Mitogen-activated protein kinases p38 and ERK1/2 regulated control of Mycobacterium avium replication in primary murine macrophages is independent of tumor necrosis factor-± and interleukin-10

Innate Immunity

Volumn 17, Issue 5, 2011, Pages 470-485

  Klug, Kirsten ^a   Ehlers, Stefan ^a,b   Uhlig, Stefan ^c   Reiling, Norbert ^a  

^a RESEARCH CENTER BORSTEL   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

cellular activation; cytokines; infectious immunity bacteria; macrophages; mitogen activated protein kinases; mycobacteria; protein kinases phosphatases; signal transduction

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; INTERLEUKIN 10; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM REPLICATION; BONE MARROW CELL; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; MACROPHAGE; MOUSE; MYCOBACTERIUM AVIUM; NONHUMAN; PROTEIN FUNCTION; WILD TYPE;

ANIMALS; CELLS, CULTURED; COLONY COUNT, MICROBIAL; DNA REPLICATION; DNA, BACTERIAL; INTERLEUKIN-10; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM AVIUM; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MURINAE; MYCOBACTERIUM AVIUM;

EID: 80053266748     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425910377799     Document Type: Article

References (53)

1. Inderlied CB, Kemper CA, Bermudez LE. The Mycobacterium avium complex. Clin Microbiol Rev. 1993 ; 6: 266-310 (Pubitemid 23231209)
2. Schorey JS, Cooper AM. Macrophage signalling upon mycobacterial infection: the MAP kinases lead the way. Cell Microbiol. 2003 ; 5: 133-142 (Pubitemid 36348030)
3. Ehlers S, Benini J, Held HD, Roeck C, Alber G, Uhlig S. Alphabeta T cell receptor-positive cells and interferon-gamma, but not inducible nitric oxide synthase, are critical for granuloma necrosis in a mouse model of mycobacteria-induced pulmonary immunopathology. J Exp Med. 2001 ; 194: 1847-1859 (Pubitemid 34028663)
4. Flynn JL, Chan J. Immunology of tuberculosis. Annu Rev Immunol. 2001 ; 19: 93-129 (Pubitemid 32368031)
5. Kaufmann SH. How can immunology contribute to the control of tuberculosis?. Nat Rev Immunol. 2001 ; 1: 20-30 (Pubitemid 33741972)
6. Russell DG. Who puts the tubercle in tuberculosis?. Nat Rev Microbiol. 2007 ; 5: 39-47 (Pubitemid 44942302)
7. Redpath S, Ghazal P, Gascoigne NR. Hijacking and exploitation of IL-10 by intracellular pathogens. Trends Microbiol. 2001 ; 9: 86-92 (Pubitemid 32155327)
8. Vergne I, Chua J, Singh SB, Deretic V. Cell biology of Mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol. 2004 ; 20: 367-394 (Pubitemid 39488643)
9. Flynn JL, Chan J. Immune evasion by Mycobacterium tuberculosis: living with the enemy. Curr Opin Immunol. 2003 ; 15: 450-455 (Pubitemid 36930083)
10. Hänsch HC, Smith DA, Mielke ME, Hahn H, Bancroft GJ, Ehlers S. Mechanisms of granuloma formation in murine Mycobacterium avium infection: the contribution of CD4+ T cells. Int Immunol. 1996 ; 8: 1299-1310 (Pubitemid 26289909)
11. Sarmento AM, Appelberg R. Relationship between virulence of Mycobacterium avium strains and induction of tumor necrosis factor alpha production in infected mice and in in vitro-cultured mouse macrophages. Infect Immun. 1995 ; 63: 3759-3764
12. Blumenthal A, Ehlers S, Ernst M, Flad HD, Reiling N. Control of mycobacterial replication in human macrophages: roles of extracellular signal-regulated kinases 1 and 2 and p38 mitogen-activated protein kinase pathways. Infect Immun. 2002 ; 70: 4961-4967
13. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature. 2001 ; 410: 37-40 (Pubitemid 32225829)
14. Rao KM. MAP kinase activation in macrophages. J Leukoc Biol. 2001 ; 69: 3-10 (Pubitemid 32095111)
15. MAPK Signalling Pathway. Mus musculus, Homo sapiens, ed.. 2009 ;:
16. Roach SK, Schorey JS. Differential regulation of the mitogen-activated protein kinases by pathogenic and nonpathogenic mycobacteria. Infect Immun. 2002 ; 70: 3040-3052 (Pubitemid 34564165)
17. Tse HM, Josephy SI, Chan ED, Fouts D, Cooper AM. Activation of the mitogen-activated protein kinase signaling pathway is instrumental in determining the ability of Mycobacterium avium to grow in murine macrophages. J Immunol. 2002 ; 168: 825-833 (Pubitemid 34049584)
18. Yadav M, Roach SK, Schorey JS. Increased mitogen-activated protein kinase activity and TNF-alpha production associated with Mycobacterium smegmatis- but not Mycobacterium avium-infected macrophages requires prolonged stimulation of the calmodulin/calmodulin kinase and cyclic AMP/protein kinase A pathways. J Immunol. 2004 ; 172: 5588-5597 (Pubitemid 38542061)
19. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 2000 ; 351: 95-105
20. Cohen P. The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol. 1997 ; 7: 353-361 (Pubitemid 27384781)
21. Reiling N, Blumenthal A, Flad HD, Ernst M, Ehlers S. Mycobacteria-induced TNF-alpha and IL-10 formation by human macrophages is differentially regulated at the level of mitogen-activated protein kinase activity. J Immunol. 2001 ; 167: 3339-3345 (Pubitemid 32852576)
22. Song CH, Lee JS, Lee SH, Lim K, Kim HJ, Park JK, et al. Role of mitogen-activated protein kinase pathways in the production of tumor necrosis factor-alpha, interleukin-10, and monocyte chemotactic protein-1 by Mycobacterium tuberculosis H37Rv-infected human monocytes. J Clin Immunol. 2003 ; 23: 194-201 (Pubitemid 36521213)
23. Surewicz K, Aung H, Kanost RA, Jones L, Hejal R, Toossi Z. The differential interaction of p38 MAP kinase and tumor necrosis factor-alpha in human alveolar macrophages and monocytes induced by Mycobacterium tuberculosis. Cell Immunol. 2004 ; 228: 34-41 (Pubitemid 38760121)
24. Shiratsuchi H, Ellner JJ, Basson MD. Extracellular-regulated kinase activation regulates replication of Mycobacterium avium intracellularly in primary human monocytes. Cell Tissue Res. 2008 ; 332: 237-244
25. Körner H, Cook M, Riminton DS, Lemckert FA, Hoek RM, Ledermann B, et al. Distinct roles for lymphotoxin-alpha and tumor necrosis factor in organogenesis and spatial organization of lymphoid tissue. Eur J Immunol. 1997 ; 27: 2600-2609 (Pubitemid 27453850)
26. Souza CD, Evanson OA, Weiss DJ. Mitogen activated protein kinase p38 pathway is an important component of the anti-inflammatory response in Mycobacterium avium subsp. paratuberculosis-infected bovine monocytes. Microb Pathog. 2006 ; 41: 59-66 (Pubitemid 44223943)
27. Souza CD, Evanson OA, Weiss DJ. Role of the mitogen-activated protein kinase pathway in the differential response of bovine monocytes to Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium. Microbes Infect. 2007 ; 9: 1545-1552 (Pubitemid 350217077)
28. Gum RJ, McLaughlin MM, Kumar S, Wang Z, Bower MJ, Lee JC, et al. Acquisition of sensitivity of stress-activated protein kinases to the p38 inhibitor, SB 203580, by alteration of one or more amino acids within the ATP binding pocket. J Biol Chem. 1998 ; 273: 15605-15610 (Pubitemid 28298174)
29. Alessi DR, Cuenda A, Cohen P, Dudley DT, Saltiel AR. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem. 1995 ; 270: 27489-27494
30. Bain J, Plater L, Elliott M, Shapiro N, Hastie CJ, McLauchlan H, et al. The selectivity of protein kinase inhibitors: a further update. Biochem J. 2007 ; 408: 297-315
31. Fratti RA, Chua J, Deretic V. Induction of p38 mitogen-activated protein kinase reduces early endosome autoantigen 1 (EEA1) recruitment to phagosomal membranes. J Biol Chem. 2003 ; 278: 46961-46967 (Pubitemid 37452278)
32. Kim HS, Loughran PA, Billiar TR. Carbon monoxide decreases the level of iNOS protein and active dimer in IL-1beta-stimulated hepatocytes. Nitric Oxide. 2008 ; 18: 256-265
33. Lali FV, Hunt AE, Turner SJ, Foxwell BM. The pyridinyl imidazole inhibitor SB203580 blocks phosphoinositide-dependent protein kinase activity, protein kinase B phosphorylation, and retinoblastoma hyperphosphorylation in interleukin-2-stimulated T cells independently of p38 mitogen-activated protein kinase. J Biol Chem. 2000 ; 275: 7395-7402 (Pubitemid 30146294)
34. Kuijl C, Savage ND, Marsman M, Tuin AW, Janssen L, Egan DA, et al. Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature. 2007 ; 450: 725-730 (Pubitemid 350207691)
35. Zimmermann S, Moelling K. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science. 1999 ; 286: 1741-1744 (Pubitemid 129515882)
36. Liu X, Jana M, Dasgupta S, Koka S, He J, Wood C, et al. Human immunodeficiency virus type 1 (HIV-1) tat induces nitric-oxide synthase in human astroglia. J Biol Chem. 2002 ; 277: 39312-39319 (Pubitemid 35190903)
37. Dewas C, Fay M, Gougerot-Pocidalo MA, El-Benna J. The mitogen-activated protein kinase extracellular signal-regulated kinase 1/2 pathway is involved in formyl-methionyl-leucyl-phenylalanine-induced p47phox phosphorylation in human neutrophils. J Immunol. 2000 ; 165: 5238-5244
38. Nathan C, Shiloh MU. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA. 2000 ; 97: 8841-8848 (Pubitemid 30626635)
39. Corcelle E, Djerbi N, Mari M, Nebout M, Fiorini C, Fenichel P, et al. Control of the autophagy maturation step by the MAPK ERK and p38: lessons from environmental carcinogens. Autophagy. 2007 ; 3: 57-59 (Pubitemid 46100716)
40. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell. 2004 ; 119: 753-766 (Pubitemid 40017683)
41. Appelberg R, Sarmento A, Castro AG. Tumour necrosis factor-alpha (TNF-alpha) in the host resistance to mycobacteria of distinct virulence. Clin Exp Immunol. 1995 ; 101: 308-313
42. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, Lowenstein CJ, et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity. 1995 ; 2: 561-572
43. Ehlers S, Benini J, Kutsch S, Endres R, Rietschel ET, Pfeffer K. Fatal granuloma necrosis without exacerbated mycobacterial growth in tumor necrosis factor receptor p55 gene-deficient mice intravenously infected with Mycobacterium avium. Infect Immun. 1999 ; 67: 3571-3579 (Pubitemid 29291531)
44. Stenger S. Immunological control of tuberculosis: role of tumour necrosis factor and more. Ann Rheum Dis. 2005 ; 64 (Suppl 4). iv24 - iv28
45. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001 ; 19: 683-765 (Pubitemid 32368050)
46. Murray PJ, Young RA. Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect Immun. 1999 ; 67: 3087-3095 (Pubitemid 29244734)
47. Sano C, Sato K, Shimizu T, Kajitani H, Kawauchi H, Tomioka H. The modulating effects of proinflammatory cytokines interferon-gamma (IFN-gamma) and tumour necrosis factor-alpha (TNF-alpha), and immunoregulating cytokines IL-10 and transforming growth factor-beta (TGF-beta), on anti-microbial activity of murine peritoneal macrophages against Mycobacterium avium-intracellulare complex. Clin Exp Immunol. 1999 ; 115: 435-442 (Pubitemid 29130357)
48. Bermudez LE, Champsi J. Infection with Mycobacterium avium induces production of interleukin-10 (IL-10), and administration of anti-IL-10 antibody is associated with enhanced resistance to infection in mice. Infect Immun. 1993 ; 61: 3093-3097 (Pubitemid 23182316)
49. Denis M, Ghadirian E. IL-10 neutralization augments mouse resistance to systemic Mycobacterium avium infections. J Immunol. 1993 ; 151: 5425-5430 (Pubitemid 23332352)
50. Jacobs M, Brown N, Allie N, Gulert R, Ryffel B. Increased resistance to mycobacterial infection in the absence of interleukin-10. Immunology. 2000 ; 100: 494-501 (Pubitemid 30608503)
51. Engele M, Stossel E, Castiglione K, Schwerdtner N, Wagner M, Bolcskei P, et al. Induction of TNF in human alveolar macrophages as a potential evasion mechanism of virulent Mycobacterium tuberculosis. J Immunol. 2002 ; 168: 1328-1337 (Pubitemid 34094503)
52. Förtsch D, Rollinghoff M, Stenger S. IL-10 converts human dendritic cells into macrophage-like cells with increased antibacterial activity against virulent Mycobacterium tuberculosis. J Immunol. 2000 ; 165: 978-987 (Pubitemid 30484767)
53. Blumenthal A, Lauber J, Hoffmann R, Ernst M, Keller C, Buer J, et al. Common and unique gene expression signatures of human macrophages in response to four strains of Mycobacterium avium that differ in their growth and persistence characteristics. Infect Immun. 2005 ; 73: 3330-3341 (Pubitemid 40745874)