Inhibition of toll-like receptor 2 (TLR-2)-mediated response in human alveolar epithelial cells by mycolic acids and Mycobacterium tuberculosis mce1 operon mutant

Pathogens and Disease

Volumn 70, Issue 2, 2014, Pages 132-140

  Sequeira, Patricia C ^a,b   Senaratne, Ryan H ^a   Riley, Lee W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

A549 cells; Alveolar epithelial cells; mce1 operon; Mycobacterium tuberculosis; Mycolic acid; Tuberculosis

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 12; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; MYCOLIC ACID; RANTES; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; BACTERIAL PROTEIN; IMMUNOSUPPRESSIVE AGENT; MAMMALIAN CELL ENTRY PROTEIN MCE1A, MYCOBACTERIUM TUBERCULOSIS;

ANIMAL CELL; ARTICLE; BACTERIAL CELL WALL; CELL SUSPENSION; CELL VIABILITY; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; INFLAMMATION; INNATE IMMUNITY; LUNG ALVEOLUS EPITHELIUM; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; EPITHELIUM CELL; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTATION;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; EPITHELIAL CELLS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; MACROPHAGES; MUTATION; MYCOBACTERIUM TUBERCULOSIS; MYCOLIC ACIDS; TOLL-LIKE RECEPTOR 2;

EID: 84902280599     PISSN: None     EISSN: 2049632X     Source Type: Journal    
DOI: 10.1111/2049-632X.12110     Document Type: Article

References (37)

1. Armstrong L, Medford AR, Uppington KM, Robertson J, Witherden IR, Tetley TD & Millar AB (2004) Expression of functional toll-like receptor-2 and -4 on alveolar epithelial cells. Am J Respir Cell Mol Biol 31: 241-245.
2. Asai Y, Jinno T & Ogawa T (2003) Oral treponemes and their outer membrane extracts activate human gingival epithelial cells through toll-like receptor 2. Infect Immun 71: 717-725.
3. Barry CE 3rd, Lee RE, Mdluli K, Sampson AE, Schroeder BG, Slayden RA & Yuan Y (1998) Mycolic acids: structure, biosynthesis and physiological function. Prog Lipid Res 37: 143-179.
4. Bermudez LE, Sangari FJ, Kolonoski P, Petrofsky M & Goodman J (2002) The efficiency of the translocation of Mycobacterium tuberculosis across a bilayer of epithelial and endothelial cells as a model of the alveolar wall is a consequence of transport within mononuclear phagocytes and invasion of alveolar epithelial cells. Infect Immun 70: 140-146.
5. Birchler T, Seibl R, Buchner K, Loeliger S, Seger R, Hossle JP, Aguzzi A & Lauener RP (2001) Human Toll-like receptor 2 mediates induction of the antimicrobial peptide human beta-defensin 2 in response to bacterial lipoprotein. Eur J Immunol 31: 3131-3137.
6. Cantrell SA, Leavell MD, Marjanovic O, Iavarone AT, Leary JA & Riley LW (2013) Free mycolic acid accumulation in the cell wall of the mce1 operon mutant strain of Mycobacterium tuberculosis. J Microbiol 51: 619-626.
7. Casali N & Riley LW (2007) A phylogenomic analysis of the Actinomycetales mce operons. BMC Genomics 8: 60.
8. Casali N, White AM & Riley LW (2006) Regulation of the Mycobacterium tuberculosis mce1 operon. J Bacteriol 188: 441-449.
9. Castranova V, Rabovsky J, Tucker JH & Miles PR (1988) The alveolar type II epithelial cell: a multifunctional pneumocyte. Toxicol Appl Pharmacol 93: 472-483.
10. Dassa E & Bouige P (2001) The ABC of ABCS: a phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 152: 211-229.
11. de la Paz Santangelo M, Klepp L, Nunez-Garcia J et al. (2009) Mce3R, a TetR-type transcriptional repressor, controls the expression of a regulon involved in lipid metabolism in Mycobacterium tuberculosis. Microbiology 155(Pt 7): 2245-2255.
12. Dunphy KY, Senaratne RH, Masuzawa M, Kendall LV & Riley LW (2010) Attenuation of Mycobacterium tuberculosis functionally disrupted in a fatty acyl-coenzyme A synthetase gene fadD5. J Infect Dis 201: 1232-1239.
13. Ehlers S (2010) DC-SIGN and mannosylated surface structures of Mycobacterium tuberculosis: a deceptive liaison. Eur J Cell Biol 89: 95-101.
14. Ferguson JS, Voelker DR, McCormack FX & Schlesinger LS (1999) Surfactant protein D binds to Mycobacterium tuberculosis bacilli and lipoarabinomannan via carbohydrate-lectin interactions resulting in reduced phagocytosis of the bacteria by macrophages. J Immunol 163: 312-321.
15. Fulton SA, Reba SM, Pai RK, Pennini M, Torres M, Harding CV & Boom WH (2004) Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and the 19-kilodalton mycobacterial lipoprotein. Infect Immun 72: 2101-2110.
16. Grover AA, Kim HK, Wiegeshaus EH & Smith DW (1967) Host-parasite relationships in experimental airborne tuberculosis. II. Reproducible infection by means of an inoculum preserved at -70 °C. J Bacteriol 94: 832-835.
17. Hall-Stoodley L, Watts G, Crowther JE, Balagopal A, Torrelles JB, Robison-Cox J, Bargatze RF, Harmsen AG, Crouch EC & Schlesinger LS (2006) Mycobacterium tuberculosis binding to human surfactant proteins A and D, fibronectin, and small airway epithelial cells under shear conditions. Infect Immun 74: 3587-3596.
18. Harding CV & Boom WH (2010) Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat Rev Microbiol 8: 296-307.
19. Herrmann JL & Lagrange PH (2005) Dendritic cells and Mycobacterium tuberculosis: which is the Trojan horse? Pathol Biol (Paris) 53: 35-40.
20. Kohwiwattanagun J, Kawamura I, Fujimura T & Mitsuyama M (2007) Mycobacterial mammalian cell entry protein 1A (Mce1A)-mediated adherence enhances the chemokine production by A549 alveolar epithelial cells. Microbiol Immunol 51: 253-261.
21. Lee HM, Yuk JM, Shin DM & Jo EK (2009) Dectin-1 is inducible and plays an essential role for mycobacteria-induced innate immune responses in airway epithelial cells. J Clin Immunol 29: 795-805.
22. Lima P, Sidders B, Morici L, Reader R, Senaratne R, Casali N & Riley LW (2007) Enhanced mortality despite control of lung infection in mice aerogenically infected with a Mycobacterium tuberculosis mce1 operon mutant. Microbes Infect 9: 1285-1290.
23. Means TK, Jones BW, Schromm AB, Shurtleff BA, Smith JA, Keane J, Golenbock DT, Vogel SN & Fenton MJ (2001) Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J Immunol 166: 4074-4082.
24. 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 interferon-induced regulation of selected genes in macrophages. Infect Immun 72: 6603-6614.
25. Pandey AK & Sassetti CM (2008) Mycobacterial persistence requires the utilization of host cholesterol. P Natl Acad Sci USA 105: 4376-4380.
26. Rivas-Santiago B, Contreras JC, Sada E & Hernandez-Pando R (2008a) The potential role of lung epithelial cells and beta-defensins in experimental latent tuberculosis. Scand J Immunol 67: 448-452.
27. Rivas-Santiago B, Hernandez-Pando R, Carranza C, Juarez E, Contreras JL, Aguilar-Leon D, Torres M & Sada E (2008b) Expression of cathelicidin LL-37 during Mycobacterium tuberculosis infection in human alveolar macrophages, monocytes, neutrophils, and epithelial cells. Infect Immun 76: 935-941.
28. Roy S, Sharma S, Sharma M, Aggarwal R & Bose M (2004) Induction of nitric oxide release from the human alveolar epithelial cell line A549: an in vitro correlate of innate immune response to Mycobacterium tuberculosis. Immunology 112: 471-480.
29. Sano H & Kuroki Y (2005) The lung collectins, SP-A and SP-D, modulate pulmonary innate immunity. Mol Immunol 42: 279-287.
30. Scanga CA, Bafica A, Feng CG, Cheever AW, Hieny S & Sher A (2004) MyD88-deficient mice display a profound loss in resistance to Mycobacterium tuberculosis associated with partially impaired Th1 cytokine and nitric oxide synthase 2 expression. Infect Immun 72: 2400-2404.
31. Segal W & Bloch H (1957) Pathogenic and immunogenic differentiation of Mycobacterium tuberculosis grown in vitro and in vivo. Am Rev Tuberc 75: 495-500.
32. Shimono N, Morici L, Casali N, Cantrell S, Sidders B, Ehrt S & Riley LW (2003) Hypervirulent mutant of Mycobacterium tuberculosis resulting from disruption of the mce1 operon. P Natl Acad Sci USA 100: 15918-15923.
33. Tailleux L, Schwartz O, Herrmann JL et al. (2003) DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197: 121-127.
34. Torrelles JB, Azad AK, Henning LN, Carlson TK & Schlesinger LS (2008) Role of C-type lectins in mycobacterial infections. Curr Drug Targets 9: 102-112.
35. Uchida Y, Casali N, White A, Morici L, Kendall LV & Riley LW (2007) Accelerated immunopathological response of mice infected with Mycobacterium tuberculosis disrupted in the mce1 operon negative transcriptional regulator. Cell Microbiol 9: 1275-1283.
36. WHO (2009) Global tuberculosis control: a short update to the 2009 report. [http://www.who.int/tb/publications/global_report/2009/update/en/index.html]
37. Wolf AJ, Linas B, Trevejo-Nunez GJ, Kincaid E, Tamura T, Takatsu K & Ernst JD (2007) Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol 179: 2509-2519.