Histone acetylation and flagellin are essential for Legionella pneumophila-induced cytokine expression

Journal of Immunology

Volumn 181, Issue 2, 2008, Pages 940-947

  Schmeck, Bernd ^a   Lorenz, Janina ^a   N'Guessan, Philippe Dje ^a   Opitz, Bastian ^a   Van Laak, Vincent ^a   Zahlten, Janine ^a   Slevogt, Hortense ^a   Witzenrath, Martin ^a   Flieger, Antje ^b   Suttorp, Norbert ^a   Hippenstiel, Stefan ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANACARDIC ACID; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYTOKINE; FLAGELLIN; HISTONE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 5; HISTONE H3; HISTONE H4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; LYSINE; PROTEIN P300; RNA POLYMERASE II; SERINE; SYNAPTOPHYSIN; TRICHOSTATIN A; ENZYME INHIBITOR; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HYDROXAMIC ACID; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN SYNTHESIS INHIBITOR;

ACETYLATION; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; EPITHELIUM CELL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; LUNG ALVEOLUS EPITHELIUM; MUTANT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TIME; DRUG EFFECT; GENETICS; IMMUNOLOGY; LUNG ALVEOLUS; METABOLISM; MICROBIOLOGY; TUMOR CELL LINE;

ACETYLATION; ANACARDIC ACIDS; CELL LINE, TUMOR; ENZYME INHIBITORS; EPITHELIAL CELLS; FLAGELLIN; HISTONE ACETYLTRANSFERASES; HISTONE DEACETYLASES; HISTONES; HUMANS; HYDROXAMIC ACIDS; INTERLEUKIN-8; LEGIONELLA PNEUMOPHILA; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROMOTER REGIONS (GENETICS); PROTEIN SYNTHESIS INHIBITORS; PULMONARY ALVEOLI; RNA POLYMERASE II;

EID: 49049090212     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.2.940     Document Type: Article

References (50)

1. Vergis, E. N., E. A. Akbas, and V. L. Yu. 2000. Legionella as a cause of severe pneumonia. Sem. Resp. Crit. Care Med. 21: 295-304.
2. Sabria, M., and M. Campins. 2003. Legionnaires' disease: update on epidemiology and management options. Am. J. Respir. Med. 2: 235-243. (Pubitemid 36869438)
3. Chang, B., J. Amemura-Maekawa, F. Kura, I. Kawamura, and H. Watanabe. 2004. Expression of IL-6 and TNF-αin human alveolar epithelial cells is induced by invading, but not by adhering, Legionella pneumophila. Microb. Pathog. 37: 295-302. (Pubitemid 40044690)
4. Schmeck, B., P. D. N'Guessan, M. Ollomang, J. Lorenz, J. Zahlten, B. Opitz, A. Flieger, N. Suttorp, and S. Hippenstiel. 2007. Legionella pneumophila-induced NF-κB- and MAPK-dependent cytokine release by lung epithelial cells. Eur. Respir. J. 29: 25-33. (Pubitemid 46091994)
5. Hippenstiel, S., B. Opitz, B. Schmeck, and N. Suttorp. 2006. Lung epithelium as a sentinel and effector system in pneumonia-molecular mechanisms of pathogen recognition and signal transduction. Respir. Res. 7: 97. (Pubitemid 44183998)
6. Opitz, B., A. Puschel, B. Schmeck, A. C. Hocke, S. Rosseau, S. Hammerschmidt, R. R. Schumann, N. Suttorp, and S. Hippenstiel. 2004. Nucleotide-binding oligomerization domain proteins are innate immune receptors for internalized Streptococcus pneumoniae. J. Biol. Chem. 279: 36426-36432.
7. Schmeck, B., J. Zahlten, K. Moog, V. van Laak, S. Huber, A. C. Hocke, B. Opitz, E. Hoffmann, M. Kracht, J. Zerrahn, et al. 2004. Streptococcus pneumoniaeinduced p38 MAPK-dependent phosphorylation of RelA at the interleukin-8 promotor. J. Biol. Chem. 279: 53241-53247. (Pubitemid 40051827)
8. Schmeck, B., S. Huber, K. Moog, J. Zahlten, A. C. Hocke, B. Opitz, S. Hammerschmidt, T. J. Mitchell, M. Kracht, S. Rosseau, et al. 2006. Pneumococci induced TLR- and Rac1-dependent NF-κB-recruitment to the IL-8 promoter in lung epithelial cells. Am. J. Physiol. 290: L730-L737. (Pubitemid 43725078)
9. Schmeck, B., K. Moog, J. Zahlten, V. van Laak, P. D. N'Guessan, B. Opitz, S. Rosseau, N. Suttorp, and S. Hippenstiel. 2006. Streptococcus pneumoniae induced c-Jun-N-terminal kinase- and AP-1-dependent IL-8 release by lung epithelial BEAS-2B cells. Respir. Res. 7: 98. (Pubitemid 44177849)
10. Strieter, R. M., J. A. Belperio, and M. P. Keane. 2003. Host innate defenses in the lung: the role of cytokines. Curr. Opin. Infect. Dis. 16: 193-198. (Pubitemid 36677311)
11. Strieter, R. M. 2002. Interleukin-8: a very important chemokine of the human airway epithelium. Am. J. Physiol. 283: L688-L689.
12. Schmeck, B., W. Beermann, V. van Laak, J. Zahlten, B. Opitz, M. Witzenrath, A. C. Hocke, T. Chakraborty, M. Kracht, S. Rosseau, et al. 2005. Intracellular bacteria differentially regulated endothelial cytokine release by MAPK-dependent histone modification. J. Immunol. 175: 2843-2850. (Pubitemid 41170501)
13. Muegge, K. 2002. Preparing the target for the bullet. Nat. Immunol. 3: 16-17.
14. Saccani, S., S. Pantano, and G. Natoli. 2002. p38-dependent marking of inflammatory genes for increased NF-κB recruitment. Nat. Immunol. 3: 69-75. (Pubitemid 34065620)
15. Schmeck, B., W. Beermann, V. van Laak, B. Opitz, A. C. Hocke, K. Meixenberger, J. Eitel, T. Chakraborty, G. Schmidt, H. Barth, et al. 2006. Listeria monocytogenes induced Rac1-dependent signal transduction in endothelial cells. Biochem. Pharmacol. 72: 1367-1374. (Pubitemid 44666741)
16. Adcock, I. M., K. Ito, and P. J. Barnes. 2005. Histone deacetylation: an important mechanism in inflammatory lung diseases. COPD 2: 445-455. (Pubitemid 43879443)
17. Opitz, B., M. Vinzing, V. van Laak, B. Schmeck, G. Heine, S. Gunther, R. Preissner, H. Slevogt, P. D. N'Guessan, J. Eitel, et al. 2006. Legionella pneumophila induces IFNβ in lung epithelial cells via IPS-1 and IRF3, which also control bacterial replication. J. Biol. Chem. 281: 36173-36179. (Pubitemid 46041351)
18. Schmeck, B., R. Gross, P. D. N'Guessan, A. C. Hocke, S. Hammerschmidt, T. J. Mitchell, S. Rosseau, N. Suttorp, and S. Hippenstiel. 2004. Streptococcus pneumoniae-induced caspase 6-dependent apoptosis in lung epithelium. Infect. Immun. 72: 4940-4947. (Pubitemid 39223376)
19. N'Guessan, P. D., M. O. Etouem, B. Schmeck, A. C. Hocke, S. Scharf, K. Vardarova, B. Opitz, A. Flieger, N. Suttorp, and S. Hippenstiel. 2007. Legionella pneumophila-induced PKC α-, MAPK-, and NF-κB-dependent COX-2 expression in human lung epithelium. Am. J. Physiol. 292: L267-L277.
20. Hoffmann, E., A. Thiefes, D. Buhrow, O. Dittrich-Breiholz, H. Schneider, K. Resch, and M. Kracht. 2005. MEK1-dependent delayed expression of Fosrelated antigen-1 counteracts c-Fos and p65 NF-κB-mediated interleukin-8 transcription in response to cytokines or growth factors. J. Biol. Chem. 280: 9706-9718. (Pubitemid 40409669)
21. Slevogt, H., B. Schmeck, C. Jonatat, J. Zahlten, W. Beermann, V. van Laak, B. Opitz, S. Dietel, P. D. N'Guessan, S. Hippenstiel, et al. 2006. Moraxella catarrhalis induces inflammatory response of bronchial epithelial cells via MAPK and NF-κB activation and histone deacetylase activity reduction. Am. J. Physiol. 290: L818-L826. (Pubitemid 43725042)
22. Maruta, K., H. Miyamoto, T. Hamada, M. Ogawa, H. Taniguchi, and S. Yoshida. 1998. Entry and intracellular growth of Legionella dumoffii in alveolar epithelial cells. Am. J. Respir. Crit. Care Med. 157: 1967-1974. (Pubitemid 28311287)
23. Mukaida, N. 2003. Pathophysiological roles of interleukin-8/CXCL8 in pulmonary diseases. Am. J. Physiol. 284: L566-L577. (Pubitemid 36343304)
24. Pease, J. E., and I. Sabroe. 2002. The role of interleukin-8 and its receptors in inflammatory lung disease: implications for therapy. Am. J. Respir. Med. 1: 19-25.
25. Teruya, H., F. Higa, M. Akamine, C. Ishikawa, T. Okudaira, K. Tomimori, N. Mukaida, M. Tateyama, K. Heuner, J. Fujita, and N. Mori. 2007. Mechanisms of Legionella pneumophila-induced interleukin-8 expression in human lung epithelial cells. BMC Microbiol. 7: 102. (Pubitemid 351169911)
26. Tateda, K., T. A. Moore, M. W. Newstead, W. C. Tsai, X. Zeng, J. C. Deng, G. Chen, R. Reddy, K. Yamaguchi, and T. J. Standiford. 2001. Chemokinedependent neutrophil recruitment in a murine model of Legionella pneumonia: potential role of neutrophils as immunoregulatory cells. Infect. Immun. 69: 2017-2024. (Pubitemid 32239664)
27. Avni, O., D. Lee, F. Macian, S. J. Szabo, L. H. Glimcher, and A. Rao. 2002. Th cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat. Immunol. 3: 643-651. (Pubitemid 34752473)
28. Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifi- cations. Nature 403: 41-45.
29. Nightingale, K. P., L. P. O'Neill, and B. M. Turner. 2006. Histone modifications: signalling receptors and potential elements of a heritable epigenetic code. Curr. Opin. Genet. Dev. 16: 125-136.
30. Claus, R., and M. Lubbert. 2003. Epigenetic targets in hematopoietic malignancies. Oncogene 22: 6489-6496.
31. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293: 1074-1080.
32. Eberharter, A., R. Ferreira, and P. Becker. 2005. Dynamic chromatin: concerted nucleosome remodelling and acetylation. Biol. Chem. 386: 745-751. (Pubitemid 41448155)
33. Backs, J., and E. N. Olson. 2006. Control of cardiac growth by histone acetylation/ deacetylation. Circ. Res. 98: 15-24. (Pubitemid 43977219)
34. Huang, S. M., and D. J. McCance. 2002. Down regulation of the interleukin-8 promoter by human papillomavirus type 16 E6 and E7 through effects on CREB binding protein/p300 and P/CAF. J. Virol. 76: 8710-8721.
35. Vanden Berghe, W., K. De Bosscher, E. Boone, S. Plaisance, and G. Haegeman. 1999. The nuclear factor-κB engages CBP/p300 and histone acetyltransferase activity for transcriptional activation of the interleukin-6 gene promoter. J. Biol. Chem. 274: 32091-32098. (Pubitemid 129503803)
36. Hippenstiel, S., B. Schmeck, J. Seybold, M. Krull, C. Eichel-Streiber, and N. Suttorp. 2002. Reduction of tumor necrosis factor-α (TNF-α) related nuclear factor-κB (NF-κB) translocation but not inhibitor κ-B (Iκ-B)-degradation by Rho protein inhibition in human endothelial cells. Biochem. Pharmacol. 64: 971-977. (Pubitemid 35232271)
37. Hoffmann, E., O. Dittrich-Breiholz, H. Holtmann, and M. Kracht. 2002. Multiple control of interleukin-8 gene expression. J. Leukocyte Biol. 72: 847-855. (Pubitemid 35365158)
38. Chen, L. F., Y. Mu, and W. C. Greene. 2002. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-κB. EMBO J. 21: 6539-6548.
39. Sheppard, K. A., D. W. Rose, Z. K. Haque, R. Kurokawa, E. McInerney, S. Westin, D. Thanos, M. G. Rosenfeld, C. K. Glass, and T. Collins. 1999. Transcriptional activation by NF-κB requires multiple coactivators. Mol. Cell. Biol. 19: 6367-6378. (Pubitemid 29399341)
40. Kalkhoven, E. 2004. CBP and p300: HATs for different occasions. Biochem. Pharmacol. 68: 1145-1155. (Pubitemid 39094280)
41. Nakatani, Y. 2001. Histone acetylases-versatile players. Genes Cells 6: 79-86.
42. Flieger, A., K. Rydzewski, S. Banerji, M. Broich, and K. Heuner. 2004. Cloning and characterization of the gene encoding the major cell-associated phospholipase A of Legionella pneumophila, plaB, exhibiting hemolytic activity. Infect. Immun. 72: 2648-2658. (Pubitemid 38542391)
43. Segal, G., M. Feldman, and T. Zusman. 2005. The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii. FEMS Microbiol. Rev. 29: 65-81.
44. Fuse, E. T., K. Tateda, Y. Kikuchi, T. Matsumoto, F. Gondaira, A. Azuma, S. Kudoh, T. J. Standiford, and K. Yamaguchi. 2007. Role of Toll-like receptor 2 in recognition of Legionella pneumophila in a murine pneumonia model. J. Med. Microbiol. 56: 305-312.
45. Akamine, M., F. Higa, N. Arakaki, K. Kawakami, K. Takeda, S. Akira, and A. Saito. 2005. Differential roles of Toll-like receptors 2 and 4 in in vitro responses of macrophages to Legionella pneumophila. Infect. Immun. 73: 352-361.
46. Hawn, T. R., A. Verbon, K. D. Lettinga, L. P. Zhao, S. S. Li, R. J. Laws, S. J. Skerrett, B. Beutler, L. Schroeder, A. Nachman, et al. 2003. A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to Legionnaires' disease. J. Exp. Med. 198: 1563-1572.
47. Hawn, T. R., W. R. Berrington, I. A. Smith, S. Uematsu, S. Akira, A. Aderem, K. D. Smith, and S. J. Skerrett. 2007. Altered inflammatory responses in TLR5- deficient mice infected with Legionella pneumophila. J. Immunol. 179: 6981-6987.
48. Smith, K. D., and A. Ozinsky. 2002. Toll-like receptor-5 and the innate immune response to bacterial flagellin. Curr. Top. Microbiol. Immunol. 270: 93-108.
49. Molofsky, A. B., B. G. Byrne, N. N. Whitfield, C. A. Madigan, E. T. Fuse, K. Tateda, and M. S. Swanson. 2006. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 203: 1093-1104.
50. Ren, T., D. S. Zamboni, C. R. Roy, W. F. Dietrich, and R. E. Vance. 2006. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS. Pathog. 2: e18.