The Fps/Fes kinase regulates the inflammatory response to endotoxin through down-regulation of TLR4, NF-κB activation, and TNF-α secretion in macrophages

Journal of Leukocyte Biology

Volumn 80, Issue 6, 2006, Pages 1522-1528

  Parsons, Sean A ^a   Greer, Peter A ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Cytokine; Endocytosis; Knockout mouse; Lipopolysaccharide; Tyrosine kinase

Indexed keywords

ENDOTOXIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; PROTEIN KINASE FES; PROTEIN MD 2; PROTEIN SUBUNIT; PROTEIN TYROSINE KINASE; SYNAPTOTAGMIN; TOLL LIKE RECEPTOR 4; TRANSFERRIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME REGULATION; ESCHERICHIA COLI; EX VIVO STUDY; GENE ACTIVATION; INFLAMMATION; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; DOWN-REGULATION; I-KAPPA B PROTEINS; IMMUNITY, NATURAL; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-FES; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33845433766     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0506350     Document Type: Article

References (50)

1. Feldman, R. A., Gabrilove, J. L., Tam, J. P., Moore, M. A., Hanafusa, H. (1985) Specific expression of the human cellular fps/fes-encoded protein NCP92 in normal and leukemic myeloid cells. Proc. Natl. Acad. Sci. USA 82, 2379-2383.
2. Robinson, D. R., Wu, Y. M., Lin, S. F. (2000) The protein tyrosine kinase family of the human genome. Oncogene 19, 5548-5557.
3. MacDonald, I., Levy, J., Pawson, T. (1985) Expression of the mammalian c-fes protein in hematopoietic cells and identification of a distinct fes-related protein. Mol. Cell. Biol. 5, 2543-2551.
4. Letwin, K., Yee, S. P., Pawson, T. (1988) Novel protein-tyrosine kinase cDNAs related to fps/fes and eph cloned using anti-phosphotyrosine antibody. Oncogene 3, 621-627.
5. Haigh, J., McVeigh, J., Greer, P. (1996) The fps/fes tyrosine kinase is expressed in myeloid, vascular endothelial, epithelial, and neuronal cells and is localized in the trans-golgi network. Cell Growth Differ. 7, 931-944.
6. Care, A., Mattia, G., Montesoro, E., Parolini, I., Russo, G., Colombo, M. P., Peschle, C. (1994) c-fes expression in ontogenetic development and hematopoietic differentiation. Oncogene 9, 739-747.
7. Sangrar, W., Gao, Y., Bates, B., Zirngibl, R., Greer, P. A. (2004) Activated Fps/Fes tyrosine kinase regulates erythroid differentiation and survival. Exp. Hematol. 32, 935-945.
8. Greer, P. (2002) Closing in on the biological functions of fps/fes and fer. Nat. Rev. Mol. Cell Biol. 3, 278-289.
9. Bellingan, G. (1999) Inflammatory cell activation in sepsis. Br. Med. Bull. 55, 12-29.
10. Zirngibl, R. A., Senis, Y., Greer, P. A. (2002) Enhanced endotoxin sensitivity in fps/fes-null mice with minimal defects in hematopoietic homeostasis. Mol. Cell. Biol. 22, 2472-2486.
11. McCafferty, D. M., Craig, A. W., Senis, Y. A., Greer, P. A. (2002) Absence of Fer protein-tyrosine kinase exacerbates leukocyte recruitment in response to endotoxin. J. Immunol. 168, 4930-4935.
12. Qi, W., Ebbert, K. V., Craig, A. W., Greer, P. A., McCafferty, D. M. (2005) Absence of Fer protein tyrosine kinase exacerbates endotoxin induced intestinal epithelial barrier dysfunction in vivo. Gut 54, 1091-1097.
13. Dunne, A. O'Neill, Luke A.J. (2003) The interleukin-1 receptor/toll-like receptor superfamily: signal transduction during inflammation and host defense. Science STKE, 170, 1-17.
14. Guha, M., Mackman, N. (2001) LPS induction of gene expression in human monocytes. Cell. Signal. 13, 85-94.
15. Chen, L. F., Greene, W. C. (2004) Shaping the nuclear action of NF-kappaB. Nat. Rev. Mol. Cell Biol. 5, 392-401.
16. Collart, M. A., Baeuerle, P., Vassalli, P. (1990) Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B. Mol. Cell. Biol. 10, 1498-1506.
17. Husebye, H., Halaas, O., Stenmark, H., Tunheim, G., Sandanger, O., Bogen, B., Brech, A., Latz, E., Espevik, T. (2006) Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25, 683-692.
18. Senis, Y., Zirngibl, R., McVeigh, J., Haman, A., Hoang, T., Greer, P. A. (1999) Targeted disruption of the murine fps/fes proto-oncogene reveals that Fps/Fes kinase activity is dispensable for hematopoiesis. Mol. Cell. Biol. 19, 7436-7446.
19. Ayscough, K. (2004) Endocytosis: actin in the driving seat. Curr. Biol. 14, R124-R126.
20. D'Souza-Schorey, C. (2005) Disassembling adherens junctions: breaking up is hard to do. Trends Cell Biol. 15, 19-26.
21. May, R. C., Machesky, L. M. (2001) Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114, 1061-1077.
22. Laurent, C. E., Delfino, F. J., Cheng, H. Y., Smithgall, T. E. (2004) The human c-Fes tyrosine kinase binds tubulin and microtubules through separate domains and promotes microtubule assembly. Mol. Cell. Biol. 24, 9351-9358.
23. Senis, Y. A., Sangrar, W., Zirngibl, R. A., Craig, A. W., Lee, D. H., Greer, P. A. (2003) Fps/Fes and Fer non-receptor protein-tyrosine kinases regulate collagen- and ADP-induced platelet aggregation. J. Thromb. Haemost. 1, 1062-1070.
24. Takahashi, S., Inatome, R., Hotta, A., Qin, Q., Hackenmiller, R., Simon, M. C., Yamamura, H., Yanagi, S. (2003) Role for Fes/Fps tyrosine kinase in microtubule nucleation through is Fes/CIP4 homology domain. J. Biol. Chem. 278, 49129-49133.
25. Mitsui, N., Inatome, R., Takahashi, S., Goshima, Y., Yamamura, H., Yanagi, S. (2002) Involvement of Fes/Fps tyrosine kinase in semaphorin3A signaling. EMBO J. 21, 3274-3285.
26. Kim, L., Wong, T. W. (1995) The cytoplasmic tyrosine kinase FER is associated with the catenin-like substrate pp120 and is activated by growth factors. Mol. Cell. Biol. 15, 4553-4561.
27. Fan, L., Di Ciano-Oliveira, C., Weed, S. A., Craig, A. W., Greer, P. A., Rotstein, O. D., Kapus, A. (2004) Actin depolymerization-induced tyrosine phosphorylation of cortactin: the role of Fer kinase. Biochem. J. 380, 581-591.
28. Rosato, R., Veltmaat, J. M., Groffen, J., Heisterkamp, N. (1998) Involvement of the tyrosine kinase fer in cell adhesion. Mol. Cell. Biol. 18, 5762-5770.
29. Sayegh, T. Y., Arora, P. D., Fan, L., Laschinger, C. A., Greer, P. A., McCulloch, C. A., Kapus, A. (2005) Phosphorylation of N-cadherin-associated cortactin by Fer kinase regulates N-cadherin mobility and intercellular adhesion strength. Mol. Biol. Cell 16, 5514-5527.
30. Xu, G., Craig, A. W., Greer, P., Miller, M., Anastasiadis, P. Z., Lilien, J., Balsamo, J. (2004) Continuous association of cadherin with beta-catenin requires the non-receptor tyrosine-kinase Fer. J. Cell Sci. 117, 3207-3219.
31. Kogata, N., Masuda, M., Kamioka, Y., Yamagishi, A., Endo, A., Okada, M., Mochizuki, N. (2003) Identification of Fer tyrosine kinase localized on microtubules as a platelet endothelial cell adhesion molecule-1 phosphorylating kinase in vascular endothelial cells. Mol. Biol. Cell 14, 3553-3564.
32. Arregui, C., Pathre, P., Lilien, J., Balsamo, J. (2000) The nonreceptor tyrosine kinase fer mediates cross-talk between N-cadherin and beta1-integrins. J. Cell Biol. 149, 1263-1274.
33. Dautry-Varsat, A. (1986) Receptor-mediated endocytosis: the intracellular journey of transferrin and its receptor. Biochimie 68, 375-381.
34. Hackenmiller, R., Kim, J., Feldman, R. A., Simon, M. C. (2000) Abnormal Stat activation, hematopoietic homeostasis, and innate immunity in c-fes-/- mice. Immunity 13, 397-407.
35. Beutler, B., Milsark, I. W., Cerami, A. C. (1985) Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science 229, 869-871.
36. Bauss, F., Droge, W., Mannel, D. N. (1987) Tumor necrosis factor mediates endotoxic effects in mice. Infect. Immun. 55, 1622-1625.
37. Salez, L., Singer, M., Balloy, V., Creminon, C., Chignard, M. (2000) Lack of IL-10 synthesis by murine alveolar macrophages upon lipopolysaccharide exposure. Comparison with peritoneal macrophages. J. Leukoc. Biol. 67, 545-552.
38. Coward, W. R., Okayama, Y., Sagara, H., Wilson, S. J., Holgate, S. T., Church, M. K. (2002) NF-kappa B and TNF-alpha: a positive autocrine loop in human lung mast cells? J. Immunol. 169, 5287-5293.
39. Wallach, D., Varfolomeev, E. E., Malinin, N. L., Goltsev, Y. V., Kovalenko, A. V., Boldin, M. P. (1999) Tumor necrosis factor receptor and Fas signaling mechanisms. Annu. Rev. Immunol. 17, 331-367.
40. Ogle, C. K., Wu, J. Z., Mao, X., Szczur, K., Alexander, J. W., Ogle, J. D. (1994) Heterogeneity of Kupffer cells and splenic, alveolar, and peritoneal macrophages for the production of TNF, IL-1, and IL-6. Inflammation 18, 511-523.
41. Latz, E., Visintin, A., Lien, E., Fitzgerald, K. A., Espevik, T., Golenbock, D. T. (2003) The LPS receptor generates inflammatory signals from the cell surface. J. Endotoxin Res. 9, 375-380.
42. Kranenburg, O., Verlaan, I., Moolenaar, W. H. (1999) Dynamin is required for the activation of mitogen-activated protein (MAP) kinase by MAP kinase kinase. J. Biol. Chem. 274, 35301-35304.
43. Richardson, D. S., Lai, A. Z., Mulligan, L. M. (2006) RET ligand-induced internalization and its consequences for downstream signaling. Oncogene 25, 3206-3211.
44. Vieira, A. V., Lamaze, C., Schmid, S. L. (1996) Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274, 2086-2089.
45. Underhill, D. M., Gantner, B. (2004) Integration of Toll-like receptor and phagocytic signaling for tailored immunity. Microbes Infect. 6, 1368-1373.
46. Craig, A. W., Zirngibl, R., Williams, K., Cole, L. A., Greer, P. A. (2001) Mice devoid of fer protein-tyrosine kinase activity are viable and fertile but display reduced cortactin phosphorylation. Mol. Cell. Biol. 21, 603-613.
47. Kim, L., Wong, T. W. (1998) Growth factor-dependent phosphorylation of the actin-binding protein cortactin is mediated by the cytoplasmic tyrosine kinase FER. J. Biol. Chem. 273, 23542-23548.
48. Damiani, M. T., Colombo, M. I. (2003) Microfilaments and microtubules regulate recycling from phagosomes. Exp. Cell Res. 289, 152-161.
49. Murray, J. W., Wolkoff, A. W. (2003) Roles of the cytoskeleton and motor proteins in endocytic sorting. Adv. Drug Deliv. Rev. 55, 1385-1403.
50. Zirngibl, R., Schulze, D., Mirski, S. E., Cole, S. P., Greer, P. A. (2001) Subcellular localization analysis of the closely related Fps/Fes and Fer protein-tyrosine kinases suggests a distinct role for Fps/Fes in vesicular trafficking. Exp. Cell Res. 266, 87-94.