Akt and SHIP modulate Francisella escape from the phagosome and induction of the Fas-mediated death pathway

PLoS ONE

Volumn 4, Issue 11, 2009, Pages

  Rajaram, Murugesan V S ^a   Butchar, Jonathan P ^a   Parsa, Kishore V L ^a   Cremer, Thomas J ^a   Amer, Amal ^a   Schlesinger, Larry S ^a   Tridandapani, Susheela ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; MEMBRANE PROTEIN; PROTEIN KINASE B; PROTEIN SHIP; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3; UNCLASSIFIED DRUG; INOSITOL 1,4,5 TRISPHOSPHATE 5 PHOSPHATASE; INOSITOL-1,4,5-TRISPHOSPHATE 5-PHOSPHATASE; PHOSPHATASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOSOL; FRANCISELLA TULARENSIS; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION REGULATION; GENE INDUCTION; HOST CELL; IMMUNOPRECIPITATION; LYSOSOME; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHAGOSOME; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL LINE; CYTOLOGY; FRANCISELLA; MACROPHAGE; METABOLISM;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS; PHAGO;

ANIMALS; ANTIGENS, CD95; BONE MARROW CELLS; CELL DEATH; CELL LINE; CYTOSOL; FRANCISELLA; LYSOSOMES; MACROPHAGES; MICE; MICE, INBRED C57BL; PHAGOCYTOSIS; PHAGOSOMES; PHOSPHORIC MONOESTER HYDROLASES; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 70949108107     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007919     Document Type: Article

References (51)

1. Fortier AH, Green SJ, Polsinelli T, Jones TR, Crawford RM, et al. (1994) Life and death of an intracellular pathogen: Francisella tularensis and the macrophage. Immunol Ser 60: 349-61.:349-361.
2. McLendon MK, Apicella MA, Allen LA (2006) Francisella tularensis: Taxonomy, Genetics, and Immunopathogenesis of a Potential Agent of Biowarfare. Annu Rev Microbiol 60: 167-85.
3. Kieffer TL, Cowley S, Nano FE, Elkins KL (2003) Francisella novicida LPS has greater immunobiological activity in mice than F. tularensis LPS, and contributes to F. novicida murine pathogenesis. Microbes Infect 5: 397-403.
4. 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.
5. Santic M, Molmeret M, Klose KE, Abu KY (2006) Francisella tularensis travels a novel, twisted road within macrophages. Trends Microbiol 14: 37-44.
6. Clemens DL, Horwitz MA (2007) Uptake and intracellular fate of Francisella tularensis in human macrophages. Ann N Y Acad Sci 1105: 160-86. Epub;%2007 Apr 13.:160-186.
7. Checroun C, Wehrly TD, Fischer ER, Hayes SF, Celli J (2006) Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc Natl Acad Sci U S A 103: 14578-14583.
8. Chong A, Wehrly TD, Nair V, Fischer ER, Barker JR, et al. (2008) The early phagosomal stage of Francisella tularensis determines optimal phagosomal escape and Francisella pathogenicity island protein expression. Infect Immun 76: 5488-5499.
9. Lauriano CM, Barker JR, Yoon SS, Nano FE, Arulanandam BP, et al. (2004) MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival. Proc Natl Acad Sci U S A 101: 4246-4249.
10. 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.
11. Lai XH, Golovliov I, Sjostedt A (2004) Expression of IglC is necessary for intracellular growth and induction of apoptosis in murine macrophages by Francisella tularensis. Microb Pathog 37: 225-230.
12. Lai XH, Sjostedt A (2003) Delineation of the molecular mechanisms of Francisella tularensis-induced apoptosis in murine macrophages. Infect Immun 71: 4642-4646.
13. Lai XH, Golovliov I, Sjostedt A (2001) Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infect Immun 69: 4691-4694.
14. Mariathasan S, Weiss DS, Dixit VM, Monack DM (2005) Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J Exp Med 202: 1043-1049.
15. 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.
16. 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-1{beta} processing and release. Proc Natl Acad Sci U S A 103(1): 141-6.
17. Parsa KV, Ganesan LP, Rajaram MV, Gavrilin MA, Balagopal A, et al. (2006) Macrophage Pro-Inflammatory Response to Francisella novicida Infection Is Regulated by SHIP. PLoS Pathog 2: e71.
18. 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.
19. Butchar JP, Rajaram MVS, Ganesan LP, Parsa KVL, Clay CD, et al. (2007) Francisella tularensis induces IL-23 production in human monocytes. Journal of Immunology 178: 4445-4454.
20. 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.
21. 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.
22. Rajaram MV, Ganesan LP, Parsa KV, Butchar JP, Gunn JS, et al. (2006) Akt/ PKB modulates macrophage inflammatory response to Francisella infection and confers a survival advantage in mice. J Immunol 177(9): 6317-24.
23. 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(52): 54416-25.
24. 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.
25. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
26. Ganesan LP, Fang H, Marsh CB, Tridandapani S (2003) The protein-tyrosine phosphatase SHP-1 associates with the phosphorylated immunoreceptor tyrosine-based activation motif of Fc gamma RIIa to modulate signaling events in myeloid cells. J Biol Chem 278: 35710-35717.
27. 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.
28. Swanson MS, Isberg RR (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63: 3609-3620.
29. McLean IW, Nakane PK (1974) Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem 22: 1077-1083.
30. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, et al. (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14: 5579-5588.
31. Krammer PH (2000) CD95's deadly mission in the immune system. Nature 407: 789-795.
32. Parsa KV, Butchar JP, Rajaram MV, Cremer TJ, Tridandapani S (2008) The tyrosine kinase Syk promotes phagocytosis of Francisella through the activation of Erk. Mol Immunol Epub ahead of print.
33. Pang H, Miranda K, Fine A (1998) Sp3 regulates fas expression in lung epithelial cells. Biochem J 333: 209-213.
34. Suske G (1999) The Sp-family of transcription factors. Gene 238: 291-300.
35. Chanteux H, Guisset AC, Pilette C, Sibille Y (2007) LPS induces IL-10 production by human alveolar macrophages via MAPKinases- and Sp1-dependent mechanisms. Respir Res 8: 71.:71.
36. Baran J, Weglarczyk K, Mysiak M, Guzik K, Ernst M, et al. (2001) Fas (CD95)-Fas ligand interactions are responsible for monocyte apoptosis occurring as a result of phagocytosis and killing of Staphylococcus aureus. Infect Immun 69: 1287-1297.
37. Rudi J, Kuck D, Strand S, von Herbay A, Mariani SM, et al. (1998) Involvement of the CD95 (APO-1/Fas) receptor and ligand system in Helicobacter pylori-induced gastric epithelial apoptosis. J Clin Invest 102: 1506-1514.
38. Wang J, Fan X, Lindholm C, Bennett M, O'Connoll J, et al. (2000) Helicobacter pylori modulates lymphoepithelial cell interactions leading to epithelial cell damage through Fas/Fas ligand interactions. Infect Immun 68: 4303-4311.
39. Debatin KM, Fahrig-Faissner A, Enenkel-Stoodt S, Kreuz W, Benner A, et al. (1994) High expression of APO-1 (CD95) on T lymphocytes from human immunodeficiency virus-1-infected children. Blood 83: 3101-3103.
40. Baumler CB, Bohler T, Herr I, Benner A, Krammer PH, et al. (1996) Activation of the CD95 (APO-1/Fas) system in T cells from human immunodeficiency virus type-1-infected children. Blood 88: 1741-1746.
41. Katsikis PD, Wunderlich ES, Smith CA, Herzenberg LA, Herzenberg LA (1995) Fas antigen stimulation induces marked apoptosis of T lymphocytes in human immunodeficiency virus-infected individuals. J Exp Med 181: 2029-2036.
42. Wickstrum JR, Bokhari SM, Fischer JL, Pinson DM, Yeh HW, et al. (2009) Francisella tularensis Induces Extensive Caspase-3 Activation and Apoptotic Cell Death in the Tissues of Infected Mice. Infect Immun.
43. Scott CC, Cuellar-Mata P, Matsuo T, Davidson HW, Grinstein S (2002) Role of 3-phosphoinositides in the maturation of Salmonella-containing vacuoles within host cells. J Biol Chem 277: 12770-12776.
44. Vieira OV, Botelho RJ, Rameh L, Brachmann SM, Matsuo T, et al. (2001) Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J Cell Biol 155: 19-25.
45. Rupper AC, Rodriguez-Paris JM, Grove BD, Cardelli JA (2001) p110-related PI 3-kinases regulate phagosome-phagosome fusion and phagosomal pH through a PKB/Akt dependent pathway in Dictyostelium. J Cell Sci 114: 1283-1295.
46. Barbieri MA, Kohn AD, Roth RA, Stahl PD (1998) Protein kinase B/akt and rab5 mediate Ras activation of endocytosis. J Biol Chem 273: 19367-19370.
47. Gutierrez MG, Mishra BB, Jordao L, Elliott E, Anes E, Griffiths G (2008) NF-kappa B activation controls phagolysosome fusion-mediated killing of mycobacteria by macrophages. J Immunol 181: 2651-2663.
48. Hoyal CR, Gutierrez A, Young BM, Catz SD, Lin JH, et al. (2003) Modulation of p47PHOX activity by site-specific phosphorylation: Akt-dependent activation of the NADPH oxidase. Proc Natl Acad Sci U S A 100: 5130-5135.
49. Chen Q, Powell DW, Rane MJ, Singh S, Butt W, et al. Akt phosphorylates p47phox and mediates respiratory burst activity in human neutrophils. J Immunol 170: 5302-5308.
50. Drecktrah D, Knodler LA, Steele-Mortimer O (2004) Modulation and utilization of host cell phosphoinositides by Salmonella spp. Infect Immun 72: 4331-4335.
51. Butchar JP, Cremer TJ, Clay CD, Gavrilin MA, Wewers MD, et al. (2008) Microarray analysis of human monocytes infected with Francisella tularensis identifies new targets of host response subversion. PLoS One 3: e2924.