Lipopolysaccharide from Salmonella enterica activates NF-κB through both classical and alternative pathways in primary B lymphocytes

Infection and Immunity

Volumn 75, Issue 10, 2007, Pages 4998-5003

  Souvannavong, Vongthip ^a,b,c   Saidji, Nabila ^b   Chaby, Richard ^a,b  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; HETERODIMER; I KAPPA B; I KAPPA B ALPHA; I KAPPA B BETA; I KAPPA B KINASE EPSILON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ISOENZYME; NUCLEAR PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P100; PROTEIN P105; PROTEIN P50; PROTEIN P52; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELL VIABILITY; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT CLASSICAL PATHWAY; CONTROLLED STUDY; CYTOSOL; FEMALE; GENE ACTIVATION; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PROCESSING; PROTEIN TRANSPORT; REGULATORY MECHANISM; SALMONELLA ENTERICA;

ANIMALS; B-LYMPHOCYTES; CELL NUCLEUS; CELLS, CULTURED; CYTOSOL; DIMERIZATION; FEMALE; I-KAPPA B KINASE; I-KAPPA B PROTEINS; IMMUNOBLOTTING; LIPOPOLYSACCHARIDES; MICE; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; NF-KAPPA B P52 SUBUNIT; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS; SALMONELLA ENTERICA; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

EID: 34848915116     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00545-07     Document Type: Article

References (52)

1. Aggarwal, B. B. 2000. Apoptosis and nuclear factor-kappa B: a tale of association and dissociation. Biochem. Pharmacol. 60:1033-1039.
2. Andersson, J., G. Moller, and O. Sjoberg. 1972. Selective induction of DNA synthesis in T and B lymphocytes. Cell. Immunol. 4:381-393.
3. Baixeras, E., L. Bosca, C. Stauber, A. Gonzalez, A. C. Carrera, J. A. Gonzalo, and C. Martinez. 1994. From apoptosis to autoimmunity: insights from the signaling pathways leading to proliferation or to programmed cell death. Immunol. Rev. 142:53-91.
4. Baldwin, A. S., Jr. 1996. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649-683.
5. Bendall, H. H., D. C. Scherer, C. R. Edson, D. W. Ballard, and E. M. Oltz. 1997. Transcription factor NF-kappaB regulates inducible Oct-2 gene expression in precursor B lymphocytes. J. Biol. Chem. 272:28826-28828.
6. Bonizzi, G., and M. Karin. 2004. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25:280-288.
7. Caamaño, J., and C. A. Hunter. 2002. NF-κB family of transcription factors: central regulators of innate and adaptive immune functions. Clin. Microbiol. Rev. 15:414-429.
8. L. Mol. Cell. Biol. 20:2687-2695.
9. Cohen, J. J. 1999. Apoptosis: mechanisms of life and death in the immune system. J. Allergy Clin. Immunol. 103:548-554.
10. Dejardin, E. 2006. The alternative NF-kappaB pathway from biochemistry to biology: pitfalls and promises for future drug development. Biochem. Pharmacol. 72:1161-1179.
11. Doerre, S., K. P. Mesires, K. M. Daley, T. McCarty, S. Knoetig, and R. B. Corley. 2005. Reductions in I kappa B epsilon and changes in NF-kappa B activity during B lymphocyte differentiation. J. Immunol. 174:983-991.
12. Enzler, T., G. Bonizzi, G. J. Silverman, D. C. Otero, G. F. Widhopf, A. Anzelon-Mills, R. C. Rickert, and M. Karin. 2006. Alternative and classical NF-kappa B signaling retain autoreactive B cells in the splenic marginal zone and result in lupus-like disease. Immunity 25:403-415.
13. Ganju, N., and A. Eastman. 2002. Bcl-X-L and calyculin A prevent translocation of Bax to mitochondria during apoptosis. Biochem. Biophys. Res. Commun. 291:1258-1264.
14. Gerondakis, S., and A. Strasser. 2003. The role of Rel/NF-kappaB transcription factors in B lymphocyte survival. Semin. Immunol. 15:159-166.
15. Girard, R., T. Pedron, S. Uematsu, V. Balloy, M. Chignard, S. Akira, and R. Chaby. 2003. Lipopolysaccharides from Legionella and Rhizobium stimulate mouse bone marrow granulocytes via Toll-like receptor 2. J. Cell Sci. 116: 293-302.
16. Grech, A. P., M. Amesbury, T. Chan, S. Gardam, A. Basten, and R. Brink. 2004. TRAF2 differentially regulates the canonical and noncanonical pathways of NF-kappaB activation in mature B cells. Immunity 21:629-642.
17. Gugasyan, R., R. Grumont, M. Grossmann, Y. Nakamura, T. Pohl, D. Nesic, and S. Gerondakis. 2000. Rel/NF-kappaB transcription factors: key mediators of B-cell activation. Immunol. Rev. 176:134-140.
18. Hatada, E. N., R. K. Do, A. Orlofsky, H. C. Liou, M. Prystowsky, I. C. MacLennan, J. Caamano, and S. Chen-Kiang. 2003. NF-kappa B1 p50 is required for BLyS attenuation of apoptosis but dispensable for processing of NF-kappa B2 p100 to p52 in quiescent mature B cells. J. Immunol. 171:761-768.
19. Hoffmann, A., and D. Baltimore. 2006. Circuitry of nuclear factor kappaB signaling. Immunol. Rev. 210:171-186.
20. Hoffmann, A., A. Levchenko, M. L. Scott, and D. Baltimore. 2002. The IkappaB-NF-kappaB signaling module: temporal control and selective gene activation. Science 298:1241-1245.
21. Israel, A. 2000. The IKK complex: an integrator of all signals that activate NF-kappaB? Trends Cell Biol. 10:129-133.
22. Karin, M. 1999. How NF-kappaB is activated: the role of the IkappaB kinase (IKK) complex. Oncogene 18:6867-6874.
23. Krammer, P. H., I. Behrmann, P. Daniel, J. Dhein, and K. M. Debatin. 1994. Regulation of apoptosis in the immune system. Curr. Opin. Immunol. 6:279-289.
24. Krappmann, D., E. Wegener, Y. Sunami, M. Esen, A. Thiel, B. Mordmuller, and C. Scheidereit. 2004. The IκB kinase complex and NF-κB act as master regulators of lipopolysaccharide-induced gene expression and control subordinate activation of AP-1. Mol. Cell. Biol. 24:6488-6500.
25. Lemaire, C., K. Andréau, C. Sidoti-deFraisse, A. Adam, and V. Souvannavong. 1999. IL-4 inhibits apoptosis and prevents mitochondrial damage without inducing the switch to necrosis observed with caspase inhibitors. Cell Death Differ. 6:813-820.
26. Li, Z. W., S. A. Omori, T. Labuda, M. Karin, and R. C. Rickert. 2003. IKK beta is required for peripheral B cell survival and proliferation. J. Immunol. 170:4630-4637.
27. Medzhitov, R., and C. A. Janeway, Jr. 1997. Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9:4-9.
28. Melchers, F., V. Braun, and C. Galanos. 1975. The lipoprotein of the outer membrane of Escherichia coli: a B-lymphocyte mitogen. J. Exp. Med. 142: 473-482.
29. Miyamoto, S., B. J. Seufzer, and S. D. Shumway. 1998. Novel IκBα proteolytic pathway in WEHI231 immature B cells. Mol. Cell. Biol. 18:19-29.
30. Mordmuller, B., D. Krappmann, M. Esen, E. Wegener, and C. Scheidereit. 2003. Lymphotoxin and lipopolysaccharide induce NF-kappaB-p52 generation by a co-translational mechanism. EMBO Rep. 4:82-87.
31. Norvell, A., L. Mandik, and J. G. Monroe. 1995. Engagement of the antigen-receptor on immature murine B lymphocytes results in death by apoptosis. J. Immunol. 154:4404-4413.
32. Ohmae, T., Y. Hirata, S. Maeda, W. Shibata, A. Yanai, K. Ogura, H. Yoshida, T. Kawabe, and M. Omata. 2005. Helicobacter pylori activates NF-kappaB via the alternative pathway in B lymphocytes. J. Immunol. 175:7162-7169.
33. Pasare, C., and R. Medzhitov. 2005. Control of B-cell responses by Toll-like receptors. Nature 438:364-368.
34. Perkins, N. D. 2007. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat. Rev. Mol. Cell. Biol. 8:49-62.
35. Perkins, N. D. 2006. Post-translational modifications regulating the activity and function of the nuclear factor-kappa B pathway. Oncogene 25:6717-6730.
36. Perkins, N. D., and T. D. Gilmore. 2006. Good cop, bad cop: the different faces of NF-kappaB. Cell Death Differ. 13:759-772.
37. Phillips, R. J., and S. Ghosh. 1997. Regulation of IκBβ in WEHI 231 mature B cells. Mol. Cell. Biol. 17:4390-4396.
38. Pomerantz, J. L., and D. Baltimore. 2002. Two pathways to NF-kappaB. Mol. Cell 10:693-695.
39. Sen, R. 2006. Control of B lymphocyte apoptosis by the transcription factor NF-kappaB. Immunity 25:871-883.
40. Sen, R., and D. Baltimore. 1986. Inducibility of kappa immunoglobulin enhancer-binding protein NF-kappa B by a posttranslational mechanism. Cell 47:921-928.
41. Senftleben, U., Y. Cao, G. Xiao, F. R. Greten, G. Krahn, G. Bonizzi, Y. Chen, Y. Hu, A. Fong, S. C. Sun, and M. Karin. 2001. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 293:1495-1499.
42. Siebenlist, U., K. Brown, and E. Claudio. 2005. Control of lymphocyte development by nuclear factor-kappaB. Nat. Rev. Immunol. 5:435-445.
43. Solan, N. J., H. Miyoshi, E. M. Carmona, G. D. Bren, and C. V. Paya. 2002. RelB cellular regulation and transcriptional activity are regulated by p100. J. Biol. Chem. 277:1405-1418.
44. Souvannavong, V., K. Andreau, A. Adam, and R. Chaby. 1999. Effect of synthetic lipids on apoptosis and expression of alkaline phosphatase in B-lymphocytes: influence on lipopolysaccharide action. FEMS Immunol. Med. Microbiol. 26:37-47.
45. Souvannavong, V., C. Lemaire, and R. Chaby. 2004. Lipopolysaccharide protects primary B lymphocytes from apoptosis by preventing mitochondrial dysfunction and Bax translocation to mitochondria. Infect. Immun. 72:3260-3266.
46. Tapping, R. I., S. Akashi, K. Miyake, P. J. Godowski, and P. S. Tobias. 2000. Toll-like receptor 4, but not toll-like receptor 2, is a signaling receptor for Escherichia and Salmonella lipopolysaccharides. J. Immunol. 165:5780-5787.
47. Ulevitch, R. J., and P. S. Tobias. 1999. Recognition of gram-negative bacteria and endotoxin by the innate immune system. Curr. Opin. Immunol. 11:19-22.
48. Wechsler-Reya, R. J., and J. G. Monroe. 1996. Lipopolysaccharide prevents apoptosis and induces responsiveness to antigen receptor cross-linking in immature B cells. Immunology 89:356-362.
49. Weil, R., and A. Israel. 2004. T-cell-receptor- and B-cell-receptor-mediated activation of NF-kappaB in lymphocytes. Curr. Opin. Immunol. 16:374-381.
50. Werner, S. L., D. Barken, and A. Hoffmann. 2005. Stimulus specificity of gene expression programs determined by temporal control of IKK activity. Science 309:1857-1861.
51. Xiao, G., E. W. Harhaj, and S. C. Sun. 2001. NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol. Cell 7:401-409.
52. Zarnegar, B., J. Q. He, G. Oganesyan, A. Hoffmann, D. Baltimore, and G. H. Cheng. 2004. Unique CD40-mediated biological program in B cell activation requires both type 1 and type 2 NF-kappa B activation pathways. Proc. Natl. Acad. Sci. USA 101:8108-8113.