Modulation of Nod2-dependent NF-κB signaling by the actin cytoskeleton

Journal of Cell Science

Volumn 120, Issue 7, 2007, Pages 1299-1310

  Legrand Poels, Sylvie ^a   Kustermans, Gaelle ^a   Bex, Françoise ^b   Kremmer, Elisabeth ^c   Kufer, Thomas A ^d   Piette, Jacques ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b FREE UNIVERSITY OF BRUSSELS   (Belgium)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d INSTITUT PASTEUR   (France)

Author keywords

Actin cystoskeleton; NF B; Nod2; Rac1

Indexed keywords

ACTIN; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CYTOCHALASIN D; F ACTIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RAC1 PROTEIN; TRITON X 100;

ANIMAL CELL; ARTICLE; BACTERIAL INFECTION; CELL MOTION; CELL STRAIN HEK293; CELL STRAIN HT29; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; GENE TRANSLOCATION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOPRECIPITATION; INTESTINE EPITHELIUM CELL; LAMELLIPODIUM; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; CELL CULTURE TECHNIQUES; CELL EXTRACTS; CELL LINE; CELLS, CULTURED; CYTOSKELETON; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; GENES, REPORTER; HT29 CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LUCIFERASES; MACROPHAGES; MICE; MICROSCOPY, FLUORESCENCE; NF-KAPPA B; NOD2 SIGNALING ADAPTOR PROTEIN; SIGNAL TRANSDUCTION; TRANSFECTION;

BACTERIA (MICROORGANISMS);

EID: 34248226821     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03424     Document Type: Article

References (51)

1. Barnich, N., Aguirre, J. E., Reinecker, H. C., Xavier, R. and Podolsky, D. K. (2005a). Membrane recruitment of NOD2 in intestinal epithelial cells is essential for nuclear factor-{kappa}B activation in muramyl dipeptide recognition. J. Cell Biol. 170, 21-26.
2. Barnich, N., Hisamatsu, T., Aguirre, J. E., Xavier, R., Reinecker, H. C. and Podolsky, D. K. (2005b). GRIM-19 interacts with nucleotide oligomerization domain 2 and serves as downstream effector of anti-bacterial function in intestinal epithelial cells. J. Biol. Chem. 280, 19021-19026.
3. Berrebi, D., Maudinas, R., Hugot, J.-P., Chamaillard, M., Chareyre, F., De Lagausie, P., Yang, C., Desreumaux, P., Giovannini, M., Cézard, J.-P. et al. (2003). Card15 gene overexpression in mononuclear and epithelial cells of the inflamed Crohn's disease colon. Gut 52, 840-846.
4. Borg, J.-P., Marchetto, S., Le Bivic, A., Ollendorff, V., Jaulin-Bastard, F., Saito, H., Fournier, E., Adélaïde, J., Margolis, B. and Birnbaum D. (2000). ERBIN: a basolateral PDZ protein that interacts with the mammalian ERBB2/HER2 receptor. Nat. Cell Biol. 2, 407-414.
5. Bretscher, A., Edwards, K. and Fehon, R. G. (2002). ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3, 586-599.
6. Chen, C. M., Gong, Y., Zhang, M. and Chen, J. J. (2004). Reciprocal cross-talk between Nod2 and TAK1 signaling pathways. J. Biol. Chem. 279, 25876-25882.
7. Christerson, L. B., Vanderbilt, C. A. and Cobb, M. H. (1999). MEKK1 interacts with alpha-actinin and localizes to stress fibers and focal adhesions. Cell Motil. Cytoskeleton 43, 186-198.
8. Clark, K. A., McElbinny, A. S., Beckerle, M. C. and Gregorio, C. C. (2002). Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18, 637-706.
9. Coue, M., Brenner, S. L., Spector, I. and Korn, E. D. (1987). Inhibition of actin polymerization by latrunculin A. FEBS Lett. 213, 316-318.
10. Desmedt, M., Rottiers, P., Dooms, H., Fiers, W. and Grooten, J. (1998). Macrophages induce cellular immunity by activating Th1 cell responses and suppressing Th2 cell responses. J. Inununol. 160, 5300-5308.
11. Dustin, M. L. and Cooper, J. A. (2000). The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat. Immunol. 1, 23-29.
12. Foxwell, B., Browne, K., Bondeson, J., Clarke, C., de Martin, R., Brennan, F. and Feldmann, M. (1998). Efficient adenoviral infection with IkappaB alpha reveals that macrophage tumor necrosis factor alpha production in rheumatoid arthritis is NF-kappaB dependent. Proc. Natl. Acad Sci. USA 95, 8211-8215.
13. Friedland, J. S., Constantin, D., Shaw, T. C. and Stylianou, E. (2001). Regulation of interleukin-8 gene expression after phagocytosis of zymosan by human monocytic cells. J. Leukoc. Biol. 70, 447-454.
14. Ghosh, S. and Karin, M. (2002). Missing pieces in the NF-kappaB puzzle. Cell 109, S81-S96.
15. Ghosh, S., May, M. J. and Kopp, E. B. (1998). NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16, 225-260.
16. Girardin, S. G., Boneca, I. G., Viala, J., Chamaillard, M., Labigne, A., Thomas, G., Philpott, D. and Sansonetti, P. J. (2003). Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol, Chem. 278, 8869-8872.
17. Grilli, M. and Memo, M. (1999). Nuclear factor-kappaB/Rel proteins: a point of convergence of signalling pathways relevant in neuronal function and dysfunction. Biochem. Pharmacol. 57, 1-7.
18. Gutierrez, O., Pipaon, C., Inohara, N., Fontalba, A., Ogura, Y., Prosper, F., Nuñez, G. and Fernandez,-Luna, J. L. (2002). Induction of Nod2 in myelomonocytic and intestinal epithelial cells via nuclear factor-kappa B activation. J. Biol. Chem. 277, 41701-41705.
19. Holsinger, L. J., Graef, I. A., Swat, W., Chi, T., Bautista, D. M., Davidson, L., Lewis, R. S., Alt, F. W. and Crabtree, G. R. (1998). Defects in actin-cap formation in Vav-deficient mice implicate an actin requirement for lymphocyte signal transduction. Curr. Biol. 8, 563-572.
20. Huang, Y. Z., Zang, M., Xiong, W. C., Luo, Z. and Mel, L. (2003). Erbin suppresses the MAP kinase pathway. J. Biol. Chem. 278, 1108-1114.
21. Hugot, J.-P., Chamaillard, M., Zouali, H., Lesage, S., Cézard, J.-P, Belaiche, J., Almer, S., Tysk, C., O'Morain, C. A., Gassull, M. et al. (2001). Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411, 599-603.
22. Inohara, N., Koseki, T., Lin, J., del Peso, L., Lucas, P. C., Chen, F. F., Ogura, Y. and Nùñez, G. (2000). An induced proximity model for NF-kappa B activation in the Nod1/RICK and REP signaling pathways. J. Biol. Chem. 275, 27823-27831.
23. Inohara, N., Ogura, Y., Fontalba, A., Gutierrez, O., Pons, R, Crespo, J., Fukase, K., Inamura, S., Kusumoto, S., Hashimoto, M. et al. (2003). Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 278, 5509-5512.
24. Inohara, N., Chamaillard, M., McDonald, C. and Nunez, G. (2005). NOD-LRR Proteins: role in host-microbial interactions and inflammatory disease. Annu. Rev. Biochem. 74, 355-383.
25. Izawa, I., Nishizawa, M., Tomono, Y., Ohtakara, K., Takahashi, T. and Inagaki, M. (2002). ERBIN associates with p0071, an armadillo protein, at cell-cell junctions of epithelial cells. Genes Cells 7, 475-485.
26. Karin, M. and Ben-Neriah, Y. (2000). Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18, 621-663.
27. Kufer, T. A., Kremmer, E., Banks, D. J. and Philpott, D. J. (2006). Role for erbin in bacterial activation of Nod2. Infect. Immun. 74, 3115-3124.
28. Kustermans, G., El Benna, J., Piette, J. and Legrand-Poels, S. (2005). Perturbation of actin dynamics induces NF-κB activation in myelomonocytic cells through an NADPH oxidase-dependent pathway. Biochem. J. 387, 531-540.
29. Lamsoul, I., Lodewick, J., Lebrun, S., Brasseur, R., Burny, A., Gaynor, R. B. and Bex, F. (2005). Exclusive ubiquitination and sumoylation on overlapping lysine residues mediate NF-κB activation by the human T-cell leukemia virus tax oncoprotein. Mol. Cell. Biol. 25, 10391-10406.
30. Li, J., Moran, T., Swanson, E., Julian, C., Harris, J., Bonen, D. K., Hedl, M., Nicolae, D. L., Abraham, C. and Cho, J. H. (2004). Regulation of IL-8 and IL-lbeta expression in Crohn's disease associated NOD2/CARD15 mutations. Hum. Mol. Genet. 13, 1715-1725.
31. Luque, I. and Gelinas, C. (1997). Rel/NF-kappa B and I kappa B factors in oncogenesis. Semin. Cancer Biol. 8, 103-111.
32. Mack, C. F., Somlyo, A. V., Hautmann, M., Somlyo, A. P. and Owens, G. K. (2001). Smooth muscle differentiation marker gene expression is regulated by RboA-mediated actin polymerization. J. Biol. Chem. 276, 341-347.
33. Maeda, S., Hsu, L. C., Liu, H. J., Bankston, L. A., Iimura, M., Kagnoff, M. F., Eckmann, L. and Karin, M. (2005). Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science 307, 734-738.
34. Massol, P., Montcourrier, P., Guillemot, J. C. and Chavrier, P. (1998). Fc receptor-mediated phagocytosis requires CDC42 and Rac1. EMBO J. 17, 6219-6229.
35. McDonald, C., Chen, F. F., Ollendorff, V., Ogura, Y., Marchetto, S., Lécine, P., Borg, J.-P. and Nuñez, G. (2005). A role for Erbin in the regulation of Nod2-dependent NF-kappaB signaling. J. Biol. Chem. 280, 40301-40309.
36. Nanninga, N. (2001). Cytokinesis in prokaryotes and eukaryotes: common principles and different solutions. Microbiol. Mol. Biol. Rev. 65, 319-333.
37. Németh, Z. H., Deitch, E. A., Davidson, M. T., Szabo, C., Vizi, E. S. and Hasko, G. (2004). Disruption of the actin cytoskelelon results in nuclear factor-kappaB activation and inflammatory mediator production in cultured human intestinal epithelial cells. J Cell. Physiol. 200, 71-81.
38. Netea, M. G, Ferwerda, G., de Jong, D. J., Jansen, T., Jacobs, L., Kramer, M., Naber, T. H. J., Drenth, J. P. H., Girardin, S. E., Kullberg, B. J. et al. (2005). Nucleotide-binding oligomerization domain-2 modulates specific TLR pathways for the induction of cytokine release. J. Immunol. 174, 6518-6523.
39. Ogura, Y., Inohara, N., Benito, A., Chen, F. E, Yamaoka, S. and Nùñez, G. (2001a). Nod2, a Nodl/Apaf-1 family member that is restricted to monocytes and activates NF-kappaB. J. Biol. Chem. 276, 4812-4818.
40. Ogura, Y., Bonen, D. K., Inohara, N., Nicolae, D. L., Chen, F. F., Ramos, R., Britton, H., Moran, T., Karaliuskas, R., Duerr, R. H. et al. (2001b). A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411, 603-606.
41. Perons, R., Montaner, S., Saniger, L., Sanchez-Perez, I., Bravo, R. and Lacal, J. C. (1997). Activation of the nuclear factor-kappaB by Rho, CDC42, and Rac-1 proteins. Genes Dev. 11, 463-475.
42. Pizarro-Cerda, J. and Cossart, P. (2006). Bacterial adhesion and entry into host cells. Cell 124, 715-727.
43. Ridley, A. L, Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
44. Rudolph, M. G., Bayer, P., Abo, A., Kuhlmann, J., Vetter, I. R. and Wittinghofer, A. (1998). The Cdc42/Rac interactive binding region motif of the Wiskott Aldrich syndrome protein (WASP) is necessary but not sufficient for tight binding to Cdc42 and structure formation. J. Biol. Chem. 273, 18067-18076.
45. Sampath, F. and Pollard, T. D. (1991). Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 30, 1973-1980.
46. Shi, J., Scita, G. and Casanova, J. E. (2005). WAVE2 signaling mediates invasion of polarized epithelial cells by Salmonella typhimurium. J. Biol. Chem. 280, 29849-29855.
47. Shtil, A. A., Mandlekar, S., Yu, R., Walter, R. J., Hagen, K., Tan, T.-H., Roninson, I. B. and Tony Kong, A.-N. (1999). Differential regulation of mitogen-activated protein kinases by microtubule-binding agents in human breast cancer cells. Oncogene 18, 377-384.
48. Sotiropoulos, A., Gineitis, D., Copeland, J. and Treisman, R. (1999). Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98, 159-169.
49. Stradal, T., Rottner, K., Disanza, A., Confalonieri, S., Innocenti, M. and Scita, G. (2004). Regulation of actin dynamics by WASP and WAVE family proteins. Trends Cell Biol. 14, 303-311.
50. van Heel, D. A., Ghosh, S., Butler, M., Hunt, K. A., Lundberg, A. M. C., Ahmad, T., McGovern, D. F. B., Onnie, C., Negoro, K., Goldthorpe, S. et al. (2005). Muramyl dipeptide and toll-like receptor sensitivity in NOD2-associated Crohn's disease. Lancet 365, 1794-1796.
51. Wittmann, T. and Waterman-Storer, C. (2001). Cell motility: can Rho GTPases and microtubules point the way? J. Cell. Sci. 114, 3795-3803.