Toll-like receptor 2-dependent extracellular signal-regulated kinase signaling in Mycobacterium tuberculosis-infected macrophages drives anti-inflammatory responses and inhibits Th1 polarization of responding T cells

Infection and Immunity

Volumn 83, Issue 6, 2015, Pages 2242-2254

  Richardson, Edward T ^a   Shukla, Supriya ^a   Sweet, David R ^a   Wearsch, Pamela A ^a,b   Tsichlis, Philip N ^c   Henry Boom, W ^a,b,d   Harding, Clifford V ^a,b,d  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TUFTS MEDICAL CENTER   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ARGINASE 1; GAMMA INTERFERON; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; CDK5R1 PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE; MYD88 PROTEIN, MOUSE; PHOSPHOTRANSFERASE; TLR2 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CD4+ T LYMPHOCYTE; COCULTURE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; ENZYME DEGRADATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE DELETION; GENE EXPRESSION; HUMAN; HUMAN CELL; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE FUNCTION; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL; TUBERCULOSIS; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; GENE; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; GENES, MHC CLASS II; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-12; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYCOBACTERIUM TUBERCULOSIS; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHOTRANSFERASES; SIGNAL TRANSDUCTION; TH1 CELLS; TOLL-LIKE RECEPTOR 2;

EID: 84929456515     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00135-15     Document Type: Article

References (64)

1. Cooper AM. 2009. Cell-mediated immune responses in tuberculosis. Annu Rev Immunol 27:393-422. http://dx.doi.org/10.1146/annurev.immunol.021908.132703.
2. Flynn JL, Chan J. 2001. Immunology of tuberculosis. Annu Rev Immunol 19:93-129. http://dx.doi.org/10.1146/annurev.immunol.19.1.93.
3. Fremond CM, Yeremeev V, Nicolle DM, Jacobs M, Quesniaux VF, Ryffel B. 2004. Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J Clin Invest 114:1790-1799. http://dx.doi.org/10.1172/JCI200421027.
4. Yahagi A, Umemura M, Tamura T, Kariyone A, Begum MD, Kawakami K, Okamoto Y, Hamada S, Oshiro K, Kohama H, Arakawa T, Ohara N, Takatsu K, Matsuzaki G. 2010. Suppressed induction of mycobacterial antigen-specific Th1-type CD4+ T cells in the lung after pulmonary mycobacterial infection. Int Immunol 22:307-318. http://dx.doi.org/10.1093/intimm/dxq010.
5. Chackerian AA, Perera TV, Behar SM. 2001. Gamma interferonproducing CD4+ T lymphocytes in the lung correlate with resistance to infection with Mycobacterium tuberculosis. Infect Immun 69:2666-2674. http://dx.doi.org/10.1128/IAI.69.4.2666-2674.2001.
6. Sullivan BM, Jobe O, Lazarevic V, Vasquez K, Bronson R, Glimcher LH, Kramnik I. 2005. Increased susceptibility of mice lacking T-bet to infection with Mycobacterium tuberculosis correlates with increased IL-10 and decreased IFN-gamma production. J Immunol 175:4593-4602. http://dx.doi.org/10.4049/jimmunol.175.7.4593.
7. Gallegos AM, Pamer EG, Glickman MS. 2008. Delayed protection by ESAT-6-specific effectorCD4+Tcells after airborneM.tuberculosis infection. JExp Med 205:2359-2368. http://dx.doi.org/10.1084/jem.20080353.
8. Shafiani S, Tucker-Heard G, Kariyone A, Takatsu K, Urdahl KB. 2010. Pathogen-specific regulatory T cells delay the arrival of effector T cells in the lung during early tuberculosis. J Exp Med 207:1409-1420. http://dx.doi.org/10.1084/jem.20091885.
9. Urdahl KB, Shafiani S, Ernst JD. 2011. Initiation and regulation of T-cell responses in tuberculosis. Mucosal Immunol 4:288-293. http://dx.doi.org/10.1038/mi.2011.10.
10. Wolf AJ, Desvignes L, Linas B, Banaiee N, Tamura T, Takatsu K, Ernst JD. 2008. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 205:105-115. http://dx.doi.org/10.1084/jem.20071367.
11. Constant SL, Brogdon JL, Piggott DA, Herrick CA, Visintin I, Ruddle NH, Bottomly K. 2002. Resident lung antigen-presenting cells have the capacity to promote Th2 T cell differentiation in situ. J Clin Invest 110: 1441-1448. http://dx.doi.org/10.1172/JCI16109.
12. Curtis MM, Rowell E, Shafiani S, Negash A, Urdahl KB, Wilson CB, Way SS. 2010. Fidelity of pathogen-specific CD4+ T cells to the Th1 lineage is controlled by exogenous cytokines, interferon-gamma expression, and pathogen lifestyle. Cell Host Microbe 8:163-173. http://dx.doi.org/10.1016/j.chom.2010.07.006.
13. Hegazy AN, Peine M, Helmstetter C, Panse I, Frohlich A, Bergthaler A, Flatz L, Pinschewer DD, Radbruch A, Lohning M. 2010. Interferons direct Th2 cell reprogramming to generate a stable GATA-3(+)T-bet(+) cell subset with combined Th2 and Th1 cell functions. Immunity 32:116-128. http://dx.doi.org/10.1016/j.immuni.2009.12.004.
14. Flynn JL, Chan J, Lin PL. 2011. Macrophages and control of granulomatous inflammation in tuberculosis. Mucosal Immunol 4:271-278. http://dx.doi.org/10.1038/mi.2011.14.
15. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C, Schoolnik GK. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: Insights into the phagosomal environment. J Exp Med 198:693-704. http://dx.doi.org/10.1084/jem.20030846.
16. Bryk R, Gold B, Venugopal A, Singh J, Samy R, Pupek K, Cao H, Popescu C, Gurney M, Hotha S, Cherian J, Rhee K, Ly L, Converse PJ, Ehrt S, Vandal O, Jiang X, Schneider J, Lin G, Nathan C. 2008. Selective killing of nonreplicating mycobacteria. Cell Host Microbe 3:137-145. http://dx.doi.org/10.1016/j.chom.2008.02.003.
17. Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT, Boom WH, Harding CV. 2001. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19 kD lipoprotein of Mycobacterium tuberculosis. J Immunol 167:910-918. http://dx.doi.org/10.4049/jimmunol.167.2.910.
18. Pai RK, Convery M, Hamilton TA, Boom WH, Harding CV. 2003. Inhibition of IFN-gamma-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J Immunol 171:175-184. http://dx.doi.org/10.4049/jimmunol.171.1.175.
19. Pennini ME, Liu Y, Yang J, Croniger CM, Boom WH, Harding CV. 2007. CCAAT/enhancer-binding protein beta and delta binding to CIITA promoters is associated with the inhibition of CIITA expression in response to Mycobacterium tuberculosis 19-kDa lipoprotein. J Immunol 179:6910-6918. http://dx.doi.org/10.4049/jimmunol.179.10.6910.
20. Pennini ME, Pai RK, Schultz DC, Boom WH, Harding CV. 2006. Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gammainduced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol 176:4323-4330. http://dx.doi.org/10.4049/jimmunol.176.7.4323.
21. Kincaid EZ, Wolf AJ, Desvignes L, Mahapatra S, Crick DC, Brennan PJ, Pavelka MS, Jr, Ernst JD. 2007. Codominance of TLR2-dependent and TLR2-independent modulation ofMHCclass II in Mycobacterium tuberculosis infection in vivo. J Immunol 179:3187-3195. http://dx.doi.org/10.4049/jimmunol.179.5.3187.
22. Cyktor JC, Carruthers B, Kominsky RA, Beamer GL, Stromberg P, Turner J. 2013. IL-10 inhibits mature fibrotic granuloma formation during Mycobacterium tuberculosis infection. J Immunol 190:2778-2790. http://dx.doi.org/10.4049/jimmunol.1202722.
23. Redford PS, Boonstra A, Read S, Pitt J, Graham C, Stavropoulos E, Bancroft GJ, O'Garra A. 2010. Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur J Immunol 40:2200-2210. http://dx.doi.org/10.1002/eji.201040433.
24. Saraiva M, O'Garra A. 2010. The regulation of IL-10 production by immune cells. Nat Rev Immunol 10:170-181. http://dx.doi.org/10.1038/nri2711.
25. Sica A, Mantovani A. 2012. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122:787-795. http://dx.doi.org/10.1172/JCI59643.
26. Biswas SK, Mantovani A. 2010. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol 11:889-896. http://dx.doi.org/10.1038/ni.1937.
27. Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958-969. http://dx.doi.org/10.1038/nri2448.
28. El Kasmi KC, Qualls JE, Pesce JT, Smith AM, Thompson RW, Henao-Tamayo M, Basaraba RJ, Konig T, Schleicher U, Koo MS, Kaplan G, Fitzgerald KA, Tuomanen EI, Orme IM, Kanneganti TD, Bogdan C, Wynn TA, Murray PJ. 2008. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat Immunol 9:1399-1406. http://dx.doi.org/10.1038/ni.1671.
29. Barnes PF, Lu S, Abrams JS, Wang E, Yamamura M, Modlin RL. 1993. Cytokine production at the site of disease in human tuberculosis. Infect Immun 61:3482-3489.
30. Lin Y, Zhang M, Hofman FM, Gong J, Barnes PF. 1996. Absence of a prominent Th2 cytokine response in human tuberculosis. Infect Immun 64:1351-1356.
31. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. 1993. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178:2243-2247. http://dx.doi.org/10.1084/jem.178.6.2243.
32. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, Stewart TA. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742. http://dx.doi.org/10.1126/science.8456300.
33. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178:2249-2254. http://dx.doi.org/10.1084/jem.178.6.2249.
34. Harding CV, Boom WH. 2010. Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat Rev Microbiol 8:296-307. http://dx.doi.org/10.1038/nrmicro2321.
35. Takeda K, Akira S. 2004. TLR signaling pathways. Semin Immunol 16: 3-9. http://dx.doi.org/10.1016/j.smim.2003.10.003.
36. Waterfield M, Jin W, Reiley W, Zhang M, Sun SC. 2004. IkappaB kinase is an essential component of the Tpl2 signaling pathway. Mol Cell Biol 24:6040-6048. http://dx.doi.org/10.1128/MCB.24.13.6040-6048.2004.
37. Dumitru CD, Ceci JD, Tsatsanis C, Kontoyiannis D, Stamatakis K, Lin JH, Patriotis C, Jenkins NA, Copeland NG, Kollias G, Tsichlis PN. 2000. TNF-alpha induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103:1071-1083. http://dx.doi.org/10.1016/S0092-8674(00)00210-5.
38. Cargnello M, Roux PP. 2011. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75:50-83. http://dx.doi.org/10.1128/MMBR.00031-10.
39. Boulton TG, Nye SH, Robbins DJ, Ip NY, Radziejewska E, Morgenbesser SD, DePinho RA, Panayotatos N, Cobb MH, Yancopoulos GD. 1991. ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65:663-675. http://dx.doi.org/10.1016/0092-8674(91)90098-J.
40. Liu Y, Chen C, Tseng H, Chang W. 2006. Lipopolysaccharide-induced transcriptional activation of interleukin-10 is mediated by MAPK-and NFkappaB-induced CCAAT/enhancer-binding protein delta in mouse macrophages. Cell Signal 18:1492-1500. http://dx.doi.org/10.1016/j.cellsig.2005.12.001.
41. Liu YW, Tseng HP, Chen LC, Chen BK, Chang WC. 2003. Functional cooperation of simian virus 40 promoter factor 1 and CCAAT/enhancerbinding protein beta and delta in lipopolysaccharide-induced gene activation of IL-10 in mouse macrophages. J Immunol 171:821-828. http://dx.doi.org/10.4049/jimmunol.171.2.821.
42. Lucas M, Zhang X, Prasanna V, Mosser DM. 2005. ERK activation following macrophage FcgammaR ligation leads to chromatin modifications at the IL-10 locus. J Immunol 175:469-477. http://dx.doi.org/10.4049/jimmunol.175.1.469.
43. Fulton SA, Cross JV, Toossi ZT, Boom WH. 1998. Regulation of interleukin-12 by interleukin-10, transforming growth factor-beta, tumor necrosis factor-alpha, and interferon-gamma in human monocytes infected with Mycobacterium tuberculosis H37Ra. J Infect Dis 178:1105-1114. http://dx.doi.org/10.1086/515698.
44. Koch F, Stanzl U, Jennewein P, Janke K, Heufler C, Kämpgen E, Romani N, Schuler G. 1996. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med 184:741-746. http://dx.doi.org/10.1084/jem.184.2.741.
45. O'Garra A, Murphy KM. 2009. From IL-10 to IL-12: how pathogens and their products stimulate APCs to induce T(H)1 development. Nat Immunol 10:929-932. http://dx.doi.org/10.1038/ni0909-929.
46. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. 2000. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164:6166-6173. http://dx.doi.org/10.4049/jimmunol.164.12.6166.
47. Malen H, De Souza GA, Pathak S, Softeland T, Wiker HG. 2011. Comparison of membrane proteins of Mycobacterium tuberculosis H37Rv and H37Ra strains. BMC Microbiol 11:18. http://dx.doi.org/10.1186/1471-2180-11-18.
48. McNab FW, Ewbank J, Rajsbaum R, Stavropoulos E, Martirosyan A, Redford PS, Wu X, Graham CM, Saraiva M, Tsichlis P, Chaussabel D, Ley SC, O'Garra A. 2013. TPL-2-ERK1/2 signaling promotes host resistance against intracellular bacterial infection by negative regulation of type I IFN production. J Immunol 191:1732-1743. http://dx.doi.org/10.4049/jimmunol.1300146.
49. Davies SP, Reddy H, Caivano M, Cohen P. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105. http://dx.doi.org/10.1042/0264-6021:3510095.
50. Sklar MD, Tereba A, Chen BD, Walker WS. 1985. Transformation of mouse bone marrow cells by transfection with a human oncogene related to c-myc is associated with the endogenous production of macrophage colony stimulating factor 1. J Cell Physiol 125:403-412. http://dx.doi.org/10.1002/jcp.1041250307.
51. Drage MG, Tsai HC, Pecora ND, Cheng TY, Arida AR, Shukla S, Rojas RE, Seshadri C, Moody DB, Boom WH, Sacchettini JC, Harding CV. 2010. Mycobacterium tuberculosis lipoprotein LprG (Rv1411c) binds triacylated glycolipid agonists of Toll-like receptor 2. Nat Struct Mol Biol 17:1088-1095. http://dx.doi.org/10.1038/nsmb.1869.
52. Pfaffl MW. 2006. Relative quantitation, p 63-82. In Dorak MT (ed), Real time PCR, 1st ed. Taylor and Francis, New York, NY.
53. Almeida AS, Lago PM, Boechat N, Huard RC, Lazzarini LC, Santos AR, Nociari M, Zhu H, Perez-Sweeney BM, Bang H, Ni Q, Huang J, Gibson AL, Flores VC, Pecanha LR, Kritski AL, Lapa e Silva JR, Ho JL. 2009. Tuberculosis is associated with a down-modulatory lung immune response that impairs Th1-type immunity. J Immunol 183:718-731. http://dx.doi.org/10.4049/jimmunol.0801212.
54. Beamer GL, Flaherty DK, Assogba BD, Stromberg P, Gonzalez-Juarrero M, de Waal Malefyt R, Vesosky B, Turner J. 2008. Interleukin-10 promotes Mycobacterium tuberculosis disease progression in CBA/J mice. J Immunol 181:5545-5550. http://dx.doi.org/10.4049/jimmunol.181.8.5545.
55. MacMicking JD, North RJ, LaCourse R, Mudgett JS, Shah SK, Nathan CF. 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad SciUSA 94:5243-5248. http://dx.doi.org/10.1073/pnas.94.10.5243.
56. Gantke T, Sriskantharajah S, Ley SC. 2011. Regulation and function of TPL-2, an IkappaB kinase-regulated MAP kinase kinase kinase. Cell Res 21:131-145. http://dx.doi.org/10.1038/cr.2010.173.
57. Means TK, Wang S, Lien E, Yoshimura A, Golenbock DT, Fenton MJ. 1999. Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J Immunol 163:3920-3927.
58. Ma X, Chow JM, Gri G, Carra G, Gerosa F, Wolf SF, Dzialo R, Trinchieri G. 1996. The interleukin 12 p40 gene promoter is primed by interferon gamma in monocytic cells. J Exp Med 183:147-157. http://dx.doi.org/10.1084/jem.183.1.147.
59. Pai RK, Pennini ME, Tobian AA, Canaday DH, Boom WH, Harding CV. 2004. Prolonged Toll-like receptor signaling by Mycobacterium tuberculosis and its 19-kilodalton lipoprotein inhibits gamma interferoninduced regulation of selected genes in macrophages. Infect Immun 72: 6603-6614. http://dx.doi.org/10.1128/IAI.72.11.6603-6614.2004.
60. Noss EH, Harding CV, Boom WH. 2000. Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol 201:63-74. http://dx.doi.org/10.1006/cimm.2000.1633.
61. Redford PS, Murray PJ, O'Garra A. 2011. The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol 4:261-270. http://dx.doi.org/10.1038/mi.2011.7.
62. Pompei L, Jang S, Zamlynny B, Ravikumar S, McBride A, Hickman SP, Salgame P. 2007. Disparity in IL-12 release in dendritic cells and macrophages in response to Mycobacterium tuberculosis is due to use of distinct TLRs. J Immunol 178:5192-5199. http://dx.doi.org/10.4049/jimmunol.178.8.5192.
63. Randhawa AK, Shey MS, Keyser A, Peixoto B, Wells RD, de Kock M, Lerumo L, Hughes J, Hussey G, Hawkridge A, Kaplan G, Hanekom WA, Hawn TR, South African Tuberculosis Vaccine Initiative Team. 2011. Association of human TLR1 and TLR6 deficiency with altered immune responses to BCG vaccination in South African infants. PLoS Pathog 7:e1002174. http://dx.doi.org/10.1371/journal.ppat.1002174.
64. Watford WT, Hissong BD, Durant LR, Yamane H, Muul LM, Kanno Y, Tato CM, Ramos HL, Berger AE, Mielke L, Pesu M, Solomon B, Frucht DM, Paul WE, Sher A, Jankovic D, Tsichlis PN, O'Shea JJ. 2008. Tpl2 kinase regulates T cell interferon-gamma production and host resistance to Toxoplasma gondii. J Exp Med 205:2803-2812. http://dx.doi.org/10.1084/jem.20081461.