Salmonella enterica serovar Typhimurium aroA strains secreting prostate-specific antigen and cholera toxin subunit B. Cancer Gene Ther. 15, 85-93 (2008).
21. U. Pertl, H. Wodrich, J. M. Ruehlmann, S. D. Gillies, H. N. Lode, R. A. Reisfeld, Immunotherapy with a posttranscriptionally modified DNA vaccine induces complete protection against metastatic neuroblastoma. Blood 101, 649-654 (2003).
22. A. G. Niethammer, R. Xiang, J. M. Ruehlmann, H. N. Lode, C. S. Dolman, S. D. Gillies, R. A. Reisfeld, Targeted interleukin 2 therapy enhances protective immunity induced by an autologous oral DNA vaccine against murine melanoma. Cancer Res. 61, 6178-6184 (2001).
23. F. Avogadri, C. Martinoli, L. Petrovska, C. Chiodoni, P. Transidico, V. Bronte, R. Longhi, M. P. Colombo, G. Dougan, M. Rescigno, Cancer immunotherapy based on killing of Salmonellainfected tumor cells. Cancer Res. 65, 3920-3927 (2005).
24. F. Avogadri, D. Mittal, F. Saccheri, M. Sarrafiore, M. Ciocca, P. Larghi, R. Orecchia, M. Rescigno, 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. 38, 1937-1947 (2008).
25. N. K. Haass, K. S. Smalley, M. Herlyn, The role of altered cell-cell communication in melanoma progression. J. Mol. Histol. 35, 309-318 (2004).
26. C. J. Wei, R. Francis, X. Xu, C. W. Lo, Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells. J. Biol. Chem. 280, 19925-19936 (2005).
27. A. Porgador, J. W. Yewdell, Y.Deng, J. R. Bennink, R.N. Germain, Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6, 715-726 (1997).
28. G. Fenteany, R. F. Standaert, W. S. Lane, S. Choi, E. J. Corey, S. L. Schreiber, Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268, 726-731 (1995).
29. G. Rotta, E. W. Edwards, S. Sangaletti, C. Bennett, S. Ronzoni, M. P. Colombo, R. M. Steinman, G. J. Randolph, M. Rescigno, Lipopolysaccharide or whole bacteria block the conversion of inflammatory monocytes into dendritic cells in vivo. J. Exp. Med. 198, 1253-1263 (2003).
30. G. Rotta, G. Matteoli, E. Mazzini, P. Nuciforo, M. P. Colombo, M. Rescigno, Contrasting roles of SPARC-related granuloma in bacterial containment and in the induction of anti-Salmonella typhimurium immunity. J. Exp. Med. 205, 657-667 (2008).
31. T. A. Groothuis, J. Neefjes, The many roads to cross-presentation. J. Exp. Med. 202, 1313-1318 (2005).
32. M. L. Albert, B. Sauter, N. Bhardwaj, Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392, 86-89 (1998).
33. A. L. Ackerman, C. Kyritsis, R. Tampé, P. Cresswell, Access of soluble antigens to the endoplasmic reticulum can explain cross-presentation by dendritic cells. Nat. Immunol. 6, 107-113 (2005).
34. J. Banchereau, A. K. Palucka, Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 5, 296-306 (2005).
35. A. Mendoza-Naranjo, P. J. Saéz, C. C. Johansson, M. Ramírez, D. Mandakovic, C. Pereda, M. N. López, R. Kiessling, J. C. Sáez, F. Salazar-Onfray, Functional gap junctions facilitate melanoma antigen transfer and cross-presentation between human dendritic cells. J. Immunol. 178, 6949-6957 (2007).
36. N. E. Blachère, R. B. Darnell, M. L. Albert, Apoptotic cells deliver processed antigen to dendritic cells for cross-presentation. PLoS Biol. 3, e185 (2005).
37. G. P. Dunn, A. T. Bruce, H. Ikeda, L. J. Old, R. D. Schreiber, Cancer immunoediting: From immunosurveillance to tumor escape. Nat. Immunol. 3, 991-998 (2002).
38. C.Winzler, P. Rovere, M. Rescigno, F. Granucci, G. Penna, L. Adorini, V. S. Zimmermann, J. Davoust, P. Ricciardi-Castagnoli, Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J. Exp. Med. 185, 317-328 (1997).
39. Acknowledgments: We thank M. Chieppa for technical assistance in confocal microscopy. Funding: M.R. was supported by grants from the Association for International Cancer Research, the Associazione Italiana per la Ricerca sul Cancro, the European Molecular Biology Organization Young Investigator Programme, the European Commission (7th framework programme), and the Italian Ministry of Health (Ricerca Finalizzata). Author contributions: F.S. did most of the experiments, with significant assistance from C.P. F.S. and C.P. analyzed all data. M.R. designed the study, analyzed all data and wrote the paper, with editorial input from F.S. and P.F. F.A. performed some of the experiments. S.B. and M.F. designed and performed microinjection experiments. Competing interests: The authors declare that they have no competing interests.