Live legionella pneumophila induces muc5ac production by airway epithelial cells independently of intracellular invasion

Canadian Journal of Microbiology

Volumn 58, Issue 2, 2012, Pages 151-157

  Morinaga, Yoshitomo ^a   Yanagihara, Katsunori ^a   Araki, Nobuko ^a   Migiyama, Yohei ^a   Nagaoka, Kentaro ^a   Harada, Yosuke ^a   Yamada, Koichi ^a   Hasegawa, Hiroo ^a   Nishino, Tomoya ^a   Izumikawa, Koichi ^a   Kakeya, Hiroshi ^a   Yamamoto, Yoshihiro ^a   Kohno, Shigeru ^a   Kamihira, Shimeru ^a  

^a NAGASAKI UNIVERSITY   (Japan)

Author keywords

Legionella pneumophila; Muc5ac; Mucin

Indexed keywords

AIRBORNE PATHOGENS; AIRWAY EPITHELIAL CELLS; AIRWAY EPITHELIUM; CYTOCHALASIN D; IMMUNE RESPONSE; IN-VITRO; INTRACELLULAR PATHOGENS; LEGIONELLA PNEUMOPHILA; MUC5AC; MUCIN; MUCIN PROTEINS;

CELLS; FORMALDEHYDE; PATHOGENS;

ENZYME ACTIVITY;

CYTOCHALASIN D; FORMALDEHYDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MUCIN 5AC; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; SYNAPTOTAGMIN I; VIRULENCE FACTOR;

BACTERIUM; BIOCHEMISTRY; BIOLOGICAL PRODUCTION; CYTOLOGY; DOSE-RESPONSE RELATIONSHIP; IMMUNE RESPONSE; INHIBITOR; MEMBRANE; METABOLITE; MUCUS; PATHOGEN; PNEUMONIA; PROTEIN; RESPIRATION;

ARTICLE; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LEGIONELLA PNEUMOPHILA; MUCUS; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; ULTRAVIOLET RADIATION;

EPITHELIAL CELLS; HUMANS; IMMUNE SYSTEM PROCESSES; LEGIONELLA PNEUMOPHILA; MAP KINASE SIGNALING SYSTEM; MUCIN 5AC; NF-KAPPA B;

LEGIONELLA PNEUMOPHILA;

EID: 84856429851     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/W11-123     Document Type: Article

References (30)

1. Akamine, M., Higa, F., Arakaki, N., Kawakami, K., Takeda, K., Akira, S., and Saito, A. 2005. Differential roles of Toll-like receptors 2 and 4 in in vitro responses of macrophages to Legionella pneumophila. Infect. Immun. 73(1): 352-361. doi:10. 1128/IAI.73.1.352-361.2005. PMID:15618172.
2. Araki, N., Yanagihara, K., Morinaga, Y., Yamada, K., Nakamura, S., Yamada, Y., et al. 2010. Azithromycin inhibits nontypeable Haemophilus influenzae-induced MUC5AC expression and secretion via inhibition of activator protein-1 in human airway epithelial cells. Eur. J. Pharmacol. 644(1-3): 209-214. doi:10.1016/j.ejphar. 2010.06.056. PMID:20619258.
3. Bitar, D.M., Molmeret, M., and Abu Kwaik, Y. 2004. Molecular and cell biology of Legionella pneumophila. Int. J. Med. Microbiol. 293(7-8): 519-527. doi:10.1078/1438-4221-00286. PMID: 15149027.
4. Chang, B., Amemura-Maekawa, J., Kura, F., Kawamura, I., and Watanabe, H. 2004. Expression of IL-6 and TNF-a in human alveolar epithelial cells is induced by invading, but not by adhering, Legionella pneumophila. Microb. Pathog. 37(6): 295-302. doi:10.1016/j.micpath.2004.10.002. PMID:15619425.
5. Chen, R., Lim, J.H., Jono, H., Gu, X.X., Kim, Y.S., Basbaum, C.B., et al. 2004. Nontypeable Haemophilus influenzae lipoprotein P6 induces MUC5AC mucin transcription via TLR2-TAK1-dependent p38 MAPK-AP1 and IKKb-IkBa-NF-kB signaling pathways. Biochem. Biophys. Res. Commun. 324(3): 1087-1094. doi:10.1016/j.bbrc.2004.09.157. PMID:15485666.
6. DeFife, K.M., Jenney, C.R., Colton, E., and Anderson, J.M. 1999. Disruption of filamentous actin inhibits human macrophage fusion. FASEB J. 13(8): 823-832. PMID:10224226.
7. Friedman, H., Yamamoto, Y., and Klein, T.W. 2002. Legionella pneumophila pathogenesis and immunity. Semin. Pediatr. Infect. Dis. 13(4): 273-279. doi:10.1053/spid.2002.127206. PMID: 12491233.
8. Horwitz, M.A. 1983. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158(4): 1319-1331. doi:10.1084/ jem.158.4.1319. PMID:6619736.
9. Imamura, Y., Yanagihara, K., Mizuta, Y., Seki, M., Ohno, H., Higashiyama, Y., et al. 2004. Azithromycin inhibits MUC5AC production induced by the Pseudomonas aeruginosa autoinducer N-(3-oxododecanoyl) homoserine lactone in NCI-H292 cells. Antimicrob. Agents Chemother. 48(9): 3457-3461. doi:10.1128/ AAC.48.9.3457-3461.2004. PMID:15328111.
10. Inoue, D., Yamaya, M., Kubo, H., Sasaki, T., Hosoda, M., Numasaki, M., et al. 2006. Mechanisms of mucin production by rhinovirus infection in cultured human airway epithelial cells. Respir. Physiol. Neurobiol. 154(3): 484-499. doi:10.1016/j.resp.2005.11.006. PMID:16377262.
11. Kraft, M., Adler, K.B., Ingram, J.L., Crews, A.L., Atkinson, T.P., Cairns, C.B., et al. 2008. Mycoplasma pneumoniae induces airway epithelial cell expression of MUC5AC in asthma. Eur. Respir. J. 31(1): 43-46. doi:10.1183/09031936.00103307. PMID:18166592.
12. Lewinsohn, D.M., Alderson, M.R., Briden, A.L., Riddell, S.R., Reed, S.G., and Grabstein, K.H. 1998. Characterization of human CD8+ T cells reactive with Mycobacterium tuberculosis-infected antigen presenting cells. J. Exp. Med. 187(10): 1633-1640. doi:10.1084/ jem.187.10.1633. PMID:9584141.
13. Li, D., Gallup, M., Fan, N., Szymkowski, D.E., and Basbaum, C.B. 1998. Cloning of the amino-terminal and 5′-flanking region of the human MUC5AC mucin gene and transcriptional up-regulation by bacterial exoproducts. J. Biol. Chem. 273(12): 6812-6820. doi:10. 1074/jbc.273.12.6812. PMID:9506983.
14. Lorenz, J., Zahlten, J., Pollok, I., Lippmann, J., Scharf, S., N'Guessan, P.D., et al. 2010. Legionella pneumophila induced ikbz-dependent expression of il-6 in lung epithelium. Eur. Respir. J. 37(3): 648-657. doi:10.1183/09031936.00200009. PMID: 20650996.
15. Morinaga, Y., Yanagihara, K., Miyashita, N., Seki, M., Izumikawa, K., Kakeya, H., et al. 2009. Azithromycin, clarithromycin and telithromycin inhibit MUC5AC induction by Chlamydophila pneumoniae in airway epithelial cells. Pulm. Pharmacol. Ther. 22(6): 580-586. doi:10.1016/j.pupt.2009.08.004. PMID: 19716898.
16. N'Guessan, P.D., Etouem, M.O., Schmeck, B., Hocke, A.C., Scharf, S., Vardarova, K., et al. 2007. Legionella pneumophila-induced PKCa-, MAPK-, and NF-kB-dependent COX-2 expression in human lung epithelium. Am. J. Physiol. Lung Cell. Mol. Physiol. 292(1): L267-L277. doi:10.1152/ajplung.00100.2006. PMID: 17012371.
17. Opitz, B., Vinzing, M., van Laak, V., Schmeck, B., Heine, G., Gunther, S., et al. 2006. Legionella pneumophila induces IFNb in lung epithelial cells via IPS-1 and IRF3, which also control bacterial replication. J. Biol. Chem. 281(47): 36173-36 179. doi:10.1074/jbc.M604638200. PMID:16984921.
18. Rose, M.C., and Voynow, J.A. 2006. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol. Rev. 86(1): 245-278. doi:10.1152/physrev.00010.2005. PMID: 16371599.
19. Saijo, T., Izumikawa, K., Takazono, T., Kosai, K., Kurihara, S., Nakamura, S., et al. 2008. A case of Legionella pneumophila pneumonia followed by invasive aspergillosis. Jpn. J. Infect. Dis. 61(5): 379-381. PMID:18806346.
20. Scharf, S., Hippenstiel, S., Flieger, A., Suttorp, N., and N'Guessan, P. D. 2010. Induction of human b-defensin-2 in pulmonary epithelial cells by Legionella pneumophila: involvement of TLR2 and TLR5, p38 MAPK, JNK, NF-kB and AP-1. Am. J. Physiol. Lung Cell. Mol. Physiol. 298(5): L687-L695. doi:10.1152/ajplung. 00365.2009. PMID:20154223.
21. Schmeck, B., N'Guessan, P.D., Ollomang, M., Lorenz, J., Zahlten, J., Opitz, B., et al. 2007. Legionella pneumophila-induced NF-kB-and MAPK-dependent cytokine release by lung epithelial cells. Eur. Respir. J. 29(1): 25-33. doi:10.1183/09031936.00141005. PMID:16971406.
22. Shao, M.X., and Nadel, J.A. 2005. Neutrophil elastase induces MUC5AC mucin production in human airway epithelial cells via a cascade involving protein kinase C, reactive oxygen species, and TNF-a-converting enzyme. J. Immunol. 175(6): 4009-4016. PMID:16148149.
23. Shao, M.X., Nakanaga, T., and Nadel, J.A. 2004. Cigarette smoke induces MUC5AC mucin overproduction via tumor necrosis factor-a-converting enzyme in human airway epithelial (NCI-H292) cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 287(2): L420-L427. doi:10.1152/ajplung.00019.2004. PMID:15121636.
24. Song, K.S., Lee, W.J., Chung, K.C., Koo, J.S., Yang, E.J., Choi, J.Y., and Yoon, J.H. 2003. Interleukin-1 b and tumor necrosis factor-a induce MUC5AC overexpression through a mechanism involving ERK/p38 mitogen-activated protein kinases-MSK1-CREB activation in human airway epithelial cells. J. Biol. Chem. 278(26): 23243-23250. doi:10.1074/jbc.M300096200. PMID:12690113.
25. Teruya, H., Higa, F., Akamine, M., Ishikawa, C., Okudaira, T., Tomimori, K., et al. 2007. Mechanisms of Legionella pneumophila-induced interleukin-8 expression in human lung epithelial cells. BMC Microbiol. 7(1): 102. doi:10.1186/1471-2180-7-102. PMID:18034886.
26. Ünal, C., Schwedhelm, K.F., Thiele, A., Weiwad, M., Schweimer, K., Frese, F., et al. 2011. Collagen IV-derived peptide binds hydrophobic cavity of Legionella pneumophila Mip and interferes with bacterial epithelial transmigration. Cell. Microbiol. 13(10): 1558-1572. doi:10.1111/j.1462-5822.2011.01641.x. PMID: 21794054.
27. Wagner, C., Khan, A.S., Kamphausen, T., Schmausser, B., Unal, C., Lorenz, U., et al. 2007. Collagen binding protein Mip enables Legionella pneumophila to transmigrate through a barrier of NCI-H292 lung epithelial cells and extracellular matrix. Cell. Microbiol. 9(2): 450-462. doi:10.1111/j.1462-5822.2006.00802.x. PMID:16953800.
28. Welsh, C.T., Summersgill, J.T., and Miller, R.D. 2004. Increases in c-Jun N-terminal kinase/stress-activated protein kinase and p38 activity in monocyte-derived macrophages following the uptake of Legionella pneumophila. Infect. Immun. 72(3): 1512-1518. doi:10.1128/IAI.72.3.1512-1518.2004. PMID:14977957.
29. Williams, O.W., Sharafkhaneh, A., Kim, V., Dickey, B.F., and Evans, C.M. 2006. Airway mucus: from production to secretion. Am. J. Respir. Cell Mol. Biol. 34(5): 527-536. doi:10.1165/rcmb.2005-0436SF. PMID:16415249.
30. Yanagihara, K., Seki, M., and Cheng, P.W. 2001. Lipopolysaccharide induces mucus cell metaplasia in mouse lung. Am. J. Respir. Cell Mol. Biol. 24(1): 66-73. PMID:11152652.