Strain specific transcriptional response in Mycobacterium tuberculosis infected macrophages

Cell Communication and Signaling

Volumn 10, Issue , 2012, Pages

  Koo, Mi Sun ^a   Subbian, Selvakumar ^a   Kaplan, Gilla ^a  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Bone marrow derived macrophage; Gene expression; Global transcriptome; Host pathogen interaction; Immune response; Intracellular stress response; Lipid metabolism; Macrophage activation pathway; Mycobacterium tuberculosis; Tuberculosis

Indexed keywords

CD209 ANTIGEN; CHOLESTEROL; CXCL9 CHEMOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPID; MONOCYTE CHEMOTACTIC PROTEIN 2; NEUTROPHIL COLLAGENASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROSTAGLANDIN;

ANIMAL CELL; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; CCL8 GENE; CD209G GENE; CELL VIABILITY; CELLULAR STRESS RESPONSE; CHOLESTEROL METABOLISM; CONTROLLED STUDY; CXCL9 GENE; FEMALE; GENE; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; INTERLEUKIN 1BETA GENE; INTERLEUKIN 6 GENE; INTRACELLULAR SIGNALING; LIPID METABOLISM; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE ACTIVATION; METABOLIC REGULATION; MICROARRAY ANALYSIS; MMP9 GENE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRAIN DIFFERENCE; TRANSCRIPTION REGULATION; TUBERCULOSIS;

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

EID: 84863213626     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-10-2     Document Type: Article

References (74)

1. Tuberculosis-metabolism and respiration in the absence of growth. HI Boshoff, CE Barry, Nat Rev Microbiol 2005 3 1 70 80 10.1038/nrmicro1065 15608701 (Pubitemid 40028470)
2. The secret trumps, impelling the pathogenicity of tubercle bacilli. PJ Cardona, J Ivanyi, Enferm Infecc Microbiol Clin 2011 29 Suppl 1 14 9 21458706
3. Mycobacterium tuberculosis cell envelope lipids and the host immune response. PC Karakousis, WR Bishai, SE Dorman, Cell Microbiol 2004 6 2 105 16 10.1046/j.1462-5822.2003.00351.x 14706097 (Pubitemid 38111592)
4. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. S Sturgill-Koszycki, PH Schlesinger, P Chakraborty, PL Haddix, HL Collins, AK Fok, RD Allen, SL Gluck, J Heuser, DG Russell, Science 1994 263 5147 678 81 10.1126/science.8303277 8303277
5. Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin. R Jayachandran, V Sundaramurthy, B Combaluzier, P Mueller, H Korf, K Huygen, T Miyazaki, I Albrecht, J Massner, J Pieters, Cell 2007 130 1 37 50 10.1016/j.cell.2007.04.043 17632055 (Pubitemid 47031320)
6. Pulmonary tuberculosis in the rabbit. G Kaplan, L Tsenova, A color atlas of comparative pathology of pulmonary tuberculosis Boca Raton: CRC Press, Leong FJ, Dartois V, Dick T, 2010 107 129
7. Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. P Peyron, J Vaubourgeix, Y Poquet, F Levillain, C Botanch, F Bardou, M Daffe, JF Emile, B Marchou, PJ Cardona, C de Chastellier, F Altare, PLoS Pathog 2008 4 11 1000204 10.1371/journal.ppat.1000204 19002241
8. Foamy macrophages and the progression of the human tuberculosis granuloma. DG Russell, PJ Cardona, MJ Kim, S Allain, F Altare, Nat Immunol 2009 10 9 943 8 10.1038/ni.1781 19692995
9. Identifying control mechanisms of granuloma formation during M. tuberculosis infection using an agent-based model. JL Segovia-Juarez, S Ganguli, D Kirschner, J Theor Biol 2004 231 3 357 76 10.1016/j.jtbi.2004.06.031 15501468 (Pubitemid 39402949)
10. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha/beta. C Manca, L Tsenova, A Bergtold, S Freeman, M Tovey, JM Musser, CE Barry, VH Freedman, G Kaplan, Proc Natl Acad Sci USA 2001 98 10 5752 7 10.1073/pnas.091096998 11320211 (Pubitemid 32435714)
11. Chronic pulmonary cavitary tuberculosis in rabbits: a failed host immune response. S Subbian, L Tsenova, G Yang, P O'Brien, S Parsons, B Peixoto, L Taylor, D Fallows, G Kaplan, Open Biology 2011 1
12. Experimental animal models of tuberculosis. JL Flynn, L Tsenova, A Izzo, G Kaplan, Handbook of Tuberculosis Weinheim: Wiley-VCH Verlag GmbH & Co, Kaufmann SHE, Britton WJ, 2008 389 426
13. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. MB Reed, P Domenech, C Manca, H Su, AK Barczak, BN Kreiswirth, G Kaplan, CE Barry, Nature 2004 431 7004 84 7 10.1038/nature02837 15343336 (Pubitemid 39215112)
14. The cell-wall core of Mycobacterium tuberculosis in the context of drug discovery. PJ Brennan, DC Crick, Curr Top Med Chem 2007 7 5 475 88 10.2174/156802607780059763 17346193 (Pubitemid 46488288)
15. Mycobacterium and the coat of many lipids. DG Russell, HC Mwandumba, EE Rhoades, J Cell Biol 2002 158 3 421 6 10.1083/jcb.200205034 12147678 (Pubitemid 34851700)
16. The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. D Sinsimer, G Huet, C Manca, L Tsenova, MS Koo, N Kurepina, B Kana, B Mathema, SA Marras, BN Kreiswirth, C Guilhot, G Kaplan, Infect Immun 2008 76 7 3027 36 10.1128/IAI.01663-07 18443098
17. Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. MJ Kim, HC Wainwright, M Locketz, LG Bekker, GB Walther, C Dittrich, A Visser, W Wang, FF Hsu, U Wiehart, L Tsenova, G Kaplan, DG Russell, EMBO Mol Med 2009 2 7 258 74
18. Phosphodiesterase 4 inhibition reduces innate immunity and improves isoniazid clearance of Mycobacterium tuberculosis in the lungs of infected mice. MS Koo, C Manca, G Yang, P O'Brien, N Sung, L Tsenova, S Subbian, D Fallows, G Muller, S Ehrt, G Kaplan, PLoS One 2011 6 2 17091 10.1371/journal.pone.0017091 21364878
19. Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. SNS Homolka, DG Russell, KH Rohde, PLoS Pathog 2010 6 7 1000988 10.1371/journal.ppat.1000988 20628579
20. Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. KH Rohde, RB Abramovitch, DG Russell, Cell Host Microbe 2007 2 5 352 64 10.1016/j.chom.2007.09.006 18005756 (Pubitemid 350056395)
21. Phosphodiesterase-4 Inhibition Alters Gene Expression and Improves Isoniazid-Mediated Clearance of Mycobacterium tuberculosis in Rabbit Lungs. S Subbian, L Tsenova, P O'Brien, G Yang, MS Koo, B Peixoto, D Fallows, V Dartois, G Muller, G Kaplan, PLoS Pathog 2011 7 9 1002262 10.1371/journal.ppat.1002262 21949656
22. Replication dynamics of Mycobacterium tuberculosis in chronically infected mice. EJ Munoz-Elias, J Timm, T Botha, WT Chan, JE Gomez, JD McKinney, Infect Immun 2005 73 1 546 51 10.1128/IAI.73.1.546-551.2005 15618194 (Pubitemid 40041149)
23. Carbon metabolism of intracellular bacteria. EJ Munoz-Elias, JD McKinney, Cell Microbiol 2006 8 1 10 22 10.1111/j.1462-5822.2005.00648.x 16367862 (Pubitemid 43355517)
24. Trans-cyclopropanation of mycolic acids on trehalose dimycolate suppresses Mycobacterium tuberculosis -induced inflammation and virulence. V Rao, F Gao, B Chen, WR Jacobs Jr, MS Glickman, J Clin Invest 2006 116 6 1660 7 10.1172/JCI27335 16741578
25. Mycobacterium tuberculosis CDC1551 induces a more vigorous host response in vivo and in vitro, but is not more virulent than other clinical isolates. C Manca, L Tsenova, CE Barry, A Bergtold, S Freeman, PA Haslett, JM Musser, VH Freedman, G Kaplan, J Immunol 1999 162 11 6740 6 10352293 (Pubitemid 29309400)
26. STAT family of transcription factors in cytokine-mediated biological responses. K Takeda, S Akira, Cytokine Growth Factor Rev 2000 11 3 199 207 10.1016/S1359-6101(00)00005-8 10817963 (Pubitemid 30337459)
27. Selective contribution of Tyk2 to cell activation by lipopolysaccharide. A Schneider, U Reichart, W Gerner, T Kolbe, A Saalmuller, M Muller, FEBS Lett 2008 582 25-26 3681 6 10.1016/j.febslet.2008.09.053 18845149
28. Partial impairment of cytokine responses in Tyk2-deficient mice. M Karaghiosoff, H Neubauer, C Lassnig, P Kovarik, H Schindler, H Pircher, B McCoy, C Bogdan, T Decker, G Brem, K Pfeffer, M Muller, Immunity 2000 13 4 549 60 10.1016/S1074-7613(00)00054-6 11070173
29. Hyperoxia arrests alveolar development through suppression of histone deacetylases in neonatal rats. L Zhu, H Li, J Tang, J Zhu, Y Zhang, Pediatr Pulmonol 2011
30. RET/PTC-induced gene expression in thyroid PCCL3 cells reveals early activation of genes involved in regulation of the immune response. E Puxeddu, JA Knauf, MA Sartor, N Mitsutake, EP Smith, M Medvedovic, CR Tomlinson, S Moretti, JA Fagin, Endocr Relat Cancer 2005 12 2 319 34 10.1677/erc.1.00947 15947106 (Pubitemid 40896450)
31. Increased expression of beta-defensin 1 (DEFB1) in chronic obstructive pulmonary disease. EGG Andresen, J Bullwinkel, C Lange, H Heine, PLoS One 2011 6 7 21898 10.1371/journal.pone.0021898 21818276
32. Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration. M Okigaki, C Davis, M Falasca, S Harroch, DP Felsenfeld, MP Sheetz, J Schlessinger, Proc Natl Acad Sci USA 2003 100 19 10740 5 10.1073/pnas.1834348100 12960403 (Pubitemid 37140098)
33. STAT3 and its activators in intestinal defense and mucosal homeostasis. P Hruz, SM Dann, L Eckmann, Curr Opin Gastroenterol 2010 26 2 109 15 10.1097/MOG.0b013e3283365279 20040863
34. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. T Hirano, K Ishihara, M Hibi, Oncogene 2000 19 21 2548 56 10.1038/sj.onc.1203551 10851053 (Pubitemid 30339210)
35. Organ-specific and differential requirement of TYK2 and IFNAR1 for LPS-induced iNOS expression in vivo. R Painz, I Walter, T Kolbe, D Rigler, C Vogl, R Steinborn, T Rulicke, M Helmreich, M Karaghiosoff, M Muller, Immunobiology 2007 212 9-10 863 75 18086385 (Pubitemid 350246254)
36. Early inflammatory reactions in atherosclerosis are induced by proline-rich tyrosine kinase/reactive oxygen species-mediated release of tumor necrosis factor-alpha and subsequent activation of the p21Cip1/Ets-1/p300 system. A Katsume, M Okigaki, A Matsui, J Che, Y Adachi, E Kishita, S Yamaguchi, K Ikeda, T Ueyama, S Matoba, H Yamada, H Matsubara, Arterioscler Thromb Vasc Biol 2011 31 5 1084 92 10.1161/ATVBAHA.110.221804 21372295
37. Strains of Mycobacterium tuberculosis differ in susceptibility to reactive nitrogen intermediates in vitro. L O'Brien, J Carmichael, DB Lowrie, PW Andrew, Infect Immun 1994 62 11 5187 90 7927804 (Pubitemid 24332835)
38. Nitric oxide induced poly(ADP-ribose) polymerase cleavage in RAW 264.7 macrophage apoptosis is blocked by Bcl-2. UK Messmer, DM Reimer, JC Reed, B Brune, FEBS Lett 1996 384 2 162 6 10.1016/0014-5793(96)00311-0 8612815 (Pubitemid 26135483)
39. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. TB Geijtenbeek, DS Kwon, R Torensma, SJ van Vliet, GC van Duijnhoven, J Middel, IL Cornelissen, HS Nottet, VN KewalRamani, DR Littman, CG Figdor, Y van Kooyk, Cell 2000 100 5 587 97 10.1016/S0092-8674(00) 80694-7 10721995
40. Mycobacteria target DC-SIGN to suppress dendritic cell function. TB Geijtenbeek, SJ Van Vliet, EA Koppel, M Sanchez-Hernandez, CM Vandenbroucke-Grauls, B Appelmelk, Y van Kooyk, J Exp Med 2003 197 1 7 17 12515809 (Pubitemid 36110253)
41. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. SI Gringhuis, J den Dunnen, M Litjens, B van Het Hof, Y van Kooyk, TB Geijtenbeek, Immunity 2007 26 5 605 16 10.1016/j.immuni.2007.03.012 17462920 (Pubitemid 46756345)
42. Human macrophage responses to clinical isolates from the Mycobacterium tuberculosis complex discriminate between ancient and modern lineages. D Portevin, S Gagneux, I Comas, D Young, PLoS Pathog 2011 7 3 1001307 10.1371/journal.ppat.1001307 21408618
43. Foamy macrophages and the progression of the human tuberculosis granuloma. DG Russell, PJ Cardona, MJ Kim, S Allain, F Altare, Nat Immunol 2009 10 9 943 8 10.1038/ni.1781 19692995
44. Toxoplasma gondii infection induces lipid metabolism alterations in the murine host. I Milovanovic, M Vujanic, I Klun, B Bobic, A Nikolic, V Ivovic, AM Trbovich, O Djurkovic-Djakovic, Mem Inst Oswaldo Cruz 2009 104 2 175 8 19430640
45. Inhibition of long-chain acyl coenzyme A synthetases during fatty acid loading induces lipotoxicity in macrophages. V Saraswathi, AH Hasty, Arterioscler Thromb Vasc Biol 2009 29 11 1937 43 10.1161/ATVBAHA.109.195362 19679826
46. Augmentation of DHCR24 expression by hepatitis C virus infection facilitates viral replication in hepatocytes. T Takano, K Tsukiyama-Kohara, M Hayashi, Y Hirata, M Satoh, Y Tokunaga, C Tateno, Y Hayashi, T Hishima, N Funata, M Sudoh, M Kohara, J Hepatol 2011 55 3 512 21 10.1016/j.jhep.2010.12.011 21184787
47. Role of cholesterol pathways in norovirus replication. KO Chang, J Virol 2009 83 17 8587 95 10.1128/JVI.00005-09 19515767
48. Essential role for cholesterol in entry of mycobacteria into macrophages. J Gatfield, J Pieters, Science 2000 288 5471 1647 50 10.1126/science.288.5471. 1647 10834844 (Pubitemid 30387431)
49. Mycobacterial persistence requires the utilization of host cholesterol. AK Pandey, CM Sassetti, Proc Natl Acad Sci USA 2008 105 11 4376 80 10.1073/pnas.0711159105 18334639 (Pubitemid 351754388)
50. The many niches and strategies used by pathogenic mycobacteria for survival within host macrophages. C de Chastellier, Immunobiology 2009 214 7 526 42 10.1016/j.imbio.2008.12.005 19261352
51. Regulation of macrophage tumoricidal function: a role for prostaglandins of the E series. RM Schultz, NA Pavlidis, WA Stylos, MA Chirigos, Science 1978 202 4365 320 1 10.1126/science.694537 694537 (Pubitemid 9059457)
52. Prostaglandins modulate macrophage Ia expression. DS Snyder, DI Beller, ER Unanue, Nature 1982 299 5879 163 5 10.1038/299163a0 6287286 (Pubitemid 12056793)
53. The role of prostaglandin E2 in the immunopathogenesis of experimental pulmonary tuberculosis. J Rangel Moreno, I Estrada Garcia, M De La Luz Garcia Hernandez, D Aguilar Leon, R Marquez, R Hernandez Pando, Immunology 2002 106 2 257 66 10.1046/j.1365-2567.2002.01403.x 12047755 (Pubitemid 34621834)
54. A delicate dance: host response to mycobacteria. KK Huynh, SA Joshi, EJ Brown, Curr Opin Immunol 2011 23 4 464 72 10.1016/j.coi.2011.06.002 21726990
55. Role of innate cytokines in mycobacterial infection. AM Cooper, KD Mayer-Barber, A Sher, Mucosal Immunol 2011 4 3 252 60 10.1038/mi.2011.13 21430655
56. The response of mycobacterium tuberculosis to reactive oxygen and nitrogen species. MI Voskuil, IL Bartek, K Visconti, GK Schoolnik, Front Microbiol 2011 2 105 21734908
57. Adjusting to a new home: Mycobacterium tuberculosis gene expression in response to an intracellular lifestyle. RW Stokes, SJ Waddell, Future Microbiol 2009 4 10 1317 35 10.2217/fmb.09.94 19995191
58. Tuberculosis chemotherapy: the influence of bacillary stress and damage response pathways on drug efficacy. DF Warner, V Mizrahi, Clin Microbiol Rev 2006 19 3 558 70 10.1128/CMR.00060-05 16847086 (Pubitemid 44134310)
59. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha -crystallin. DR Sherman, M Voskuil, D Schnappinger, R Liao, MI Harrell, GK Schoolnik, Proc Natl Acad Sci USA 2001 98 13 7534 9 10.1073/pnas.121172498 11416222 (Pubitemid 32567983)
60. The enduring hypoxic response of Mycobacterium tuberculosis. TR Rustad, MI Harrell, R Liao, DR Sherman, PLoS One 2008 3 1 1502 10.1371/journal.pone. 0001502 18231589 (Pubitemid 351827196)
61. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. HD Park, KM Guinn, MI Harrell, R Liao, MI Voskuil, M Tompa, GK Schoolnik, DR Sherman, Mol Microbiol 2003 48 3 833 43 10.1046/j.1365-2958.2003.03474.x 12694625 (Pubitemid 36819066)
62. Microaerophilic induction of the alpha-crystallin chaperone protein homologue (hspX) mRNA of Mycobacterium tuberculosis. LE Desjardin, LG Hayes, CD Sohaskey, LG Wayne, KD Eisenach, J Bacteriol 2001 183 18 5311 6 10.1128/JB.183.18.5311-5316.2001 11514514 (Pubitemid 32802602)
63. Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. CD Sohaskey, LG Wayne, J Bacteriol 2003 185 24 7247 56 10.1128/JB.185.24.7247-7256.2003 14645286 (Pubitemid 37509842)
64. Up-regulation of narX, encoding a putative 'fused nitrate reductase' in anaerobic dormant Mycobacterium bovis BCG. B Hutter, T Dick, FEMS Microbiol Lett 1999 178 1 63 9 10.1111/j.1574-6968.1999.tb13760.x 10483724 (Pubitemid 29381491)
65. Role of the dosR-dosS two-component regulatory system in Mycobacterium tuberculosis virulence in three animal models. PJ Converse, PC Karakousis, LG Klinkenberg, AK Kesavan, LH Ly, SS Allen, JH Grosset, SK Jain, G Lamichhane, YC Manabe, DN McMurray, EL Nuermberger, WR Bishai, Infect Immun 2009 77 3 1230 7 10.1128/IAI.01117-08 19103767
66. The Mycobacterium tuberculosis cmaA2 gene encodes a mycolic acid trans-cyclopropane synthetase. MS Glickman, SM Cahill, WR Jacobs Jr, J Biol Chem 2001 276 3 2228 33 10.1074/jbc.C000652200 11092877 (Pubitemid 32109706)
67. Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. V Rao, N Fujiwara, SA Porcelli, MS Glickman, J Exp Med 2005 201 4 535 43 10.1084/jem.20041668 15710652 (Pubitemid 40289544)
68. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. OH Vandal, LM Pierini, D Schnappinger, CF Nathan, S Ehrt, Nat Med 2008 14 8 849 54 10.1038/nm.1795 18641659
69. Structural insight into serine protease Rv3671c that Protects M. tuberculosis from oxidative and acidic stress. T Biswas, J Small, O Vandal, T Odaira, H Deng, S Ehrt, OV Tsodikov, Structure 2011 18 10 1353 63
70. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. JD McKinney, K Honer zu Bentrup, EJ Munoz-Elias, A Miczak, B Chen, WT Chan, D Swenson, JC Sacchettini, WR Jacobs Jr, DG Russell, Nature 2000 406 6797 735 8 10.1038/35021074 10963599
71. Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. D Schnappinger, S Ehrt, MI Voskuil, Y Liu, JA Mangan, IM Monahan, G Dolganov, B Efron, PD Butcher, C Nathan, GK Schoolnik, J Exp Med 2003 198 5 693 704 10.1084/jem.20030846 12953091 (Pubitemid 37087769)
72. Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. J Timm, FA Post, LG Bekker, GB Walther, HC Wainwright, R Manganelli, WT Chan, L Tsenova, B Gold, I Smith, G Kaplan, JD McKinney, Proc Natl Acad Sci USA 2003 100 24 14321 6 10.1073/pnas.2436197100 14623960 (Pubitemid 37499235)
73. Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. S Ehrt, D Schnappinger, S Bekiranov, J Drenkow, S Shi, TR Gingeras, T Gaasterland, G Schoolnik, C Nathan, J Exp Med 2001 194 8 1123 40 10.1084/jem.194.8.1123 11602641 (Pubitemid 32995782)
74. A Mycobacterium marinum mel2 mutant is defective for growth in macrophages that produce reactive oxygen and reactive nitrogen species. S Subbian, PK Mehta, SL Cirillo, LE Bermudez, JD Cirillo, Infect Immun 2007 75 1 127 34 10.1128/IAI.01000-06 17030568 (Pubitemid 46047886)