Phosphodiesterase-4 inhibition alters gene expression and improves isoniazid - mediated clearance of mycobacterium tuberculosis in rabbit lungs

PLoS Pathogens

Volumn 7, Issue 9, 2011, Pages

  Subbian, Selvakumar ^a   Tsenova, Liana ^a,b   O'Brien, Paul ^a   Yang, Guibin ^a   Koo, Mi Sun ^a   Peixoto, Blas ^a   Fallows, Dorothy ^a   Dartois, Veronique ^c   Muller, George ^d   Kaplan, Gilla ^a  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^b NEW YORK CITY COLLEGE OF TECHNOLOGY   (United States)

^c Novartis Institute for Tropical Diseases   (Singapore)

^d CELGENE CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CC 3052; ISONIAZID; PHOSPHODIESTERASE IV; PHOSPHODIESTERASE IV INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYCLIC AMP; DRUG DERIVATIVE; THALIDOMIDE; TUBERCULOSTATIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HOST PATHOGEN INTERACTION; IMMUNOMODULATION; IN VITRO STUDY; LUNG TUBERCULOSIS; MACROPHAGE; MALE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; TUBERCULOSIS; ANIMAL; ANTIBIOTIC RESISTANCE; BACTERIAL LOAD; BIOSYNTHESIS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; PATHOLOGY; RABBIT;

ANIMALIA; BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS; ORYCTOLAGUS CUNICULUS;

ANIMALS; ANTITUBERCULAR AGENTS; BACTERIAL LOAD; CYCLIC AMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; DRUG RESISTANCE, BACTERIAL; FEMALE; GENE EXPRESSION REGULATION; ISONIAZID; LUNG; MACROPHAGES; MALE; MYCOBACTERIUM TUBERCULOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHODIESTERASE 4 INHIBITORS; RABBITS; THALIDOMIDE; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80053452071     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002262     Document Type: Article

References (130)

1. Dye C, Williams BG, (2010) The population dynamics and control of tuberculosis. Science 328: 856-861.
2. de Chastellier C, (2009) The many niches and strategies used by pathogenic mycobacteria for survival within host macrophages. Immunobiology 214: 526-542.
3. Saunders BM, Britton WJ, (2007) Life and death in the granuloma: immunopathology of tuberculosis. Immunol Cell Biol 85: 103-111.
4. Cosma CL, Sherman DR, Ramakrishnan L, (2003) The secret lives of the pathogenic mycobacteria. Annu Rev Microbiol 57: 641-676.
5. Pieters J, (2008) Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3: 399-407.
6. Jordao L, Bleck CK, Mayorga L, Griffiths G, Anes E, (2008) On the killing of mycobacteria by macrophages. Cell Microbiol 10: 529-548.
7. Paige C, Bishai WR, (2009) Penitentiary or penthouse condo: the tuberculous granuloma from the microbe's point of view. Cell Microbiol 12: 301-309.
8. Stokes RW, Waddell SJ, (2009) Adjusting to a new home: Mycobacterium tuberculosis gene expression in response to an intracellular lifestyle. Future Microbiol 4: 1317-1335.
9. Steinberg BE, Grinstein S, (2008) Pathogen destruction versus intracellular survival: the role of lipids as phagosomal fate determinants. J Clin Invest 118: 2002-2011.
10. Chan J, Flynn J, (2004) The immunological aspects of latency in tuberculosis. Clin Immunol 110: 2-12.
11. Flannagan RS, Cosio G, Grinstein S, (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7: 355-366.
12. Rohde KH, Abramovitch RB, Russell DG, (2007) Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe 2: 352-364.
13. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, et al. (2003) Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 198: 693-704.
14. Dutta NK, Mehra S, Didier PJ, Roy CJ, Doyle LA, et al. (2010) Genetic requirements for the survival of tubercle bacilli in primates. J Infect Dis 201: 1743-1752.
15. Tailleux L, Waddell SJ, Pelizzola M, Mortellaro A, Withers M, et al. (2008) Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS One 3: e1403.
16. Hampshire T, Soneji S, Bacon J, James BW, Hinds J, et al. (2004) Stationary phase gene expression of Mycobacterium tuberculosis following a progressive nutrient depletion: a model for persistent organisms? Tuberculosis (Edinb) 84: 228-238.
17. Flynn JL, Chan J, (2001) Immunology of tuberculosis. Annu Rev Immunol 19: 93-129.
18. Koul A, Herget T, Klebl B, Ullrich A, (2004) Interplay between mycobacteria and host signalling pathways. Nat Rev Microbiol 2: 189-202.
19. Sahiratmadja E, Alisjahbana B, de Boer T, Adnan I, Maya A, et al. (2007) Dynamic changes in pro- and anti-inflammatory cytokine profiles and gamma interferon receptor signaling integrity correlate with tuberculosis disease activity and response to curative treatment. Infect Immun 75: 820-829.
20. Salgame P, (2005) Host innate and Th1 responses and the bacterial factors that control Mycobacterium tuberculosis infection. Curr Opin Immunol 17: 374-380.
21. MacMicking JD, (2009) Recognizing macrophage activation and host defense. Cell Host Microbe 5: 405-407.
22. Liu PT, Modlin RL, (2008) Human macrophage host defense against Mycobacterium tuberculosis. Curr Opin Immunol 20: 371-376.
23. Ehrt S, Schnappinger D, (2009) Mycobacterial survival strategies in the phagosome: defence against host stresses. Cell Microbiol 11: 1170-1178.
24. Quesniaux VF, Jacobs M, Allie N, Grivennikov S, Nedospasov SA, et al. (2010) TNF in host resistance to tuberculosis infection. Curr Dir Autoimmun 11: 157-179.
25. Ly LH, McMurray DN, (2009) The Yin-Yang of TNFalpha in the guinea pig model of tuberculosis. Indian J Exp Biol 47: 432-439.
26. Bekker LG, Freeman S, Murray PJ, Ryffel B, Kaplan G, (2001) TNF-alpha controls intracellular mycobacterial growth by both inducible nitric oxide synthase-dependent and inducible nitric oxide synthase-independent pathways. J Immunol 166: 6728-6734.
27. Hao S, Baltimore D, (2009) The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules. Nat Immunol 10: 281-288.
28. Botha T, Ryffel B, (2003) Reactivation of latent tuberculosis infection in TNF-deficient mice. J Immunol 171: 3110-3118.
29. Bekker LG, Haslett P, Maartens G, Steyn L, Kaplan G, (2000) Thalidomide-induced antigen-specific immune stimulation in patients with human immunodeficiency virus type 1 and tuberculosis. J Infect Dis 181: 954-965.
30. Kast RE, (2000) Tumor necrosis factor has positive and negative self regulatory feed back cycles centered around cAMP. Int J Immunopharmacol 22: 1001-1006.
31. Zidek Z, (1999) Adenosine- cyclic AMP pathways and cytokine expression. Eur Cytokine Netw 10: 319-328.
32. Eigler A, Siegmund B, Emmerich U, Baumann KH, Hartmann G, et al. (1998) Anti-inflammatory activities of cAMP-elevating agents: enhancement of IL-10 synthesis and concurrent suppression of TNF production. J Leukoc Biol 63: 101-107.
33. Serezani CH, Ballinger MN, Aronoff DM, Peters-Golden M, (2008) Cyclic AMP: master regulator of innate immune cell function. Am J Respir Cell Mol Biol 39: 127-132.
34. Souness JE, Griffin M, Maslen C, Ebsworth K, Scott LC, et al. (1996) Evidence that cyclic AMP phosphodiesterase inhibitors suppress TNF alpha generation from human monocytes by interacting with a 'low-affinity' phosphodiesterase 4 conformer. Br J Pharmacol 118: 649-658.
35. Souness JE, Aldous D, Sargent C, (2000) Immunosuppressive and anti-inflammatory effects of cyclic AMP phosphodiesterase (PDE) type 4 inhibitors. Immunopharmacology 47: 127-162.
36. Deree J, Martins JO, Melbostad H, Loomis WH, Coimbra R, (2008) Insights into the regulation of TNF-alpha production in human mononuclear cells: the effects of non-specific phosphodiesterase inhibition. Clinics (Sao Paulo) 63: 321-328.
37. Lee TW, Fedorak RN, (2010) Tumor necrosis factor-alpha monoclonal antibodies in the treatment of inflammatory bowel disease: clinical practice pharmacology. Gastroenterol Clin North Am 39: 543-557.
38. Taylor PC, (2010) Pharmacology of TNF blockade in rheumatoid arthritis and other chronic inflammatory diseases. Curr Opin Pharmacol 10: 308-315.
39. Murdaca G, Colombo BM, Puppo F, (2009) Anti-TNF-alpha inhibitors: a new therapeutic approach for inflammatory immune-mediated diseases: an update upon efficacy and adverse events. Int J Immunopathol Pharmacol 22: 557-565.
40. Sampaio EP, Sarno EN, Galilly R, Cohn ZA, Kaplan G, (1991) Thalidomide selectively inhibits tumor necrosis factor alpha production by stimulated human monocytes. J Exp Med 173: 699-703.
41. Moreira AL, Sampaio EP, Zmuidzinas A, Frindt P, Smith KA, et al. (1993) Thalidomide exerts its inhibitory action on tumor necrosis factor alpha by enhancing mRNA degradation. J Exp Med 177: 1675-1680.
42. Tramontana JM, Utaipat U, Molloy A, Akarasewi P, Burroughs M, et al. (1995) Thalidomide treatment reduces tumor necrosis factor alpha production and enhances weight gain in patients with pulmonary tuberculosis. Mol Med 1: 384-397.
43. Corral LG, Kaplan G, (1999) Immunomodulation by thalidomide and thalidomide analogues. Ann Rheum Dis 58 (Suppl 1): I107-113.
44. Marriott JB, Muller G, Stirling D, Dalgleish AG, (2001) Immunotherapeutic and antitumour potential of thalidomide analogues. Expert Opin Biol Ther 1: 675-682.
45. Bartlett JB, Michael A, Clarke IA, Dredge K, Nicholson S, et al. (2004) Phase I study to determine the safety, tolerability and immunostimulatory activity of thalidomide analogue CC-5013 in patients with metastatic malignant melanoma and other advanced cancers. Br J Cancer 90: 955-961.
46. Marriott JB, Westby M, Cookson S, Guckian M, Goodbourn S, et al. (1998) CC-3052: a water-soluble analog of thalidomide and potent inhibitor of activation-induced TNF-alpha production. J Immunol 161: 4236-4243.
47. Corral LG, Haslett PA, Muller GW, Chen R, Wong LM, et al. (1999) Differential cytokine modulation and T cell activation by two distinct classes of thalidomide analogues that are potent inhibitors of TNF-alpha. J Immunol 163: 380-386.
48. Marriott JB, Clarke IA, Dredge K, Muller G, Stirling D, et al. (2002) Thalidomide and its analogues have distinct and opposing effects on TNF-alpha and TNFR2 during co-stimulation of both CD4(+) and CD8(+) T cells. Clin Exp Immunol 130: 75-84.
49. Koo MS, Manca C, Yang G, O'Brien P, Sung N, et al. (2011) Phosphodiesterase 4 inhibition reduces innate immunity and improves isoniazid clearance of Mycobacterium tuberculosis in the lungs of infected mice. PLoS One 6: e17091.
50. Sirgel FA, Donald PR, Odhiambo J, Githui W, Umapathy KC, et al. (2000) A multicentre study of the early bactericidal activity of anti-tuberculosis drugs. J Antimicrob Chemother 45: 859-870.
51. Fox W, Ellard GA, Mitchison DA, (1999) Studies on the treatment of tuberculosis undertaken by the British Medical Research Council tuberculosis units, 1946-1986, with relevant subsequent publications. Int J Tuberc Lung Dis 3: S231-279.
52. Mitchison DA, (2003) Role of isoniazid in once-weekly rifapentine treatment of pulmonary tuberculosis. Am J Respir Crit Care Med 167: 1298-1299.
53. Weiner M, Burman W, Vernon A, Benator D, Peloquin CA, et al. (2003) Low isoniazid concentrations and outcome of tuberculosis treatment with once-weekly isoniazid and rifapentine. Am J Respir Crit Care Med 167: 1341-1347.
54. Betts JC, McLaren A, Lennon MG, Kelly FM, Lukey PT, et al. (2003) Signature gene expression profiles discriminate between isoniazid-, thiolactomycin-, and triclosan-treated Mycobacterium tuberculosis. Antimicrob Agents Chemother 47: 2903-2913.
55. Boshoff HI, Myers TG, Copp BR, McNeil MR, Wilson MA, et al. (2004) The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J Biol Chem 279: 40174-40184.
56. Wilson M, DeRisi J, Kristensen HH, Imboden P, Rane S, et al. (1999) Exploring drug-induced alterations in gene expression in Mycobacterium tuberculosis by microarray hybridization. Proc Natl Acad Sci U S A 96: 12833-12838.
57. Karakousis PC, Williams EP, Bishai WR, (2008) Altered expression of isoniazid-regulated genes in drug-treated dormant Mycobacterium tuberculosis. J Antimicrob Chemother 61: 323-331.
58. JoAnne L, Flynn LT, Izzo Angelo, Kaplan Gilla, eds. (2008) Experimental Animal Models of Tuberculosis. KGaA, Weinheim Wiley-VCH Verlag GmBH&Co pp. 389-426.
59. Lee BY, Jethwaney D, Schilling B, Clemens DL, Gibson BW, et al. The Mycobacterium bovis bacille Calmette-Guerin phagosome proteome. Mol Cell Proteomics 9: 32-53.
60. Ma Y, Liu H, Tu-Rapp H, Thiesen HJ, Ibrahim SM, et al. (2004) Fas ligation on macrophages enhances IL-1R1-Toll-like receptor 4 signaling and promotes chronic inflammation. Nat Immunol 5: 380-387.
61. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS, et al. (2008) Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76: 2333-2340.
62. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, et al. (2003) Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48: 833-843.
63. Bartek IL, Rutherford R, Gruppo V, Morton RA, Morris RP, et al. (2009) The DosR regulon of M. tuberculosis and antibacterial tolerance. Tuberculosis (Edinb) 89: 310-316.
64. Homolka S, Niemann S, Russell DG, Rohde KH, (2010) Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog 6: e1000988.
65. Sohaskey CD, Wayne LG, (2003) Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J Bacteriol 185: 7247-7256.
66. Humpel A, Gebhard S, Cook GM, Berney M, (2010) The SigF regulon in Mycobacterium smegmatis reveals roles in adaptation to stationary phase, heat, and oxidative stress. J Bacteriol 192: 2491-2502.
67. Schnappinger D, Schoolnik GK, Ehrt S (2006) Expression profiling of host pathogen interactions: how Mycobacterium tuberculosis and the macrophage adapt to one another. Microbes Infect 8: 1132-1140.
68. Waddell SJ, Stabler RA, Laing K, Kremer L, Reynolds RC, et al. (2004) The use of microarray analysis to determine the gene expression profiles of Mycobacterium tuberculosis in response to anti-bacterial compounds. Tuberculosis (Edinb) 84: 263-274.
69. Kaplan G, Tsenova L, (2010) Pulmonary Tuberculosis in the Rabbit. In: Leong F.J DV, Dick T, editors. A color atlas of comparative pathology of pulmonary tuberculosis Singapore CRC Press pp. 107-130.
70. Karakousis PC, Yoshimatsu T, Lamichhane G, Woolwine SC, Nuermberger EL, et al. (2004) Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J Exp Med 200: 647-657.
71. Jindani A, Aber VR, Edwards EA, Mitchison DA, (1980) The early bactericidal activity of drugs in patients with pulmonary tuberculosis. Am Rev Respir Dis 121: 939-949.
72. Vilcheze C, Jacobs WR Jr, (2007) The mechanism of isoniazid killing: clarity through the scope of genetics. Annu Rev Microbiol 61: 35-50.
73. Russell DG, (2001) Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2: 569-577.
74. Beavo JA, Conti M, Heaslip RJ, (1994) Multiple cyclic nucleotide phosphodiesterases. Mol Pharmacol 46: 399-405.
75. Conti M, Beavo J, (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76: 481-511.
76. Shepherd MC, Baillie GS, Stirling DI, Houslay MD, (2004) Remodelling of the PDE4 cAMP phosphodiesterase isoform profile upon monocyte-macrophage differentiation of human U937 cells. Br J Pharmacol 142: 339-351.
77. Agarwal N, Lamichhane G, Gupta R, Nolan S, Bishai WR, (2009) Cyclic AMP intoxication of macrophages by a Mycobacterium tuberculosis adenylate cyclase. Nature 460: 98-102.
78. Tasken K, Aandahl EM, (2004) Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev 84: 137-167.
79. Bengis-Garber C, Gruener N, (1996) Protein kinase A downregulates the phosphorylation of p47 phox in human neutrophils: a possible pathway for inhibition of the respiratory burst. Cell Signal 8: 291-296.
80. Kalamidas SA, Kuehnel MP, Peyron P, Rybin V, Rauch S, et al. (2006) cAMP synthesis and degradation by phagosomes regulate actin assembly and fusion events: consequences for mycobacteria. J Cell Sci 119: 3686-3694.
81. Lin PL, Plessner HL, Voitenok NN, Flynn JL, (2007) Tumor necrosis factor and tuberculosis. J Investig Dermatol Symp Proc 12: 22-25.
82. Akira S, Takeda K, (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511.
83. Bonizzi G, Karin M, (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25: 280-288.
84. Ly LH, Jeevan A, McMurray DN, (2009) Neutralization of TNFalpha alters inflammation in guinea pig tuberculous pleuritis. Microbes Infect 11: 680-688.
85. Roberts EA, Chua J, Kyei GB, Deretic V, (2006) Higher order Rab programming in phagolysosome biogenesis. J Cell Biol 174: 923-929.
86. Thuong NT, Dunstan SJ, Chau TT, Thorsson V, Simmons CP, et al. (2008) Identification of tuberculosis susceptibility genes with human macrophage gene expression profiles. PLoS Pathog 4: e1000229.
87. Volpe E, Cappelli G, Grassi M, Martino A, Serafino A, et al. (2006) Gene expression profiling of human macrophages at late time of infection with Mycobacterium tuberculosis. Immunology 118: 449-460.
88. Shui W, Gilmore SA, Sheu L, Liu J, Keasling JD, et al. (2009) Quantitative proteomic profiling of host-pathogen interactions: the macrophage response to Mycobacterium tuberculosis lipids. J Proteome Res 8: 282-289.
89. Rohde K, Yates RM, Purdy GE, Russell DG, (2007) Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 219: 37-54.
90. Cappelli G, Volpe E, Grassi M, Liseo B, Colizzi V, et al. (2006) Profiling of Mycobacterium tuberculosis gene expression during human macrophage infection: upregulation of the alternative sigma factor G, a group of transcriptional regulators, and proteins with unknown function. Res Microbiol 157: 445-455.
91. Deb C, Lee CM, Dubey VS, Daniel J, Abomoelak B, et al. (2009) A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One 4: e6077.
92. Kaplan G, Post FA, Moreira AL, Wainwright H, Kreiswirth BN, et al. (2003) Mycobacterium tuberculosis growth at the cavity surface: a microenvironment with failed immunity. Infect Immun 71: 7099-7108.
93. Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, et al. (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198: 705-713.
94. Sirakova TD, Dubey VS, Deb C, Daniel J, Korotkova TA, et al. (2006) Identification of a diacylglycerol acyltransferase gene involved in accumulation of triacylglycerol in Mycobacterium tuberculosis under stress. Microbiology 152: 2717-2725.
95. Shiloh MU, Manzanillo P, Cox JS, (2008) Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 3: 323-330.
96. Primm TP, Andersen SJ, Mizrahi V, Avarbock D, Rubin H, et al. (2000) The stringent response of Mycobacterium tuberculosis is required for long-term survival. J Bacteriol 182: 4889-4898.
97. Klinkenberg LG, Lee JH, Bishai WR, Karakousis PC, (2011) The stringent response is required for full virulence of Mycobacterium tuberculosis in guinea pigs. J Infect Dis 202: 1397-1404.
98. Rosenkrands I, Slayden RA, Crawford J, Aagaard C, Barry CE 3rd, et al. (2002) Hypoxic response of Mycobacterium tuberculosis studied by metabolic labeling and proteome analysis of cellular and extracellular proteins. J Bacteriol 184: 3485-3491.
99. Converse PJ, Karakousis PC, Klinkenberg LG, Kesavan AK, Ly LH, et al. (2009) Role of the dosR-dosS two-component regulatory system in Mycobacterium tuberculosis virulence in three animal models. Infect Immun 77: 1230-1237.
100. Kesavan AK, Brooks M, Tufariello J, Chan J, Manabe YC, (2009) Tuberculosis genes expressed during persistence and reactivation in the resistant rabbit model. Tuberculosis (Edinb) 89: 17-21.
101. Sachdeva P, Misra R, Tyagi AK, Singh Y, (2009) The sigma factors of Mycobacterium tuberculosis: regulation of the regulators. FEBS J 277: 605-626.
102. Rao V, Fujiwara N, Porcelli SA, Glickman MS, (2005) Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J Exp Med 201: 535-543.
103. Rao V, Gao F, Chen B, Jacobs WR Jr, Glickman MS, (2006) Trans-cyclopropanation of mycolic acids on trehalose dimycolate suppresses Mycobacterium tuberculosis-induced inflammation and virulence. J Clin Invest 116: 1660-1667.
104. Leistikow RL, Morton RA, Bartek IL, Frimpong I, Wagner K, et al. (2009) The Mycobacterium tuberculosis DosR regulon assists in metabolic homeostasis and enables rapid recovery from nonrespiring dormancy. J Bacteriol 192: 1662-1670.
105. Chauhan S, Sharma D, Singh A, Surolia A, Tyagi JS, (2011) Comprehensive insights into Mycobacterium tuberculosis DevR (DosR) regulon activation switch. Nucleic Acids Res. E-pub ahead of print doi:10.1093/nar/gkr37.
106. Saint-Joanis B, Souchon H, Wilming M, Johnsson K, Alzari PM, et al. (1999) Use of site-directed mutagenesis to probe the structure, function and isoniazid activation of the catalase/peroxidase, KatG, from Mycobacterium tuberculosis. Biochem J 338 (Pt 3): 753-760.
107. Parikh SL, Xiao G, Tonge PJ, (2000) Inhibition of InhA, the enoyl reductase from Mycobacterium tuberculosis, by triclosan and isoniazid. Biochemistry 39: 7645-7650.
108. Wengenack NL, Jensen MP, Rusnak F, Stern MK, (1999) Mycobacterium tuberculosis KatG is a peroxynitritase. Biochem Biophys Res Commun 256: 485-487.
109. Timmins GS, Deretic V, (2006) Mechanisms of action of isoniazid. Mol Microbiol 62: 1220-1227.
110. Fontan PA, Aris V, Alvarez ME, Ghanny S, Cheng J, et al. (2008) Mycobacterium tuberculosis sigma factor E regulon modulates the host inflammatory response. J Infect Dis 198: 877-885.
111. Morris RP, Nguyen L, Gatfield J, Visconti K, Nguyen K, et al. (2005) Ancestral antibiotic resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 102: 12200-12205.
112. Nguyen L, Thompson CJ, (2006) Foundations of antibiotic resistance in bacterial physiology: the mycobacterial paradigm. Trends Microbiol 14: 304-312.
113. Adams KN, Takaki K, Connolly LE, Wiedenhoft H, Winglee K, et al. (2011) Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145: 39-53.
114. Gupta AK, Katoch VM, Chauhan DS, Sharma R, Singh M, et al. (2011) Microarray analysis of efflux pump genes in multidrug-resistant Mycobacterium tuberculosis during stress induced by common anti-tuberculous drugs. Microb Drug Resist 16: 21-28.
115. Vilcheze C, Baughn AD, Tufariello J, Leung L, Kuo M, et al. (2011) Novel inhibitors of InhA efficiently kill Mycobacterium tuberculosis under aerobic and anaerobic conditions. Antimicrob Agents Chemother 55: 3889-98.
116. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, et al. (1995) Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2: 561-572.
117. Chakravarty SD, Zhu G, Tsai MC, Mohan VP, Marino S, et al. (2008) Tumor necrosis factor blockade in chronic murine tuberculosis enhances granulomatous inflammation and disorganizes granulomas in the lungs. Infect Immun 76: 916-926.
118. Bernstein DM, Laney C, Morris EK, Loftus EF, (2005) False beliefs about fattening foods can have healthy consequences. Proc Natl Acad Sci U S A 102: 13724-13731.
119. Lynch MJ, Hill EV, Houslay MD, (2006) Intracellular targeting of phosphodiesterase-4 underpins compartmentalized cAMP signaling. Curr Top Dev Biol 75: 225-259.
120. Pasipanodya JG, Miller TL, Vecino M, Munguia G, Garmon R, et al. (2007) Pulmonary impairment after tuberculosis. Chest 131: 1817-1824.
121. Saliu OY, Sofer C, Stein DS, Schwander SK, Wallis RS, (2006) Tumor-necrosis-factor blockers: differential effects on mycobacterial immunity. J Infect Dis 194: 486-492.
122. La Maestra L, Zaninoni A, Marriott JB, Lazzarin A, Dalgleish AG, et al. (2000) The thalidomide analogue CC-3052 inhibits HIV-1 and tumour necrosis factor-alpha (TNF-alpha) expression in acutely and chronically infected cells in vitro. Clin Exp Immunol 119: 123-129.
123. Guckian M, Dransfield I, Hay P, Dalgleish AG, (2000) Thalidomide analogue CC-3052 reduces HIV+ neutrophil apoptosis in vitro. Clin Exp Immunol 121: 472-479.
124. Spina D, (2008) PDE4 inhibitors: current status. Br J Pharmacol 155: 308-315.
125. Bartlett JB, Dredge K, Dalgleish AG, (2004) The evolution of thalidomide and its IMiD derivatives as anticancer agents. Nat Rev Cancer 4: 314-322.
126. Schafer PH, Parton A, Gandhi AK, Capone L, Adams M, et al. (2010) Apremilast, a cAMP phosphodiesterase-4 inhibitor, demonstrates anti-inflammatory activity in vitro and in a model of psoriasis. Br J Pharmacol 159: 842-855.
127. Tsenova L, Bergtold A, Freedman VH, Young RA, Kaplan G, (1999) Tumor necrosis factor alpha is a determinant of pathogenesis and disease progression in mycobacterial infection in the central nervous system. Proc Natl Acad Sci U S A 96: 5657-5662.
128. Tsenova L, Sokol K, Freedman VH, Kaplan G, (1998) A combination of thalidomide plus antibiotics protects rabbits from mycobacterial meningitis-associated death. J Infect Dis 177: 1563-1572.
129. Talaat AM, Lyons R, Howard ST, Johnston SA, (2004) The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc Natl Acad Sci U S A 101: 4602-4607.
130. Subbian S, Mehta PK, Cirillo SL, Cirillo JD, (2007) The Mycobacterium marinum mel2 locus displays similarity to bacterial bioluminescence systems and plays a role in defense against reactive oxygen and nitrogen species. BMC Microbiol 7: 4.