Multi-Scale Modeling Predicts a Balance of Tumor Necrosis Factor-α and Interleukin-10 Controls the Granuloma Environment during Mycobacterium tuberculosis Infection

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Cilfone, Nicholas A ^a   Perry, Cory R ^b   Kirschner, Denise E ^b   Linderman, Jennifer J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; BACTERIAL LOAD; CELL AGGREGATION; COMPUTER MODEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GRANULOMA; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; MACROPHAGE ACTIVATION; MATHEMATICAL MODEL; MYCOBACTERIUM TUBERCULOSIS; OUTCOME ASSESSMENT; PROCESS CONTROL; SIGNAL TRANSDUCTION; SPATIAL ANALYSIS; TUBERCULOSIS;

COMPUTATIONAL BIOLOGY; GRANULOMA; HUMANS; INTERLEUKIN-10; MACROPHAGES; MODELS, THEORETICAL; MYCOBACTERIUM TUBERCULOSIS; SIGNAL TRANSDUCTION; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84880273351     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068680     Document Type: Article

References (113)

1. Comas I, Gagneux S, (2009) The past and future of tuberculosis research. PLoS pathogens 5: e1000600 doi:10.1371/journal.ppat.1000600.
2. Daley CL, (2010) Update in tuberculosis 2009. American journal of respiratory and critical care medicine 181: 550-555 doi:10.1164/rccm.201001-0140UP.
3. Flynn JL, (2004) Immunology of tuberculosis and implications in vaccine development. Tuberculosis 84: 93-101 doi:10.1016/j.tube.2003.08.010.
4. Flynn JL, Chan J, (2001) Immunology of tuberculosis. Annual review of immunology 19: 93-129 doi:10.1146/annurev.immunol.19.1.93.
5. Gideon HP, Flynn JL, (2011) Latent tuberculosis: what the host "sees"? Immunologic research 50: 202-212 doi:10.1007/s12026-011-8229-7.
6. Ford CB, Lin PL, Chase MR, Shah RR, Iartchouk O, et al. (2011) Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nature genetics 43: 482-486 doi:10.1038/ng.811.
7. Davis JM, Ramakrishnan L, (2008) "The very pulse of the machine": the tuberculous granuloma in motion. Immunity 28: 146-148 doi:10.1016/j.immuni.2008.01.002.
8. Tsai MC, Chakravarty S, Zhu G, Xu J, Tanaka K, et al. (2006) Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cellular Microbiology 8: 218-232 doi:10.1111/j.1462-5822.2005.00612.x.
9. Lin PL, Pawar S, Myers A, Pegu A, Fuhrman C, et al. (2006) Early events in Mycobacterium tuberculosis infection in cynomolgus macaques. Infection and immunity 74: 3790-3803 doi:10.1128/IAI.00064-06.
10. Flynn JL, (2006) Lessons from experimental Mycobacterium tuberculosis infections. Microbes and infection/Institut Pasteur 8: 1179-1188 doi:10.1016/j.micinf.2005.10.033.
11. Ramakrishnan L, (2012) Revisiting the role of the granuloma in tuberculosis. Nature reviews Immunology 12: 352-366 doi:10.1038/nri3211.
12. Russell DG, Barry CE, Flynn JL, (2010) Tuberculosis: what we don't know can, and does, hurt us. Science (New York, NY) 328: 852-856 doi:10.1126/science.1184784.
13. Fallahi-Sichani M, El-Kebir M, Marino S, Kirschner DE, Linderman JJ, (2011) Multiscale computational modeling reveals a critical role for TNF-α receptor 1 dynamics in tuberculosis granuloma formation. Journal of immunology (Baltimore, Md: 1950) 186: 3472-3483 doi:10.4049/jimmunol.1003299.
14. Ray JCJ, Flynn JL, Kirschner DE, (2009) Synergy between individual TNF-dependent functions determines granuloma performance for controlling Mycobacterium tuberculosis infection. Journal of immunology (Baltimore, Md: 1950) 182: 3706-3717 doi:10.4049/jimmunol.0802297.
15. Algood HMS, Lin PL, Yankura D, Jones A, Chan J, et al. (2004) TNF influences chemokine expression of macrophages in vitro and that of CD11b+ cells in vivo during Mycobacterium tuberculosis infection. Journal of immunology (Baltimore, Md: 1950) 172: 6846-6857.
16. Lin PL, Flynn JL, (2010) Understanding latent tuberculosis: a moving target. Journal of immunology (Baltimore, Md: 1950) 185: 15-22 doi:10.4049/jimmunol.0903856.
17. 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.
18. Egen JG, Rothfuchs AG, Feng CG, Winter N, Sher A, et al. (2008) Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 28: 271-284 doi:10.1016/j.immuni.2007.12.010.
19. Davis JM, Ramakrishnan L, (2009) The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136: 37-49 doi:10.1016/j.cell.2008.11.014.
20. Redford P, Murray P, O'Garra A, (2011) The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal immunology 4: 1-10 doi:10.1038/mi.2011.7.
21. Saraiva M, O'Garra A, (2010) The regulation of IL-10 production by immune cells. Nature Reviews Immunology 10: 170-181 doi:10.1038/nri2711.
22. O'Garra A, Vieira P, Vieira P, Goldfeld AE, (2004) IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. Journal of Clinical Investigation 114: 1-7 doi:10.1172/JCI200423215.1372.
23. Cyktor JC, Turner J (2011) IL-10 and Immunity Against Prokaryotic and Eukaryotic Intracellular Pathogens. Infection and immunity. doi:10.1128/IAI.00047-11.
24. O'Garra A, Barrat F, Castro A, (2008) Strategies for use of IL-10 or its antagonists in human disease. Immunological Reviews 223: 114-131.
25. Duell BL, Tan CK, Carey AJ, Wu F, Cripps AW,et al. (2012) Recent insights into microbial triggers of interleukin-10 production in the host and the impact on infectious disease pathogenesis. FEMS immunology and medical microbiology. doi:10.1111/j.1574-695X.2012.00931.x.
26. Moore KW, De Waal Malefyt R, Coffman RL, O'Garra A, (2001) Interleukin-10 and the interleukin-10 receptor. Annual review of immunology 1: 683-765.
27. Redpath S, Ghazal P, Gascoigne NR, (2001) Hijacking and exploitation of IL-10 by intracellular pathogens. Trends in microbiology 9: 86-92.
28. Roncarolo MG, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK, (2006) Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunological Reviews 212: 28-50 doi:10.1111/j.0105-2896.2006.00420.x.
29. Mosser D, Zhang X (2008) Interleukin-10: new perspectives on an old cytokine. Immunological reviews: 205-218.
30. Fickenscher H, Hör S, Küpers H, Knappe A, Wittmann S, et al. (2002) The interleukin-10 family of cytokines. Trends in Immunology 23: 89-96.
31. Mege J, Meghari S, Honstettre A, Capo C, Raoult D, (2006) The two faces of interleukin 10 in human infectious diseases. Lancet Infectious Disease 6: 557-569.
32. Ouyang W, Rutz S, Crellin NK, Valdez P, Hymowitz SG, (2011) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annual review of immunology 29: 71-109 doi:10.1146/annurev-immunol-031210-101312.
33. Bouabe H, Liu Y, Moser M, Bösl MR, Heesemann J, (2011) Novel Highly Sensitive IL-10-{beta}-Lactamase Reporter Mouse Reveals Cells of the Innate Immune System as a Substantial Source of IL-10 In Vivo. Journal of immunology (Baltimore, Md: 1950) 187: 3165-3176 doi:10.4049/jimmunol.1101477.
34. Yssel H, De Waal Malefyt R, Roncarolo MG, Abrams JS, Lahesmaa R, et al. (1992) IL-10 is produced by subsets of human CD4+ T cell clones and peripheral blood T cells. Journal of immunology (Baltimore, Md: 1950) 149: 2378-2384.
35. Smallie T, Ricchetti G, Horwood NJ, Feldmann M, Clark AR, et al. (2010) IL-10 inhibits transcription elongation of the human TNF gene in primary macrophages. The Journal of experimental medicine 207: 2081-2088 doi:10.1084/jem.20100414.
36. Balcewicz-Sablinska M, Gan H, Remold HG, (1999) Interleukin 10 produced by macrophages inoculated with Mycobacterium avium attenuates mycobacteria-induced apoptosis by reduction of TNF-α activity. The Journal of Infectious Diseases 180: 1230-1237.
37. Brennan FM, Green P, Amjadi P, Robertshaw HJ, Alvarez-Iglesias M, et al. (2008) Interleukin-10 regulates TNF-α-converting enzyme (TACE/ADAM17) involving a TIMP3 dependent and independent mechanism. European Journal of Immunology 38: 1106-1117 doi:10.1002/eji.200737821.
38. Dagvadorj J, Naiki Y, Tumurkhuu G, Hassan F, Islam S, et al. (2008) Interleukin-10 inhibits tumor necrosis factor-alpha production in lipopolysaccharide-stimulated RAW 264.7 cells through reduced MyD88 expression. Innate Immunity 14: 109-115 doi:10.1177/1753425908089618.
39. Murray PJ, (2005) The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proceedings of the National Academy of Sciences 102: 8686-8691 doi:10.1073/pnas.0500419102.
40. Lang R, Patel D, Morris JJ, Rutschman RL, Murray PJ, (2002) Shaping gene expression in activated and resting primary macrophages by IL-10. Journal of immunology (Baltimore, Md: 1950) 169: 2253-2263.
41. Denys A, Udalova IA, Smith C, Williams LM, Ciesielski CJ, et al. (2002) Evidence for a dual mechanism for IL-10 suppression of TNF-alpha production that does not involve inhibition of p38 mitogen-activated protein kinase or NF-kappa B in primary human macrophages. The Journal of Immunology 168: 4837-4845.
42. Bogdan C, Vodovotz Y, Nathan C (1991) Macrophage Deactivation by Interleukin 10. The Journal of Experimental Medicine 174.
43. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A, (1991) IL-10 inhibits cytokine production by activated macrophages. The Journal of Immunolgy 147: 3815-3822.
44. Agbanoma G, Li C, Ennis D, Palfreeman AC, Williams LM, et al. (2012) Production of TNF-α in macrophages activated by T cells, compared with lipopolysaccharide, uses distinct IL-10-dependent regulatory mechanism. Journal of immunology (Baltimore, Md: 1950) 188: 1307-1317 doi:10.4049/jimmunol.1100625.
45. Hosokawa Y, Hosokawa I, Ozaki K, Nakae H, Matsuo T, (2009) Cytokines differentially regulate CXCL10 production by interferon-gamma-stimulated or tumor necrosis factor-alpha-stimulated human gingival fibroblasts. Journal of periodontal research 44: 225-231 doi:10.1111/j.1600-0765.2008.01124.x.
46. Ikeda T, Sato K, Kuwada N, Matsumura T, Yamashita T, et al. (2002) Interleukin-10 differently regulates monocyte chemoattractant protein-1 gene expression depending on the environment in a human monoblastic cell line, UG3. Journal of leukocyte biology 72: 1198-1205.
47. Cheeran MC-J, Hu S, Sheng WS, Peterson PK, Lokensgard JR, (2003) CXCL10 production from cytomegalovirus-stimulated microglia is regulated by both human and viral interleukin-10. Journal of virology 77: 4502-4515 doi:10.1128/JVI.77.8.4502.
48. Marfaing-Koka A, Maravic M, Humbert M, Galanaud P, Emilie D, (1996) Contrasting effects of IL-4, IL-10 and corticosteroids on RANTES production by human monocytes. International immunology 8: 1587-1594.
49. Tang Q, Bluestone J, (2008) The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nature immunology 9: 239-244 doi:10.1038/ni1572.
50. Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, et al. (2008) Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28: 546-558 doi:10.1016/j.immuni.2008.02.017.
51. Shevach EM, (2009) Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 30: 636-645 doi:10.1016/j.immuni.2009.04.010.
52. Higgins DM, Sanchez-Campillo J, Rosas-Taraco AG, Lee EJ, Orme IM, et al. (2009) Lack of IL-10 alters inflammatory and immune responses during pulmonary Mycobacterium tuberculosis infection. Tuberculosis (Edinburgh, Scotland) 89: 149-157 doi:10.1016/j.tube.2009.01.001.
53. Shaler CR, Kugathasan K, McCormick S, Damjanovic D, Horvath C, et al. (2011) Pulmonary mycobacterial granuloma increased IL-10 production contributes to establishing a symbiotic host-microbe microenvironment. The American journal of pathology 178: 1622-1634 doi:10.1016/j.ajpath.2010.12.022.
54. Pitt JM, Stavropoulos E, Redford PS, Beebe AM, Bancroft GJ, et al. (2012) Blockade of IL-10 signaling during bacillus Calmette-Guérin vaccination enhances and sustains Th1, Th17, and innate lymphoid IFN-γ and IL-17 responses and increases protection to Mycobacterium tuberculosis infection. Journal of immunology (Baltimore, Md: 1950) 189: 4079-4087 doi:10.4049/jimmunol.1201061.
55. Turner J, Gonzalez-Juarrero M, Ellis DL, Basaraba RJ, Kipnis A, et al. (2002) In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice. Journal of immunology (Baltimore, Md: 1950) 169: 6343-6351.
56. Beamer GL, Flaherty DK, Assogba BD, Stromberg P, Gonzalez-Juarrero M, et al. (2008) Interleukin-10 promotes Mycobacterium tuberculosis disease progression in CBA/J mice. Journal of immunology (Baltimore, Md: 1950) 181: 5545-5550.
57. Redford PS, Boonstra A, Read S, Pitt J, Graham C, et al. (2010) Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. European journal of immunology 40: 2200-2210 doi:10.1002/eji.201040433.
58. Junqueira-Kipnis AP, Kipnis A, Henao Tamayo M, Harton M, Gonzalez Juarrero M, et al. (2005) Interleukin-10 production by lung macrophages in CBA xid mutant mice infected with Mycobacterium tuberculosis. Immunology 115: 246-252 doi:10.1111/j.1365-2567.2005.02136.x.
59. Roach DR, Martin E, Bean AG, Rennick DM, Briscoe H, et al. (2001) Endogenous inhibition of antimycobacterial immunity by IL-10 varies between mycobacterial species. Scandinavian journal of immunology 54: 163-170.
60. North RJ, (1998) Mice incapable of making IL-4 or IL-10 display normal resistance to infection with Mycobacterium tuberculosis. Clinical and Experimental Immunology 113: 55-58 doi:10.1046/j.1365-2249.1998.00636.x.
61. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, et al. (2006) Interleukin-10 determines viral clearance or persistence in vivo. Nature medicine 12: 1301-1309 doi:10.1038/nm1492.
62. Jung Y-J, Ryan L, LaCourse R, North RJ, (2003) Increased interleukin-10 expression is not responsible for failure of T helper 1 immunity to resolve airborne Mycobacterium tuberculosis infection in mice. Immunology 109: 295-299.
63. Wigginton JE, Kirschner D, (2001) A model to predict cell-mediated immune regulatory mechanisms during human infection with Mycobacterium tuberculosis. Journal of immunology (Baltimore, Md: 1950) 166: 1951-1967.
64. Marino S, Myers A, Flynn JL, Kirschner DE, (2010) TNF and IL-10 are major factors in modulation of the phagocytic cell environment in lung and lymph node in tuberculosis: a next-generation two-compartmental model. Journal of theoretical biology 265: 586-598 doi:10.1016/j.jtbi.2010.05.012.
65. Saunders BM, Briscoe H, Britton WJ, (2004) T cell-derived tumour necrosis factor is essential, but not sufficient, for protection against Mycobacterium tuberculosis infection. Clinical and experimental immunology 137: 279-287 doi:10.1111/j.1365-2249.2004.02518.x.
66. Harris J, Hope JC, Keane J, (2008) Tumor necrosis factor blockers influence macrophage responses to Mycobacterium tuberculosis. The Journal of infectious diseases 198: 1842-1850 doi:10.1086/593174.
67. Gutierrez MG, Mishra BB, Jordao L, Elliott E, Anes E, et al. (2008) NF-kappa B activation controls phagolysosome fusion-mediated killing of mycobacteria by macrophages. Journal of immunology (Baltimore, Md: 1950) 181: 2651-2663.
68. Mosser DM, Edwards JP, (2008) Exploring the full spectrum of macrophage activation. Nature reviews Immunology 8: 958-969 doi:10.1038/nri2448.
69. Tay S, Hughey JJ, Lee TK, Lipniacki T, Quake SR, et al. (2010) Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 466: 267-271 doi:10.1038/nature09145.
70. Wajant H, Pfizenmaier K, Scheurich P, (2003) Tumor necrosis factor signaling. Cell death and differentiation 10: 45-65 doi:10.1038/sj.cdd.4401189.
71. Zhou Z, Connell MC, MacEwan DJ, (2007) TNFR1-induced NF-kappaB, but not ERK, p38MAPK or JNK activation, mediates TNF-induced ICAM-1 and VCAM-1 expression on endothelial cells. Cellular signalling 19: 1238-1248 doi:10.1016/j.cellsig.2006.12.013.
72. Keane J, Shurtleff B, Kornfeld H, (2002) TNF-dependent BALB/c murine macrophage apoptosis following Mycobacterium tuberculosis infection inhibits bacillary growth in an IFN-gamma independent manner. Tuberculosis (Edinburgh, Scotland) 82: 55-61 doi:10.1054/tube.322.
73. Wanidworanun C, Strober W, (1993) Predominant role of tumor necrosis factor-alpha in human monocyte IL-10 synthesis. Journal of immunology (Baltimore, Md: 1950) 151: 6853-6861.
74. Flynn JL, Chan J, Lin PL, (2011) Macrophages and control of granulomatous inflammation in tuberculosis. Mucosal immunology 4: 271-278 doi:10.1038/mi.2011.14.
75. Platzer C, Meisel C, Vogt K, Platzer M, Volk HD, (1995) Up-regulation of monocytic IL-10 by tumor necrosis factor-alpha and cAMP elevating drugs. International immunology 7: 517-523.
76. 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. Infection and immunity 76: 916-926 doi:10.1128/IAI.01011-07.
77. Lin PL, Myers A, Smith L, Bigbee C, Bigbee M, et al. (2010) Tumor necrosis factor neutralization results in disseminated disease in acute and latent Mycobacterium tuberculosis infection with normal granuloma structure in a cynomolgus macaque model. Arthritis and rheumatism 62: 340-350 doi:10.1002/art.27271.
78. Fallahi-Sichani M, Kirschner DE, Linderman JJ, (2012) NF-κB Signaling Dynamics Play a Key Role in Infection Control in Tuberculosis. Frontiers in physiology 3: 170 doi:10.3389/fphys.2012.00170.
79. Fallahi-Sichani M, Flynn JL, Linderman JJ, Kirschner DE, (2012) Differential Risk of Tuberculosis Reactivation among Anti-TNF Therapies Is Due to Drug Binding Kinetics and Permeability. Journal of immunology (Baltimore, Md: 1950) 188: 3169-3178 doi:10.4049/jimmunol.1103298.
80. Fallahi-Sichani M, Schaller MA, Kirschner DE, Kunkel SL, Linderman JJ, (2010) Identification of key processes that control tumor necrosis factor availability in a tuberculosis granuloma. PLoS computational biology 6: e1000778 doi:10.1371/journal.pcbi.1000778.
81. Wallis RS, (2009) Infectious complications of tumor necrosis factor blockade. Current opinion in infectious diseases 22: 403-409 doi:10.1097/QCO.0b013e32832dda55.
82. Wallis RS, (2008) Tumour necrosis factor antagonists: structure, function, and tuberculosis risks. The Lancet infectious diseases 8: 601-611 doi:10.1016/S1473-3099(08)70227-5.
83. Lucas TA, (2008) Operator Splitting for an Immunology Model Using Reaction-Diffusion Equations with Stochastic Source Terms. SIAM Journal on Numerical Analysis 46: 3113-3135 doi:10.1137/070701595.
84. Guo Z, Sloot PM, Tay JC, (2008) A hybrid agent-based approach for modeling microbiological systems. Journal of theoretical biology 255: 163-175 doi:10.1016/j.jtbi.2008.08.008.
85. Ma J, Chen T, Mandelin J, Ceponis A, Miller NE, et al. (2003) Regulation of macrophage activation. Cellular and molecular life sciences: CMLS 60: 2334-2346 doi:10.1007/s00018-003-3020-0.
86. Theus SA, Cave MD, Eisenach KD, (2005) Intracellular macrophage growth rates and cytokine profiles of Mycobacterium tuberculosis strains with different transmission dynamics. The Journal of infectious diseases 191: 453-460 doi:10.1086/425936.
87. Grosset J, (2003) Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary. Antimicrobial agents and chemotherapy 47: 833-836 doi:10.1128/AAC.47.3.833.
88. Vesosky B, Rottinghaus EK, Stromberg P, Turner J, Beamer G, (2010) CCL5 participates in early protection against Mycobacterium tuberculosis. Journal of leukocyte biology 87: 1153-1165 doi:10.1189/jlb.1109742.
89. Algood HMS, Flynn JL, (2004) CCR5-deficient mice control Mycobacterium tuberculosis infection despite increased pulmonary lymphocytic infiltration. Journal of immunology (Baltimore, Md: 1950) 173: 3287-3296.
90. Chabot V, Reverdiau P, Iochmann S, Rico A, Sénécal D, et al. (2006) CCL5-enhanced human immature dendritic cell migration through the basement membrane in vitro depends on matrix metalloproteinase-9. Journal of leukocyte biology 79: 767-778 doi:10.1189/jlb.0804464.
91. Wu K, Koo J, Jiang X, Chen R, Cohen SN, et al. (2012) Improved control of tuberculosis and activation of macrophages in mice lacking protein kinase R. PloS one. 7: e30512 doi:10.1371/journal.pone.0030512.
92. Giacomini E, Iona E, Ferroni L, Miettinen M, Fattorini L, et al. (2001) Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. Journal of immunology (Baltimore, Md: 1950) 166: 7033-7041.
93. Meyaard L, Hovenkamp E, Otto SA, Miedema F, (1996) IL-12-induced IL-10 production by human T cells as a negative feedback for IL-12-induced immune responses. Journal of immunology (Baltimore, Md: 1950) 156: 2776-2782.
94. Orme IM, Roberts AD, Griffin JP, Abrams JS, (1993) Cytokine secretion by CD4 T lymphocytes acquired in response to Mycobacterium tuberculosis infection. Journal of immunology (Baltimore, Md: 1950) 151: 518-525.
95. Shaw TC, Thomas LH, Friedland JS, (2000) Regulation of IL-10 secretion after phagocytosis of Mycobacterium tuberculosis by human monocytic cells. Cytokine 12: 483-486 doi:10.1006/cyto.1999.0586.
96. Tan JC, Indelicato SR, Narula SK, Zavodny PJ, Chou CC, (1993) Characterization of interleukin-10 receptors on human and mouse cells. The Journal of biological chemistry 268: 21053-21059.
97. Weber-Nordt RM, Meraz MA, Schreiber RD, (1994) Lipopolysaccharide-dependent induction of IL-10 receptor expression on murine fibroblasts. Journal of immunology (Baltimore, Md: 1950) 153: 3734-3744.
98. Figueiredo AS, Höfer T, Klotz C, Sers C, Hartmann S, et al. (2009) Modelling and simulating interleukin-10 production and regulation by macrophages after stimulation with an immunomodulator of parasitic nematodes. The FEBS journal 276: 3454-3469 doi:10.1111/j.1742-4658.2009.07068.x.
99. Moya C, Huang Z, Cheng P, Jayaraman A, Hahn J, (2011) Investigation of IL-6 and IL-10 signalling via mathematical modelling. IET systems biology 5: 15 doi:10.1049/iet-syb.2009.0060.
100. Lauffenburger DA, Linderman JJ (1993) Receptors: Models For Binding, Trafficking, and Signaling New York: Oxford University Press.
101. Wei SH-Y, Ming-Lum A, Liu Y, Wallach D, Ong CJ, et al. (2006) Proteasome-mediated proteolysis of the interleukin-10 receptor is important for signal downregulation. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research 26: 281-290 doi:10.1089/jir.2006.26.281.
102. Fallahi-Sichani M, Flynn JL, Linderman JJ, Kirschner DE, (2012) Differential risk of tuberculosis reactivation among anti-TNF therapies is due to drug binding kinetics and permeability. Journal of immunology (Baltimore, Md: 1950) 188: 3169-3178 doi:10.4049/jimmunol.1103298.
103. Schreiber T, Ehlers S, Heitmann L, Rausch A, Mages J, et al. (2009) Autocrine IL-10 induces hallmarks of alternative activation in macrophages and suppresses antituberculosis effector mechanisms without compromising T cell immunity. Journal of immunology (Baltimore, Md: 1950) 183: 1301-1312 doi:10.4049/jimmunol.0803567.
104. Verreck FAW, De Boer T, Langenberg DML, Hoeve MA, Kramer M, et al. (2004) Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proceedings of the National Academy of Sciences of the United States of America 101: 4560-4565 doi:10.1073/pnas.0400983101.
105. Joyce DA, Gibbons DP, Green P, Steer JH, Feldmann M, et al. (1994) Two inhibitors of pro-inflammatory cytokine release, interleukin-10 and interleukin-4, have contrasting effects on release of soluble p75 tumor necrosis factor receptor by cultured monocytes. European journal of immunology 24: 2699-2705 doi:10.1002/eji.1830241119.
106. Hart PH, Hunt EK, Bonder CS, Watson CJ, Finlay-Jones JJ, (1996) Regulation of surface and soluble TNF receptor expression on human monocytes and synovial fluid macrophages by IL-4 and IL-10. Journal of immunology (Baltimore, Md: 1950) 157: 3672-3680.
107. Barakat HZ, Clark JA, (1966) On the Solution of the Diffusion Equations by Numerical Methods. Journal of Heat Transfer 88: 421-427.
108. Marino S, Hogue IB, Ray CJ, Kirschner DE, (2008) A methodology for performing global uncertainty and sensitivity analysis in systems biology. Journal of theoretical biology 254: 178-196 doi:10.1016/j.jtbi.2008.04.011.
109. Marino S, El-Kebir M, Kirschner D, (2011) A hybrid multi-compartment model of granuloma formation and T cell priming in tuberculosis. Journal of theoretical biology 280: 50-62 doi:10.1016/j.jtbi.2011.03.022.
110. Bird RB, Stewart WE, Lightfoot EN (1994) Transport Phenomena. New York: John Wiley & Sons.
111. Riley JK, Takeda K, Akira S, Schreiber RD, (1999) Interleukin-10 Receptor Signaling through the JAK-STAT Pathway. 274: 16513-16521.
112. Dannenberg AM, (1989) Immune mechanisms in the pathogenesis of pulmonary tuberculosis. Reviews of Infectious Diseases 11Suppl 2: S369-78.
113. Newton SM, Smith RJ, Wilkinson KA, Nicol MP, Garton NJ, et al. (2006) A deletion defining a common Asian lineage of Mycobacterium tuberculosis associates with immune subversion. Proceedings of the National Academy of Sciences of the United States of America 103: 15594-15598 doi:10.1073/pnas.0604283103.