Macrophage pro-inflammatory response to Francisella novicida infection is regulated by SHIP

PLoS Pathogens

Volumn 2, Issue 7, 2006, Pages 0681-0690

  Parsa, Kishore V L ^a   Ganesan, Latha P ^a   Rajaram, Murugesan V S ^a   Gavrilin, Mikhail A ^a   Balagopal, Ashwin ^a   Mohapatra, Nrusingh P ^a   Wewers, Mark D ^a   Schlesinger, Larry S ^a   Gunn, John S ^a   Tridandapani, Susheela ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INOSITOL; INTERLEUKIN 10; INTERLEUKIN 12; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SH2; AUTACOID; CYTOKINE; INOSITOL 1,4,5 TRISPHOSPHATE 5 PHOSPHATASE; INOSITOL-1,4,5-TRISPHOSPHATE 5-PHOSPHATASE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVATION; FRANCISELLA; GENETIC TRANSCRIPTION; IMMUNITY; IMMUNOBLOTTING; INFLAMMATION; MACROPHAGE ACTIVATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHOSPHORYLATION; PROTEIN DOMAIN; TULAREMIA; ANIMAL; BIOSYNTHESIS; CELL CULTURE; GRAM NEGATIVE INFECTION; MACROPHAGE; METABOLISM; PATHOLOGY;

FRANCISELLA TULARENSIS; FRANCISELLA TULARENSIS SUBSP. NOVICIDA; MURINAE; NEGIBACTERIA;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELLS, CULTURED; CYTOKINES; DOWN-REGULATION; FRANCISELLA; GRAM-NEGATIVE BACTERIAL INFECTIONS; INFLAMMATION MEDIATORS; INTERLEUKIN-10; MACROPHAGES; MICE; NF-KAPPA B; PHOSPHORIC MONOESTER HYDROLASES; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 33746592575     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0020071     Document Type: Article

References (47)

1. Golovliov I, Baranov V, Krocova Z, Kovarova H, Sjostedt A (2003) An attenuated strain of the facultative intracellular bacterium Francisella tularensis can escape the phagosome of monocytic cells. Infect Immun 71: 5940-5950.
2. Clemens DL, Lee BY, Horwitz MA (2004) Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infect Immun 72: 3204-3217.
3. Santic M, Molmeret M, Klose KE, Jones S, Kwaik YA (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.
4. Nano FE, Zhang N, Cowley SC, Klose KE, Cheung KK, et al. (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186: 6430-6436.
5. Lindgren H, Golovliov I, Baranov V, Ernst RK, Telepnev M, et al. (2004) Factors affecting the escape of Francisella tularensis from the phagolysosome. J Med Microbiol 53: 953-958.
6. Santic M, Molmeret M, Abu KY (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-gamma. Cell Microbiol 7: 957-967.
7. Anthony LS, Ghadirian E, Nestel FP, Kongshavn PA (1989) The requirement for gamma interferon in resistance of mice to experimental tularemia. Microb Pathog 7: 421-428.
8. Golovliov I, Kuoppa K, Sjostedt A, Tarnvik A, Sandstrom G (1996) Cytokine expression in the liver of mice infected with a highly virulent strain of Francisella tularensis. FEMS Immunol Med Microbiol 13: 239-244.
9. Stenmark S, Sunnemark D, Bucht A, Sjostedt A (1999) Rapid local expression of interleukin-12, tumor necrosis factor alpha, and gamma interferon after cutaneous Francisella tularensis infection in tularemia-immune mice. Infect Immun 67: 1789-1797.
10. Lopez MC, Duckett NS, Baron SD, Metzger DW (2004) Early activation of NK cells after lung infection with the intracellular bacterium, Francisella tularensis LVS. Cell Immunol 232: 75-85.
11. Elkins KL, Cooper A, Colombini SM, Cowley SC, Kieffer TL (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.
12. Bolger CE, Forestal CA, Italo JK, Benach JL, Furie MB (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 Leukoc Biol 77: 893-897.
13. Telepnev M, Golovliov I, Sjostedt A (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.
14. Lioubin MN, Algate PA, Tsai S, Carlberg K, Aebersold R, et al. (1996) p150 SHIP, a signal transduction molecule with inositol polyphosphate-5- phosphatase activity. Genes Dev 10: 1084-1095.
15. Krystal G (2000) Lipid phosphatases in the immune system. Immunology 12: 397-403.
16. Fang H, Pengal RA, Cao X, Ganesan LP, Wewers MD, et al. (2004) Lipopolysaccharide-induced macrophage inflammatory response is regulated by SHIP. J Immunol 173: 360-366.
17. Liu L, Damen JE, Ware M, Hughes M, Krystal G (1997) SHIP, a new player in cytokine-induced signalling. Leukemia 11: 181-184.
18. Phee H, Jacob A, Coggeshall KM (2000) Regulation of SHIP enzymatic activity by membrane targeting. J Biol Chem 275: 19090-19097.
19. Tridandapani S, Kelley T, Pradhan M, Cooney D, Justement LB, et al. (1997) Recruitment and phosphorylation of SHIP and Shc to the B cell Fc gamma ITIM peptide motif. Mol Cell Biol 17: 4305-4311.
20. Tamir I, Stolpa JC, Helgason CD, Nakamura K, Bruhns P, et al. (2000) The RasGAP-binding protein p62dok is a mediator of inhibitory FcgammaRIIB signals in B cells. Immunology 12: 347-358.
21. Tridandapani S, Kelley T, Cooney D, Pradhan M, Coggeshall KM (1997) Negative signaling in B cells: SHIP Grbs Shc. Immunol Today 18: 424-427.
22. Tridandapani S, Chacko GW, Van Bruggen MCJ, Coggeshall KM (1997) Negative signaling in B cells causes reduced Ras activity by reducing Shc-Grb2 interactions. J Immunol 158: 1125-1132.
23. Tridandapani S, Phee H, Shivakumar L, Kelley T, Coggeshall KM (1998) Role of SHIP in Fcγ RIIb-mediated inhibition of Ras activation in B cells. Mol Immunol 35: 1135-1146.
24. Tridandapani S, Wang Y, Marsh CB, Anderson CL (2002) Src homology 2 domain-containing inositol polyphosphate phosphatase regulates NFkappa B-mediated gene transcription by phagocytic Fc gamma Rs in human myeloid cells. J Immunol 169: 4370-4378.
25. Nakamura K, Malykhin A, Coggeshall KM (2002) The Src homology 2 domain-containing inositol 5-phosphatase negatively regulates Fcgamma receptor-mediated phagocytosis through immunoreceptor tyrosine-based activation motif-bearing phagocytic receptors. Blood 100: 3374-3382.
26. Cox D, Dale BM, Kishiwada M, Helgason CD, Greenberg S (2001) A regulatory role for Src homology 2 domain-containing inositol 5′-phosphatase (SHIP) in phagocytosis mediated by Fc gamma receptors and complement receptor 3 (alpha(M)beta(2); CD11b/CD18. J Exp Med 193: 61-71.
27. Rauh MJ, Kalesnikoff J, Hughes M, Sly L, Lam V, et al. (2003) Role of Src homology 2-containing-inositol 5′-phosphatase (SHIP) in mast cells and macrophages. Biochem Soc Trans 31: 286-291.
28. An H, Xu H, Zhang M, Zhou J, Feng T, et al. (2005) Src homology 2 domain-containing inositol-5-phosphatase 1 (SHIP1) negatively regulates TLR4-mediated LPS response primarily through phosphatase activity- and PI-3K-independent mechanism. Blood 105: 4685-4692.
29. Rauh MJ, Ho V, Pereira C, Sham A, Sly LM, et al. (2005) SHIP represses the generation of alternatively activated macrophages. Immunity 23: 361-374.
30. Strassheim D, Kim JY, Park JS, Mitra S, Abraham E (2005) Involvement of SHIP in TLR2-induced neutrophil activation and acute lung injury. J Immunol 174: 8064-8071.
31. Elkins KL, Rhinehart-Jones T, Nacy CA, Winegar RK, Fortier AH (1993) T-cell-independent resistance to infection and generation of immunity to Francisella tularensis. Infect Immun 61: 823-829.
32. Elkins KL, Rhinehart-Jones TR, Culkin SJ, Yee D, Winegar RJ (1996) Minimal requirements for murine resistance to infection with Francisella tularensis LVS. Infect Immun 64: 3288-3293.
33. Drecktrah D, Knodler LA, Steele-Mortimer O (2004) Modulation and utilization of host cell phosphoinositides by Salmonella spp. Infect Immun 72: 4331-4335.
34. Brumell JH, Grinstein S (2003) Role of lipid-mediated signal transduction in bacterial internalization. Cell Microbiol 5: 287-297.
35. Clemens DL, Lee BY, Horwitz MA (2005) Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect Immun 73: 5892-5902.
36. Ancuta P, Pedron T, Girard R, Sandstrom G, Chaby R (1996) Inability of the Francisella tularensis lipopolysaccharide to mimic or to antagonize the induction of cell activation by endotoxins. Infect Immun 64: 2041-2046.
37. Chen W, KuoLee R, Shen H, Busa M, Conlan JW (2004) Toll-like receptor 4 (TLR4) does not confer a resistance advantage on mice against low-dose aerosol infection with virulent type A Francisella tularensis. Microb Pathog 37: 185-191.
38. Chen W, KuoLee R, Shen H, Busa M, Conlan JW (2005) Toll-like receptor 4 (TLR4) plays a relatively minor role in murine defense against primary intradermal infection with Francisella tularensis LVS. Immunol Lett 97: 151-154.
39. Gavrilin MA, Bouakl IJ, Knatz NL, Duncan MD, Hall MW, et al. (2005) Internalization and phagosome escape required for Francisella to induce human monocyte IL-1beta processing and release. Proc Natl Acad Sci U S A 103: 141-146.
40. Sly LM, Rauh MJ, Kalesnikoff J, Song CH, Krystal G (2004) LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity 21: 227-239.
41. Baran CP, Tridandapani S, Helgason CD, Humphries RK, Krystal G, et al. (2003) The inositol 5′-phosphatase SHIP-1 and the Src kinase Lyn negatively regulate macrophage colony-stimulating factor-induced Akt activity. J Biol Chem 278: 38628-38636.
42. Isnardi I, Lesourne R, Bruhns P, Fridman WH, Cambier JC, et al. (2004) Two distinct tyrosine-based motifs enable the inhibitory receptor Fcgamma RIIB to cooperatively recruit the inositol phosphatases SHIP1/2 and the sdapters Grb2/Grap. J Biol Chem 279: 51931-51938.
43. Trotta R, Parihar R, Yu J, Becknell B, Allard J, et al. (2005) Differential expression of SHIP1 in CD56bright and CD56dim NK cells provides a molecular basis for distinct functional responses to monokine costimulation. Blood 105: 3011-3018.
44. Parihar R, Trotta R, Roda JM, Ferketich AK, Tridandapani S, et al. (2005) Src homology 2-containing inositol 5′-phosphatase 1 negatively regulates IFN-gamma production by natural killer cells stimulated with antibody-coated tumor cells and interleukin-12. Cancer Res 65: 9099-9107.
45. Horwitz MA (1984) Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: Engulfment within a pseudopod coil. Cell 36: 27-33.
46. Ai J, Maturu A, Johnson W, Wang Y, Marsh CB, et al. (2005) The inositol phosphatase SHIP-2 downregulates FcgammaR-mediated phagocytosis in murine macrophages independently of SHIP-1. Blood 107: 813-820.
47. Ganesan LP, Wei G, Pengal RA, Moldovan L, Moldovan N, et al. (2004) The serine/threonine kinase Akt promotes Fc gamma receptor-mediated phagocytosis in murine macrophages through the activation of p70S6 kinase. J Biol Chem 279: 54416-54425.