DAP10 contributes to CD8+ T cell-mediated cytotoxic effector mechanisms during Mycobacterium tuberculosis infection

Immunobiology

Volumn 216, Issue 5, 2011, Pages 639-647

  Heßmann, Manuela ^a   Rausch, Alexandra ^a   Rückerl, Dominik ^a   Adams, Pamela Scott ^b   Simon, Markus ^c   Gilfillan, Susan ^d   Colonna, Marco ^d   Ehlers, Stefan ^a,e   Hölscher, Christoph ^a,e  

^a RESEARCH CENTER BORSTEL   (Germany)

^b TRUDEAU INSTITUTE   (United States)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^d WASHINGTON UNIVERSITY   (United States)

^e UNIVERSITY OF KIEL   (Germany)

Author keywords

Bacterial infection; Costimulation; Cytotoxicity; Rodent; T cells

Indexed keywords

ADAPTOR PROTEIN; DNAX ACTIVATION PROTEIN; GAMMA INTERFERON; NATURAL KILLER CELL RECEPTOR NKG2D; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL MEDIATED CYTOTOXICITY; CELLULAR IMMUNITY; CONTROLLED STUDY; INFECTION RESISTANCE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; TUBERCULOSIS;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL COUNT; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; HUMANS; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM TUBERCULOSIS; RECEPTORS, IMMUNOLOGIC; TUBERCULOSIS, PULMONARY;

EID: 79953289766     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2010.09.010     Document Type: Article

References (52)

1. Altman J.D., Moss P.A., Goulder P.J., Barouch D.H., McHeyzer-Williams M.G., Bell J.I., McMichael A.J., Davis M.M. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996, 274:94.
2. Anfossi N., Lucas M., Diefenbach A., Buhring H.J., Raulet D., Tomasello E., Vivier E. Contrasting roles of DAP10 and KARAP/DAP12 signaling adaptors in activation of the RBL-2H3 leukemic mast cell line. Eur. J. Immunol. 2003, 33:3514.
3. Bauer S., Groh V., Wu J., Steinle A., Phillips J.H., Lanier L.L., Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999, 285:727.
4. Behar S.M., Dascher C.C., Grusby M.J., Wang C.R., Brenner M.B. Susceptibility of mice deficient in CD1D or TAP1 to infection with Mycobacterium tuberculosis. J. Exp. Med. 1999, 189:1973.
5. Billadeau D.D., Upshaw J.L., Schoon R.A., Dick C.J., Leibson P.J. NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat. Immunol. 2003, 4:557.
6. Borchers M.T., Harris N.L., Wesselkamper S.C., Zhang S., Chen Y., Young L., Lau G.W. The NKG2D-activating receptor mediates pulmonary clearance of Pseudomonas aeruginosa. Infect. Immun. 2006, 74:2578.
7. Cooper A.M., Magram J., Ferrante J., Orme I.M. Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with Mycobacterium tuberculosis. J. Exp. Med. 1997, 186:39.
8. Cooper A.M., D'Souza C., Frank A.A., Orme I.M. The course of Mycobacterium tuberculosis infection in the lungs of mice lacking expression of either perforin- or granzyme-mediated cytolytic mechanisms. Infect. Immun. 1997, 65:1317.
9. Diefenbach A., Tomasello E., Lucas M., Jamieson A.M., Hsia J.K., Vivier E., Raulet D.H. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat. Immunol. 2002, 3:1142.
10. D'Souza C.D., Cooper A.M., Frank A.A., Ehlers S., Turner J., Bendelac A., Orme I.M. A novel nonclassic beta2-microglobulin-restricted mechanism influencing early lymphocyte accumulation and subsequent resistance to tuberculosis in the lung. Am. J. Respir. Cell Mol. Biol. 2000, 23:188.
11. Flynn J.L. Immunology of tuberculosis and implications in vaccine development. Tuberculosis (Edinb) 2004, 84:93.
12. Flynn J.L., Chan J. Immunology of tuberculosis. Annu. Rev. Immunol. 2001, 19:93.
13. Flynn J.L., Ernst J.D. Immune responses in tuberculosis. Curr. Opin. Immunol. 2000, 12:432.
14. Gilfillan S., Ho E.L., Cella M., Yokoyama W.M., Colonna M. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat. Immunol. 2002, 3:1150.
15. Graham D.B., Cella M., Giurisato E., Fujikawa K., Miletic A.V., Kloeppel T., Brim K., Takai T., Shaw A.S., Colonna M., Swat W. Vav1 controls DAP10-mediated natural cytotoxicity by regulating actin and microtubule dynamics. J. Immunol. 2006, 177:2349.
16. Groh V., Rhinehart R., Randolph-Habecker J., Topp M.S., Riddell S.R., Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2001, 2:255.
17. Grotzke J.E., Lewinsohn D.M. Role of CD8+ T lymphocytes in control of Mycobacterium tuberculosis infection. Microbes Infect. 2005, 7:776.
18. Herz J., Pardo J., Kashkar H., Schramm M., Kuzmenkina E., Bos E., Wiegmann K., Wallich R., Peters P.J., Herzig S., Schmelzer E., Kronke M., Simon M.M., Utermohlen O. Acid sphingomyelinase is a key regulator of cytotoxic granule secretion by primary T lymphocytes. Nat. Immunol. 2009, 10:761.
19. Hölscher C., Atkinson R.A., Arendse B., Brown N., Myburgh E., Alber G., Brombacher F. A protective and agonistic function of IL-12p40 in mycobacterial infection. J. Immunol. 2001, 167:6957.
20. Hölscher C., Hölscher A., Rückerl D., Yoshimoto T., Yoshida H., Mak T., Saris C., Ehlers S. The IL-27 receptor chain WSX-1 differentially regulates antibacterial immunity and survival during experimental tuberculosis. J. Immunol. 2005, 174:3534.
21. Junqueira-Kipnis A.P., Kipnis A., Jamieson A., Juarrero M.G., Diefenbach A., Raulet D.H., Turner J., Orme I.M. NK cells respond to pulmonary infection with Mycobacterium tuberculosis, but play a minimal role in protection. J. Immunol. 2003, 171:6039.
22. Kagi D., Ledermann B., Burki K., Seiler P., Odermatt B., Olsen K.J., Podack E.R., Zinkernagel R.M., Hengartner H. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 1994, 369:31.
23. + T cells and NK cells. J. Immunol. 2005, 175:7819.
24. Kaufmann S.H. How can immunology contribute to the control of tuberculosis?. Nat. Rev. Immunol. 2001, 1:20.
25. Kaufmann S.H., Cole S.T., Mizrahi V., Rubin E., Nathan C. Mycobacterium tuberculosis and the host response. J. Exp. Med. 2005, 201:1693.
26. + T cells. J. Immunol. 2005, 174:4480.
27. MacMicking J.D., Nathan C., Hom G., Chartrain N., Fletcher D.S., Trumbauer M., Stevens K., Xie Q.W., Sokol K., Hutchinson N., et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 1995, 81:641.
28. MacMicking J.D., North R.J., LaCourse R., Mudgett J.S., Shah S.K., Nathan C.F. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:5243.
29. MacMicking J.D., Taylor G.A., McKinney J.D. Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 2003, 302:654.
30. Markiewicz M.A., Carayannopoulos L.N., Naidenko O.V., Matsui K., Burack W.R., Wise E.L., Fremont D.H., Allen P.M., Yokoyama W.M., Colonna M., Shaw A.S. Costimulation through NKG2D enhances murine CD8+ CTL function: similarities and differences between NKG2D and CD28 costimulation. J. Immunol. 2005, 175:2825.
31. Mogues T., Goodrich M.E., Ryan L., LaCourse R., North R.J. The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J. Exp. Med. 2001, 193:271.
32. Oddo M., Renno T., Attinger A., Bakker T., MacDonald H.R., Meylan P.R. Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J. Immunol. 1998, 160:5448.
33. Orme I.M. The kinetics of emergence and loss of mediator T lymphocytes acquired in response to infection with Mycobacterium tuberculosis. J. Immunol. 1987, 138:293.
34. Orr M.T., Sun J.C., Hesslein D.G.T., Arase H., Phillips J.H., Takai T., Lanier L.L. Ly49H signaling through DAP10 is essential for optimal natural killer cell responses to mouse cytomegalovirus infection. J. Exp. Med. 2009, jem.20090168.
35. + T cells. Eur. J. Immunol. 2006, 36:1156.
36. Roberts A.I., Lee L., Schwarz E., Groh V., Spies T., Ebert E.C., Jabri B. NKG2D receptors induced by IL-15 costimulate CD28-negative effector CTL in the tissue microenvironment. J. Immunol. 2001, 167:5527.
37. Rolph M.S., Raupach B., Kobernick H.H., Collins H.L., Perarnau B., Lemonnier F.A., Kaufmann S.H. MHC class Ia-restricted T cells partially account for beta2-microglobulin-dependent resistance to Mycobacterium tuberculosis. Eur. J. Immunol. 2001, 31:1944.
38. + T cells primed for production of type 1 cytokines in the lungs of Mycobacterium tuberculosis-infected mice. Infect. Immun. 1999, 67:3980.
39. + T cells participate in the memory immune response to Mycobacterium tuberculosis. Infect. Immun. 2001, 69:4320.
40. + CTL from lungs of Mycobacterium tuberculosis-infected mice express perforin in vivo and lyse infected macrophages. J. Immunol. 2000, 165:353.
41. Sousa A.O., Mazzaccaro R.J., Russell R.G., Lee F.K., Turner O.C., Hong S., Van Kaer L., Bloom B.R. Relative contributions of distinct MHC class I-dependent cell populations in protection to tuberculosis infection in mice. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:4204.
42. Stenger S., Hanson D.A., Teitelbaum R., Dewan P., Niazi K.R., Froelich C.J., Ganz T., Thoma-Uszynski S., Melian A., Bogdan C., Porcelli S.A., Bloom B.R., Krensky A.M., Modlin R.L. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 1998, 282:121.
43. Tang F., Chen Z., Ciszewski C., Setty M., Solus J., Tretiakova M., Ebert E., Han J., Lin A., Guandalini S., Groh V., Spies T., Green P., Jabri B. Cytosolic PLA2 is required for CTL-mediated immunopathology of celiac disease via NKG2D and IL-15. J. Exp. Med. 2009, 206:707.
44. + T cells requires the production of gamma interferon. Infect. Immun. 1998, 66:830.
45. Turner J., D'Souza C.D., Pearl J.E., Marietta P., Noel M., Frank A.A., Appelberg R., Orme I.M., Cooper A.M. CD8- and CD95/95L-dependent mechanisms of resistance in mice with chronic pulmonary tuberculosis. Am. J. Respir. Cell Mol. Biol. 2001, 24:203.
46. Upshaw J.L., Arneson L.N., Schoon R.A., Dick C.J., Billadeau D.D., Leibson P.J. NKG2D-mediated signaling requires a DAP10-bound Grb2-Vav1 intermediate and phosphatidylinositol-3-kinase in human natural killer cells. Nat. Immunol. 2006, 7:524.
47. van Pinxteren L.A., Cassidy J.P., Smedegaard B.H., Agger E.M., Andersen P. Control of latent Mycobacterium tuberculosis infection is dependent on CD8 T cells. Eur. J. Immunol. 2000, 30:3689.
48. Vankayalapati R., Garg A., Porgador A., Griffith D.E., Klucar P., Safi H., Girard W.M., Cosman D., Spies T., Barnes P.F. Role of NK cell-activating receptors and their ligands in the lysis of mononuclear phagocytes infected with an intracellular bacterium. J. Immunol. 2005, 175:4611.
49. + T cells: evidence for a protective role in virus-induced encephalitis. J. Virol. 2008, 82:3031.
50. WHO Global tuberculosis control - surveillance, planning, financing 2008, WHO, Geneva, Switzerland.
51. Wiemann K., Mittrucker H.W., Feger U., Welte S.A., Yokoyama W.M., Spies T., Rammensee H.G., Steinle A. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. J. Immunol. 2005, 175:720.
52. + T cells require perforin to kill target cells and provide protection in vivo. J. Immunol. 2008, 181:8595.