Non-FcεR bearing mast cells secrete sufficient interleukin-4 to control Francisella tularensis replication within macrophages

Cytokine

Volumn 55, Issue 2, 2011, Pages 211-220

  Thathiah, Prea ^a   Sanapala, Shilpa ^a   Rodriguez, Annette R ^a   Yu, Jieh Juen ^a   Murthy, Ashlesh K ^a   Guentzel, M Neal ^a   Forsthuber, Thomas G ^a   Chambers, James P ^a   Arulanandam, Bernard P ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

Francisella tularensis; IL 4; Innate immunity; Mast cells; Respiratory infection

Indexed keywords

INTERLEUKIN 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL REPRODUCTION; CELL ACTIVATION; CELL INFILTRATION; CELL SECRETION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FRANCISELLA TULARENSIS; IMMUNOREGULATION; IN VITRO STUDY; MACROPHAGE; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SUPERNATANT;

ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; COCULTURE TECHNIQUES; FRANCISELLA TULARENSIS; INTERLEUKIN-4; MACROPHAGES; MAST CELLS; MICE; MICE, INBRED C57BL; RECEPTORS, IGE; TULAREMIA; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS;

EID: 79959555307     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2011.04.009     Document Type: Article

References (52)

1. Metcalfe D.D., Baram D., Mekori Y.A. Mast cells. Physiol Rev 1997, 77:1033-1079.
2. Wasserman S.I. Mast cell-mediated inflammation in asthma. Ann Allergy 1989, 63:546-550.
3. Echtenacher B., Mannel D.N., Hultner L. Critical protective role of mast cells in a model of acute septic peritonitis. Nature 1996, 381:75-77.
4. Galli S.J. New concepts about the mast cell. N Engl J Med 1993, 328:257-265.
5. Stevens R.L., Austen K.F. Recent advances in the cellular and molecular biology of mast cells. Immunol Today 1989, 10:381-386.
6. Malaviya R., Gao Z., Thankavel K., van der Merwe P.A., Abraham S.N. The mast cell tumor necrosis factor alpha response to FimH-expressing Escherichia coli is mediated by the glycosylphosphatidylinositol-anchored molecule CD48. Proc Natl Acad Sci U S A 1999, 96:8110-8115.
7. Malaviya R., Ikeda T., Ross E., Abraham S.N. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature 1996, 381:77-80.
8. Cowley S.C., Hamilton E., Frelinger J.A., Su J., Forman J., Elkins K.L. CD4-CD8 T cells control intracellular bacterial infections both in vitro and in vivo. J Exp Med 2005, 202:309-319.
9. Saslaw S., Eigelsbach H.T., Prior J.A., Wilson H.E., Carhart S. Tularemia vaccine study. II. Respiratory challenge. Arch Intern Med 1961, 107:702-714.
10. Sjostedt A. Virulence determinants and protective antigens of Francisella tularensis. Curr Opin Microbiol 2003, 6:66-71.
11. Elkins K.L., Cowley S.C., Bosio C.M. Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect 2003, 5:135-142.
12. Ketavarapu J.M., Rodriguez A.R., Yu J.J., Cong Y., Murthy A.K., Forsthuber T.G., et al. Mast cells inhibit intramacrophage Francisella tularensis replication via contact and secreted products including IL-4. Proc Natl Acad Sci U S A 2008, 105:9313-9318.
13. Klinker J.F., Laugwitz K.L., Hageluken A., Seifert R. Activation of GTP formation and high-affinity GTP hydrolysis by mastoparan in various cell membranes. G-protein activation via nucleoside diphosphate kinase, a possible general mechanism of mastoparan action. Biochem Pharmacol 1996, 51:217-223.
14. Kowluru A., Seavey S.E., Rabaglia M.E., Metz S.A. Non-specific stimulatory effects of mastoparan on pancreatic islet nucleoside diphosphokinase activity: dissociation from insulin secretion. Biochem Pharmacol 1995, 49:263-266.
15. Schindler R., Day M., Fischer G.A. Culture of neoplastic mast cells and their synthesis of 5-hydroxytryptamine and histamine in vitro. Cancer Res 1959, 19:47-51.
16. Miller L., Alber G., Varin-Blank N., Ludowyke R., Metzger H. Transmembrane signaling in P815 mastocytoma cells by transfected IgE receptors. J Biol Chem 1990, 265:12444-12453.
17. Furuno T., Teshima R., Kitani S., Sawada J., Nakanishi M. Surface expression of CD63 antigen (AD1 antigen) in P815 mastocytoma cells by transfected IgE receptors. Biochem Biophys Res Commun 1996, 219:740-744.
18. Anthony L.S., Ghadirian E., Nestel F.P., Kongshavn P.A. The requirement for gamma interferon in resistance of mice to experimental tularemia. Microb Pathog 1989, 7:421-428.
19. Elkins K.L., Rhinehart-Jones T., Nacy C.A., Winegar R.K., Fortier A.H. T-cell-independent resistance to infection and generation of immunity to Francisella tularensis. Infect Immun 1993, 61:823-829.
20. Leiby D.A., Fortier A.H., Crawford R.M., Schreiber R.D., Nacy C.A. In vivo modulation of the murine immune response to Francisella tularensis LVS by administration of anticytokine antibodies. Infect Immun 1992, 60:84-89.
21. Rodriguez A.R., Yu J.-J., Murthy A.K., Guentzel M.N., Klose K.E., Forsthuber T.G., Chambers J.P., Berton M.T., Arulanandam B.P. Mast/ IL-4 control of Francisella tularensis replication and host cell death is associated with increased ATP production and phagosomal acidification. Mucosal Immunol 2010, 6:217-226.
22. Barker J.R., Chong A., Wehrly T.D., Yu J.J., Rodriguez S.A., Liu J., et al. The Francisella tularensis pathogenicity island encodes a secretion system that is required for phagosome escape and virulence. Mol Microbiol 2009, 74:1459-1470.
23. Lai X.H., Shirley R.L., Crosa L., Kanistanon D., Tempel R., Ernst R.K., et al. Mutations of Francisella novicida that alter the mechanism of its phagocytosis by murine macrophages. PLoS One 2010, 5:e11857.
24. Mielcarek N., Hornquist E.H., Johansson B.R., Locht C., Abraham S.N., Holmgren J. Interaction of Bordetella pertussis with mast cells, modulation of cytokine secretion by pertussis toxin. Cell Microbiol 2001, 3:181-188.
25. Paul W.E. Interleukin 4/B cell stimulatory factor 1: one lymphokine, many functions. FASEB J 1987, 1:456-461.
26. Gordon J.R., Galli S.J. Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature 1990, 346:274-276.
27. Lopez M.C., Duckett N.S., Baron S.D., Metzger D.W. Early activation of NK cells after lung infection with the intracellular bacterium, Francisella tularensis LVS. Cell Immunol 2004, 232:75-85.
28. Sherman M.A., Secor V.H., Lee S.K., Lopez R.D., Brown M.A. STAT6-independent production of IL-4 by mast cells. Eur J Immunol 1999, 29:1235-1242.
29. Bradding P., Feather I.H., Howarth P.H., Mueller R., Roberts J.A., Britten K., et al. Interleukin 4 is localized to and released by human mast cells. J Exp Med 1992, 176:1381-1386.
30. Bird J.J., Brown D.R., Mullen A.C., Moskowitz N.H., Mahowald M.A., Sider J.R., et al. Helper T cell differentiation is controlled by the cell cycle. Immunity 1998, 9:229-237.
31. Sherman M.A. The role of STAT6 in mast cell IL-4 production. Immunol Rev 2001, 179:48-56.
32. Sherman M.A., Nachman T.Y., Brown M.A. Cutting edge: IL-4 production by mast cells does not require c-maf. J Immunol 1999, 163:1733-1736.
33. Flesch lEA K.S. Cytokines and antibacterial defence in listerial and mycobacterial infections. Lung 1990, 168:1025-1032.
34. Kolls J.K., McCray P.B., Chan Y.R. Cytokine-mediated regulation of antimicrobial proteins. Nat Rev Immunol 2008, 8:829-835.
35. Jain-Vora S., LeVine A.M., Chroneos Z., Ross G.F., Hull W.M., Whitsett J.A. Interleukin-4 enhances pulmonary clearance of Pseudomonas aeruginosa. Infect Immun 1998, 66:4229-4236.
36. Hart P.H., Vitti G.F., Burgess D.R., Whitty G.A., Piccoli D.S., Hamilton J.A. Potential antiinflammatory effects of interleukin 4: suppression of human monocyte tumor necrosis factor alpha, interleukin 1, and prostaglandin E2. Proc Natl Acad Sci U S A 1989, 86:3803-3807.
37. Hart P.H., Cooper R.L., Finlay-Jones J.J. IL-4 suppresses IL-1 beta, TNF-alpha and PGE2 production by human peritoneal macrophages. Immunology 1991, 72:344-349.
38. Manna S.K., Aggarwal B.B. Interleukin-4 down-regulates both forms of tumor necrosis factor receptor and receptor-mediated apoptosis, NF-kappaB, AP-1, and c-Jun N-terminal kinase. Comparison with interleukin-13. J Biol Chem 1998, 273:33333-33341.
39. Lemaire C., Andr au K., Fraisse C.S., Adam A., Souvannavong V. IL-4 inhibits apoptosis and prevents mitochondrial damage without inducing the switch to necrosis observed with caspase inhibitors. Cell Death Differ 1999, 6:813-820.
40. Cowley S.C., Elkins K.L. Multiple T cell subsets control Francisella tularensis LVS intracellular growth without stimulation through macrophage interferon gamma receptors. J Exp Med 2003, 198:379-389.
41. Collazo C.M., Meierovics A.I., De Pascalis R., Wu T.H., Lyons C.R., Elkins K.L. T cells from lungs and livers of Francisella tularensis-immune mice control the growth of intracellular bacteria. Infect Immun 2009, 77:2010-2021.
42. Anthony L.S., Morrissey P.J., Nano F.E. Growth inhibition of Francisella tularensis live vaccine strain by IFN-gamma-activated macrophages is mediated by reactive nitrogen intermediates derived from l-arginine metabolism. J Immunol 1992, 148:1829-1834.
43. Shirey K.A., Cole L.E., Keegan A.D., Vogel S.N. Francisella tularensis live vaccine strain induces macrophage alternative activation as a survival mechanism. J Immunol 2008, 181:4159-4167.
44. Stassen M., Hultner L., Schmitt E. Classical and alternative pathways of mast cell activation. Crit Rev Immunol 2002, 22:115-140.
45. McLachlan J.B., Shelburne C.P., Hart J.P., Pizzo S.V., Goyal R., Brooking-Dixon R., et al. Mast cell activators: a new class of highly effective vaccine adjuvants. Nat Med 2008, 14:536-541.
46. Higashijima T., Burnier J., Ross E.M. Regulation of Gi and Go by mastoparan, related amphiphilic peptides, and hydrophobic amines. Mechanism and structural determinants of activity. J Biol Chem 1990, 265:14176-14186.
47. Lorenz D., Wiesner B., Zipper J., Winkler A., Krause E., Beyermann M., et al. Mechanism of peptide-induced mast cell degranulation. Translocation and patch-clamp studies. J Gen Physiol 1998, 112:577-591.
48. Palomaki V.A., Laitinen J.T. The basic secretagogue compound 48/80 activates G proteins indirectly via stimulation of phospholipase d-lysophosphatidic acid receptor axis and 5-HT1A receptors in rat brain sections. Br J Pharmacol 2006, 147:596-606.
49. Golovliov I., Baranov V., Krocova Z., Kovarova H., Sjostedt A. An attenuated strain of the facultative intracellular bacterium Francisella tularensis can escape the phagosome of monocytic cells. Infect Immun 2003, 71:5940-5950.
50. Clemens D.L., Lee B.Y., Horwitz M.A. Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infect Immun 2004, 72:3204-3217.
51. Telepnev M., Golovliov I., Sjostedt A. 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 2005, 38:239-247.
52. Golovliov I., Kuoppa K., Sjostedt A., Tarnvik A., Sandstrom G. Cytokine expression in the liver of mice infected with a highly virulent strain of Francisella tularensis. FEMS Immunol Med Microbiol 1996, 13:239-244.