Subversion and utilization of the host cell cyclic adenosine 5′-monophosphate/protein kinase A pathway by Brucella during macrophage infection

Journal of Immunology

Volumn 170, Issue 11, 2003, Pages 5607-5614

  Gross, Antoine ^a   Bouaboula, Monsif ^b   Casellas, Pierre ^b   Liautard, Jean Pierre ^a   Dornand, Jacques ^a  

^a UNIV MONTPELLIER   (France)

^b SANOFI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; G PROTEIN COUPLED RECEPTOR;

ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BRUCELLA; BRUCELLOSIS; DOMESTIC ANIMAL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNITY; MACROPHAGE; MACROPHAGE FUNCTION; MICROBIAL ACTIVITY; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 0038528218     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.11.5607     Document Type: Article

References (53)

1. Kuhn, M., and W. Goebel. 1998. Host cell signalling during Listeria monocytogenes infection. Trends Microbiol. 6:11.
2. Nakao, H., and T. Takeda. 2000. Escherichia coli Shiga toxin. J. Nat. Toxins 9:299.
3. Amer, A. O., and M. S. Swanson. 2002. A phagosome of one's own: a microbial guide to life in the macrophage. Curr. Opin. Microbiol. 5:56.
4. Navarre, W. W., and A. Zychlinsky. 2000. Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell. Microbiol. 2:265.
5. Cheng, L. W., and O. Schneewind. 2000. Type III machines of Gram-negative bacteria: delivering the goods. Trends Microbiol. 8:214.
6. Zhou, D., and J. Galan. 2001. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microb. Infect. 3:1293.
7. Guzman-Verri, C., E. Chaves-Olarte, C. von Eichel-Streiber, I. Lopez-Goni, M. Thelestam, S. Arvidson, J. P. Gorvel, and E. Moreno. 2001. GTPases of the Rho subfamily are required for Brucella abortus internalization in nonprofessional phagocytes: direct activation of Cdc42. J. Biol. Chem. 276:44435.
8. Rittig, M. G., M. T. Alvarez-Martinez, F. Porte, J. P. Liautard, and B. Rouot. 2001. Intracellular survival of Brucella spp. in human monocytes involves conventional uptake but special phagosomes. Infect. Immun. 69:3995.
9. Kusumawati, A., C. Cazevieille, F. Porte, S. Bettache, J. P. Liautard, and J. Sri Widada. 2000. Early events and implication of F-actin and annexin I associated structures in the phagocytic uptake of Brucella suis by the J-774A.1 murine cell line and human monocytes. Microb. Pathog. 28:343.
10. Arenas, G. N., A. S. Staskevich, A. Aballay, and L. S. Mayorga. 2000. Intracellular trafficking of Brucella abortus in J774 macrophages. Infect. Immun. 68:4255.
11. Baldwin, C. L., and A. J. Winter. 1994. Macrophages and Brucella. Immunol. Ser. 60:363.
12. Porte, F., J. P. Liautard, and S. Kohler. 1999. Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect. Immun. 67:4041.
13. Naroeni, A., N. Jouy, S. Ouahrani-Bettache, J. P. Liautard, and F. Porte. 2001. Brucella suis-impaired specific recognition of phagosomes by lysosomes due to phagosomal membrane modifications. Infect. Immun. 69:486.
14. -/- macrophages is responsible for a high susceptibility to intracellular bacterial infection. J. Immunol. 162:3519.
15. Caron, E., A. Gross, J. P. Liautard, and J. Dornand. 1996. Brucella species release a specific, protease-sensitive, inhibitor of TNF-α expression, active on human macrophage-like cells. J. Immunol. 156:2885.
16. Gross, A., A. Terraza, S. Ouahrani-Bettache, J. P. Liautard, and J. Dornand. 2000. In vitro Brucella suis infection prevents the programmed cell death of human monocytic cells. Infect. Immun. 68:342.
17. Boschiroli, M. L., S. Ouahrani-Bettache, V. Foulongne, S. Michaux-Charachon, G. Bourg, A. Allardet-Servent, C. Cazevieille, J. P. Liautard, M. Ramuz, and D. O'Callaghan. 2002. The Brucella suis virB operon is induced intracellularly in macrophages. Proc. Natl. Acad. Sci. USA 99:1544.
18. O'Callaghan, D., C. Cazevieille, A. Allardet-Servent, M. L. Boschiroli, G. Bourg, V. Foulongne, P. Frutos, Y. Kulakov, and M. Ramuz. 1999. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33:1210.
19. Comerci, D. J., M. J. Martinez-Lorenzo, R. Sieira, J. P. Gorvel, and R. A. Ugalde. 2001. Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell. Microbiol. 3:159.
20. Hong, P. C., R. M. Tsolis, and T. A. Ficht. 2000. Identification of genes required for chronic persistence of Brucella abortus in mice. Infect. Immun. 68:4102.
21. Gross, A., A. Terraza, J. Marchant, M. Bouaboula, S. Ouahrani-Bettache, J. P. Liautard, P. Casellas, and J. Dornand. 2000. A beneficial aspect of a CB1 cannabinoid receptor antagonist: SR141716A is a potent inhibitor of macrophage infection by the intracellular pathogen Brucella suis. J. Leukocyte Biol. 67:335.
22. Howlett, A. C., F. Barth, T. I., Bonner, G. Cabral, P. Casellas, W. A. Devane, C. C. Felder, M. Herkenham, K. Mackie, B. R. Martin, et al. 2002. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol. Rev. 54:161.
23. Ouahrani-Bettache, S., F. Porte, J. Teyssier, J. P. Liautard, and S. Kohler. 1999. pBBR1-GFP: a broad-host-range vector for prokaryotic promoter studies. BioTechniques 26:620.
24. Gross, A., S. Spiesser, A. Terraza, B. Rouot, E. Caron, and J. Dornand. 1998. Expression and bactericidal activity of nitric oxide synthase in Brucella suisinfected murine macrophages. Infect. Immun. 66:1309.
25. Shaywitz, A. J., and M. E. Greenberg. 1999. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68:821.
26. Gupta, D., Q. Wang, C. Vinson, and R. Dziarski. 1999. Bacterial peptidoglycan induces CD14-dependent activation of transcription factors CREB/ATF and AP-1. J. Biol. Chem. 274:14012.
27. Bhat, N. R., D. L. Feinstein, Q. Shen, and A. N. Bhat. 2002. p38 MAPK-mediated transcriptional activation of inducible nitric-oxide synthase in glial cells: roles of nuclear factors, nuclear factors κB, cAMP response element-binding protein, CCAAT/enhancer binding protein-β, and activating transcription factor-2. J. Biol. Chem. 277:29584.
28. Naroeni, A., and F. Porte. 2002. Role of cholesterol and the ganglioside GM(I) in entry and short-term survival of Brucella suis in murine macrophages. Infect. Immun. 70:1640.
29. Watarai, M., S. Makino, Y. Fujii, K. Okamoto, and T. Shirahata. 2002. Modulation of Brucella-induced macropinocytosis by lipid rafts mediates intracellular replication. Cell. Microbiol. 4:341.
30. Shin, J. S., and S. N. Abraham. 2001. Caveolae as portals of entry for microbes. Microb. Infect. 3:755.
31. Triantafilou, M., K. Miyake, D. T. Golenbock, and K. Triantafilou. 2002. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 115:2603.
32. Schwencke, C., M. Yamamoto, S. Okumura, Y. Toya, S. J. Kim, and Y. Ishikawa. 1999. Compartmentation of cyclic adenosine 3′,5′-monophosphate signaling in caveolae. Mol. Endocrinol. 13:1061.
33. Campbell, G. A., L. G. Adams, and B. A. Sowa. 1994. Mechanisms of binding of Brucella abortus to mononuclear phagocytes from cows naturally resistant or susceptible to brucellosis. Vet. Immunol. Immunopathol. 41:295.
34. Novak, K. F., B. Dougherty, and M. Pelaez. 2001. Actinobacillus actinomycetem comitans harbors type IV secretion system genes on a plasmid and in the chromosome. Microbiology 147:3027.
35. Locht, C. 1999. Molecular aspects of Bordetella pertussis pathogenesis. Int. Microbiol. 2:137.
36. Canning, P. C., J. A. Roth, and B. L. Deyoe. 1986. Release of 5′-guanosine monophosphate and adenine by Brucella abortus and their role in the intracellular survival of the bacteria. J. Infect. Dis. 154:464.
37. Goldstein, J., T. Hoffman, C. Frasch, E. F. Lizzio, P. R. Beining, D. Hochstein, Y. L. Lee, R. D. Angus, and B. Golding. 1992. Lipopolysaccharide (LPS) from Brucella abortus is less toxic than that from Escherichia coli, suggesting the possible use of B. abortus or LPS from B. abortus as a carrier in vaccines. Infect. Immun. 60:1385.
38. MacKenzie, S. J., and M. D. Houslay. 2000. Action of rolipram on specific PDE4 cAMP phosphodiesterase isoforms and on the phosphorylation of cAMP-response-element-binding protein (CREB) and p38 mitogen-activated protein (MAP) kinase in U937 monocytic cells. Biochem. J. 347:571.
39. 2 production in murine peritoneal macrophages infected with Ehrlichia risticii. Infect. Immun. 61:4333.
40. Lee, E. H., and Y. Rikihisa. 1998. Protein kinase A-mediated inhibition of γ interferon-induced tyrosine phosphorylation of Janus kinases and latent cytoplasmic transcription factors in human monocytes by Ehrlichia chaffeensis. Infect. Immun. 66:2514.
41. Porte, F., A. Naroeni, S. Ouahrani-Bettache, and J. P. Liautard. 2003. Role of the Brucella suis LPS O-antigen in phagosomal genesis and in inhibition of phagolysosomal fusion in murine macrophages. Infect. Immun. 71:1481.
42. Caron, E., J. P. Liautard, and S. Kohler. 1994. Differentiated U937 cells exhibit increased bactericidal activity upon LPS activation and discriminate between virulent and avirulent Listeria and Brucella species. J. Leukocyte Biol. 56:174.
43. Ko, J., A. Gendron-Fitzpatrick, and G. A. Splitter. 2002. Susceptibility of IFN regulatory factor-1 and IFN consensus sequence binding protein-deficient mice to brucellosis. J. Immunol. 168:2433.
44. Fischer, T., R. Zumbihl, J. Armand, P. Casellas, and B. Rouot. 1995. Prolonged elevation of intracellular cyclic AMP levels in U937 cells increases the number of receptors for and the responses to formylmethionyl-leucylphenylalanine, independently of the differentiation process. Biochem. J. 311:995.
45. Beshay, E., F. Croze, and G. J. Prud'homme. 2001. The phosphodiesterase inhibitors pentoxifylline and rolipram suppress macrophage activation and nitric oxide production in vitro and in vivo. Clin. Immunol. 98:272.
46. Muller Igaz, L., D. Refojo, M. A. Costas, F. Holsboer, and E. Arzt. 2002. CRE-mediated transcriptional activation is involved in cAMP protection of T-cell receptor-induced apoptosis but not in cAMP potentiation of glucocorticoid-mediated programmed cell death. Biochim. Biophys. Acta Mol. Cell Res. 1542:139.
47. Von Knethen, A., and B. Brune. 2000. Attenuation of macrophage apoptosis by the cAMP-signaling system. Mol. Cell. Biochem. 212:35.
48. Kambayashi, T., R. P. Wallin, and H. G. Ljunggren. 2001. cAMP-elevating agents suppress dendritic cell function. J. Leukocyte Biol. 70:903.
49. Jubier-Maurin, V., R. A. Boigegrain, A. Cloeckaert, A. Gross, M. T. Alvarez-Martinez, A. Terraza, J. Liautard, S. Kohler, B. Rouot, J. Dornand, and J. P. Liautard. 2001. Major outer membrane protein Omp25 of Brucella suis is involved in inhibition of tumor necrosis factor α production during infection of human macrophages. Infect. Immun. 69:4823.
50. Ting, L. M., A. C. Kim, A. Cattamanchi, and J. D. Ernst. 1999. Mycobacterium tuberculosis inhibits IFN-γ transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163:3898.
51. Kammer, G. M. 1988. The adenylate cyclase-cAMP-protein kinase A pathway and regulation of the immune response. Immunol. Today 9:222.
52. Burzyn, D., C. C. Jancic, S. Zittermann, M. I. Keller Sarmiento, L. Fainboim, R. E. Rosenstein, and H. E. Chuluyan. 2002. Decrease in cAMP levels modulates adhesion to fibronectin and immunostimulatory ability of human dendritic cells. J. Leukocyte Biol. 72:93.
53. 2. J. Exp. Med. 180:2365.