Mycobacterium tuberculosis lipids regulate cytokines, TLR-2/4 and MHC class II expression in human macrophages

Tuberculosis

Volumn 88, Issue 3, 2008, Pages 212-220

  Rocha Ramírez, Luz María ^a,b   Estrada García, Iris ^c   López Marín, Luz María ^d   Segura Salinas, Erika ^d   Méndez Aragón, Patricia ^c   Van Soolingen, Dick ^e   Torres González, Rubén ^b   Chacón Salinas, Rommel ^c   Estrada Parra, Sergio ^c   Maldonado Bernal, Carmen ^b   López Macías, Constantino ^b   Isibasi, Armando ^b  

^a HOSPITAL INFANTIL DE MÉXICO FEDERICO GÓMEZ   (Mexico)

^b INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^c INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^d INSTITUTO DE INVESTIGACIONES BIOMÉDICAS   (Mexico)

^e NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

Author keywords

M. tuberculosis Beijing; Macrophages monocytes; MHC class II; Mycobacterial lipids; TLR

Indexed keywords

CYTOKINE; INTERLEUKIN 10; LIPID; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN EXPRESSION; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CYTOKINE PRODUCTION; DOWN REGULATION; GENOTYPE; HUMAN; HUMAN CELL; INNATE IMMUNITY; LIPID ANALYSIS; MACROPHAGE ACTIVATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS REGULATION; UPREGULATION;

CYTOKINES; GENE EXPRESSION REGULATION; HLA-DR ANTIGENS; HUMANS; IMMUNITY, NATURAL; LIPIDS; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; VIRULENCE;

EID: 43049181323     PISSN: 14729792     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tube.2007.10.003     Document Type: Article

References (62)

1. Frieden R.T., Sterling T.R., Munsiff S.S., Watt C.J., and Dye C. Tuberculosis. Lancet 362 (2003) 887-889
2. Nunn P., Williams B., Floyd K., Dye C., Elzinga G., and Raviglione M. Tuberculosis control in the era of HIV. Nat Rev Immunol 5 (2005) 819-826
3. Kusner D.J. Mechanism of mycobacterial persistence in tuberculosis. Clin Immunol 114 (2005) 239-247
4. Salgame P. Host innate and TH1 response and the bacterial factors that control Mycobacterium tuberculosis infection. Curr Opin Immunol 17 (2005) 374-380
5. Manca C., Reed M.B., Freeman S., Mathema B., Krieswirth B., Barry III C.E., et al. Differential monocyte activation underlies strain-specific Mycobacterium tuberculosis pathogenesis. Infect Immun 72 (2004) 5511-5514
6. Barry III C.E. Interpreting cell wall 'virulence factors' of Mycobacterium tuberculosis. Trends Microbiol 9 (2001) 237-241
7. Mendelson M., Walters S., Smith I., and Kaplan G. Strain-specific mycobacterial lipids and the stimulation of protective immunity to tuberculosis. Tuberculosis 85 5/6 (2005) 407-413
8. Cox J.S., Chen B., McNeil M., and Jacobs Jr. W.R. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402 (1999) 79-83
9. Underhill D.M., Ozinky A., Smith K.D., and Aderem A. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc Natl Acad Sci USA 96 (1999) 14459-14463
10. Usynski S.T., Stenger S., Takeuchi O., Ochoa M.T., Engele M., Sieling P.A., et al. Induction of direct antimicrobial activity through mammalian toll-like receptors. Science 291 (2001) 1544-1547
11. Brightbill H.D., Libraty D.H., Krutzik S.R., Yang R.B., Belisle J.T., et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285 (1999) 732-736
12. Heldwein K.A., and Fenton M.J. The role of toll-like receptors in immunity against mycobacterial infection. Microbes Infect 4 (2002) 937-944
13. Jang S., Uematsu S., Akira S., and Padmini S. IL-6 and IL-10 induction from dendritic cells in response to Mycobacterium tuberculosis is predominantly dependent on TLR2-mediated recognition. J Immunol 174 (2004) 3392-3397
14. Murray P.S., Wang L., Onufryk K.C., Tepper R.I., and Young R.A. T cell-derived IL-10 antagonizes macrophage function in mycobacterial infection. J Immunol 158 (1997) 315-321
15. Means T.K., Wang S., Lien E., Yoshimura A., Golenbock D.T., and Fenton M.J. Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J Immunol 163 (1999) 3920-3927
16. Means T.K., Jones B.W., Schromm A.B., Shurtleff B.A., Smith J.A., Keane J., et al. Differential effects of toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J Immunol 166 (2001) 4074-4082
17. Kamat A.B., Alt J., Debbabi H., and Behar S.M. Toll-like receptor 4-defective C3H/HeJ mice are not more susceptible than other C3H substrains to infection with Mycobacterium tuberculosis. Infect Immun 71 (2003) 4112-4118
18. Shim T.S., Turner O.C., and Orme I.M. Toll-like receptor 4 plays no role in susceptibility of mice to Mycobacterium tuberculosis infection. Tuberculosis 83 (2003) 367-371
19. Gomes M.S., Florido M., Cordeiro J.V., Teixeira C.M., Takeuchi O., Akira S., et al. Limited role of Toll-like receptor-2 in resistance to Mycobacterium avium. Immunology 111 (2004) 179-185
20. Drennan M.B., Nicolle D., Quesniaux V., Jacobs M., Allie N., Mpagi J., et al. Toll-like receptor 2-deficient mice succumb to Mycobacterium tuberculosis infection. Am J Pathol 164 (2004) 49-57
21. Abel B., Thiebelmont N., Quesniaux V.J.F., Brown N., Mpagi J., Miyake K., et al. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice. J Immunol 169 (2002) 3151-3162
22. Ryffel B., Fremond C., Jacobs M., Parida S., Botha T., Schnyder B., et al. Innate immunity to mycobacterial infection in mice: critical role for toll-like receptors. Tuberculosis 85 (2005) 395-405
23. Reilling N., Holscher C., Fehrenbach A., Kroger S., Kirschning C.J., Goyert S., et al. Cutting edge: toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J Immunol 169 (2002) 3480-3484
24. Muñoz M., Luquin M., Barcelo M.G., Julian E., Ausina V., and Lanéelle M.A. Distribution of surface-exposed antigenic glycolipids in recent clinical isolates of Mycobacterium tuberculosis. Res Microbiol 148 (1997) 405-412
25. Ortalo-Magne A., Lemassu A., Lanéelle M.A., Bardou F., Silve G., Gounon P., et al. Identification of the surface-exposed lipids on the cell envelopes of Mycobacterium tuberculosis and other mycobacterial species. J Bacteriol 178 (1996) 456-461
26. López B., Aguilar D., Orozco H., Burger M., Espitia C., Ritacco V., et al. A marked difference in the pathogenesis and immune response induced by different Mycobacterium tuberculosis genotypes. Clin Exp Immunol 133 (2003) 30-37
27. Dormans J., Burger M., Aguilar D., Hernandez-Pando R., Kremer K., Roholl P., et al. Correlation of virulence, pathology, bacterial load and delayed type hypersensitivity response after infection with different Mycobacterium tuberculosis genotypes in a BALB/c mouse model. Clin Exp Immunol 137 (2004) 460-468
28. Camacho L.R., Ensergueix D., Pérez E., Gicquel B., and Guilhot C. Identification of virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34 (1999) 257-267
29. Smith I. Mycobacterium tuberculosis pathogenesis and molecular determinant of virulence. Clin Microb Rev 16 (2003) 463-496
30. Reed M.B., Domenech P., Manca C., Su H., Barczak A.K., Kreiswirth B.N., et al. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431 (2004) 84-87
31. López-Marín L.M., Laneelle M.A., Prome D., Lanéelle G., Prome J.C., and Daffe M. Structure of a novel sulfate-containing mycobacterial glycolipid. Biochemistry 31 (1992) 11106-11111
32. Folch J., Lees M., and Sloane-Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226 (1957) 497-509
33. Soto C.Y., Cama M., Gibert I., and Luquin M. Application of an easy and reliable method for sulfolipid-I detection in the study of its distribution in Mycobacterium tuberculosis strains. FEMS Microbiol Lett 187 1 (2000) 103-107
34. Gehring A.J., Rojas R.E., Canaday D.H., Lakey D.L., Harding C.V., and Boom W.H. The Mycobacterium tuberculosis 19 kilodalton lipoprotein inhibits gamma interferon-regulated HLA-DR and Fcγ-R1 on human macrophages through toll-like receptors. Infect Immun 71 (2003) 4487-4497
35. Lee K.W., Lee Y., Kim D.S., and Kwon H.J. Direct role of NF-kappa B activation in toll-like receptors-triggered HLA-DR expression. Eur J Immunol 36 5 (2006) 1254-1266
36. Sreevatsan S., Pan X., Stockbauer K.E., Connell N.D., Kreiswirth B.N., Whittam T.S., et al. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci USA 94 (1997) 9869-9874
37. Gagneux S., DeRiemer K., Van T., Kato-Maeda M., de Jong B.C., Narayanan S., et al. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103 (2006) 2869-2873
38. Tsolaki A.G., Hirsh A.E., DeRiemer K., Enciso J.A., Wong M.Z., Hannan M., et al. Functional and evolutionary genomics of Mycobacterium tuberculosis: insights from genomic deletions in 100 strains. Proc Natl Acad Sci USA 101 (2004) 4865-4870
39. Beatty W.L., Rhodes E.R., Ulrich H.J., Chaterjee D., Heuser J.E., and Russell D.G. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1 (2000) 235-247
40. Kolattukudy P.E., Fernandes N.D., Azad A.K., Fitzmaurice A.M., and Sirakova T.D. Biochemistry and molecular genetics of cell-wall lipid biosynthesis in mycobacteria. Mol Microbiol 24 (1997) 263-270
41. Fratti R.A., Chua J., Vergne I., and Deretic V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci USA 100 (2003) 5437-5442
42. Tsenova L., Ellison E., Harbacheuski R., Moreira A.L., Kurepina N., Reed M.B., et al. Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J Infect Dis 192 (2005) 98-106
43. Barczak A.K., Domenech P., Boshoff H.I., Reed M.B., Manca C., Kaplan G., et al. In vivo phenotypic dominance in mouse mixed infections with Mycobacterium tuberculosis clinical isolates. J Infect Dis 192 (2005) 600-606
44. Russell D.G., Muwandumba H.C., and Rhoades E.E. Mycobacterium and the coat of many lipids. J Cell Biol 158 (2002) 421-426
45. Oswald I.P., Wynn T.A., Sher A., and James S.L. Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proc Natl Acad Sci USA 89 (1992) 8676-8680
46. Rook G.A., Taverne J., Leveton C., and Steele J. The role of gamma-interferon, vitamin D3 metabolites and tumour necrosis factor in the pathogenesis of tuberculosis. Immunology 62 (1987) 229-234
47. Gomez-Reino J.J., Carmona L., Valverde V.R., Mola E.M., Montero M.D., and BIOBADASER Group. Treatment of rheumatoid arthritis with tumor necrosis factor inhibitors may predispose to significant increase in tuberculosis risk: a multicenter active-surveillance report. Arthritis Rheum 48 (2003) 2122-2127
48. Bekker L.G., Moreira A.L., Bergtold A., Freeman S., Ryffel B., and Kaplan G. Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent. Infect Immun 68 (2000) 6954-6961
49. Moore K.W., de Waal Malefyt R., Coffman R.L., and O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19 (2001) 683-765
50. Chacon-Salinas R., Serafin-Lopez J., Ramos-Payan R., Mendez-Aragon P., Hernandez-Pando R., Van Soolingen D., et al. Differential pattern of cytokine expression by macrophages infected in vitro with different Mycobacterium tuberculosis genotypes. Clin Exp Immunol 140 (2005) 443-449
51. Van Crevel R., Ottenhoff T.H., and vander Meer J.W. Innate immunity to Mycobacterium tuberculosis. Clin Microb Rev 15 (2002) 294-309
52. Barnes P.F. Type I cytokines and the pathogenesis of tuberculosis. Am J Res Crit Care 161 (2000) 1773-1774
53. Gil D.P., León L.G., Correa L.I., Maya J.R., Paris S.C., García L.F., et al. Differential induction of apoptosis and necrosis in monocytes from patients with tuberculosis and healthy control subjects. J Infect Dis 189 (2004) 2120-2128
54. Rojas M., Olivier M., Gros P., Barrera L.F., and Garcia L.F. TNF-alpha and IL-10 modulate the induction of apoptosis by virulent Mycobacterium tuberculosis in murine macrophages. J Immunol 162 (1999) 6122-6131
55. Silva R.F., Li Q., and Ellner J.J. Expression of virulence of Mycobacterium tuberculosis within human monocytes: virulence correlates with intracellular growth and induction of tumor necrosis alpha but not with evasion of lymphocyte-dependent monocyte effector function. Infect Immun 66 (1998) 1190-1192
56. Reed M.B., Gagneux S., Deriemer K., Small P.M., and Barry3rd C.E. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol 189 (2007) 2583-2589
57. Sirakova T.D., Dubey V.S., Deb C., Daniel J., Korotkova T.A., Abomoelak B., et al. Identification of a diacylglycerol acyltransferase gene involved in accumulation of triacylglycerol in Mycobacterium tuberculosis under stress. Microbiology 152 (2006) 2717-2725
58. Muzio M., Bosisio D., Polentarutti N., D'amico G., Stoppacciaro A., Mancinelli R., et al. Differential expression and regulation of toll-like receptors (TLRs) in human leukocytes: selective expression of TLR3 in dendritic cells. J Immunol 164 (2000) 5998-6004
59. Zarember K.A., and Godowski P.J. Tissue expression of human toll-like receptors and differential regulation of toll-like receptor mRNAs in leukocytes in response to microbes, their products and cytokines. J Immunol 168 (2002) 554-561
60. Chang S.T., Linderman J.J., and Kirschner D.E. Multiple mechanisms allow Mycobacterium tuberculosis to continuously inhibit MHC class II-mediated antigen presentation by macrophages. Proc Natl Acad Sci USA 102 (2005) 4330-4335
61. Pecora N.D., Gehring A.J., Canaday D.H., Boom W.H., and Harding C.V. Mycobacterium tuberculosis Lpr A is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function. J Immunol 177 (2006) 422-429
62. Sanchez M.D., Garcia Y., Montes C., Paris S.C., Rojas M., Barrera L.F., et al. Functional and phenotypic changes in monocytes from patients with tuberculosis are reversed with treatment. Microbes Infect 8 (2006) 2492-2500