Functional complexity of the Leishmania granuloma and the potential of in silico modeling

Frontiers in Immunology

Volumn 4, Issue FRB, 2013, Pages

  Moore, John W J ^a   Moyo, Daniel ^a   Beattie, Lynette ^a   Andrews, Paul S ^a   Timmis, Jon ^a   Kaye, Paul M ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Granuloma; Imaging; In silico modeling; Inflammation; Leishmaniasis; Visceral

Indexed keywords

CD8 ANTIGEN; COMPLEMENT RECEPTOR;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INTERACTION; CELL MATURATION; COMPUTER MODEL; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; IMMUNITY; INFLAMMATION; KUPFFER CELL; LEISHMANIA DONOVANI; LEISHMANIASIS; LIVER GRANULOMA; MACROPHAGE; MONOCYTE; NATURAL KILLER T CELL; NONHUMAN; PARASITE LOAD; REGULATORY T LYMPHOCYTE; SHORT SURVEY; TISSUE INJURY;

EID: 84883665528     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00035     Document Type: Short Survey

References (66)

1. An, G., and Christley, S. (2012). Addressing the translational dilemma: dynamic knowledge representation of inflammation using agent-based modeling. Crit. Rev. Biomed. Eng. 40, 323-340.
2. + T cells. PLoS Pathog. 6:e1000805. doi: 10.1371/journal.ppat.1000805
3. Beattie, L., Svensson, M., Bune, A., Brown, N., Maroof, A., Zubairi, S., et al. (2010b). Leishmania donovani-induced expression of signal regulatory protein alpha on Kupffer cells enhances hepatic invariant NKT-cell activation. Eur. J. Immunol. 40, 117-123.
4. Brown, B. N., Price, I. M., Toapanta, F. R., DeAlmeida, D. R., Wiley, C. A., Ross, T. M., et al. (2011). An agent-based model of inflammation and fibrosis following particulate exposure in the lung. Math. Biosci. 231, 186-196.
5. Cervia, J. S., Rosen, H., and Murray, H. W. (1993). Effector role of blood monocytes in experimental visceral leishmaniasis. Infect. Immun. 61, 1330-1333.
6. Curry, A. J., and Kaye, P. M. (1992). Recombinant interleukin-1 alpha augments granuloma formation and cytokine production but not parasite clearance in mice infected with Leishmania donovani. Infect. Immun. 60, 4422-4426.
7. Davis, J. M., and Ramakrishnan, L. (2009). The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136, 37-49.
8. Deak, E., Jayakumar, A., Cho, K. W., Goldsmith-Pestana, K., Dondji, B., Lambris, J. D., et al. (2010). Murine visceral leishmaniasis: IgM and polyclonal B-cell activation lead to disease exacerbation. Eur. J. Immunol. 40, 1355-1368.
9. Dong, X., Foteinou, P. T., Calvano, S. E., Lowry, S. F., and Androulakis, I. P. (2010). Agent-based modeling of endotoxin-induced acute inflammatory response in human blood leukocytes. PLoS ONE 5:e9249. doi: 10.1371/journal.pone.0009249
10. Duarte, M. I., de Andrade, H. F. Jr., Takamura, C. F., Sesso, A., and Tuon, F. F. (2009). TGF-beta and mesenchymal hepatic involvement after visceral leishmaniasis. Parasitol. Res. 104, 1129-1136.
11. Egen, J. G., Rothfuchs, A. G., Feng, C. G., Horwitz, M. A., Sher, A., and Germain, R. N. (2011). Intravital imaging reveals limited antigen presentation and T cell effector function in mycobacterial granulomas. Immunity 34, 807-819.
12. Egen, J. G., Rothfuchs, A. G., Feng, C. G., Winter, N., Sher, A., and Germain, R. N. (2008). Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 28, 271-284.
13. El Hag, I. A., Hashim, F. A., el Toum, I. A., Homeida, M., el Kalifa, M., and el Hassan, A. M. (1994). Liver morphology and function in visceral leishmaniasis (Kala-azar). J. Clin. Pathol. 47, 547-551.
14. Engwerda, C. R., Ato, M., Stager, S., Alexander, C. E., Stanley, A. C., and Kaye, P. M. (2004). Distinct roles for lymphotoxin-alpha and tumor necrosis factor in the control of Leishmania donovani infection. Am. J. Pathol. 165, 2123-2133.
15. Fallahi-Sichani, M., El-Kebir, M., Marino, S., Kirschner, D. E., and Linderman, J. J. (2011). Multiscale computational modeling reveals a critical role for TNF-alpha receptor 1 dynamics in tuberculosis granuloma formation. J. Immunol. 186, 3472-3483.
16. Fallahi-Sichani, M., Schaller, M. A., Kirschner, D. E., Kunkel, S. L., and Linderman, J. J. (2010). Identification of key processes that control tumor necrosis factor availability in a tuberculosis granuloma. PLoS Comput. Biol. 6:e1000778. doi: 10.1371/journal.pcbi.1000778
17. Flugge, A. J., Timmis, J., Andrews, P., Moore, J., and Kaye, P. (2009). "Modelling and simulation of granuloma formation in visceral leishmaniasis," in 2009 IEEE Congress on Evolutionary Computation (CEC), Trondheim, 3052-3059.
18. Gammack, D., Ganguli, S., Marino, S., Segovia-Juarez, J., and Kirschner, D. E. (2005). Understanding the immune response in tuberculosis using different mathematical models and biological scales. Multiscale Model Simul. 3, 312-345.
19. Geissmann, F., Cameron, T. O., Sidobre, S., Manlongat, N., Kronenberg, M., Briskin, M. J., et al. (2005). Intravascular immune surveillance by CXCR6+ NKT cells patrolling liver sinusoids. PLoS Biol. 3:e113. doi: 10.1371/journal.pbio.0030113
20. Germain, R. N., Meier-Schellersheim, M., Nita-Lazar, A., and Fraser, I. D. (2011). Systems biology in immunology: a computational modeling perspective. Annu. Rev. Immunol. 29, 527-585.
21. Gressner, A. M., and Bachem, M. G. (1995). Molecular mechanisms of liver fibrogenesis - a homage to the role of activated fat-storing cells. Digestion 56, 335-346.
22. Gupta, G., Bhattacharjee, S., Bhattacharyya, S., Bhattacharya, P., Adhikari, A., Mukherjee, A., et al. (2009). CXC chemokine-mediated protection against visceral leishmaniasis: involvement of the proinflammatory response. J. Infect. Dis. 200, 1300-1310.
23. Hassan, M. F., Zhang, Y., Engwerda, C. R., Kaye, P. M., Sharp, H., and Bickle, Q. D. (2006). The Schistosoma mansoni hepatic egg granuloma provides a favorable microenvironment for sustained growth of Leishmania donovani. Am. J. Pathol. 169, 943-953.
24. Hoehme, S., Brulport, M., Bauer, A., Bedawy, E., Schormann, W., Hermes, M., et al. (2010). Prediction and validation of cell alignment along microvessels as order principle to restore tissue architecture in liver regeneration. Proc. Natl. Acad. Sci. U.S.A. 107, 10371-10376.
25. Holcombe, M., Coakley, S., and Smallwood, R. (2006). "A general framework for agent-based modelling of complex systems," in Proceedings of the 2006 European Conference on Complex Systems (Paris, France: European Complex Systems Society).
26. Kaye, P. M., Svensson, M., Ato, M., Maroof, A., Polley, R., Stager, S., et al. (2004). The immunopathology of experimental visceral leishmaniasis. Immunol. Rev. 201, 239-253.
27. Kirschner, D. E., Chang, S. T., Riggs, T. W., Perry, N., and Linderman, J. J. (2007). Toward a multiscale model of antigen presentation in immunity. Immunol. Rev. 216, 93-118.
28. Lee, W. Y., Moriarty, T. J., Wong, C. H., Zhou, H., Strieter, R. M., van Rooijen, N., et al. (2010). An intravascular immune response to Borrelia burgdorferi involves Kupffer cells and iNKT cells. Nat. Immunol. 11, 295-302.
29. Li, N. Y., Verdolini, K., Clermont, G., Mi, Q., Rubinstein, E. N., Hebda, P. A., et al. (2008). A patient-specific in silico model of inflammation and healing tested in acute vocal fold injury. PLoS ONE 3:e2789. doi: 10.1371/journal.pone.0002789
30. Marino, S., Myers, A., Flynn, J. L., and Kirschner, D. E. (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. J. Theor. Biol. 265, 586-598.
31. Marino, S., Pawar, S., Fuller, C. L., Reinhart, T. A., Flynn, J. L., and Kirschner, D. E. (2004). Dendritic cell trafficking and antigen presentation in the human immune response to Mycobacterium tuberculosis. J. Immunol. 173, 494-506.
32. Maroof, A., Beattie, L., Zubairi, S., Svensson, M., Stager, S., and Kaye, P. M. (2008). Posttranscriptional regulation of II10 gene expression allows natural killer cells to express immunoregulatory function. Immunity 29, 295-305.
33. McFarlane, E., Carter, K. C., McKenzie, A. N., Kaye, P. M., Brombacher, F., and Alexander, J. (2011). Endogenous IL-13 plays a crucial role in liver granuloma maturation during Leishmania donovani infection, independent of IL-4Ralpha-responsive macrophages and neutrophils. J. Infect. Dis. 204, 36-43.
34. Moore, J. W., Beattie, L., Dalton, J. E., Owens, B. M., Maroof, A., Coles, M. C., et al. (2012). B cell: T cell interactions occur within hepatic granulomas during experimental visceral leishmaniasis. PLoS ONE 7:e34143. doi: 10.1371/journal.pone.0034143
35. Muller, A. J., Filipe-Santos, O., Eberl, G., Aebischer, T., Spath, G. F., and Bousso, P. (2012). CD4+ T cells rely on a cytokine gradient to control intracellular pathogens beyond sites of antigen presentation. Immunity 37, 147-157.
36. Murray, H. W. (2000). Mononuclear cell recruitment, granuloma assembly, and response to treatment in experimental visceral leishmaniasis: intracellular adhesion molecule 1-dependent and -independent regulation. Infect. Immun. 68, 6294-6299.
37. Murray, H. W. (2001). Tissue granuloma structure-function in experimental visceral leishmaniasis. Int. J. Exp. Pathol. 82, 249-267.
38. Murray, H. W., Jungbluth, A., Ritter, E., Montelibano, C., and Marino, M. W. (2000). Visceral leishmaniasis in mice devoid of tumor necrosis factor and response to treatment. Infect. Immun. 68, 6289-6293.
39. Murray, H. W., Squires, K. E., Miralles, C. D., Stoeckle, M. Y., Granger, A. M., Granelli-Piperno, A., et al. (1992). Acquired resistance and granuloma formation in experimental visceral leishmaniasis. Differential T cell and lymphokine roles in initial versus established immunity. J. Immunol. 148, 1858-1863.
40. Murray, H. W., Stern, J. J., Welte, K., Rubin, B. Y., Carriero, S. M., and Nathan, C. F. (1987). Experimental visceral leishmaniasis: production of interleukin 2 and interferon-gamma, tissue immune reaction, and response to treatment with interleukin 2 and interferon-gamma. J. Immunol. 138, 2290-2297.
41. Murray, H. W., Tsai, C. W., Liu, J., and Ma, X. (2006). Visceral Leishmania donovani infection in interleukin-13-/- mice. Infect. Immun. 74, 2487-2490.
42. Pearson, R. D., and Sousa, A. Q. (1996). Clinical spectrum of leishmaniasis. Clin. Infect. Dis. 22, 1-13.
43. Ray, J. C. J., Flynn, J. L., and Kirschner, D. E. (2009). Synergy between individual TNF-dependent functions determines granuloma performance for controlling Mycobacterium tuberculosis infection. J. Immunol. 182, 3706-3717.
44. Read, S., Malmstrom, V., and Powrie, F. (2000). Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J. Exp. Med. 192, 295-302.
45. Robert-Gangneux, F., Drogoul, A. S., Rostan, O., Piquet-Pellorce, C., Cayon, J., Lisbonne, M., et al. (2012). Invariant NKT cells drive hepatic cytokinic microenvironment favoring efficient granuloma formation and early control of Leishmania donovani infection. PLoS ONE 7:e33413. doi: 10.1371/journal.pone.0033413
46. Sanchez, M. A., Diaz, N. L., Zerpa, O., Negron, E., Convit, J., and Tapia, F. J. (2004). Organ-specific immunity in canine visceral leishmaniasis: analysis of symptomatic and asymptomatic dogs naturally infected with Leishmania chagasi. Am. J. Trop. Med. Hyg. 70, 618-624.
47. Sato, N., Kuziel, W. A., Melby, P. C., Reddick, R. L., Kostecki, V., Zhao, W., et al. (1999). Defects in the generation of IFN-gamma are overcome to control infection with Leishmania donovani in CC chemokine receptor (CCR) 5-, macrophage inflammatory protein-1 alpha-, or CCR2-deficient mice. J. Immunol. 163, 5519-5525.
48. Schreiber, H. A., Hulseberg, P. D., Lee, J., Prechl, J., Barta, P., Szlavik, N., et al. (2010). Dendritic cells in chronic mycobacterial granulomas restrict local anti-bacterial T cell response in a murine model. PLoS ONE 5:e11453. doi: 10.1371/journal.pone.0011453
49. Scott-Browne, J. P., Shafiani, S., Tucker-Heard, G., Ishida-Tsubota, K., Fontenot, J. D., Rudensky, A. Y., et al. (2007). Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J. Exp. Med. 204, 2159-2169.
50. Segovia-Juarez, J. L., Ganguli, S., and Kirschner, D. (2004). Identifying control mechanisms of granuloma formation during M. tuberculosis infection using an agent-based model. J. Theor. Biol. 231, 357-376.
51. Shi, C., and Pamer, E. G. (2011). Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11, 762-774.
52. Smelt, S. C., Cotterell, S. E., Engwerda, C. R., and Kaye, P. M. (2000). B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. J. Immunol. 164, 3681-3688.
53. Stager, S., Alexander, J., Carter, K. C., Brombacher, F., and Kaye, P. M. (2003). Both interleukin-4 (IL-4) and IL-4 receptor alpha signaling contribute to the development of hepatic granulomas with optimal antileishmanial activity. Infect. Immun. 71, 4804-4807.
54. Stanley, A. C., and Engwerda, C. R. (2007). Balancing immunity and pathology in visceral leishmaniasis. Immunol. Cell Biol. 85, 138-147.
55. Stanley, A. C., Zhou, Y., Amante, F. H., Randall, L. M., Haque, A., Pellicci, D. G., et al. (2008). Activation of invariant NKT cells exacerbates experimental visceral leishmaniasis. PLoS Pathog. 4:e1000028. doi: 10.1371/journal.ppat.1000028
56. Stern, J. J., Oca, M. J., Rubin, B. Y., Anderson, S. L., and Murray, H. W. (1988). Role of L3T4+ and LyT-2+ cells in experimental visceral leishmaniasis. J. Immunol. 140, 3971-3977.
57. + T cells to control of Mycobacterium tuberculosis infection. J. Immunol. 176, 4296-4314.
58. Svensson, M., Zubairi, S., Maroof, A., Kazi, F., Taniguchi, M., and Kaye, P. M. (2005). Invariant NKT cells are essential for the regulation of hepatic CXCL10 gene expression during Leishmania donovani infection. Infect. Immun. 73, 7541-7547.
59. Taflin, C., Miyara, M., Nochy, D., Valeyre, D., Naccache, J. M., Altare, F., et al. (2009). FoxP3+ regulatory T cells suppress early stages of granuloma formation but have little impact on sarcoidosis lesions. Am. J. Pathol. 174, 497-508.
60. Takahashi, T., Tagami, T., Yamazaki, S., Uede, T., Shimizu, J., Sakaguchi, N., et al. (2000). Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 192, 303-310.
61. Trede, N. S., Zapata, A., and Zon, L. I. (2001). Fishing for lymphoid genes. Trends Immunol. 22, 302-307.
62. Walsh, C. M., Smith, P., and Fallon, P. G. (2007). Role for CTLA-4 but not CD25+ T cells during Schistosoma mansoni infection of mice. Parasite Immunol. 29, 293-308.
63. Willett, C. E., Cortes, A., Zuasti, A., and Zapata, A. G. (1999). Early hematopoiesis and developing lymphoid organs in the zebrafish. Dev. Dyn. 214, 323-336.
64. Wilson, M. E., Young, B. M., Davidson, B. L., Mente, K. A., and McGowan, S. E. (1998). The importance of TGF-beta in murine visceral leishmaniasis. J. Immunol. 161, 6148-6155.
65. Wynn, T. A., and Barron, L. (2010). Macrophages: master regulators of inflammation and fibrosis. Semin. Liver Dis. 30, 245-257.
66. Zubairi, S., Sanos, S. L., Hill, S., and Kaye, P. M. (2004). Immunotherapy with OX40L-Fc or anti-CTLA-4 enhances local tissue responses and killing of Leishmania donovani. Eur. J. Immunol. 34, 1433-1440.