Protein kinase D interaction with TLR5 is required for inflammatory signaling in response to bacterial flagellin

Journal of Immunology

Volumn 178, Issue 9, 2007, Pages 5735-5743

  Ivison, Sabine M ^a   Graham, Nicholas R ^a   Bernales, Cecily Q ^a   Kifayet, Arnawaz ^a   Ng, Natalie ^a   Shobab, Leila A ^a   Steiner, Theodore S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; FLAGELLIN; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE C; PROTEIN KINASE D; PROTEIN SERINE THREONINE KINASE; TOLL LIKE RECEPTOR 5;

ARTICLE; CELL STRAIN CACO 2; CELL STRAIN HEK293; CONTROLLED STUDY; ENTEROAGGREGATIVE ESCHERICHIA COLI; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; GEL MOBILITY SHIFT ASSAY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INFLAMMATION; MASS SPECTROMETRY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 34247574203     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.9.5735     Document Type: Article

References (39)

1. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
2. Kawai, T., and S. Akira. 2006. TLR signaling. Cell Death Differ. 13: 816-825.
3. Sierro, F., B. Dubois, A. Coste, D. Kaiserlian, J. P. Kraehenbuhl, and J. C. Sirard. 2001. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. USA 98: 13722-13727.
4. Steiner, T. S., J. P. Nataro, C. E. Poteet-Smith, J. A. Smith, and R. L. Guerrant. 2000. Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J. Clin. Invest. 105: 1769-1777.
5. Moors, M. A., L. Li, and S. B. Mizel. 2001. Activation of interleukin-1 receptor-associated kinase by Gram-negative flagellin. Infect. Immun. 69: 4424-4429.
6. Khan, M. A., J. Kang, and T. S. Steiner. 2004. Enteroaggregative Escherichia coli flagellin-induced interleukin-8 secretion requires Toll-like receptor 5-dependent p38 MAP kinase activation. Immunology 112: 651-660.
7. Tallant, T., A. Deb, N. Kar, J. Lupica, M. J. de Veer, and J. A. DiDonato. 2004, Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-κB and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol. 4: 33.
8. Rhee, S. H., A. C. Keates, M. P. Moyer, and C. Pothoulakis. 2004. MEK is a key modulator for TLR5-induced interleukin-8 and MIP3α gene expression in non-transformed human colonic epithelial cells. J. Biol. Chem. 279: 25179-25188.
9. Ogushi, K., A. Wada, T. Niidome, N. Mori, K Oishi, T. Nagatake, A. Takahashi, H. Asakura, S. Makino, H. Hojo, et al. 2001. Salmonella enteritidis FliC (flagella filament protein) induces human β-defensin-2 mRNA production by Caco-2 cells. J. Biol. Chem. 276: 30521-30526.
10. Harrington, S. M., M. C. Strauman, C. M. Abe, and J. P. Nataro. 2005. Aggregative adherence fimbriae contribute to the inflammatory response of epithelial cells infected with enteroaggregative Escherichia coli. Cell. Microbiol. 7: 1565-1578.
11. Rozengurt, E., O. Rey, and R. T. Waldron. 2005. Protein kinase D signaling. J. Biol. Chem. 280: 13205-13208.
12. Rykx, A., L. De Kimpe, S. Mikhalap, T. Vantus, T. Seufferlein, J. R. Vandenheede, and J. Van Lint. 2003. Protein kinase D: a family affair. FEBS Lett. 546: 81-86.
13. Parhar, K., A. Ray, U. Steinbrecher, C. Nelson, and B. Salh. 2003. The p38 mitogen-activated protein kinase regulates interleukin-1β-induced IL-8 expression via an effect on the IL-8 promoter in intestinal epithelial cells. Immunology 108: 502-512.
14. Donnelly, M. A., and T. S. Steiner. 2002. Two nonadjacent regions in enteroaggregative Escherichia coli flagellin are required for activation of Toll-like receptor 5. J. Biol. Chem. 277: 40456-40461.
15. Xu, Y., X. Tao, B. Shen, T. Horng, R. Medzhitov, J. L. Manley, and L. Tong, 2000. Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 408: 111-115.
16. Cherkasov, A. 2003. Inductive electronegativity scale: iterative calculation of inductive partial charges. J. Chem. Inf. Comput. Sci. 43: 2039-2047.
17. Cherkasov, A. 2005. "Inductive" descriptors: 10 successful years in QSAR. Current Computer-Aided Drug Design 1: 21-42.
18. Ivison, S. M., M. A. Khan, N. R. Graham, C. Q. Bernales, A. Kaleem, C. O. Tirling, A. Cherkasov, and T. S. Steiner. 2007. A phosphorylation site in the Toll-like receptor 5 TIR domain is required for inflammatory signalling in response to flagellin. Biochem. Biophys. Res. Commun. 352: 936-941.
19. Hutti, J. E., E. T. Jarrell, J. D. Chang, D. W. Abbott, P. Storz, A. Toker, L. C. Cantley, and B. E. Turk. 2004. A rapid method for determining protein kinase phosphorylation specificity. Nat. Methods 1: 27-29.
20. Doppler, H., P. Storz, J. Li, M. J. Comb, and A. Toker. 2005. A phosphorylation state-specific antibody recognizes Hsp27, a novel substrate of protein kinase D. J. Biol. Chem. 280: 15013-15019.
21. Nishikawa, K., A. Toker, F. J. Johannes, Z. Songyang, and L. C. Cantley. 1997. Determination of the specific substrate sequence motifs of protein kinase C isozymes. J. Biol. Chem. 272: 952-960.
22. Gschwendt, M., S. Dieterich, J. Rennecke, W. Kittstein, H.-J. Mueller, and F.-J. Johannes. 1996. Inhibition of protein kinase Cμ by various inhibitors: differentiation from protein kinase c isoenzymes. FEBS Lett. 392: 77-80.
23. Bambou, J.-C., A. Giraud, S. Menard, B. Begue, S. Rakotobe, M. Heyman, F. Taddei, N. Cerf-Bensussan, and V. Gaboriau-Routhiau. 2004. In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J. Biol. Chem. 279: 42984-42992.
24. Storz, P., and A. Toker. 2003. Protein kinase D mediates a stress-induced NF-κB activation and survival pathway. EMBO J. 22: 109-120.
25. Ghanekar, Y., and M. Lowe. 2005. Signalling for secretion. Nat. Cell Biol. 7: 851-853.
26. Lodes, M. J., Y. Cong, C. O. Elson, R. Mohamath, C. J. Landers, S. R. Targan, M. Fort, and R. M. Hershberg. 2004. Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Invest. 113: 1296-1306.
27. Hawn, T. R., H. Wu, J. M. Grossman, B. H. Hahn, B. P. Tsao, and A. Aderem. 2005. A stop codon polymorphism of Toll-like receptor 5 is associated with resistance to systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 102: 10593-10597.
28. Zeng, H., A. Q. Carlson, Y. Guo, Y. Yu, L. S. Collier-Hyams, J. L. Madara, A. T. Gewirtz, and A. S. Neish. 2003. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171: 3668-3674.
29. 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.
30. Brändlin, I., S. Hübner, T. Eiseler, M. Martinez-Moya, A. Horschinek, A. Hausser, G. Link, S. Rupp, P. Storz, K. Pfizenmaier, and F.-J. Johannes. 2002. Protein kinase C (PKC)η-mediated PKCμ activation modulates ERK and JNK signal pathways. J. Biol. Chem. 277: 6490-6496.
31. Lemonnier, J., C. Ghayor, J. Guicheux, and J. Caverzasio. 2004. Protein kinase C-independent activation of protein kinase D is involved in BMP-2-induced activation of stress mitogen-activated protein kinases JNK and p38 and osteoblastic cell differentiation. J. Biol. Chem. 279: 259-264.
32. Chen, J., G. Lu, and Q. J. Wang. 2005. Protein kinase C-independent effects of protein kinase D3 in glucose transport in L6 myotubes. Mol. Pharmacol. 67: 152-162.
33. Saccani, S., S. Pantano, and G. Natoli. 2002. p38-dependent marking of inflammatory genes for increased NF-κB recruitment. Nat. Immunol. 3: 69-75.
34. Tebo, J., S. Der, M. Frevel, K. S. Khabar, B. R. Williams, and T. A. Hamilton. 2003. Heterogeneity in control of mRNA stability by AU-rich elements. J. Biol. Chem. 278: 12085-12093.
35. Yu, Y., H. Zeng, S. Lyons, A. Carlson, D. Merlin, A. S. Neish, and A. T. Gewirtz. 2003. TLR5-mediated activation of p38 MAPK regulates epithelial IL-8 expression via posttranscriptional mechanism. Am. J. Physiol. 285: G282-G290.
36. Sidorenko, S. P., C. L. Law, S. J. Klaus, K. A. Chandran, M. Takata, T. Kurosaki, and E. A. Clark. 1996. Protein kinase Cμ (PKCμ) associates with the B cell antigen receptor complex and regulates lymphocyte signaling. Immunity 5: 353-363.
37. Matthews, S. A., E. Rozengurt, and D. Cantrell. 1999. Characterization of serine 916 as an in vivo autophosphorylation site for protein kinase D/protein kinase Cμ. J. Biol. Chem. 274: 26543-26549.
38. Vigorito, E., D. Kovesdi, and M. Turner. 2005. Synergistic activation of PKD by the B cell antigen receptor and CD19 requires PI3K, Vav1 and PLCγ. Cell. Signal. 18: 1455-1460.
39. Haxhinasto, S. A., and G. A. Bishop. 2003. A novel interaction between protein kinase D and TNF receptor-associated factor molecules regulates B cell receptor-CD40 synergy. J. Immunol. 171: 4655-4662.