CD81 controls immunity to listeria infection through rac-dependent inhibition of proinflammatory mediator release and activation of cytotoxic T cells

Journal of Immunology

Volumn 194, Issue 12, 2015, Pages 6090-6101

  Del Hoyo, Gloria Martínez ^a   Ramírez Huesca, Marta ^a   Levy, Shoshana ^b   Boucheix, Claude ^c   Rubinstein, Eric ^c   De La Escalera, María Minguito ^d   González Cintado, Leticia ^d   Ardavín, Carlos ^d   Veiga, Esteban ^e   Yáñez Mó, María ^e   Sánchez Madrid, Francisco ^a,f  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSERM   (France)

^d CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^e HOSPITAL UNIVERSITARIO SANTA CRISTINA   (Spain)

^f Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; CD8ALPHA ANTIGEN; NITRIC OXIDE; RAC PROTEIN; STAT1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; ALPHA BETA INTERFERON RECEPTOR; AUTACOID; PROTEIN BINDING;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; IMMUNITY; IMMUNOREGULATION; INFECTION SENSITIVITY; INFLAMMATION; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; LISTERIOSIS; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; ANIMAL; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOLOGY; DISEASE MODEL; DISEASE RESISTANCE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LISTERIA; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; PHAGOCYTOSIS; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD81; CELL DIFFERENTIATION; CELL SURVIVAL; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DISEASE RESISTANCE; INFLAMMATION MEDIATORS; LISTERIA; LISTERIOSIS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; NITRIC OXIDE; PHAGOCYTOSIS; PHOSPHORYLATION; PROTEIN BINDING; RAC GTP-BINDING PROTEINS; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, CYTOTOXIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84931475479     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402957     Document Type: Article

References (55)

1. Hemler, M. E. 2005. Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6: 801-811.
2. Yáñez-Mó, M., O. Barreiro, M. Gordon-Alonso, M. Sala-Valdés, and F. Sánchez-Madrid. 2009. Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol. 19: 434-446.
3. van Spriel, A. B., and C. G. Figdor. 2010. The role of tetraspanins in the pathogenesis of infectious diseases. Microbes Infect. 12: 106-112.
4. Kropshofer, H., S. Spindeldreher, T. A. Röhn, N. Platania, C. Grygar, N. Daniel, A. Wölpl, H. Langen, V. Horejsi, and A. B. Vogt. 2002. Tetraspan microdomains distinct from lipid rafts enrich select peptide-MHC class II complexes. Nat. Immunol. 3: 61-68.
5. Unternaehrer, J. J., A. Chow, M. Pypaert, K. Inaba, and I. Mellman. 2007. The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface. Proc. Natl. Acad. Sci. USA 104: 234-239.
6. Levy, S. 2014. Function of the tetraspanin molecule CD81 in B and T cells. Immunol. Res. 58: 179-185.
7. Rocha-Perugini, V., M. Zamai, J. M. González-Granado, O. Barreiro, E. Tejera, M. Yañez-Mó, V. R. Caiolfa, and F. Sanchez-Madrid. 2013. CD81 controls sustained T cell activation signaling and defines the maturation stages of cognate immunological synapses. Mol. Cell. Biol. 33: 3644-3658.
8. Maecker, H. T., M. S. Do, and S. Levy. 1998. CD81 on B cells promotes interleukin 4 secretion and antibody production during T helper type 2 immune responses. Proc. Natl. Acad. Sci. USA 95: 2458-2462.
9. Miyazaki, T., U. Müller, and K. S. Campbell. 1997. Normal development but differentially altered proliferative responses of lymphocytes in mice lacking CD81. EMBO J. 16: 4217-4225.
10. Tsitsikov, E. N., J. C. Gutierrez-Ramos, and R. S. Geha. 1997. Impaired CD19 expression and signaling, enhanced antibody response to type II T independent antigen and reduction of B-1 cells in CD81-deficient mice. Proc. Natl. Acad. Sci. USA 94: 10844-10849.
11. Deng, J., R. H. Dekruyff, G. J. Freeman, D. T. Umetsu, and S. Levy. 2002. Critical role of CD81 in cognate T-B cell interactions leading to Th2 responses. Int. Immunol. 14: 513-523.
12. Pileri, P., Y. Uematsu, S. Campagnoli, G. Galli, F. Falugi, R. Petracca, A. J. Weiner, M. Houghton, D. Rosa, G. Grandi, and S. Abrignani. 1998. Binding of hepatitis C virus to CD81. Science 282: 938-941.
13. Gordón-Alonso, M., M. Yañez-Mó, O. Barreiro, S. Alvarez, M. A. Muñoz-Fernández, A. Valenzuela-Fernández, and F. Sánchez-Madrid. 2006. Tetraspanins CD9 and CD81 modulate HIV-1-induced membrane fusion. J. Immunol. 177: 5129-5137.
14. Silvie, O., E. Rubinstein, J. F. Franetich, M. Prenant, E. Belnoue, L. Rénia, L. Hannoun, W. Eling, S. Levy, C. Boucheix, and D. Mazier. 2003. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat. Med. 9: 93-96.
15. Tham, T. N., E. Gouin, E. Rubinstein, C. Boucheix, P. Cossart, and J. Pizarro-Cerda. 2010. Tetraspanin CD81 is required for Listeria monocytogenes invasion. Infect. Immun. 78: 204-209.
16. Pamer, E. G. 2004. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4: 812-823.
17. Tam, M. A., and M. J. Wick. 2004. Dendritic cells and immunity to Listeria: TipDCs are a new recruit. Trends Immunol. 25: 335-339.
18. Pizarro-Cerdá, J., and P. Cossart. 2009. Listeria monocytogenes membrane trafficking and lifestyle: the exception or the rule? Annu. Rev. Cell Dev. Biol. 25: 649-670.
19. Condotta, S. A., M. J. Richer, V. P. Badovinac, and J. T. Harty. 2012. Probing CD8 T cell responses with Listeria monocytogenes infection. Adv. Immunol. 113: 51-80.
20. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19: 59-70.
21. + dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity 35: 236-248.
22. + T cells by exogenous cell-associated antigens. Immunity 17: 211-220.
23. Joffre, O. P., E. Segura, A. Savina, and S. Amigorena. 2012. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12: 557-569.
24. Kerksiek, K. M., F. Niedergang, P. Chavrier, D. H. Busch, and T. Brocker. 2005. Selective Rac1 inhibition in dendritic cells diminishes apoptotic cell uptake and cross-presentation in vivo. Blood 105: 742-749.
25. + dendritic cells. Immunity 30: 544-555.
26. Tejera, E., V. Rocha-Perugini, S. López-Martín, D. Pérez-Hernández, A. I. Bachir, A. R. Horwitz, J. Vázquez, F. Sánchez-Madrid, and M. Yáñez-Mo. 2013. CD81 regulates cell migration through its association with Rac GTPase. Mol. Biol. Cell 24: 261-273.
27. Witte, C. E., K. A. Archer, C. S. Rae, J. D. Sauer, J. J. Woodward, and D. A. Portnoy. 2012. Innate immune pathways triggered by Listeria monocytogenes and their role in the induction of cell-mediated immunity. Adv. Immunol. 113: 135-156.
28. Honda, K., A. Takaoka, and T. Taniguchi. 2006. Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360.
29. Maecker, H. T., and S. Levy. 1997. Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J. Exp. Med. 185: 1505-1510.
30. Cruz-Adalia, A., G. Ramirez-Santiago, C. Calabia-Linares, M. Torres-Torresano, L. Feo, M. Galán-Díez, E. Fernández-Ruiz, E. Pereiro, P. Guttmann, M. Chiappi, et al. 2014. T cells kill bacteria captured by transinfection from dendritic cells and confer protection in mice. Cell Host Microbe 15: 611-622.
31. Vaudaux, P., and F. A. Waldvogel. 1979. Gentamicin antibacterial activity in the presence of human polymorphonuclear leukocytes. Antimicrob. Agents Chemother. 16: 743-749.
32. Yarilina, A., K. H. Park-Min, T. Antoniv, X. Hu, and L. B. Ivashkiv. 2008. TNF activates an IRF1-dependent autocrine loop leading to sustained expression of chemokines and STAT1-dependent type I interferon-response genes. Nat. Immunol. 9: 378-387.
33. Park, E. J., K. A. Ji, S. B. Jeon, W. H. Choi, I. O. Han, H. J. You, J. H. Kim, I. Jou, and E. H. Joe. 2004. Rac1 contributes to maximal activation of STAT1 and STAT3 in IFN-γ-stimulated rat astrocytes. J. Immunol. 173: 5697-5703.
34. Domínguez, P. M., M. López-Bravo, U. Kalinke, and C. Ardavín. 2011. Statins inhibit iNOS-mediated microbicidal potential of activated monocyte-derived dendritic cells by an IFN-β-dependent mechanism. Eur. J. Immunol. 41: 3330-3339.
35. + dendritic cells are required for efficient entry of Listeria monocytogenes into the spleen. Immunity 25: 619-630.
36. + DCs to promote long-term T cell responses. Cell Host Microbe 16: 68-80.
37. Kang, S. J., H. E. Liang, B. Reizis, and R. M. Locksley. 2008. Regulation of hierarchical clustering and activation of innate immune cells by dendritic cells. Immunity 29: 819-833.
38. Rydström, A., and M. J. Wick. 2007. Monocyte recruitment, activation, and function in the gut-associated lymphoid tissue during oral Salmonella infection. J. Immunol. 178: 5789-5801.
39. + inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29: 306-317.
40. Benvenuti, F., S. Hugues, M. Walmsley, S. Ruf, L. Fetler, M. Popoff, V. L. Tybulewicz, and S. Amigorena. 2004. Requirement of Rac1 and Rac2 expression by mature dendritic cells for T cell priming. Science 305: 1150-1153.
41. West, M. A., A. R. Prescott, E. L. Eskelinen, A. J. Ridley, and C. Watts. 2000. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr. Biol. 10: 839-848.
42. Kernbauer, E., V. Maier, D. Stoiber, B. Strobl, C. Schneckenleithner, V. Sexl, U. Reichart, B. Reizis, U. Kalinke, A. Jamieson, et al. 2012. Conditional Stat1 ablation reveals the importance of interferon signaling for immunity to Listeria monocytogenes infection. PLoS Pathog. 8: e1002763.
43. Archer, K. A., J. Durack, and D. A. Portnoy. 2014. STING-dependent type I IFN production inhibits cell-mediated immunity to Listeria monocytogenes. PLoS Pathog. 10: e1003861.
44. McNab, F., K. Mayer-Barber, A. Sher, A. Wack, and A. O'Garra. 2015. Type I interferons in infectious disease. Nat. Rev. Immunol. 15: 87-103.
45. Pontiroli, F., O. Dussurget, I. Zanoni, M. Urbano, O. Beretta, F. Granucci, P. Ricciardi-Castagnoli, P. Cossart, and M. Foti. 2012. The timing of IFNβ production affects early innate responses to Listeria monocytogenes and determines the overall outcome of lethal infection. PLoS ONE 7: e43455.
46. Montoya, M., G. Schiavoni, F. Mattei, I. Gresser, F. Belardelli, P. Borrow, and D. F. Tough. 2002. Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 99: 3263-3271.
47. Carrero, J. A., B. Calderon, and E. R. Unanue. 2004. Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J. Exp. Med. 200: 535-540.
48. Stockinger, S., T. Materna, D. Stoiber, L. Bayr, R. Steinborn, T. Kolbe, H. Unger, T. Chakraborty, D. E. Levy, M. Müller, and T. Decker. 2002. Production of type I IFN sensitizes macrophages to cell death induced by Listeria monocytogenes. J. Immunol. 169: 6522-6529.
49. Dresing, P., S. Borkens, M. Kocur, S. Kropp, and S. Scheu. 2010. A fluorescence reporter model defines "Tip-DCs" as the cellular source of interferon β in murine listeriosis. PLoS ONE 5: e15567.
50. Stockinger, S., R. Kastner, E. Kernbauer, A. Pilz, S. Westermayer, B. Reutterer, D. Soulat, G. Stengl, C. Vogl, T. Frenz, et al. 2009. Characterization of the interferon-producing cell in mice infected with Listeria monocytogenes. PLoS Pathog. 5: e1000355.
51. van Spriel, A. B., M. Sofi, K. H. Gartlan, A. van der Schaaf, I. Verschueren, R. Torensma, R. A. Raymakers, B. E. Loveland, M. G. Netea, G. J. Adema, et al. 2009. The tetraspanin protein CD37 regulates IgA responses and anti-fungal immunity. PLoS Pathog. 5: e1000338.
52. Suzuki, M., I. Tachibana, Y. Takeda, P. He, S. Minami, T. Iwasaki, H. Kida, S. Goya, T. Kijima, M. Yoshida, et al. 2009. Tetraspanin CD9 negatively regulates lipopolysaccharide-induced macrophage activation and lung inflammation. J. Immunol. 182: 6485-6493.
53. Gutiérrez-López, M. D., A. Gilsanz, M. Yáñez-Mó, S. Ovalle, E. M. Lafuente, C. Domínguez, P. N. Monk, I. González-Alvaro, F. Sánchez-Madrid, and C. Cabañas. 2011. The sheddase activity of ADAM17/TACE is regulated by the tetraspanin CD9. Cell. Mol. Life Sci. 68: 3275-3292.
54. Quast, T., F. Eppler, V. Semmling, C. Schild, Y. Homsi, S. Levy, T. Lang, C. Kurts, and W. Kolanus. 2011. CD81 is essential for the formation of membrane protrusions and regulates Rac1-activation in adhesion-dependent immune cell migration. Blood 118: 1818-1827.
55. Reinicke, A. T., K. D. Omilusik, G. Basha, and W. A. Jefferies. 2009. Dendritic cell cross-priming is essential for immune responses to Listeria monocytogenes. PLoS ONE 4: e7210.