Mycobacterium tuberculosis 6-kDa early secreted antigenic target (ESAT-6) protein downregulates Lipopolysaccharide induced c-myc expression by modulating the extracellular signal regulated kinases 1/2

BMC Immunology

Volumn 8, Issue , 2007, Pages

  Ganguly, Niladri ^a   Giang, Pham H ^a   Basu, Sandip K ^a   Mir, Fayaz ^a,b   Siddiqui, Imran ^a   Sharma, Pawan ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY SECRETORY ANTIGENIC TARGET 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MYC PROTEIN; SECRETORY PROTEIN; VANADATE SODIUM; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; ESAT 6 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; ESAT-6 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; HYBRID PROTEIN; IMMEDIATE EARLY PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL SURVIVAL; CAUSE OF DEATH; CELL NUCLEUS; CELL STIMULATION; CONTROLLED STUDY; CYTOPLASM; DEPHOSPHORYLATION; DOWN REGULATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; HOST CELL; IMMUNE RESPONSE; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYMPTOM; ANIMAL; CELL LINE; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; SECRETION;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; CELL LINE; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; IMMEDIATE-EARLY PROTEINS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MYCOBACTERIUM TUBERCULOSIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-MYC; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 36448953072     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-8-24     Document Type: Article

References (60)

1. Raviglione MC: The TB epidemic from 1992 to 2002. Tuberculosis (Edinb) 2003, 83:4-14. 10.1016/S1472-9792(02)00071-9 12758183
2. Rosenberger CMDFinlay BB: Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat Rev Mol Cell Biol 2003, 4:385-396. 10.1038/nrm1104 12728272
3. Koul A Herget T Klebl B Ullrich A: Interplay between mycobacteria and host signalling pathways. Nat Rev Microbiol 2004, 2:189-202. 10.1038/ nrmicro840 15083155
4. Malik Z Iyer SS Kusner DJ Mycobacterium tuberculosis phagosomes exhibit altered calmodulin-dependent signal transduction: Contribution to inhibition of phagosome-lysosome fusion and intracellular survival in human macrophages J Immunol 2001 166 3392 3401 11207296
5. Malik ZA Thompson CR Hashimi S Porter B Iyer SS Kusner DJ: Cutting edge: Mycobacterium tuberculosis blocks Ca2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J Immunol 2003, 170:2811-2815. 12626530
6. Ting LM Kim AC Cattamanchi A Ernst JD: Mycobacterium tuberculosis inhibits IFN-gamma transcriptional responses without inhibiting activation of STAT1. J Immunol 1999, 163:3898-3906. 10490990
7. Noss EH Harding CV Boom WH: Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol 2000, 201:63-74. 10.1006/cimm.2000.1633 10805975
8. Balcewicz-Sablinska MK Keane J Kornfeld H Remold HG: Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol 1998, 161:2636-2641. 9725266
9. Keane J Remold HG Kornfeld H: Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 2000, 164:2016-2020. 10657653
10. Harboe M Oettinger T Wiker HG Rosenkrands I Andersen P: Evidence for occurrence of the ESAT-6 protein in Mycobacterium tuberculosis and virulent Mycobacterium bovis and for its absence in Mycobacterium bovis BCG. Infect Immun 1996, 64:16-22. 173721 8557334
11. Berthet FX Rasmussen PB Rosenkrands I Andersen P Gicquel B: A Mycobacterium tuberculosis operon encoding ESAT-6 and a novel low-molecular-mass culture filtrate protein (CFP-10). Microbiology 1998, 144:3195-3203. 9846755
12. Skjot RL Oettinger T Rosenkrands I Ravn P Brock I Jacobsen S Andersen P: Comparative evaluation of low-molecular-mass proteins from Mycobacterium tuberculosis identifies members of the ESAT-6 family as immunodominant T-cell antigens. Infect Immun 2000, 68:214-220. 97123 10603390
13. Colangeli R Spencer JS Bifani P Williams A Lyashchenko K Keen MA Hill PJ Belisle J Gennaro ML: MTSA-10, the product of the Rv3874 gene of Mycobacterium tuberculosis, elicits tuberculosis-specific, delayed-type hypersensitivity in guinea pigs. Infect Immun 2000, 68:990-993. 97238 10639479 10.1128/IAI.68.2.990-993.2000
14. Trajkovic V Singh G Singh B Singh S Sharma P: Effect of Mycobacterium tuberculosis-specific 10-kilodalton antigen on macrophage release of tumor necrosis factor alpha and nitric oxide. Infect Immun 2002, 70:6558-6566. 132989 12438325 10.1128/IAI.70.12.6558-6566.2002
15. Pym AS Brodin P Brosch R Huerre M Cole ST: Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 2002. 46:709-717. 10.1046/ j.1365-2958.2002.03237.x 12410828
16. Pym AS Brodin P Majlessi L Brosch R Demangel C Williams A Griffiths KE Marchal G Leclerc C Cole ST: Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat Med 2003, 9:533-539. 10.1038/nm859 12692540
17. Brodin P de Jonge MI Majlessi L Leclerc C Nilges M Cole ST Brosch R: Functional analysis of early secreted antigenic target-6, the dominant T-cell antigen of Mycobacterium tuberculosis, reveals key residues involved in secretion, complex formation, virulence, and immunogenicity. J Biol Chem 2005, 280:33953-33959. 10.1074/jbc.M503515200 16048998
18. Brodin P Majlessi L Marsollier L de Jonge MI Bottai D Demangel C Hinds J Neyrolles O Butcher PD Leclerc C Cole ST Brosch R: Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 2006, 74:88-98. 1346617 16368961 10.1128/ IAI.74.1.88-98.2006
19. Mahairas GG Sabo PJ Hickey MJ Singh DC Stover CK: Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol 1996, 178: 1274-1282. 177799 8631702
20. Lewis KN Liao R Guinn KM Hickey MJ Smith S Behr MA Sherman DR: Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J Infect Dis 2003, 187:117-123. 1458498 12508154 10.1086/ 345862
21. Guinn KM Hickey MJ Mathur SK Zakel KL Grotzke JE Lewinsohn DM Smith S Sherman DR: Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol 2004, 51:359-370. 1458497 14756778 10.1046/ j.1365-2958.2003.03844.x
22. Fortune SM Jaeger A Sarracino DA Chase MR Sassetti CM Sherman DR Bloom BR Rubin EJ: Mutually dependent secretion of proteins required for mycobacterial virulence. Proc Natl Acad Sci USA 2005, 102:10676-10681. 1176248 16030141 10.1073/pnas.0504922102
23. Johnson GL Lapadat R: Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002, 298:1911-1912. 10.1126/science.1072682 12471242
24. van der Bruggen T Nijenhuis S van Raaij E Verhoef J van Asbeck BS: Lipopolysaccharide-induced tumor necrosis factor alpha production by human monocytes involves the raf-1/MEK1-MEK2/ERK1-ERK2 pathway. Infect Immun 1999, 67:3824-3829. 96660 10417144
25. 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. 11544323
26. Carter AB Monick MM Hunninghake GW: Both Erk and p38 kinases are necessary for cytokine gene transcription. Am J Respir Cell Mol Biol 1999, 20:751-758. 10101008
27. Kyriakis JM AvPuch J: Sounding the alarm: protein kinase cascades activated by stress and inflammation. J Biol Chem 1996, 271:24313-24316. 10.1074/jbc.271.40.24313 8798679
28. Bhattacharyya A Pathak S Basak C Law S Kundu M Basu J: Execution of macrophage apoptosis by Mycobacterium avium through apoptosis signal-regulating kinase 1/p38 mitogen-activated protein kinase signaling and caspase 8 activation. J Biol Chem 2003, 278:26517-26525. 10.1074/jbc.M300852200 12724324
29. Feng GJ Goodridge HS Harnett MM Wei XQ Nikolaev AV Higson AP Liew FY: Extracellular signal-related kinase (ERK) and p38 mitogen-activated protein (MAP) kinases differentially regulate the lipopolysaccharide-mediated induction of inducible nitric oxide synthase and IL-12 in macrophages: Leishmania phosphoglycans subvert macrophage IL-12 production by targeting ERK MAP kinase. J Immunol 1999, 163:6403-6412. 10586030
30. Roux PP Blenis J: ERK and p38 MAPK-actAvated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 2004, 68:320-344. 419926 15187187 10.1128/MMBR.68.2.320-344.2004
31. Rescan C Coutant A Talarmin H Theret N Glaise D Guguen-Guillouzo C Baffet G: Mechanism in the sequential control of cell morphology and S phase entry by epidermal growth factor involves distinct MEK/ERK activations. Mol Biol Cell 2001, 12:725-738. 30976 11251083
32. Ruckdeschel K Machold J Roggenkamp A Schubert S Pierre J Zumbihl R Liautard JP Heesemann J Rouot B: Yersinia enterocolitica promotes deactivation of macrophage mitogen-activated protein kinases extracellular signal-regulated kinase-1/2, p38, and c-Jun NH2-terminal kinase. Correlation with its inhibitory effect on tumor necrosis factor-alpha production. J Biol Chem 1997, 272:15920-15927. 10.1074/ jbc.272.25.15920 9188492
33. 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 128221 12183542 10.1128/ IAI.70.9.4961-4967.2002
34. Roach SK Schorey JS: Differential regulation of the mitogen-activated protein kinases by pathogenic and nonpathogenic mycobacteria. Infect Immun 2002, 70:3040-3052. 128028 12010996 10.1128/IAI.70.6.3040-3052.2002
35. Lemaitre JM Buckle RS Mechali M: C-Myc in the control of cell proliferation and embryonic development. Adv Cancer Res 1996, 70:95-144. 8902055
36. Herbst A Hemann MT Tworkowski KA Salghetti SE Lowe SW Tansey WP: A conserved element in Myc that negatively regulates its proapoptotic activity. EMBO Rep 2005, 6:177-183. 1299243 15678160 10.1038/ sj.embor.7400333
37. Brunet A Roux D Lenormand P Dowd S Keyse S Pouyssegur J: Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. Embo J 1999, 18:664-674. 1171159 9927426 10.1093/emboj/18.3.664
38. Deak M Clifton AD Lucocq LM Alessi DR: Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. Embo J 1998, 17:4426-4441. 1170775 9687510 10.1093/emboj/17.15.4426
39. Arndt PG Suzuki N Avdi NJ Malcolm KC Worthen GS: Lipopolysaccharide-induced c-Jun NH2-terminal kinase activation in human neutrophils: Role of phosphatidylinositol 3-Kinase and Syk-mediated pathways. J Biol Chem 2004, 279:10883-10891. 10.1074/jbc.M309901200 14699155
40. Durando MM Meier KE Cook JA: Endotoxin activation of mitogen-activated protein kinase in THP-1 cells; diminished activation following endotoxin desensitization. J Leukoc Biol 1998, 64:259-264. 9715266
41. Geppert TD Whitehurst CE: Thompson P Beutler B Lipopolysaccharide signals activation of tumor necrosis factor biosynthesis through the ras/ raf-1/MEK/MAPK pathway. Mol Med 1994, 1:93-103. 8790605
42. Hopkins HA Monick MM: Hunninghake GW Lipopolysaccharide upregulates surface expression of CD14 on human alveolar macrophages. Am J Physiol 1995. 269:L849-854. 8572247
43. Meng F Lowell CA: Lipopolysaccharide (LPS)-induced macrophage activation and signal transduction in the absence of Src-family kinases Hck, Fgr, and Lyn. J Exp Med 1997, 185:1661-1670. 10.1084/jem.185.9.1661 9151903
44. Sweet MJ Hume DA: Endotoxin signal transduction in macrophages. J Leukoc Biol 1996, 60:8-26. 8699127
45. Weinstein SL Gold MR DeFranco AL: Bacterial lipopolysaccharide stimulates protein tyrosine phosphorylation in macrophages. Proc Natl Acad Sci USA 1991, 88:4148-4152. 51615 1709735 10.1073/pnas.88.10.4148
46. Yang RB Mark MR Gurney AL Godowski PJ: Signaling events induced by lipopolysaccharide-activated toll-like receptor 2. J Immunol 1999, 163:639-643. 10395652
47. Shi L Kishore R McMullen MR Nagy LE: Lipopolysaccharide stimulation of ERK1/2 increases TNF-alpha production via Egr-1. Am J Physiol Cell Physiol 2002, 282:C1205-1211. 11997234
48. Sugano M Tsuchida K Makino N: A protein tyrosine phosphatase inhibitor accelerates angiogenesis in a rat model of hindlimb ischemia. J Cardiovasc Pharmacol 2004, 44:460-465. 10.1097/ 01.fjc.0000143275.45289.0a 15454854
49. Cheng M Wang D Roussel MF: Expression of c-Myc in response to colony-stimulating factor-1 requires mitogen-activated protein kinase kinase-1. J Biol Chem 1999, 274:6553-6558. 10.1074/jbc.274.10.6553 10037749
50. Kanazawa S Soucek L Evan Okamoto GT Peterlin BM: C-Myc recruits P-TEFb for transcription, cellular proliferation and apoptosis. Oncogene 2003, 22:5707-5711. 10.1038/sj.onc.1206800 12944920
51. Murphy LO MacKeigan JP Blenis J: A network of immediate early gene products propagates subtle differences in mitogen-activated protein kinase signal amplitude and duration. Mol Cell Biol 2004, 24:144-153. 303364 14673150 10.1128/MCB.24.1.144-153.2004
52. Marampon F Ciccarelli C Zani BM: Down-regulation of c-Myc following MEK/ ERK inhibition halts the expression of malignant phenotype in rhabdomyosarcoma and in non muscle-derived human tumors. Mol Cancer 2006, 5:31. 1560159 16899113 10.1186/1476-4598-5-31
53. Lester RD Jo M Campana WM Gonias SL: Erythropoietin promotes MCF-7 breast cancer cell migration by an ERK/mitogen-activated protein kinase-dependent pathway and is primarily responsible for the increase in migration observed in hypoxia. J Biol Chem 2005, 280:39273-39277. 10.1074/jbc.M509446200 16207704
54. Lu R Wang X Chen ZF Sun DF Tian XQ Fang JY: Inhibition of the Extracellular Signal-regulated Kinase/Mitogen-activated Protein Kinase Pathway Decreases DNA Methylation in Colon Cancer Cells. J Biol Chem 2007, 282:12249-12259. 10.1074/jbc.M608525200 17307743
55. Adler HS Kubsch S Graulich E Ludwig S Knop J Steinbrink K: Activation of MAP kinase p38 is critical for the cell cycle controlled suppressor function of regulatory T cells. Blood 2007, 109:4351-4359. 10.1182/ blood-2006-09-047563 17244678
56. Zhou Y Wang Q Mark Evers B Chung DH: Oxidative stress-induced intestinal epithelial cell apoptosis is mediated by p38 MAPK. Biochem Biophys Res Commun 2006, 350:860-865. 10.1016/j.bbrc.2006.09.103 17034759
57. Renshaw PS Panagiotidou P Whelan A Gordon SV Hewinson RG Williamson RA Carr MD Conclusive evidence that the major T-cell antigens of the Mycobactrium tuberculosis complex ESAT-6 and CFP-10 form a tight 1:1 complex and characterization of the structural properties of ESAT-6, CFP-10 and the ESAT-6*CFP-10 complex. Implications for pathogenesis and virulence J Biol Chem 2002 277 21598 21603 10.1074/ jbc.M201625200 11940590
58. Gao LY Guo S McLaughlin B Morisaki H Engel JN Brown EJ: A mycobacterial virulence gene cluster extending RD1 region is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 2004, 53:1677-1693. 10.1111/j.1365-2958.2004.04261.x 15341647
59. Okkels LM Muller EC Schmid M Rosenkrands I Kaufmann SH Andersen P Jungblut PR: CFP-10 discriminates between nonacetylated and acetylated ESAT-6 of Mycobacterium tuberculosis by differential interaction. Proteomics 2004, 4:2954-2960. 10.1002/pmic.200400906 15378760
60. Pathak SK Basu S Basu KK Banerjee A Pathak S Bhattacharyya A Kaisho T Kundu M Basu J: Direct extracellular interaction between the early secreted antigen ESAT-6 of Mycobacterium tuberculosis and TLR2 inhibits TLR signaling in macrophages. Nat Immunol 2007, 8:610-618. 10.1038/ ni1468 17486091