Innate, antigen-independent role for T cells in the activation of the immune system by Propionibacterium acnes

European Journal of Immunology

Volumn 40, Issue 9, 2010, Pages 2506-2516

  Tchaptchet, Sandrine ^a   Kirberg, Jörg ^a,c   Freudenberg, Nikolaus ^b   Schamel, Wolfgang W A ^a   Galanos, Chris ^a   Freudenberg, Marina A ^a  

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

^b UNIVERSITY OF FREIBURG   (Germany)

^c PAUL EHRLICH INSTITUT   (Germany)

Author keywords

Liver granuloma; LPS hypersensitivity; NK cells; Propionibacterium acnes; T cells

Indexed keywords

BACTERIAL ANTIGEN; CYTOKINE; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; GENETICS; GRANULOMA; HUMAN; IMMUNIZATION; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; LIVER; METABOLISM; MICROBIOLOGY; MOUSE; NATURAL KILLER CELL; OPPORTUNISTIC INFECTION; PATHOLOGY; PROPIONIBACTERIUM ACNES; T LYMPHOCYTE;

ANIMALS; ANTIGENS, BACTERIAL; CYTOKINES; GRANULOMA; HUMANS; IMMUNITY, INNATE; IMMUNIZATION; KILLER CELLS, NATURAL; LIVER; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; OPPORTUNISTIC INFECTIONS; PROPIONIBACTERIUM ACNES; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES;

EID: 77956470166     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939860     Document Type: Article

References (55)

1. Freudenberg, M. A., Tchaptchet, S., Keck, S., Fejer, G., Huber, M., Schutze, N., Beutler, B. and Galanos, C., Lipopolysaccharide sensing an important factor in the innate immune response to Gram-negative bacterial infections: Benefits and hazards of LPS hypersensitivity. Immunobiology 2008. 213: 193-203.
2. Galanos, C., Freudenberg, M. A., Matsuura, M. and Coumbos, A., Hypersensitivity to endotoxin and mechanisms of host-response. Prog. Clin. Biol. Res. 1988. 272: 295-308.
3. Gumenscheimer, M., Mitov, I., Galanos, C. and Freudenberg, M. A., Beneficial or deleterious effects of a preexisting hypersensitivity to bacterial components on the course and outcome of infection. Infect. Immun. 2002. 70: 5596-5603.
4. Freudenberg, M. A., Kopf, M. and Galanos, C., Lipopolysaccharide sensitivity of interferon-gamma-receptor deficient mice. J. Endotoxin Res. 1996. 3: 291-295.
5. Katschinski, T., Galanos, C., Coumbos, A. and Freudenberg, M. A., Gamma interferon mediates Propionibacterium acnes-induced hypersensitivity to lipopolysaccharide in mice. Infect. Immun. 1992. 60: 1994-2001.
6. Dinges, M. M. and Schlievert, P. M., Role of T cells and gamma interferon during induction of hypersensitivity to lipopolysaccharide by toxic shock syndrome toxin 1 in mice. Infect. Immun. 2001. 69: 1256-1264.
7. Vogel, S. N., Weedon, L. L., Wahl, L. M. and Rosenstreich, D. L., BCG-induced enhancement of endotoxin sensitivity in C3H/HeJ mice. II. T cell modulation of macrophage sensitivity to LPS in vitro. Immunobiology 1982. 160: 479-493.
8. Munder, M., Mallo, M., Eichmann, K. and Modolell, M., Murine macrophages secrete interferon gamma upon combined stimulation with interleukin (IL)-12 and IL-18: A novel pathway of autocrine macrophage activation. J. Exp. Med. 1998. 187: 2103-2108.
9. Ohteki, T., Fukao, T., Suzue, K., Maki, C., Ito, M., Nakamura, M. and Koyasu, S., Interleukin 12-dependent interferon gamma production by CD8alpha+ lymphoid dendritic cells. J. Exp. Med. 1999. 189: 1981-1986.
10. Puddu, P., Fantuzzi, L., Borghi, P., Varano, B., Rainaldi, G., Guillemard, E., Malorni, W. et al., IL-12 induces IFN-gamma expression and secretion in mouse peritoneal macrophages. J. Immunol. 1997. 159: 3490-3497.
11. Yoshimoto, T., Okamura, H., Tagawa, Y. I., Iwakura, Y. and Nakanishi, K., Interleukin 18 together with interleukin 12 inhibits IgE production by induction of interferon-gamma production from activated B cells. Proc. Natl. Acad. Sci. USA 1997. 94: 3948-3953.
12. North, R. J., T cell dependence of macrophage activation and mobilization during infection with Mycobacterium tuberculosis. Infect. Immun. 1974. 10: 66-71.
13. Nakayama, Y., Shimizu, Y., Hirano, K., Ebata, K., Minemura, M., Watanabe, A. and Sugiyama, T., CTLA-4Ig suppresses liver injury by inhibiting acquired immune responses in a mouse model of fulminant hepatitis. Hepatology 2005. 42: 915-924.
14. Halpern, B. N., Prevot, A. R., Biozzi, G., Stiffel, C., Mouton, D., Morard, J. C., Bouthillier, Y. and Decreusefond, C., Stimulation of the phagocytic activity of the reticuloendothelial system by Corynebacterium parvum. J. Reticuloendothel. Soc. 1964. 83: 77-96.
15. Cummins, C. S. and Linn, D. M., Reticulostimulating properties of killed vaccines of anaerobic coryneforms and other organisms. J. Natl. Cancer Inst. 1977. 59: 1697-1708.
16. Fisher, B., Wolmark, N., Saffer, E. and Fisher, E. R., Inhibitory effect of prolonged Corynebacterium parvum and cyclophosphamide administration on the growth of established tumors. Cancer 1975. 35: 134-143.
17. Riveros-Moreno, V. and Niblock, A., Chemical properties of the principle in C. parvum that produces splenomegaly in mice. Immunology 1979. 36: 495-499.
18. Scott, M. T. and Milas, L., The distribution and persistence in vivo of Corynebacterium parvum in relation to its antitumor activity. Cancer Res. 1977. 37: 1673-1679.
19. Tsuji, H., Mukaida, N., Harada, A., Kaneko, S., Matsushita, E., Nakanuma, Y., Tsutsui, H., et al., Alleviation of lipopolysaccharide-induced acute liver injury in Propionibacterium acnes-primed IFN-gamma-deficient mice by a concomitant reduction of TNF-alpha, IL-12, and IL-18 production. J. Immunol. 1999. 162: 1049-1055.
20. Kalis, C., Gumenscheimer, M., Freudenberg, N., Tchaptchet, S., Fejer, G., Heit, A., Akira, S. et al., Requirement for TLR9 in the immunomodulatory activity of Propionibacterium acnes. J. Immunol. 2005. 174: 4295-4300.
21. Merlin, T., Sing, A., Nielsen, P. J., Galanos, C. and Freudenberg, M. A., Inherited IL-12 unresponsiveness contributes to the high LPS resistance of the Lps(d) C57BL/10ScCr mouse. J. Immunol. 2001. 166: 566-573.
22. Wysocka, M., Kubin, M., Vieira, L. Q., Ozmen, L., Garotta, G., Scott, P. and Trinchieri, G., Interleukin-12 is required for interferon-gamma production and lethality in lipopolysaccharide-induced shock in mice. Eur. J. Immunol. 1995. 25: 672-676.
23. Tsutsui, H., Matsui, K., Kawada, N., Hyodo, Y., Hayashi, N., Okamura, H., Higashino, K. and Nakanishi, K., IL-18 accounts for both TNF-alpha- and Fas ligand-mediated hepatotoxic pathways in endotoxin-induced liver injury in mice. J. Immunol. 1997. 159: 3961-3967.
24. Peng, S. L., The T-box transcription factor T-bet in immunity and autoimmunity. Cell. Mol. Immunol. 2006. 3: 87-95.
25. Trinchieri, G., Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 2003. 3: 133-146.
26. Schulz, O., Edwards, A. D., Schito, M., Aliberti, J., Manickasingham, S., Sher, A. and Reis e Sousa, C., CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity 2000. 13: 453-462.
27. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J. and Carbone, F. R., T cell receptor antagonist peptides induce positive selection. Cell 1994. 76: 17-27.
28. Pircher, H., Burki, K., Lang, R., Hengartner, H. and Zinkernagel, R. M., Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 1989. 342: 559-561.
29. Krieg, A. M., CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 2002. 20: 709-760.
30. Sparwasser, T., Hultner, L., Koch, E. S., Luz, A., Lipford, G. B. and Wagner, H., Immunostimulatory CpG-oligodeoxynucleotides cause extramedullary murine hemopoiesis. J. Immunol. 1999. 162: 2368-2374.
31. Matsui, K., Yoshimoto, T., Tsutsui, H., Hyodo, Y., Hayashi, N., Hiroishi, K., Kawada, N. et al., Propionibacterium acnes treatment diminishes CD4+ NK1.1+ T cells but induces type I T cells in the liver by induction of IL-12 and IL-18 production from Kupffer cells. J. Immunol. 1997. 159: 97-106.
32. Tanaka, Y., Takahashi, A., Watanabe, K., Takayama, K., Yahata, T., Habu, S. and Nishimura, T., A pivotal role of IL-12 in Th1-dependent mouse liver injury. Int. Immunol. 1996. 8: 569-576.
33. Pugh-Humphreys, R. G. and Thomson, A. W., An ultrastructural study of peritoneal mononuclear phagocytes from Corynebacterium parvum-injected mice. Br. J. Exp. Pathol. 1979. 60: 259-268.
34. Imamura, M., Tsutsui, H., Yasuda, K., Uchiyama, R., Yumikura-Futatsugi, S., Mitani, K., Hayashi, S. et al., Contribution of TIR domain-containing adapter inducing IFN-beta-mediated IL-18 release to LPS-induced liver injury in mice. J. Hepatol. 2009. 51: 333-341.
35. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M. et al., A Toll-like receptor recognizes bacterial DNA. Nature 2000. 408: 740-745.
36. Yoneyama, H., Harada, A., Imai, T., Baba, M., Yoshie, O., Zhang, Y., Higashi, H. et al., Pivotal role of TARC, a CC chemokine, in bacteria-induced fulminant hepatic failure in mice. J. Clin. Invest. 1998. 102: 1933-1941.
37. De Wilde, V., Benghiat, F. S., Novalrivas, M., Lebrun, J. F., Kubjak, C., Oldenhove, G., Verdebout, J. M. et al., Endotoxin hyperresponsiveness upon CD4+ T cell reconstitution in lymphopenic mice: control by natural regulatory T cells. Eur. J. Immunol. 2008. 38: 48-53.
38. Sakaguchi, S., Yamaguchi, T., Nomura, T. and Ono, M., Regulatory T cells and immune tolerance. Cell 2008. 133: 775-787.
39. Okazaki, T., Ozaki, S., Nagaoka, T., Kozuki, M., Sumita, S., Tanaka, M., Osakada, F. et al., Antigen-specific T(h)1 cells as direct effectors of Propionibacterium acnes-primed lipopolysaccharide-induced hepatic injury. Int. Immunol. 2001. 13: 607-613.
40. Sakao, Y., Takeda, K., Tsutsui, H., Kaisho, T., Nomura, F., Okamura, H., Nakanishi, K. and Akira, S., IL-18-deficient mice are resistant to endotoxin-induced liver injury but highly susceptible to endotoxin shock. Int. Immunol. 1999. 11: 471-480.
41. Abe, C., Iwai, K., Mikami, R. and Hosoda, Y., Frequent isolation of Propionibacterium acnes from sarcoidosis lymph nodes. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 1984. 256: 541-547.
42. Hiramatsu, J., Kataoka, M., Nakata, Y., Okazaki, K., Tada, S., Tanimoto, M. and Eishi, Y., Propionibacterium acnes DNA detected in bronchoalveolar lavage cells from patients with sarcoidosis. Sarcoidosis Vasc. Diffuse Lung Dis. 2003. 20: 197-203.
43. Perry, A. L. and Lambert, P. A., Propionibacterium acnes. Lett. Appl. Microbiol. 2006. 42: 185-188.
44. Yasuhara, T., Tada, R., Nakano, Y., Tei, M., Mochida, C., Kamei, M. and Kinoshita, S., The presence of Propionibacterium spp. in the vitreous fluid of uveitis patients with sarcoidosis. Acta Ophthalmol. Scand. 2005. 83: 364-369.
45. Garcia, S., DiSanto, J. and Stockinger, B., Following the development of a CD4 T cell response in vivo: from activation to memory formation. Immunity 1999. 11: 163-171.
46. Kirberg, J., Berns, A. and von Boehmer, H., Peripheral T cell survival requires continual ligation of the T cell receptor to major histocompatibility complex-encoded molecules. J. Exp. Med. 1997. 186: 1269-1275.
47. Shinkai, Y., Rathbun, G., Lam, K. P., Oltz, E. M., Stewart, V., Mendelsohn, M., Charron, J. et al., RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 1992. 68: 855-867.
48. Agenes, F., Dangy, J. P. and Kirberg, J., T cell receptor contact to restricting MHC molecules is a prerequisite for peripheral interclonal T cell competition. J. Exp. Med. 2008. 205: 2735-2743.
49. Malissen, M., Pereira, P., Gerber, D. J., Malissen, B. and DiSanto, J. P., The common cytokine receptor gamma chain controls survival of gamma/delta T cells. J. Exp. Med. 1997. 186: 1277-1285.
50. Barnden, M. J., Allison, J., Heath, W. R. and Carbone, F. R., Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 1998. 76: 34-40.
51. Kitamura, D., Roes, J., Kuhn, R. and Rajewsky, K., A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 1991. 350: 423-426.
52. Galanos, C., Luderitz, O. and Westphal, O., Preparation and properties of a standardized lipopolysaccharide from salmonella abortus equi (Novo-Pyrexal). Zentralbl. Bakteriol. Orig. A 1979. 243: 226-244.
53. Dong, Z. J., Wei, H. M., Sun, R., Tian, Z. G. and Gao, B., Isolation of murine hepatic lymphocytes using mechanical dissection for phenotypic and functional analysis of NK1.1+ cells. World J. Gastroenterol. 2004. 10: 1928-1933.
54. Chomczynski, P. and Sacchi, N., Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987. 162: 156-159.
55. Sing, A., Merlin, T., Knopf, H. P., Nielsen, P. J., Loppnow, H., Galanos, C. and Freudenberg, M. A., Bacterial induction of beta interferon in mice is a function of the lipopolysaccharide component. Infect. Immun. 2000. 68: 1600-1607.