Pseudomonas aeruginosa quorum-sensing molecule homoserine lactone modulates inflammatory signaling through PERK and eI-F2a

Journal of Immunology

Volumn 193, Issue 3, 2014, Pages 1459-1467

  Grabiner, Mark A ^a   Fu, Zhu ^a   Wu, Tara ^a   Barry, Kevin C ^a   Schwarzer, Christian ^a   Machen, Terry E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 2ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; METHIONINE; N (3 OXODODECANOYL)HOMOSERINE LACTONE; PROTEIN KINASE; PROTEIN KINASE RNA LIKE ER KINASE; SULFUR 35; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST CULTURE; HOST PATHOGEN INTERACTION; INFLAMMATION; MOUSE; MOUSE EMBRYONIC FIBROBLAST; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN SYNTHESIS INHIBITION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; QUORUM SENSING; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; WILD TYPE;

4-BUTYROLACTONE; ANIMALS; CELL LINE; EIF-2 KINASE; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC INITIATION FACTOR-2; INFLAMMATION MEDIATORS; MICE; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SIGNAL TRANSDUCTION;

EID: 84906098504     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303437     Document Type: Article

References (36)

1. Hoiby, N., E. W. Flensborg, B. Beck, B. Friis, S. V. Jacobsen, and L. Jacobsen. 1977. Pseudomonas aeruginosa infection in cystic fibrosis: diagnostic and prognostic significance of Pseudomonas aeruginosa precipitins determined by means of crossed immunoelectrophoresis. Scand. J. Respir. Dis. 58: 65-79.
2. Schuster, M., and E. P. Greenberg. 2006. A network of networks: quorumsensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296: 73-81.
3. Rumbaugh, K. P. 2007. Convergence of hormones and autoinducers at the host/pathogen interface. Anal. Bioanal. Chem. 387: 425-435.
4. Irie, Y., and M. Parsek. 2008. Quorum sensing and microbial biofilms. In Bacterial Biofilms. Springer-Verlag, Dusseldorf, Germany, p. 67-84.
5. Tateda, K., Y. Ishii, M. Horikawa, T. Matsumoto, S. Miyairi, J. C. Pechere, T. J. Standiford, M. Ishiguro, and K. Yamaguchi. 2003. The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect. Immun. 71: 5785-5793.
6. Li, L., D. Hooi, S. R. Chhabra, D. Pritchard, and P. E. Shaw. 2004. Bacterial Nacylhomoserine lactone-induced apoptosis in breast carcinoma cells correlated with down-modulation of STAT3. Oncogene 23: 4894-4902.
7. Jacobi, C. A., F. Schiffner, M. Henkel, M. Waibel, B. Stork, M. Daubrawa, L. Eberl, M. Gregor, and S. Wesselborg. 2009. Effects of bacterial N-acyl homoserine lactones on human Jurkat T lymphocytes-OdDHL induces apoptosis via the mitochondrial pathway. Int. J. Med. Microbiol. 299: 509-519.
8. Li, H., L. Wang, L. Ye, Y. Mao, X. Xie, C. Xia, J. Chen, Z. Lu, and J. Song. 2009. Influence of Pseudomonas aeruginosa quorum sensing signal molecule N-(3-oxododecanoyl) homoserine lactone on mast cells. Med. Microbiol. Immunol. 198: 113-121.
9. Schwarzer, C., S. Wong, J. Shi, E. Matthes, B. Illek, J. P. Ianowski, R. J. Arant, E. Isacoff, H. Vais, J. K. Foskett, et al. 2010. Pseudomonas aeruginosa homoserine lactone activates store-operated cAMP and cystic fibrosis transmembrane regulator-dependent Cl-secretion by human airway epithelia. J. Biol. Chem. 285: 34850-34863.
10. Schwarzer, C., Z. Fu, M. Patanwala, L. Hum, M. Lopez-Guzman, B. Illek, W. Kong, S. V. Lynch, and T. E. Machen. 2012. Pseudomonas aeruginosa biofilm-associated homoserine lactone C12 rapidly activates apoptosis in airway epithelia. Cell. Microbiol. 14: 698-709.
11. Telford, G., D. Wheeler, P. Williams, P. T. Tomkins, P. Appleby, H. Sewell, G. S. Stewart, B. W. Bycroft, and D. I. Pritchard. 1998. The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity. Infect. Immun. 66: 36-42.
12. Smith, R. S., E. R. Fedyk, T. A. Springer, N. Mukaida, B. H. Iglewski, and R. P. Phipps. 2001. IL-8 production in human lung fibroblasts and epithelial cells activated by the Pseudomonas autoinducer N-3-oxododecanoyl homoserine lactone is transcriptionally regulated by NF-kB and activator protein-2. J. Immunol. 167: 366-374.
13. Smith, R. S., R. Kelly, B. H. Iglewski, and R. P. Phipps. 2002. The Pseudomonas autoinducer N-(3-oxododecanoyl) homoserine lactone induces cyclooxygenase-2 and prostaglandin E2 production in human lung fibroblasts: implications for inflammation. J. Immunol. 169: 2636-2642.
14. Kravchenko, V. V., G. F. Kaufmann, J. C. Mathison, D. A. Scott, A. Z. Katz, M. R. Wood, A. P. Brogan, M. Lehmann, J. M. Mee, K. Iwata, et al. 2006. N-(3-oxo-acyl)homoserine lactones signal cell activation through a mechanism distinct from the canonical pathogen-associated molecular pattern recognition receptor pathways. J. Biol. Chem. 281: 28822-28830.
15. Jahoor, A., R. Patel, A. Bryan, C. Do, J. Krier, C. Watters, W. Wahli, G. Li, S. C. Williams, and K. P. Rumbaugh. 2008. Peroxisome proliferator-activated receptors mediate host cell proinflammatory responses to Pseudomonas aeruginosa autoinducer. J. Bacteriol. 190: 4408-4415.
16. Kravchenko, V. V., G. F. Kaufmann, J. C. Mathison, D. A. Scott, A. Z. Katz, D. C. Grauer, M. Lehmann, M. M. Meijler, K. D. Janda, and R. J. Ulevitch. 2008. Modulation of gene expression via disruption of NF-kappaB signaling by a bacterial small molecule. Science 321: 259-263.
17. Glucksam-Galnoy, Y., R. Sananes, N. Silberstein, P. Krief, V. V. Kravchenko, M. M. Meijler, and T. Zor. 2013. The bacterial quorum-sensing signal molecule N-3-oxo-dodecanoyl-L-homoserine lactone reciprocally modulates pro-and antiinflammatory cytokines in activated macrophages. J. Immunol. 191: 337-344.
18. Shiner, E. K., D. Terentyev, A. Bryan, S. Sennoune, R. Martinez-Zaguilan, G. Li, S. Gyorke, S. C. Williams, and K. P. Rumbaugh. 2006. Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling. Cell. Microbiol. 8: 1601-1610.
19. Kaufman, R. J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13: 1211-1233.
20. Harding, H. P., Y. Zhang, and D. Ron. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274.
21. Bertolotti, A., Y. Zhang, L. M. Hendershot, H. P. Harding, and D. Ron. 2000. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2: 326-332.
22. Hinnebusch, A. G. 1994. The eIF-2a kinases: regulators of protein synthesis in starvation and stress. In Seminars in Cell Biology. Elsevier, Philadelphia, PA, p. 417-426.
23. Valentine, C. D., H. Zhang, P. W. Phuan, J. Nguyen, A. S. Verkman, and P. M. Haggie. 2014. Small molecule screen yields inhibitors of Pseudomonas homoserine lactone-induced host responses. Cell. Microbiol. 16: 1-14.
24. Christensen, S. B., A. Andersen, J.-C. J. Poulsen, and M. Treiman. 1993. Derivatives of thapsigargin as probes of its binding site on endoplasmic reticulum Ca2+ ATPase: stereoselectivity and important functional groups. FEBS Lett. 335: 345-348.
25. Schwarzer, C., Z. Fu, S. Shuai, S. Babbar, G. Zhao, C. Li, and T. E. Machen. 2014. Pseudomonas aeruginosa homoserine lactone triggers apoptosis and Bak/Bax-independent release of mitochondrial cytochrome C in fibroblasts. Cell. Microbiol.
26. Hybiske, K., Z. Fu, C. Schwarzer, J. Tseng, J. Do, N. Huang, and T. E. Machen. 2007. Effects of cystic fibrosis transmembrane conductance regulator and DeltaF508CFTR on inflammatory response, ER stress, and Ca2+ of airway epithelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 293: L1250-L1260.
27. Krappmann, D., and C. Scheidereit. 1997. Regulation of NF-kB activity by IkBa and IkBb stability. Immunobiology 198: 3-13.
28. Wu, S., M. Tan, Y. Hu, J.-L. Wang, D. Scheuner, and R. J. Kaufman. 2004. Ultraviolet light activates NFkappaB through translational inhibition of IkappaBalpha synthesis. J. Biol. Chem. 279: 34898-34902.
29. Jordan, R., L. Wang, T. M. Graczyk, T. M. Block, and P. R. Romano. 2002. Replication of a cytopathic strain of bovine viral diarrhea virus activates PERK and induces endoplasmic reticulum stress-mediated apoptosis of MDBK cells. J. Virol. 76: 9588-9599.
30. Kravchenko, V. V., and G. F. Kaufmann. 2013. Bacterial inhibition of inflammatory responses via TLR-independent mechanisms. Cell. Microbiol. 15: 527-536.
31. Valentine, C. D., M. O. Anderson, F. R. Papa, and P. M. Haggie. 2013. X-box binding protein 1 (XBP1s) is a critical determinant of Pseudomonas aeruginosa homoserine lactone-mediated apoptosis. PLoS Pathog. 9: e1003576.
32. Hybiske, K., J. K. Ichikawa, V. Huang, S. J. Lory, and T. E. Machen. 2004. Cystic fibrosis airway epithelial cell polarity and bacterial flagellin determine host response to Pseudomonas aeruginosa. Cell. Microbiol. 6: 49-63.
33. Tseng, J., J. Do, J. H. Widdicombe, and T. E. Machen. 2006. Innate immune responses of human tracheal epithelium to Pseudomonas aeruginosa flagellin, TNF-a, and IL-1b. Am. J. Physiol. Cell Physiol. 290: C678-C690.
34. Martino, M. E., J. C. Olsen, N. B. Fulcher, M. C. Wolfgang, W. K. O'Neal, and C. M. Ribeiro. 2009. Airway epithelial inflammation-induced endoplasmic reticulum Ca2+ store expansion is mediated by X-box binding protein-1. J. Biol. Chem. 284: 14904-14913.
35. Vikström, E., F. Tafazoli, and K.-E. Magnusson. 2006. Pseudomonas aeruginosa quorum sensing molecule N-(3 oxododecanoyl)-l-homoserine lactone disrupts epithelial barrier integrity of Caco-2 cells. FEBS Lett. 580: 6921-6928.
36. Vikström, E., L. Bui, P. Konradsson, and K. E. Magnusson. 2009. The junctional integrity of epithelial cells is modulated by Pseudomonas aeruginosa quorum sensing molecule through phosphorylation-dependent mechanisms. Exp. Cell Res. 315: 313-326.