Inhibition of Francisella tularensis LVS infection of macrophages results in a reduced inflammatory response: Evaluation of a therapeutic strategy for intracellular bacteria

FEMS Immunology and Medical Microbiology

Volumn 62, Issue 3, 2011, Pages 348-361

  D'Elia, Riccardo ^a   Jenner, Dominic C ^a   Laws, Thomas R ^a   Stokes, Margaret G M ^a   Jackson, Matthew C ^a   Essex Lopresti, Angela E ^a   Atkins, Helen S ^a  

^a DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

Author keywords

Francisella tularensis; Macrophages; Phagocytosis

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANTIINFECTIVE AGENT; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CELL SURFACE MARKER; CYTOCHALASIN B; FLUORESCEIN ISOTHIOCYANATE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; NOCODAZOLE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WORTMANNIN; XVA 143;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ANTIBODY LABELING; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOTOXICITY; DRUG EFFECT; FEMALE; FLOW CYTOMETRY; FRANCISELLA TULARENSIS; INFLAMMATION; LUNG HOMOGENATE; LUNG PARENCHYMA; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; ANTI-BACTERIAL AGENTS; CYTOKINES; FEMALE; FLOW CYTOMETRY; FRANCISELLA TULARENSIS; LUNG; MACROPHAGES; MICE; MICE, INBRED BALB C; PHAGOCYTOSIS; PNEUMONIA, BACTERIAL; STATISTICS, NONPARAMETRIC; TULAREMIA;

EID: 79960359852     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2011.00817.x     Document Type: Article

References (54)

1. Aderem A & Underhill DM (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17: 593-623.
2. Allen LAH & Aderem A (1996) Mechanisms of phagocytosis. Curr Opin Immunol 8: 36-40.
3. Anthony LSD, Ghadirian E, Nestel FP & Kongshavn PAL (1989) The requirement for gamma interferon in resistance of mice to experimental tularemia. Microb Pathogenesis 7: 421-428.
4. Anthony LSD, Burke RD & Nano FE (1991) Growth of Francisella spp. in rodent macrophages. Infect Immun 59: 3291-3296.
5. Balagopal A, MacFarlane AS, Mohapatra N, Soni S, Gunn JS & Schlesinger LS (2006) Characterization of the receptor-ligand pathways important for entry and survival of Francisella tularensis in human macrophages. Infect Immun 74: 5114-5125.
6. Bell JF, Owen CR & Larson CL (1955) Virulence of Bacterium tularense. 1. A study of the virulence of Bacterium tularense in mice, guinea pigs, and rabbits. J Infect Dis 97: 162-166.
7. Ben Nasr A, Haithcoat J, Masterson JE, Gunn JS, Eaves-Pyles T & Klimpel GR (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 Leukocyte Biol 80: 774-786.
8. 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 Leukocyte Biol 77: 893-897.
9. Buddingh GJ & Womack FC (1941) Observations on the infection of chick embryos with Bacterium tularense, Brucella, and Pasteurella pestis. J Exp Med 74: 213-222.
10. Clemens DL, Lee BY & Horwitz MA (2005) Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect Immun 73: 5892-5902.
11. Craven RR, Hall JD, Fuller JR, Taft-Benz S & Kawula TH (2008) Francisella tularensis invasion of lung epithelial cells. Infect Immun 76: 2833-2842.
12. Eigelsbach HT, Hornick RB & Tulis JJ (1967) Recent studies on live tularemia vaccine. Med Ann Dist Columbia 36: 282-286.
13. 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.
14. Ellis J, Oyston PCF, Green M & Titball RW (2002) Tularemia. Clin Microbiol Rev 15: 631-646.
15. Evans ME, Gregory DW, Schaffner W & Mcgee ZA (1985) Tularemia - a 30-year experience with 88 cases. Medicine 64: 251-269.
16. Ezekowitz RAB, Sastry K, Bailly P & Warner A (1990) Molecular characterization of the human macrophage mannose receptor - demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J Exp Med 172: 1785-1794.
17. Ferby IM, Waga I, Hoshino M, Kume K & Shimizu T (1996) Wortmannin inhibits mitogen-activated protein kinase activation by platelet-activating factor through a mechanism independent of p85/p110-type phosphatidylinositol 3-kinase. J Biol Chem 271: 11684-11688.
18. Fortier AH, Green SJ, Polsinelli T, Jones TR, Crawford RM, Leiby DA, Elkins KL, Meltzer MS & Nacy CA (1994) Life and death of an intracellular pathogen: Francisella tularensis and the macrophage. Immunol Ser 60: 349-361.
19. Goral J & Kovacs EJ (2004) In vivo ethanol exposure suppresses macrophage inflammatory responses mediated by toll-like receptors (TLR) 2, 4 and 9. Alcohol Clin Exp Res 28: 36A.
20. Haas A (2007) The phagosome: compartment with a license to kill. Traffic 8: 311-330.
21. Hajishengallis G, Shakhatreh MAK, Wang M & Liang S (2007) Complement receptor 3 blockade promotes IL-12-mediated clearance of Porphyromonas gingivalis and negates its virulence in vivo. J Immunol 179: 2359-2367.
22. Hall JD, Woolard MD, Gunn BM, Craven RR, Taft-Benz S, Frelinger JA & Kawula TH (2008) Infected-host-cell repertoire and cellular response in the lung following inhalation of Francisella tularensis Schu S4, LVS, or U112. Infect Immun 76: 5843-5852.
23. Hu L, McDaniel JP & Kopecko DJ (2006) Signal transduction events involved in human epithelial cell invasion by Campylobacter jejuni 81-176. Microb Pathogenesis 40: 91-100.
24. Hu LM, Zaloudek C, Mills GB, Gray J & Jaffe RB (2000) In vivo and in vitro ovarian carcinoma growth inhibition by a phosphatidylinositol 3-kinase inhibitor (LY294002). Clin Cancer Res 6: 880-886.
25. Johansson A, Farlow J, Larsson P et al. (2004) Worldwide genetic relationships among Francisella tularensis isolates determined by multiple-locus variable-number tandem repeat analysis. J Bacteriol 186: 5808-5818.
26. Letoha T, Somlai C, Takacs T et al. (2005) The proteasome inhibitor MG132 protects against acute pancreatitis. Free Radical Bio Med 39: 1142-1151.
27. Lieberman LA & Higgins DE (2009) A small-molecule screen identifies the antipsychotic drug pimozide as an inhibitor of Listeria monocytogenes infection. Antimicrob Agents Ch 53: 756-764.
28. Medina EA, Mossis IR & Berton MT (2010) Phosphatidylinositol 3-kinase activation attenuates the TLR2-mediated macrophage proinflammatory cytokine response to Francisella tularensis live vaccine strains. J Immunol 185: 7562-7572.
29. Meric M, Willke A, Finke EJ, Grunow R, Sayan M, Erdogan S & Gedikoglu S (2008) Evaluation of clinical, laboratory, and therapeutic features of 145 tularemia cases: the role of quinolones in oropharyngeal tularemia. APMIS 116: 66-73.
30. Olsufjev NG & Meshcheryakova IS (1982) Infraspecific taxonomy of tularemia agent Francisella tularensis McCoy et Chapin. J Hyg Epidemiol Microbiol Immunol 26: 291-299.
31. Oyston PCF (2008) Francisella tularensis: unravelling the secrets of an intracellular pathogen. J Med Microbiol 57: 921-930.
32. Oyston PCF (2009) Francisella tularensis vaccines. Vaccine 27 (suppl 4): D48-D51.
33. Perez-Castrillon JL, Bachiller-Luque P, Martin-Luquero M, Mena-Martin FJ & Herreros V (2001) Tularemia epidemic in northwestern Spain: clinical description and therapeutic response. Clin Infect Dis 33: 573-576.
34. Piercy T, Steward J, Lever MS & Brooks TJG (2005) In vivo efficacy of fluoroquinolones against systemic tularaemia infection in mice. J Antimicrob Chemoth 56: 1069-1073.
35. Pierini LM (2006) Uptake of serum-opsonized Francisella tularensis by macrophages can be mediated by class A scavenger receptors. Cell Microbiol 8: 1361-1370.
36. Rosenberg HF & Allen LA (2006) Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape. J Leukocyte Biol 80: 1222-1223.
37. Rosenshine I, Duronio V & Finlay BB (1992) Tyrosine protein-kinase inhibitors block invasion-promoted bacterial uptake by epithelial cells. Infect Immun 60: 2211-2217.
38. Russell P, Eley SM, Fulop MJ, Bell DL & Titball RW (1998) The efficacy of ciprofloxacin and doxycycline against experimental tularaemia. J Antimicrob Chemoth 41: 461-465.
39. Sajjan US, Yang JH, Hershenson MB & Lipuma JJ (2006) Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells. Cell Microbiol 8: 1456-1466.
40. Schulert GS & Allen LAH (2006) Differential infection of mononuclear phagocytes by Francisella tularensis: role of the macrophage mannose receptor. J Leukocyte Biol 80: 563-571.
41. Schulte R, Zumbihl R, Kampik D, Fauconnier A & Autenrieth IB (1998) Wortmannin blocks Yersinia invasin-triggered internalization, but not interleukin-8 production by epithelial cells. Med Microbiol Immun 187: 53-60.
42. Shepard CC (1959) Nonacid-fast bacteria and hela cells - their uptake and subsequent intracellular growth. J Bacteriol 77: 701-714.
43. Sjostedt A (2007) Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann N Y Acad Sci 1105: 1-29.
44. 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.
45. Steward J, Piercy I, Lever MS, Simpson AJH & Brooks TJG (2006) Treatment of murine pneumonic Francisella tularensis infection with gatifloxacin, moxifloxacin or ciprofloxacin. Int J Antimicrob Ag 27: 439-443.
46. Stuart LM & Ezekowitz RAB (2005) Phagocytosis: elegant complexity. Immunity 22: 539-550.
47. Svensson M & Wick MJ (1999) Classical MHC class I peptide presentation of a bacterial fusion protein by bone marrow-derived dendritic cells. Eur J Immunol 29: 180-188.
48. Tamilselvam B & Daefler S (2008) Francisella targets cholesterol-rich host cell membrane domains for entry into macrophages. J Immunol 180: 8262-8271.
49. Taylor ME, Conary JT, Lennartz MR, Stahl PD & Drickamer K (1990) Primary structure of the mannose receptor contains multiple motifs resembling carbohydrate-recognition domains. J Biol Chem 265: 12156-12162.
50. Teranishi F, Takahashi N, Gao N, Akamo Y, Takeyama H, Manabe T & Okamoto T (2009) Phosphoinositide 3-kinase inhibitor (wortmannin) inhibits pancreatic cancer cell motility and migration induced by hyaluronan in vitro and peritoneal metastasis in vivo. Cancer Sci 100: 770-777.
51. Tigertt WD (1962) Soviet viable Pasteurella tularensis vaccines - review of selected articles. Bacteriol Rev 26: 354-373.
52. Titball RW, Sjostedt A, Pavelka MS & Nano FE (2007) Biosafety and selectable markers. Ann N Y Acad Sci 1105: 405-417.
53. Valentin-Weigand P, Benkel P, Rohde M & Chhatwal GS (1996) Entry and intracellular survival of group B streptococci in J774 macrophages. Infect Immun 64: 2467-2473.
54. Wadsworth SJ & Goldfine H (1999) Listeria monocytogenes phospholipase C-dependent calcium signaling modulates bacterial entry into J774 macrophage-like cells. Infect Immun 67: 1770-1778.