TLR9 is required for protective innate immunity in gram-negative bacterial pneumonia: Role of dendritic cells

Journal of Immunology

Volumn 179, Issue 6, 2007, Pages 3937-3946

  Bhan, Urvashi ^a   Lukacs, Nicholas W ^b   Osterholzer, John J ^a   Newstead, Michael W ^a   Zeng, Xianying ^a   Moore, Thomas A ^a   McMillan, Tracy R ^a   Krieg, Arthur M ^c   Akira, Shizuo ^d   Standiford, Theodore J ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c PFIZER INC   (United States)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; TOLL LIKE RECEPTOR 9; TLR9 PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL PNEUMONIA; BAGG ALBINO MOUSE; BONE MARROW; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; GRAM NEGATIVE INFECTION; INNATE IMMUNITY; KLEBSIELLA PNEUMONIAE; LUNG ALVEOLUS MACROPHAGE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; ANIMAL; BIOSYNTHESIS; BONE MARROW CELL; CELL CULTURE; CELL MOTION; ENDOTRACHEAL INTUBATION; ENTEROBACTER INFECTION; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; BONE MARROW CELLS; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINES; CYTOKINES; DENDRITIC CELLS; FEMALE; IMMUNITY, NATURAL; INTUBATION, INTRATRACHEAL; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LUNG; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PNEUMONIA, BACTERIAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 9;

EID: 35748965880     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.6.3937     Document Type: Article

References (72)

1. Nelson, S., C. M. Mason, J. Kolls, and W. R. Summer. 1995. Pathophysiology of pneumonia. Clin. Chest Med. 16: 1-12.
2. Toews, G. B., G. N. Gross, and A. K. Pierce. 1980. The relationship of inoculum size to lung bacterial clearance and phagocytic cell response in mice. Am. Rev. Respir. Dis. 120: 559-566.
3. Lipscomb, M. F., J. M. Onofrio, and E. J. Nash. 1983. A morphological study of the role of phagocytes in the clearance of Staphylococcus aureus from the lung. J. Reticuloendothel. Soc. 33: 429-442.
4. Broug-Holub, E., G. B. Toews, J. F. van Iwaarden, R. M. Strieter, S. L. Kunkel, R. Paine, and T. J. Standiford. 1997. Alveolar macrophages are required for protective pulmonary defenses in murine Klebsiella pneumonia: elimination of alveolar macrophages increases neutrophil recruitment but decreases bacterial clearance and survival. Infect. Immun. 65: 1139-1146.
5. Tsai, W. C., R. M. Strieter, B. Mehrad, M. W. Newstead, X. Zeng, and T. J. Standiford. 2000. CXC chemokine receptor CXCR2 is essential for protective innate host response in murine Pseudomonas aeruginosa pneumonia. Infect. Immun. 68: 289-296.
6. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and control of immunity. Nature 392: 245-252.
7. Kradin, R. L., H. Sakamoto, F. I. Preffer, D. Dombkowski, K. M. Springer, and C. P. Leary. 2000. Accumulation of macrophages with dendritic cell characteristics in the pulmonary response to Listeria. Am. J. Respir. Crit. Care Med. 161: 535-542.
8. McWilliam, A. S., D. Nelson, J. A. Thomas, and P. G. Holt. 1994. Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces. J. Exp. Med. 179: 1331-1336.
9. Liu, C. H., Y. T. Fan, A. Dias, L. Esper, R. A. Corn, A. Bafica, F. S. Machado, and J. Aliberti. 2006. Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J. Immunol. 177: 31-35.
10. Moore, T. A., B. B. Moore, and T. J. Standiford. 2000. γδ-T cells are critical for survival and early proinflammatory cytokine gene expression during murine Klebsiella pneumonia. J. Immunol. 165: 2643-2650.
11. Ferlazzo, G., B. Morandi, A. D'Agostino, R. Meazza, G. Melioli, A. Moretta, and L. Moretta. 2003. The interaction between NK cells and dendritic cells in bacterial infections results in rapid induction of NK cell activation and in the lysis of uninfected dendritic cells. Eur. J. Immunol. 33: 306-313.
12. Deng, J. C., K. Tateda, X. Zeng, and T. J. Standiford. 2001. Transient transgenic expression of γ interferon promotes Legionella pneumophila clearance in immunocompetent hosts. Infect. Immun. 69: 6382-6390.
13. Greenberger, M. J., S. L. Kunkel, R. M. Strieter, N. W. Lukacs, J. Bramson, J. Gauldie, F. L. Graham, M. Hitt, J. M. Danforth, and T. J. Standiford. 1996. IL-12 gene therapy protects mice in lethal Klebsiella pneumonia. J. Immunol. 157: 3006-3012.
14. Khan, I. A., J. A. Maclean, F. S. Lee, L. Casiotti, E. DeHaan, J. D. Schwartzman, and A. D. Luster. 2000. IP-10 is critical to effector T cell trafficking and host survival in Toxoplasma gondii infection. Immunity 12: 483-494.
15. Zeng, X., T. A. Moore, M. W. Newstead, J. C. Deng, S. L. Kunkel, A. D. Luster, and T. J. Standiford. 2005. IP-10, but not MIG, promotes protective type 1 immunity in murine Klebsiella pneumonia. Infect. Immun. 73: 8226-8236.
16. Aderem, A., and R. J. Ulevitch. 2000. Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
17. Akira, S., and H. Hemmi. 2003. Recognition of pathogen-associated molecular patterns by TLR family. Immunol. Lett. 85: 85-95.
18. An, H., Y. Yu, M. Zhang, H. Xu, R. Qi, X. Yan, S. Liu, W. Wang, Z. Guo, J. Guo, et al. 2002. Involvement of ERK, p38 and NF-κB signal transduction in regulation of TLR2, TLR4 and TLR9 gene expression induced by lipopolysaccharide in mouse dendritic cells. Immunology 106: 38-45.
19. Jeyaseelan, S., S. K. Young, M. Yamamoto, P. G. Arndt, S. Akira, J. K. Kolls, and S. K. Worthen. 2006. Toll/IL-1R domain-containing adaptor protein (TIRAP) is a critical mediator of antibacterial defense in the lung against Klebsiella pneumoniae but not Pseudomonas aeruginosa. J. Immunol. 177: 538-547.
20. Wang, X., C. Moser, J. Louboutin, E. S. Lysenko, D. J. Weiner, J. N. Weiser, and J. M. Wilson. 2002. Toll-like receptor 4 mediates innate immune responses to Haemophilus influenza infection in mouse lung. J. Immunol. 168: 810-815.
21. Schuur, J. R., E. Young, P. Byrne, C. Steele, J. E. Shellito, and J. K. Kolls. 2005. Central role of Toll-like receptor 4 signaling and host defense in experimental pneumonia caused by Gram-negative bacteria. Infect. Immun. 73: 532-545.
22. Weiss, D. S., B. Raupach, K. Takeda, S. Akira, and A. Zychlinsky. 2004. Toll-like receptors are temporally involved in host defense. J. Immunol. 172: 4463-4469.
23. Skerrett, S. J., H. D. Liggitt, A. M. Hajjar, and C. B. Wilson. 2004. Cutting edge: myeloid differentiation factor 88 is essential for pulmonary host defense against Pseudomonas aeruginosa but not Staphylococcus aureus. J. Immunol. 172: 3377-3381.
24. Feng, G. C., C. A. Scanga, C. M. Collazo-Custodio, A. W. Cheever, S. Hieny, P. Caspar, and A. Sher. 2003. Mice lacking myeloid differentiation factor 88 display profound defects in host resistance and immune responses to Mycobacterium avium infection not exhibited by Toll-like receptor 2 (TLR2)- and TLR4-deficient animals. J. Immunol. 171: 4758-4764.
25. Archer, K. A., and C. R. Roy. 2006. MyD88-dependent responses involving Toll-like receptor 2 are important for protection and clearance of Legionella pneumophila in a mouse model of Legionnaires' disease. Infect. Immun. 74: 3325-3333.
26. Hawn, T. R., K. D. Smith, A. Aderem, and S. J. Skerrett. 2006. Myeloid differentiation primary response gene (MyD88)- and Toll-like receptor 2-deficient mice are susceptible to infection with aerosolized Legionella pneumophila. J. Infect. Dis. 193: 1693-1702.
27. Krieg, A. M., A. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546-549.
28. Klinman, D. M., A. Yi, S. L. Beaucage, J. Conover, and A. M. Krieg. 1996. CpG motifs expressed by bacterial DNA rapidly induce lymphocytes to secrete IL-6, IL-12 and IFNγ. Proc. Natl. Acad. Sci. USA 93: 2879-2883.
29. Hemmi, H., O. Takeuchi, T. Kawai, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
30. Takeshita, F., C. A. Leifer, I. Gursel, K. J. Ishii, S. Takesita, M. Gursel, and D. M. Klinman. 2001. Cutting edge: role of Toll-like receptor 9 in CpG DNA-induced activation of human cells. J. Immunol. 167: 3555-3558.
31. Malmgaard, L., J. Melchjorsen, A. G. Bowie, S. C. Mogensen, and S. R. Paludan. 2004. Viral activation of macrophages through TLR-dependent and -independent pathways. J. Immunol. 173: 6890-6898.
32. Wagner, H. 2004. The immunobiology of the TLR9 subfamily. Trends Immunol. 25: 381-386.
33. Latz, E., A. Schoenemeyer, A. Visintin, K. A. Fitzgerald, B. G. Monks, C. F. Knetter, E. Lien, N. J. Nilsen, T. Espevik, and D. T. Golenbock. 2004. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5: 190-198.
34. Yasuda, K., Y. Ogawa, I. Yamane, M. Nishikawa, and Y. Takakura. 2005. Macrophage activation by a DNA/cationic liposome complex requires endosomal acidification and TLR9-dependent and-independent pathways. J. Leukocyte Biol. 77: 71-80.
35. Huang, L. Y., K. J. Ishii, S. Akira, J. Aliberti, and B. Golding. 2005. Th1-like cytokine induction by heat-killed Brucella abortus is dependent on triggering of TLR9. J. Immunol. 175: 3964-3970.
36. Matsumoto, S., M. Matsumoto, K. Umemori, Y. Ozeki, M. Furugen, T. Tatsuo, Y. Hirayama, S. Yamamoto, T. Yamada, and K. Kobayashi. 2005. DNA augments antigenicity of mycobacterial DNA-binding protein 1 and confers protection against Mycobacterium tuberculosis infection in mice. J. Immunol. 175: 441-449.
37. Takeshita, F., I. Gursel, K. J. Ishii, K. Suzuki, M. Gursel, and D. M. Klinman. 2004. Signal transduction pathways mediated by the interaction of CpG DNA with Toll-like receptor 9. Semin. Immunol. 16: 17-22.
38. Kadowaki, N., S. Ho, S. Antonenko, R. de Wall Malefyt, R. A. Kastelein, F. Bazan, and Y. J. Liu. 2001. Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194: 863-869.
39. Jarrossay, D., G. Napolitani, M. Colonna, F. Sallustro, and A. Lanzavecchia. 2001. Specialization and complementarity in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells. Eur. J. Immunol. 31: 3388-3393.
40. Krug, A., A. R. French, W. Barchet, J. A. A. Fischer, A. Dzionek, J. T. Pingel, M. M. Orihuela, S. Akira, W. M. Yokoyama, and M. Colonna. 2004. TRL9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21: 107-119.
41. Pichyangkul, S., K. Yongvanitchit, U. Kum-arb, H. Hemmi, S. Akira, A. M. Krieg, D. G. Heppner, V. A. Stewart, H. Hasegawa, S. Looareesuwan, et al. 2004. Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a toll-like receptor 9-dependent pathway. J. Immunol. 172: 4926-4933.
42. Liang, H., Y. Nishioka, C. F. Reich, D. S. Pisetsky, H. Wagner, and K. Heeg. 1996. Activation of human B cells by phosphorothioate oligodeoxynucleotides. J. Clin. Invest. 98: 1119-1129.
43. Kikuchi, T., T. Kobayashi, K. Gomi, T. Suzuki, Y. Tokue, A. Watanabe, and T. Nukiwa. 2004. Dendritic cells pulsed with live and dead Legionella pneumophila elicit distinct immune responses. J. Immunol. 172: 1727-1734.
44. Sester, D. P., K. J. Stacey, M. J. Sweet, S. J. Beasley, S. L. Cronau, and D. A. Hume. 1999. The actions of bacterial DNA on murine macrophages. J. Leukocyte Biol. 66: 542-544.
45. Li, J., Z. Ma, Z. L. Tang, T. Stevens, B. Pitt, and S. Li. 2004. CpG DNA-mediated immune response in pulmonary endothelial cells. Am. J. Physiol. 287: L552-L558.
46. Platz, J., C. Beisswenger, A. Dalpke, R. Koczulla, O. Pinkenburg, C. Vogelmeier, and R. Bals. 2004. Microbial DNA induces a host defense reaction of human respiratory epithelial cells. J. Immunol. 173: 1219-1223.
47. Chu, R. S., O. S. Targoni, A. M. Krieg, P. V. Lehmann, and C. V. Harding. 1997. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J. Exp. Med. 186: 1623-1631.
48. Kline, J. N., T. J. Waldschmidt, T. R. Businga, J. E. Lemish, J. V. Weinstock, P. S. Thorne, and A. M. Krieg. 1998. Modulation of airway inflammation by CpG oligodeoxynucleotides in a murine model of asthma. J. Immunol. 160: 2555-2559.
49. Zimmermann, S., O. Egeter, S. Hausmann, G. B. Lipford, M. Rocken, H. Wagner, and K. Heeg. 1998. CpG oligodeoxynucleotides trigger protective and curative Th1 responses in lethal murine leishmaniasis. J. Immunol. 160: 3627-3630.
50. Krieg, A. M., L. Love-Homan, A. K. Yi, and J. T. Harty. 1998. CpG DNA induces sustained IL-12 expression in vivo and resistance to Listeria monocytogenes challenge. J. Immunol. 161: 2428-2434.
51. Walker, P. S., T. Scharton-Kersten, A. M. Krieg, L. Love-Homan, E. D. Rowton, M. C. Udey, and J. C. Vogel. 1999. Immunostimulatory oligodeoxynucleotides promote protective immunity and provide systemic therapy for leishmaniasis via IL-12- and IFN-γ-dependent mechanisms. Proc. Natl. Acad. Sci. USA 96: 6970-6975.
52. Klinman, D. M., J. Conover, and C. Coban. 1999. Repeated administration of synthetic oligodeoxynucleotides expressing CpG motifs provides long-term protection against bacterial infection. Infect. Immun. 67: 5658-5663.
53. Elkins, K. L., T. R. Rhinehart-Jones, S. Stibitz, J. S. Conover, and D. M. Klinman. 1999. Bacterial DNA containing CpG motifs stimulates lymphocyte-dependent protection of mice against lethal infection with intracellular bacteria. J. Immunol. 162: 2291-2298.
54. Freidag, B. L., G. B. Melton, F. Collins, D. M. Klinman, A. Cheever, L. Stobie, W. Suen, and R. A. Seder. 2000. CpG oligodeoxynucleotides and interleukin-12 improve the efficacy of Mycobacterium bovis BCG vaccination in mice challenged with M. tuberculosis. Infect. Immun. 68: 2948-2953.
55. Juffermans, N. P., J. C. Leemans, S. Florquin, A. Verbon, A. H. Kolk, P. Speelman, S. J. van Deventer, and T. van der Poll. 2002. CpG oligodeoxynucleotides enhance host defense during murine tuberculosis. Infect. Immun. 70: 147-152.
56. Deng, J. C., T. A. Moore, M. W. Newstead, X. Zeng, and T. J. Standiford. 2004. CpG oligodeoxynucleotides stimulate protective innate immunity against pulmonary Klebsiella infection. J. Immunol. 173: 5148-5155.
57. Mogensen, T. H., S. R. Paludan, M. Kilian, and L. Ostergaard. 2006. Live Streptococcus pneumoniae, Haemophilus influenzae and Neisseria meningitides activate the inflammatory response through toll-like receptors 2, 4, and 9 in species-specific patterns. J. Leukocyte Biol. 80: 267-277.
58. Minns, L. A., L. C. Menard, D. M. Foureau, S. Darche, C. Ronet, D. W. Mielcarz, D. Buzoni-Gatel, and L. H. Kasper. 2006. TLR9 is required for the gut-associated lymphoid tissue response following oral infection of Toxoplasma gondii. J. Immunol. 176: 7589-7597.
59. Albiger, B., S. Dahlberg, A. Sandgren, F. Wartha, K. Beiter, H. Katsuragi, S. Akira, S. Normark, and B. Henriques-Normark. 2007. Toll-like receptor 9 acts as an early stage in host defence against pneumococcal infection. Cell. Microbiol. 9: 1162-1171.
60. Smit, J. J., B. C. Rudd, and N. W. Lukacs. 2006. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J. Exp. Med. 203: 1153-1159.
61. Tsai, W. C., R. M. Strieter, D. A. Zisman, J. M. Wilkowski, K. A. Bucknell, G.-H. Chen, and T. J. Standiford. 1997. Nitric oxide is required for effective innate immunity against Klebsiella pneumoniae. Infect. Immun. 65: 1870-1875.
62. Moore, T. A., H. Lau, A. L. Cogen, C. L. Monteleon, and T. J. Standiford. 2003. Anti-TNFα therapy during murine Klebsiella pneumoniae bacteremia: increased mortality in the absence of liver injury. Shock 20: 309-315.
63. neg bone marrow precursors in a mouse model of asthma. Blood 100: 3663-3671.
64. Xu, L. L., M. K. Warren, W. L. Rose, W. Gong, and J. M. Want. 1996. Human recombinant monocyte chemotactic protein and other C-C chemokines bind and induce directional migration of dendritic cells in vitro. J. Leukocyte Biol. 60: 365-371.
65. Vanbervliet, B., B. Homey, I. Durand, C. Massacrier, S. Ait-Yahia, O. deBouteiller, A. Vicari, and C. Caux. 2002. Sequential involvement of CCR2 and CCR6 ligands for immature dendritic cell recruitment: possible role at inflamed epithelial surfaces. Eur. J. Immunol. 32: 231-242.
66. Yang, S., R. K. Batra, S. Hillinger, K. L. Reckamp, R. M. Strieter, S. M. Dubinett, and S. Sharma. 2006. Intrapulmonary administration of CCL21 gene-modified dendritic cells reduces tumor burden in spontaneous murine bronchoalveolar cell carcinoma. Cancer Res. 66: 3205-3213.
67. Saikh, K. U., T. L. Kissner, A. Sultana, G. Rythel, and R. G. Ulrich. 2004. Human monocytes infected with Yersinia pestis express cell surface TLR9 and differentiate into dendritic cells. J. Immunol. 173: 7426-7434.
68. Hayashi, F., T. K. Means, and A. D. Luster. 2003. Toll-like receptors stimulate human neutrophil function. Blood 102: 2660-2669.
69. Jozsef, L., T. Khreiss, D. El Kebir, and J. G. Filep. 2006. Activation of TLR-9 induces IL-8 secretion through peroxynitrite signaling in human neutrophils. J. Immunol. 176: 1195-1202.
70. Suzuki, K., T. Suda, T. Naito, K. Ide, K. Chida, and H. Nakamura. 2005. Impaired Toll-like receptor 9 expression in alveolar macrophages with no sensitivity to CpG DNA. Am. J. Respir. Crit. Care Med. 171: 707-713.
71. + T cells. Nat. Med. 6: 1154-1159.
72. Zheng, M., J. E. Shellito, L. Marrero, Q. Zhong, S. Julian, P. Ye, V. Wallace, P. Schwarzenberger, and J. K. Kolls. 2001. CD4 T cell-independent vaccination against Pneumocystis carinii in mice. J. Clin. Invest. 108: 1469-1474.