Cholesterol Oxidase Is Indispensable in the Pathogenesis of Mycobacterium tuberculosis

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Klink, Magdalena ^a   Brzezinska, Marta ^a   Szulc, Izabela ^a   Brzostek, Anna ^a   Kielbik, Michal ^a   Sulowska, Zofia ^a   Dziadek, Jaroslaw ^a  

^a INSTITUTE OF MEDICAL BIOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHOLESTEROL OXIDASE; INTERLEUKIN 10; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CHOLESTEROL OXIDASE GENE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MACROPHAGE; MOLECULAR PATHOLOGY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTOSIS; SIGNAL TRANSDUCTION; WILD TYPE;

BACTERIAL PROTEINS; CHOLESTEROL OXIDASE; GENE DELETION; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGE-1 ANTIGEN; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TUBERCULOSIS;

EID: 84883628218     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073333     Document Type: Article

References (54)

1. Jo EK, Yang CS, Choi CH, Harding CV, (2007) Intracellular signalling cascades regulating innate immune responses to Mycobacteria: branching out from Toll-like receptors. Cell Microbiol 9: 1087-1098.
2. Jo EK, (2008) Mycobacterial interaction with innate receptors: TLRs, C-type lectins, and NLRs. Curr Opin Infect Dis 21: 279-286.
3. Krishnan J, Selvarajoo K, Tsuchiya M, Lee G, Choi S, (2007) Toll-like receptor signal transduction. Exp Mol Med 39: 421-438.
4. Velasco-Velázquez MA, Barrera D, González-Arenas A, Rosales C, Agramonte-Hevia J, (2003) Macrophage-Mycobacterium tuberculosis interactions: role of complement receptor 3. Microb Pathog 35: 125-131.
5. Schafer G, Jacobs M, Wilkinson RJ, Brown GD, (2009) Non-opsonic recognition of Mycobacterium tuberculosis by phagocytes. J Innate Immun 1: 231-243.
6. Berrington WR, Hawn TR, (2007) Mycobacterium tuberculosis, macrophages, and the innate immune response: does common variation matter? Immunol Rev 219: 167-186.
7. Jacobs M, Togbe D, Fremond C, Samarina A, Allie N, et al. (2007) Tumor necrosis factor is critical to control tuberculosis infection. Microbes Infect 9: 623-628.
8. Raja A, (2004) Immunology of tuberculosis. Indian J Med Res 120: 213-232.
9. Brzostek A, Pawelczyk J, Rumijowska-Galewicz A, Dziadek B, Dziadek J, (2009) Mycobacterium tuberculosis is able to accumulate and utilize cholesterol. J Bacteriol 191: 6584-6591.
10. Hu Y, van der Geize R, Besra GS, Gurcha SS, Liu A, et al. (2010) 3-Ketosteroid 9alpha-hydroxylase is an essential factor in the pathogenesis of Mycobacterium tuberculosis. Mol Microbiol 75: 107-121.
11. Ouellet H, Johnston JB, de Montellano PR, (2011) Cholesterol catabolism as a therapeutic target in Mycobacterium tuberculosis. Trends Microbiol 19: 530-539.
12. Pandey AK, Sassetti CM, (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci U S A 105: 4376-4380.
13. Yam KC, D'Angelo I, Kalscheuer R, Zhu H, Wang JX, et al. (2009) Studies of a ring-cleaving dioxygenase illuminate the role of cholesterol metabolism in the pathogenesis of Mycobacterium tuberculosis. PloS Pathog 5: e1000344.
14. Brzezinska M, Szulc I, Brzostek A, Klink M, Kielbik M, et al. (2013) The role of 3-ketosteroid 1(2)-dehydrogenase in the pathogenicity of Mycobacterium tuberculosis. BMC Microbiol 13: 43 doi:---10.1186/1471-2180-13-43.
15. Brzostek A, Rumijowska-Galewicz A, Dziadek B, Wojcik EA, Dziadek J, (2013) ChoD and HsdD can be dispensable for cholesterol degradation in mycobacteria. J Steroid Biochem Mol Biol 134: 1-7.
16. Kreit J, Sampson NS, (2009) Cholesterol oxidase: physiological functions. FEBS J 276: 6844-6856.
17. Vrielnik A, (2010) Cholesterol oxidase: structure and function. Cholesterol binding and cholesterol transport proteins. Springer Sciences+Business Media B.V. Subcell Biochem 51: 137-158.
18. Xiong Y, Chalmers MJ, Gao FP, Cross TA, Marshall AG, (2005) Identification of Mycobacterium tuberculosis H37Rv integral membrane proteins by one-dimensional gel electrophoresis and liquid chromatography electrospray ionization tandem mass spectrometry. J Proteome Res 4: 855-861.
19. Malen H, Pathak S, Softeland T, de Souza GA, Wiker HG, (2010) Definition of novel cell envelope associated proteins in Triton X-114 extracts of Mycobacterium tuberculosis H37Rv. BMC Microbiol 10: 132 doi:---10.1186/1471-2180-10-132.
20. de Souza GA, Arntzen MO, Fortuin S, Schurch AC, Malen H, et al. (2011) Proteogenomic analysis of polymorphisms and gene annotation divergences in prokaryotes using a clustered mass spectrometry-friendly database. Mol Cell Proteomics M110.002527 doi: 10.1074/mcp.M110.002527.
21. Brzostek A, Dziadek B, Rumijowska-Galewicz A, Pawelczyk J, Dziadek J, (2007) Cholesterol oxidase is required for virulence of Mycobacterium tuberculosis. FEMS Microbiol Lett 275: 106-112.
22. Uhia I, Galan B, Morales V, Garcia JL, (2011) Initial step in the catabolism of cholesterol by Mycobacterium smegmatis mc2 155. Environ Microbiol 13: 943-959.
23. Yang X, Gao J, Smith I, Dubnau E, Sampson NS, (2011) Cholesterol is not an essential source of nutrition for Mycobacterium tuberculosis during infection. J Bacteriol 193: 1473-1476.
24. Kudo K, Sano H, Takahashi H, Kuronuma K, Yokota S, et al. (2004) Pulmonary collectins enhance phagocytosis of Mycobacterium avium through increased activity of mannose receptor. J Immunol 172: 7592-7602.
25. Bonar A, Chmiela M, Rudnicka W, Rozalska B, (2005) Mannose-binding lectin enhances the attachment and phagocytosis of mycobacteria in vitro. Arch Immunol Ther Exp 53: 437-441.
26. Houben EN, Nguyen L, Pieters J, (2006) Interaction of pathogenic mycobacteria with the host immune system. Curr Opin Microbiol 9: 76-85.
27. Nesbitt NM, Yang X, Fontán P, Kolesnikova I, Smith I, et al. (2009) A thiolase of Mycobacterium tuberculosis is required for virulence and production of androstenedione and androstadienedione from cholesterol. Infect Immun 78: 275-282.
28. Chang JC, Miner MD, Pandey AK, Gill WP, Harik NS, et al. (2009) igr genes and Mycobacterium tuberculosis cholesterol metabolism. J Bacteriol 191: 5232-5239.
29. Thomas ST, Vanderven BC, Sherman DR, Russell DG, Sampson NS, (2011) Pathway profiling in Mycobacterium tuberculosis: elucidation of a cholesterol-derived catabolite and the enzymes that catalyze its metabolism. J Biol Chem 286: 43668-43678.
30. Jagannath C, Actor JK, Hunter RL Jr, (1998) Induction of nitric oxide in human monocytes and monocyte cell lines by Mycobacterium tuberculosis. Nitric Oxide 2: 174-186.
31. Miller BH, Fratti RA, Poschet JF, Timmins GS, Master SS, et al. (2004) Mycobacteria inhibit nitric oxide synthase recruitment to phagosomes during macrophage infection. Infect Immun 72: 2872-2878.
32. Yang CS, Yuk JM, Jo EK, (2009) The role of nitric oxide in mycobacterial infections. Immune Netw 9: 46-52.
33. Lee JS, Yang CS, Shin DM, Yuk JM, Son JW, et al. (2009) Nitric oxide synthesis is modulated by 1,25-Dihydroxyvitamin D3 and interferon-gamma in human macrophages after mycobacterial infection. Immune Netw 9: 192-202.
34. Rivero-Lezcano OM, Gonzalez-Cortes C, Reyes-Ruvalcaba D, Diez-Tascon C, (2010) CCL20 is overexpressed in Mycobacterium tuberculosis-infected monocytes and inhibits the production of reactive oxygen species (ROS). Clin Exp Immunol 162: 289-297.
35. Yang CS, Shin DM, Kim KH, Lee ZW, Lee CH, et al. (2009) NADPH oxidase 2 interaction with TLR2 is required for efficient innate immune responses to mycobacteria via cathelicidin expression. J Immunol 182: 3696-3705.
36. Gan L, Li L, (2010) Interleukin-1 Receptor-Associated Kinase-1 (IRAK-1) functionally associates with PKCepsilon and VASP in the regulation of macrophage migration. Mol Immunol 47: 278-282.
37. Tiwari RL, Singh V, Singh A, Barthwal MK, (2011) IL-1R-associated kinase-1 mediates protein kinase Cδ-induced IL-1β production in monocytes. J Immunol 187: 2632-2645.
38. Rooyakkers AW, Stokes RW, (2005) Absence of complement receptor 3 results in reduced binding and ingestion of Mycobacterium tuberculosis but has no significant effect on the induction of reactive oxygen and nitrogen intermediates or on the survival of the bacteria in resident and interferon-gamma activated macrophages. Microb Pathog 39: 57-67.
39. Schorey JS, Cooper AM, (2003) Macrophage signalling upon mycobacterial infection: the MAP kinases lead the way. Cell Microbiol 5: 133-142.
40. Chan ED, Morris KR, Belisle JT, Hill P, Remigio LK, et al. (2001) Induction of inducible nitric oxide synthase-NO* by lipoarabinomannan of Mycobacterium tuberculosis is mediated by MEK1-ERK, MKK7-JNK, and NF-kappaB signaling pathways. Infect Immun 69: 2001-2010.
41. Dang PM, Morel F, Gougerot-Pocidalo MA, El Benna J, (2003) Phosphorylation of the NADPH oxidase component p67(PHOX) by ERK2 and P38MAPK: selectivity of phosphorylated sites and existence of an intramolecular regulatory domain in the tetratricopeptide-rich region. Biochemistry 42: 4520-4526.
42. Dang PM, Stensballe A, Boussetta T, Raad H, Dewas C, et al. (2006) A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J Clin Invest 116: 2033-2043.
43. Yoshida A, Inagawa H, Kohchi C, Nishizawa T, Soma G, (2009) The role of toll-like receptor 2 in survival strategies of Mycobacterium tuberculosis in macrophage phagosomes. Anticancer Res 29: 907-910.
44. Underhill DM, Ozinsky A, Hajjar AM, Stevens A, Wilson CB, et al. (1999) The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401: 811-815.
45. Welin A, Lerm M, (2012) Inside or outside the phagosome? The controversy of the intracellular localization of Mycobacterium tuberculosis. Tuberculosis 92: 113-120.
46. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, et al. (2012) Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 8: e1002507 doi:10.1371.
47. Nguyen DH, Taub DD, (2003) Inhibition of chemokine receptor function by membrane cholesterol oxidation. Exp Cell Res 291: 36-45.
48. Madan-Lala R, Peixoto KV, Re F, Rengarajan J, (2011) Mycobacterium tuberculosis Hip1 dampens macrophage proinflammatory responses by limiting toll-like receptor 2 activation. Infect Immun 79: 4828-4838.
49. Gorudko IV, Mukhortava AV, Caraher B, Ren M, Cherenkevich SN, et al. (2011) Lectin-induced activation of plasma membrane NADPH oxidase in cholesterol-depleted human neutrophils. Arch Biochem Biophys 516: 173-181.
50. Fessler MB, Parks JS, (2011) Intracellular lipid flux and membrane microdomains as organizing principles in inflammatory cell signaling. J Immunol 187: 1529-1535.
51. O'Leary S, O'Sullivan MP, Keane J, (2011) IL-10 blocks phagosome maturation in Mycobacterium tuberculosis-infected human macrophages. Am J Respir Cell Mol Biol 45: 172-180.
52. 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.
53. Surewicz K, Aung H, Kanost RA, Jones L, Hejal R, et al. (2004) The differential interaction of p38 MAP kinase and tumor necrosis factor-alpha in human alveolar macrophages and monocytes induced by Mycobacterium tuberculosis. Cell Immunol 228: 34-41.
54. Mootoo A, Stylianou E, Arias MA, Reljic R, (2009) TNF-alpha in tuberculosis: a cytokine with a split personality. Inflamm Allergy Drug Targets 8: 53-62.