MiR-155 induction by F. novicida but not the virulent F. tularensis results in SHIP down-regulation and enhanced pro-inflammatory cytokine response

PLoS ONE

Volumn 4, Issue 12, 2009, Pages

  Cremer, Thomas J ^a   Ravneberg, David H ^a   Clay, Corey D ^a   Piper Hunter, Melissa G ^a   Marsh, Clay B ^a   Elton, Terry S ^a   Gunn, John S ^a   Amer, Amal ^a   Kanneganti, Thirumala Devi ^b   Schlesinger, Larry S ^a   Butchar, Jonathan P ^a   Tridandapani, Susheela ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 6; MICRORNA; PHOSPHATASE; SH2 DOMAIN CONTAINING INOSITOL PHOSPHATASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AUTACOID; INOSITOL 1,4,5 TRISPHOSPHATE 5 PHOSPHATASE; INOSITOL-1,4,5-TRISPHOSPHATE 5-PHOSPHATASE; INTERLEUKIN 1BETA CONVERTING ENZYME; MIRN155 MICRORNA, HUMAN; MIRN155 MICRORNA, MOUSE; TOLL LIKE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; DOWN REGULATION; FRANCISELLA; FRANCISELLA NOVICIDA; FRANCISELLA TULARENSIS; GENE INDUCTION; GRAM NEGATIVE BACTERIUM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INTRACELLULAR BACTERIUM; MOUSE; NONHUMAN; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL LINE; CYTOLOGY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; GRAM NEGATIVE INFECTION; IMMUNOLOGY; METABOLISM; MICROBIAL VIABILITY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIRULENCE;

FRANCISELLA; FRANCISELLA TULARENSIS; NEGIBACTERIA;

ANIMALS; BASE SEQUENCE; CASPASE 1; CELL LINE; CYTOKINES; DOWN-REGULATION; ENDOCYTOSIS; ENZYME ACTIVATION; FRANCISELLA; FRANCISELLA TULARENSIS; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS; INFLAMMATION MEDIATORS; MICE; MICROBIAL VIABILITY; MICRORNAS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHOSPHORIC MONOESTER HYDROLASES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; VIRULENCE;

EID: 77949500446     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008508     Document Type: Article

References (53)

1. Lofgren S, Tarnvik A, Bloom GD, Sjoberg W (1983) Phagocytosis and Killing of Francisella-Tularensis by Human Polymorphonuclear Leukocytes. Infection and Immunity 39: 715-720.
2. Lai XH, Golovliov I, Sjostedt A (2001) Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infection and Immunity 69: 4691-4694.
3. Clemens DL, Horwitz MA (2007) Uptake and intracellular fate of Francisella tularensis in human macrophages. Francisella Tularensis: Biology, Pathogenicity, Epidemiology, and Biodefense. Ann N Y Acad Sci 1105: 160-186.
4. Oyston PCF, Sjostedt A, Titball RW (2004) Tularaemia: Bioterrorism defence renews interest in Francisella tularensis. Nature Reviews Microbiology 2: 967-978.
5. McLendon MK, Apicella MA, Allen LA (2006) Francisella tularensis: taxonomy, genetics, and Immunopathogenesis of a potential agent of biowarfare. Annu Rev Microbiol 60: 167-185.
6. Petersen JM, Schriefer ME (2005) Tularemia: emergence/re-emergence. Vet Res 36: 455-467.
7. Ellis J, Oyston PC, Green M, Titball RW (2002) Tularemia. Clin Microbiol Rev 15: 631-646.
8. Parsa KVL, Butchar JP, Rajaram MVS, Cremer TJ, Gunn JS, et al. (2008) Francisella gains a survival advantage within mononuclear phagocytes by suppressing the host IFN gamma response. Molecular Immunology 45: 3428-3437.
9. Telepnev M, Golovliov I, Grundstrom T, Tarnvik A, Sjostedt A (2003) Francisella tularensis inhibits Toll-like receptor-mediated activation of intracellular signalling and secretion of TNF-alpha and IL-1 from murine macrophages. Cellular Microbiology 5: 41-51.
10. Hajjar AM, Harvey MD, Shaffer SA, Goodlett DR, Sjostedt A, et al. (2006) Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infection and Immunity 74: 6730-6738.
11. 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.
12. Bosio CM, Bielefeldt-Ohmann H, Belisle JT (2007) Active suppression of the pulmonary immune response by Francisella tularensis Schu4. Journal of Immunology 178: 4538-4547.
13. Gunn JS, Ernst RK (2007) The structure and function of Francisella lipopolysaccharide. Francisella Tularensis: Biology, Pathogenicity, Epidemiology, and Biodefense 1105: 202-218.
14. Katz J, Zhang P, Martin M, Vogel SN, Michalek SM (2006) Toll-like receptor 2 is required for inflammatory responses to Francisella tularensis LVS. Infect Immun 74: 2809-2816.
15. Malik M, Bakshi CS, Sahay B, Shah A, Lotz SA, et al. (2006) Toll-like receptor 2 is required for control of pulmonary infection with Francisella tularensis. Infection and Immunity 74: 3657-3662.
16. Lembo A, Pelletier M, Iyer R, Timko M, Dudda JC, et al. (2008) Administration of a synthetic TLR4 agonist protects mice from pneumonic tularemia. Journal of Immunology 180: 7574-7581.
17. Parsa KVL, Ganesan LP, Rajaram MVS, Gavrilin MA, Balagopal A, et al. (2006) Macrophage pro-inflammatory response to Francisella novicida infection is regulated by SHIP. PLoS Pathogens 2: 681-690.
18. Rajaram MVS, Ganesan LP, Parsa KVL, Butchar JP, Gunn JS, et al. (2006) Akt/protein kinase B modulates macrophage inflammatory response to Francisella infection and confers a survival advantage in mice. Journal of Immunology 177: 6317-6324.
19. Rajaram MV, Butchar JP, Parsa KV, Cremer TJ, Amer A, et al. (2009) Akt and SHIP Modulate Francisella Escape from the Phagosome and Induction of the Fas-Mediated Death Pathway. PLoS ONE 4: e7919.
20. Santic M, Al Khodor S, Abu KY (2009) Cell biology and molecular ecology of Francisella tularensis. Cell Microbiol In Press.
21. O'Connell RM, Chaudhuri AA, Rao DS, Baltimore D (2009) Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci U S A 106: 7113-7118.
22. Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301: 336-338.
23. Taganov KD, Boldin MP, Chang KJ, Baltimore D (2006) NF-kappaBdependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 103: 12481-12486.
24. O'Connell RM, Taganov KD, Boldin MP, Cheng GH, Baltimore D (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci U S A 104: 1604-1609.
25. Eis PS, Tam W, Sun L, Chadburn A, Li Z, et al. (2005) Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci U S A 102: 3627-3632.
26. Martin MM, Lee EJ, Buckenberger JA, Schmittgen TD, Elton TS (2006) MicroRNA-155 regulates human angiotensin II type 1 receptor expression in fibroblasts. Journal of Biological Chemistry 281: 18277-18284.
27. Yin QY, Wang X, McBride J, Fewell C, Flemington E (2008) B-cell receptor activation induces BIC/miR-155 expression through a conserved AP-1 element. Journal of Biological Chemistry 283: 2654-2662.
28. Covert MW, Leung TH, Gaston JE, Baltimore D (2005) Achieving stability of lipopolysaccharide-induced NF-kappaB activation. Science 309: 1854-1857.
29. Vallabhapurapu S, Karin M (2009) Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 27: 693-733.
30. Gatto G, Rossi A, Rossi D, Kroening S, Bonatti S, et al. (2008) Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-kappa B pathway. Nucleic Acids Research 36: 6608-6619.
31. 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 45: 3012-3021.
32. 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. Cellular Microbiology 7: 969-979.
33. Gavrilin MA, Bouakl IJ, Knatz NL, Duncan MD, Hall MW, et al. (2006) 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: 141-146.
34. Henry T, Brotcke A, Weiss DS, Thompson LJ, Monack DM (2007) Type I interferon signaling is required for activation of the inflammasome during Francisella infection. Journal of Experimental Medicine 204: 987-994.
35. Aman MJ, Lamkin TD, Okada H, Kurosaki T, Ravichandran KS (1998) The inositol phosphatase SHIP inhibits Akt/PKB activation in B cells. Journal of Biological Chemistry 273: 33922-33928.
36. Costinean S, Zanesi N, Pekarsky Y, Tili E, Volinia S, et al. (2006) Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proc Natl Acad Sci U S A 103: 7024-7029.
37. Martin MM, Buckenberger JA, Jiang J, Malana GE, Nuovo GJ, et al. (2007) The human angiotensin II type 1 receptor+1166 A/C polymorphism attenuates MicroRNA-155 binding. Journal of Biological Chemistry 282: 24262-24269.
38. Teng G, Papavasiliou FN (2009) Shhh! Silencing by microRNA-155. Philosophical Transactions of the Royal Society B-Biological Sciences 364: 631-637.
39. Clurman BE, Hayward WS (1989) Multiple Proto-Oncogene Activations in Avian-Leukosis Virus-Induced Lymphomas Evidence for Stage-Specific Events. Molecular and Cellular Biology 9: 2657-2664.
40. Tam W, BenYehuda D, Hayward WS (1997) bic, a novel gene activated by proviral insertions in avian leukosis virus-induced lymphomas, is likely to function through its noncoding RNA. Molecular and Cellular Biology 17: 1490-1502.
41. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros WH, et al. (2007) A viral microRNA functions as an orthologue of cellular miR-155. Nature 450: 1096-1099.
42. Zhao YG, Yao YX, Xu HT, Lambeth L, Smith LP, et al. (2008) A Functional MicroRNA-155 Ortholog Encoded by the Oncogenic Marek's Disease Virus. Journal of Virology 83: 489-492.
43. Lu F, Weidmer A, Liu CG, Volinia S, Croce CM, et al. (2008) Epstein-Barr Virus-Induced miR-155 Attenuates NF-kappa B Signaling and Stabilizes Latent Virus Persistence. Journal of Virology 82: 10436-10443.
44. Vigorito E, Perks KL, Abreu-Goodger C, Bunting S, Xiang Z, et al. (2007) microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27: 847-859.
45. Thai TH, Calado DP, Casola S, Ansel KM, Xiao CC, et al. (2007) Regulation of the germinal center response by microRNA-155. Science 316: 604-608.
46. Mehta P, Butchar JP, Tridandapani S (2009) Targeting the SH2 Domain Containing Inositol Phosphatase (SHIP) for Therapy. Curr Enzyme Inhib In Press.
47. Ben Nasr A, Haithcoat J, Masterson JE, Gunn JS, Eaves-Pyles T, et al. (2006) Critical role for serum opsonins and complement receptors CR3 (CD11b/CD18) and CR4 (CD11c/CD18) in phagocytosis of Francisella tularensis by human dendritic cells (DC): uptake of Francisella leads to activation of immature DC and intracellular survival of the bacteria. J Leukoc Biol 80: 774-786.
48. Schulert GS, Allen LA (2006) Differential infection of mononuclear phagocytes by Francisella tularensis: role of the macrophage mannose receptor. J Leukoc Biol 80: 563-571.
49. Clay CD, Soni S, Gunn JS, Schlesinger LS (2008) Evasion of complement mediated lysis and complement C3 deposition are regulated by Francisella tularensis lipopolysaccharide O antigen. Journal of Immunology 181: 5568-5578.
50. Chase JC, Bosio CM (2009) Presence of CD14 overcomes evasion of innate immune responses by virulent Francisella tularensis in human dendritic cells in vitro and pulmonary cells in vivo. Infection and Immunity In Press.
51. Strassheim D, Kim JY, Park JS, Mitra S, Abraham E (2005) Involvement of SHIP in TLR2-induced neutrophil activation and acute lung injury. Journal of Immunology 174: 8064-8071.
52. O'Connell RM, Rao DS, Chaudhuri AA, Boldin MP, Taganov KD, et al. (2008) Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. Journal of Experimental Medicine 205: 585-594.
53. Helgason CD, Damen JE, Rosten PM, Grewal R, Sorensen P, et al. (1998) Targeted disruption of ship leads to hemopoietic perturbations, lung pathology, and a shortened lifespan. Experimental Hematology 26: 815.