Akt/protein kinase B modulates macrophage inflammatory response to Francisella infection and confers a survival advantage in mice

Journal of Immunology

Volumn 177, Issue 9, 2006, Pages 6317-6324

  Rajaram, Murugesan V S ^a   Ganesan, Latha P ^a   Parsa, Kishore V L ^b   Butchar, Jonathan P ^a   Gunn, John S ^b   Tridandapani, Susheela ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; PROTEIN KINASE B;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; FRANCISELLA; FRANCISELLA NOVICIDA; GRAM NEGATIVE BACTERIUM; GRAM NEGATIVE INFECTION; INFLAMMATION; MACROPHAGE; MONOCYTE; MOUSE; NEWBORN; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; SURVIVAL; TRANSGENIC MOUSE; WILD TYPE;

EID: 33750381299     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.9.6317     Document Type: Article

References (35)

1. Fortier, A. H., S. J. Green, T. Polsinelli, T. R. Jones, R. M. Crawford, D. A. Leiby, K. L. Elkins, M. S. Meltzer, and C. A. Nacy. 1994. Life and death of an intracellular pathogen: Francisella tularensis and the macrophage. Immunol. Ser. 60: 349-361.
2. Santic, M., M. Molmerel, K. E. Klose, S. Jones, and Y. A. Kwaik. 2005. The Francisella tularensis pathogenicity island protein IglC and its regulator MglA are essential for modulating phagosome biogenesis and subsequent bacterial escape into the cytoplasm. Cell. Microbiol. 7: 969-979.
3. Lauriano, C. M., J. R. Barker, F. E. Nano, B. P. Arulanandam, and K. E. Klose. 2003. Allelic exchange in Francisella tularensis using PCR products. FEMS Microbiol. Lett. 229: 195-202.
4. Lauriano. C. M., J. R. Barker, S. S. Yoon, F. E. Nano, B. P. Arulanandam, D. J. Hassett, and K. E. Klose. 2004. MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival. Proc. Natl. Acad. Sci. USA 101: 4246-4249.
5. Mariathasan, S., D. S. Weiss, V. M. Dixit, and D. M. Monack. 2005. Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J. Exp. Med. 202: 1043-1049.
6. Bolger, C. E., C. A. Forestal, J. K. Italo, J. L. Benach, and M. B. Furie. 2005. The live vaccine strain of Francisella tularensis replicates in human and murine macrophages but induces only the human cells to secrete proinflammatory cytokines. J. Leukocyte Biol. 77: 893-897.
7. Telepnev, M., I. Golovliov, and A. Sjostedt. 2005. Francisella tularensis LVS initially activates but subsequently down-regulates intracellular signaling and cytokine secretion in mouse monocytic and human peripheral blood mononuclear cells. Microb. Pathog. 38: 239-247.
8. Stenmark, S., D. Sunnemark, A. Bucht, and A. Sjostedt. 1999. Rapid local expression of interleukin-12, tumor necrosis factor α, and γ interferon after cutaneous Francisella tularensis infection in tularemia-immune mice. Infect. Immun. 67: 1789-1797.
9. Gavrilin, M. A., I. J. Bouakl, N. L. Knatz, M. D. Duncan, M. W. Hall, J. S. Gunn, and M. D. Wewers. 2005. Internalization and phagosome escape required for Francisella to induce human monocyte IL-1β processing and release. Proc. Natl. Acad. Sci. USA 103: 141-146.
10. Elkins, K. L., A. Cooper, S. M. Colombini, S. C. Cowley, and T. L. Kieffer. 2002. In vivo clearance of an intracellular bacterium, Francisella tularensis LVS, is dependent on the p40 subunit of interleukin-12 (IL-12) but not on IL-12 p70. Infect. Immun. 70: 1936-1948.
11. Duckett, N. S., S. Olmos, D. M. Durrant, and D. W. Metzger. 2005. Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain. Infect. Immun. 73: 2306-2311.
12. Santic, M., M. Molmeret, and K. Y. Abu. 2005. Modulation of biogenesis of the Francisella tularensis subsp. novicida-containing phagosome in quiescent human macrophages and its maturation into a phagolysosome upon activation by IFN-γ. Cell Microbiol. 7: 957-967.
13. Anthony, L. S., E. Ghadirian, F. P. Nestel, and P. A. Kongshavn. 1989. The requirement for γ interferon in resistance of mice to experimental tularemia. Microb. Pathog. 7: 421-428.
14. Golovliov, I., K. Kuoppa, A. Sjostedt, A. Tarnvik, and G. Sandstrom. 1996. Cytokine expression in the liver of mice infected with a highly virulent strain of Francisella tularensis. FEMS Immunol. Med. Microbiol. 13: 239-244.
15. Stokoe, D., L. R. Stephens, T. Copeland, P. R. J. Gaffney, C. B. Reese, G. F. Painter, A. B. Holmes, F. McCormick, and P. T. Hawkins. 1997. Dual role phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277: 567-570.
16. Bellacosa, A., T. O. Chan, N. N. Ahmed, K. Datta, S. Malstrom, D. Stokoe, F. McCormick, J. Feng, and P. Tsichlis. 1998. Akt activation by growth factors is a multiple-step process: the role of the PH domain. Oncogene 17: 313-325.
17. Toker, A., and L. C. Cantley. 1997. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387: 673-676.
18. Burgering, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599-602.
19. Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13: 2905-2927.
20. Brazil, D. P., J. Park, and B. A. Hemmings. 2002. PKB binding proteins: getting in on the Akt. Cell 111: 293-303.
21. Scheid, M. P., and J. R. Woodgett. 2001. PKB/AKT: functional insights from genetic models. Nat. Rev. Mol. Cell Biol. 2: 760-768.
22. Ozes, O. N., L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, and D. B. Donner. 1999. NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401: 82-85.
23. Romashkova, J. A., and S. S. Makarov. 1999. NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401: 86-90.
24. Guha, M., and N. Mackman. 2002. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277: 32124-32132.
25. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6: 777-784.
26. Pengal, R. A., L. P. Ganesan, G. Wei, H. Fang, M. C. Ostrowski, and S. Tridandapani. 2005. Lipopolysaccharide-induced production of interleukin-10 is promoted by the serine/threonine kinase Akt. Mol. Immunol. 43: 1557-1564.
27. Fang, H., R. A. Pengal, X. Cao, L. P. Ganesan, M. D. Wewers, C. B. Marsh, and S. Tridandapani. 2004. Lipopolysaccharide-induced macrophage inflammatory response is regulated by SHIP. J. Immunol. 173: 360-366.
28. Ganesan, L. P., G. Wei, R. A. Pengal, L. Moldovan, N. Moldovan, M. C. Ostrowski, and S. Tridandapani. 2004. The serine/threonine kinase Akt promotes Fey receptor-mediated phagocytosis in murine macrophages through the activation of p70S6 kinase. J. Biol. Chem. 279: 54416-54425.
29. Ganesan, L. P., H. Fang, C. B. Marsh, and S. Tridandapani. 2003. The protein-tyrosine phosphatase SHP-1 associates with the phosphorylated immunoreceptor tyrosine-based activation motif of FcγRIIa to modulate signaling events in myeloid cells. J. Biol. Chem. 278: 35710-35717.
30. Pengal, R. A., L. P. Ganesan, H. Fang, C. B. Marsh, C. L. Anderson, and S. Tridandapani. 2003. SHIP-2 inositol phosphatase is inducibly expressed in human monocytes and serves to regulate Fcγ receptor-mediated signaling. J. Biol. Chem. 278: 22657-22663.
31. Wewers, M. D., H. A. Dare, A. V. Winnard, J. M. Parker, and D. K. Miller. 1997. IL-1β-converting enzyme (ICE) is present and functional in human alveolar macrophages: macrophage IL-1β release limitation is ICE independent. J. Immunol. 159: 5964-5972.
32. Parsa, K. V., L. P. Ganesan, M. V. Rajaram, M. A. Gavrilin, A. Balagopal, N. P. Mohapatra, M. D. Wewers, L. S. Schlesinger, J. S. Gunn, and S. Tridandapani. 2006. Macrophage pro-inflammatory response to Francisella novicida infection is regulated by SHIP. PLoS Pathog. 2: e71.
33. Katz, J., P. Zhang M. Martin, S. N. Vogel, and S. M. Michalek. 2006. Toll-like receptor 2 is required for inflammatory responses to Francisella tularensis LVS. Infect. Immun. 74: 2809-2816.
34. Oppmann, B., R. Lesley, B. Blom, J. C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
35. Drecktrah, D., L. A. Knodler, and O. Steele-Mortimer. 2004. Modulation and utilization of host cell phosphoinositides by Salmonella spp. Infect. Immun. 72: 4331-4335.