The timing of TNF and IFN-γ signaling affects macrophage activation strategies during Mycobacterium tuberculosis infection

Journal of Theoretical Biology

Volumn 252, Issue 1, 2008, Pages 24-38

  Ray, J Christian J ^a   Wang, Jian ^b   Chan, John ^b   Kirschner, Denise E ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Cytokine; Feedback; Immune system; Mathematical model; Response time

Indexed keywords

GAMMA INTERFERON; NITRIC OXIDE; TUMOR NECROSIS FACTOR;

BACTERIUM; IMMUNE RESPONSE; IMMUNE SYSTEM; NUMERICAL MODEL; SIGNALING; TUBERCULOSIS;

ARTICLE; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; MACROPHAGE ACTIVATION; MATHEMATICAL MODEL; MYCOBACTERIUM TUBERCULOSIS; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; TUBERCULOSIS;

ANIMALS; CYTOKINES; FEEDBACK, BIOCHEMICAL; INTERFERON TYPE II; MACROPHAGE ACTIVATION; MACROPHAGES; MODELS, IMMUNOLOGICAL; MYCOBACTERIUM TUBERCULOSIS; SIGNAL TRANSDUCTION; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 41949133862     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2008.01.010     Document Type: Article

References (64)

1. Aaronson D.S., and Horvath C.M. A road map for those who know JAK-STAT. Science 296 5573 (2002) 1653-1655
2. Algood H., Chan J., and Flynn J. Chemokines and tuberculosis. Cytokine Growth Factor Rev. 14 6 (2003) 467-477
3. Alves R., and Savageau M.A. Extending the method of mathematically controlled comparison to include numerical comparisons. Bioinformatics 16 9 (2000) 786-798
4. Blower S.M., and Dowlatabadi H. Sensitivity and uncertainty analysis of complex models of disease transmission: an HIV model, as an example. Int. Stat. Rev. 62 (1994) 229-243
5. Bonecini-Almeida M.G., Chitale S., Boutsikakis I., Geng J., Doo H., He S., and Ho J.L. Induction of in vitro human macrophage anti-Mycobacterium tuberculosis activity: requirement for IFN-gamma and primed lymphocytes. J. Immunol. 160 (1998) 4490-4499
6. Brown M.C., and Taffet S.M. Lipoarabinomannans derived from different strains of Mycobacterium tuberculosis differentially stimulate the activation of NF-κB and KBF1 in murine macrophages. Infect. Immun. 63 5 (1995) 1960-1968
7. Bryk R., Griffin P., and Nathan C. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407 (2000) 211-215
8. Chan J., and Flynn J. The immunological aspects of latency in tuberculosis. Clin. Immunol. 110 1 (2004) 2-12
9. Chan J., Xing Y., Magliozzo R.S., and Bloom B.R. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175 (1992) 1111-1122
10. Chan E.D., Morris K.R., Belisle J.T., Hill P., Remigio L.K., Brennan P.J., and Riches D.W. Induction of inducible nitric oxide synthase-NO by lipoarabinomannan of Mycobacterium tuberculosis is mediated by MEK1-ERK, MKK7-JNK, and NF-κB signaling pathways. Infect. Immun. 69 4 (2001) 2001-2010
11. Collins H.L., and Kaufmann S.H. The many faces of host responses to tuberculosis. Immunology 103 1 (2001) 1-9
12. Cooper A., Dalton D., Stewart T., Griffin J., Russell D., and Orme I. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 178 6 (1993) 2243-2247
13. Couture M., Yeh S., Wittenberg B., Wittenberg J., Ouellet Y., Rousseau D., and Guertin M. A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 96 20 (1999) 11223-11228
14. Decker T., Lohmann-Matthes M.L., and Gifford G.E. Cell-associated tumor necrosis factor (TNF) as a killing mechanism of activated cytotoxic macrophages. J. Immunol. 138 3 (1987) 957-962
15. DeVoss J.J., Rutter K., Schroeder B.G., Su H., Zhu Y., and Barry III C.E. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc. Natl. Acad. Sci. USA 97 (2000) 1252-1257
16. Ding A., Nathan C., and Stuehr D. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141 7 (1988) 2407-2412
17. Ehrt S., Shiloh M.U., Ruan J., Choi M., Gunzburg S., Nathan C., Xie Q., and Riley L.W. A novel antioxidant gene from Mycobacterium tuberculosis. J. Exp. Med. 186 (1997) 1885-1896
18. Flesch I., and Kaufmann S. Mycobacterial growth inhibition by interferon-gamma-activated bone marrow macrophages and differential susceptibility among strains of Mycobacterium tuberculosis. J. Immunol. 138 12 (1987) 4408-4413
19. Flynn J.L., and Chan J. Immunology of tuberculosis. Annu. Rev. Immunol. 19 (2001) 93-129
20. Fujihara M., Muroi M., Tanamoto K., Suzuki T., Azuma H., and Ikeda H. Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacol. Ther. 100 2 (2003) 171-194
21. Graham J., and Clark-Curtiss J. Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proc. Natl. Acad. Sci. USA 96 20 (1999) 11554-11559
22. Grebenchtchikov N., van der Ven-Jongekrijg J., Pesman G.J., Geurts-Moespot A., van der Meer J.W., and Sweep F.C. Development of a sensitive ELISA for the quantification of human tumour necrosis factor-alpha using 4 polyclonal antibodies. Eur. Cytokine Netw. 16 3 (2005) 215-222
23. Harant H., de Martin R., Andrew P., Foglar E., Dittrich C., and Lindley I. Synergistic activation of interleukin-8 gene transcription by all-trans-retinoic acid and tumor necrosis factor-alpha involves the transcription factor NF-kappaB. J. Biol. Chem. 271 43 (1996) 26954-26961
24. Harrison P.M., and Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275 (1996) 161-203
25. Haspel R.L., Salditt-Georgieff M., and Darnell Jr. J.E. The rapid inactivation of nuclear tyrosine phosphorylated Stat1 depends upon a protein tyrosine phosphatase. EMBO J. 15 (1996) 6262-6268
26. Hattori Y., Kasai K., and Gross S. NO suppresses while peroxynitrite sustains NF-κB: a paradigm to rationalize cytoprotective and cytotoxic actions attributed to NO. Cardiovascular Research 63 1 (2004) 31-40
27. Heldwein K.A., and Fenton M.J. The role of Toll-like receptors in immunity against mycobacterial infection. Microbes Infect. 4 (2002) 937-944
28. Hentze M.W., and Kuhn L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA 93 (1996) 8175-8182
29. Hlavacek W.S., and Savageau M.A. Subunit structure of regulator proteins influences the design of gene circuitry: analysis of perfectly coupled and completely uncoupled circuits. J. Mol. Biol. 248 (1995) 739-755
30. Hoffmann A., Levchenko A., Scott M., and Baltimore D. The Ikappa B-NF-kappa B signaling module: temporal control and selective gene activation. Science 298 5596 (2002) 1241-1245
31. Howell D. Statistical Methods for Psychology (1987), Duxbury Press, Boston
32. Huse M., Lillemeier B.R., Kuhns M., Chen D., and Davis M. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7 3 (2006) 247-255
33. Irvine D. The method of controlled mathematical comparison. In: Voit E. (Ed). Canonical Nonlinear Modeling. S-System Approach to Understanding Complexity (1991), Van Nostrand Reinhold, New York 90-109
34. Kakhlon O., Gruenbaum Y., and Cabantchik Z. Repression of ferritin expression increases the labile iron pool, oxidative stress, and short-term growth of human erythroleukemia cells. Blood 97 9 (2001) 2863-2871
35. Kim S., and Ponka P. Role of nitric oxide in cellular iron metabolism. Biometals 16 (2003) 125-135
36. Lorsbach R.B., Murphy W.J., Lowenstein C.J., Snyder S.H., and Russell S.W. Expression of the nitric oxide synthase gene in mouse macrophages activated for tumor cell killing. Molecular basis for the synergy between interferon-gamma and lipopolysaccharide. J. Biol. Chem. 268 (1993) 1908-1913
37. Manca C., Tsenova L., Barry C., Bergtold A., Freeman S., Haslett P., Musser J., Freedman V., and Kaplan G. Mycobacterium tuberculosis CDC1551 induces a more vigorous host response in vivo and in vitro, but is not more virulent than other clinical isolates. J. Immunol. 162 11 (1999) 6740-6746
38. McKay M.D., Conover W.J., and Beckman R.J. A comparison of three methods of selecting values of input variables in the analysis of output from a computer code. Technometrics 21 (1979) 239-245
39. 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
40. Miller R., and Britigan B. Role of oxidants in microbial pathophysiology. Clin. Microbiol. Rev. 10 1 (1997) 1-18
41. Nathan C., and Shiloh M.U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97 (2000) 8841-8848
42. Nathan C.F., Murray H.W., Wiebe M.E., and Rubin B.Y. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158 3 (1983) 670-689
43. Nigou J., Vercellone A., and Puzo G. New structural insights into the molecular deciphering of mycobacterial lipoglycan binding to C-type lectins: lipoarabinomannan glycoform characterization and quantification by capillary electrophoresis at the subnanomole level. J. Mol. Biol. 299 5 (2000) 1353-1362
44. Ohno H., Zhu G., Mohan V., Chu D., Kohno S., Jacobs W., and Chan J. The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell Microbiol. 5 9 (2003) 637-648
45. Olakanmi O., Schlesinger L.S., Ahmed A., and Britigan B.E. Intraphagosomal Mycobacterium tuberculosis acquires iron from both extracellular transferrin and intracellular iron pools. Impact of interferon-gamma and hemochromatosis. J. Biol. Chem. 277 (2002) 49727-49734
46. Paul S., Laochumroonvoranpong P., and Kaplan G. Comparable growth rates of virulent and avirulent Mycobacterium tuberculosis in human macrophages in vitro. J. Infect. Dis. 177 (1996) 1723
47. Raghu B., Sarma G.R., and Venkatesan P. Effect of iron on the growth and siderophore production of mycobacteria. Biochem. Mol. Biol. Int. 31 (1993) 341-348
48. Ray J.C.J., and Kirschner D.E. Requirement for multiple activation signals by anti-inflammatory feedback in macrophages. J. Theor. Biol. 241 2 (2006) 276-294
49. Rook G., Steele J., Ainsworth M., and Champion B. Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant gamma-interferon on human monocytes and murine peritoneal macrophages. Immunology 59 3 (1986) 333-338
50. Ruan J., John G.S., Ehrt S., Riley L., and Nathan C. noxR3, a novel gene from Mycobacterium tuberculosis, protects Salmonella typhimurium from nitrosative and oxidative stress. Infect. Immun. 67 (1999) 3276-3283
51. Sato K., Akaki T., and Tomioka H. Differential potentiation of anti-mycobacterial activity and reactive nitrogen intermediate-producing ability of murine peritoneal macrophages activated by interferon-gamma (IFN-gamma) and tumour necrosis factor-alpha (TNF-alpha). Clin. Exp. Immunol. 112 (1998) 63-68
52. Savageau, M.A., 1996. Power-law formalism: a canonical nonlinear approach to modeling and analysis. In: Proceedings of World Congress of Nonlinear Analysts 92. vol. 4, pp. 3323-3334.
53. Savageau M.A. Design principles for elementary gene circuits: elements, methods, and examples. Chaos 11 (2001) 142-159
54. Savageau M.A. Alternative designs for a genetic switch: analysis of switching times using the piecewise power-law representation. Math. Biosci. 180 (2002) 237-253
55. Schaible U.E., and Kaufmann S.H.E. Iron and microbial infection. Nat. Rev. Microbiol. 2 12 (2004) 946-953
56. Schwacke J., and Voit E. Improved methods for the mathematically controlled comparison of biochemical systems. Theor. Biol. Med. Model 1 (2004) 1
57. Shaffer J.P. Multiple hypothesis testing. Ann. Rev. Psych. 46 (1995) 561-584
58. Shaughnessy L.M., and Swanson J.A. The role of the activated macrophage in clearing Listeria monocytogenes infection. Front Biosci. 12 (2007) 2683-2692
59. Silver R., Li Q., and Ellner J. Expression of virulence of Mycobacterium tuberculosis within human monocytes: virulence correlates with intracellular growth and induction of tumor necrosis factor alpha but not with evasion of lymphocyte-dependent monocyte effector functions. Infect. Immun. 66 3 (1998) 1190-1199
60. Springer B., Master S., Sander P., Zahrt T., McFalone M., Song J., Papavinasasundaram K.G., Colston M.J., Boettger E., and Deretic V. Silencing of oxidative stress response in Mycobacterium tuberculosis: expression patterns of ahpC in virulent and avirulent strains and effect of ahpC inactivation. Infect. Immun. 69 (2001) 5967-5973
61. Voskuil M., Visconti K., and Schoolnik G. Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 84 3/4 (2004) 218-227
62. Weiss G., Werner-Felmayer G., Werner E.R., Grunewald K., Wachter H., and Hentze M.W. Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J. Exp. Med. 180 (1994) 969-976
63. Yu K., Mitchell C., Xing Y., Magliozzo R.S., Bloom B.R., and Chan J. Toxicity of nitrogen oxides and related oxidants on mycobacteria: M. tuberculosis is resistant to peroxynitrite anion. Tuberc. Lung. Dis. 79 4 (1999) 191-198
64. Zhang M., Gong J., Lin Y., and Barnes P. Growth of virulent and avirulent Mycobacterium tuberculosis strains in human macrophages. Infect. Immun. 66 2 (1998) 794-799