A systemic granulomatous response to Schistosoma mansoni eggs alters responsiveness of bone marrow-derived macrophages to Toll-like receptor agonists

Journal of Leukocyte Biology

Volumn 83, Issue 2, 2008, Pages 314-324

  Joshi, Amrita D ^a   Raymond, Tracy ^a   Coelho, Ana L ^a   Kunkel, Steven L ^a   Hogaboam, Cory M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Alternative activation; Classical activation; Soluble egg antigen

Indexed keywords

INTERLEUKIN 10; TOLL LIKE RECEPTOR;

ANIMAL MODEL; ARTICLE; BONE MARROW; CYTOKINE PRODUCTION; FEMALE; GRANULOMATOSIS; IMMUNE RESPONSE; IMMUNOREACTIVITY; MACROPHAGE; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHISTOSOMA MANSONI;

ANIMALS; CHEMOKINE CCL17; CHEMOKINES; CPG ISLANDS; CYSTEINE; CYTOKINES; FEMALE; GENE EXPRESSION REGULATION; GRANULOMA, RESPIRATORY TRACT; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; LIPOPROTEINS; LUNG DISEASES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MYELOID CELLS; OVUM; POLY I-C; SCHISTOSOMA MANSONI; SPECIFIC PATHOGEN-FREE ORGANISMS; TH2 CELLS; TOLL-LIKE RECEPTORS;

MUS; SCHISTOSOMA MANSONI;

EID: 38949090987     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1007689     Document Type: Article

References (55)

1. Wynn, T. A., Thompson, R. W., Cheever, A. W., Mentink-Kane, M. M. (2004) Immunopathogenesis of schistosomiasis. Immunol. Rev. 201, 156-167.
2. Pearce, E. J., MacDonald, A. S. (2002) The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2, 499-511.
3. Wynn, T. A. (2004) Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat. Rev. Immunol. 4, 583-594.
4. Okano, M., Satoskar, A. R., Nishizaki, K., Harn Jr., D. A. (2001) Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. J. Immunol. 167, 442-450.
5. Chensue, S. W., Terebuh, P. D., Warmington, K. S., Hershey, S. D., Evanoff, H. L., Kunkel, S. L., Higashi, G. I. (1992) Role of IL-4 and IFN in Schistosoma mansoni egg-induced hypersensitivity granuloma formation. Orchestration, relative contribution, and relationship to macrophage function. J. Immunol. 148, 900-906.
6. Wynn, T. A., Eltoum, I., Cheever, A. W., Lewis, F. A., Gause, W. C., Sher, A. (1993) Analysis of cytokine mRNA expression during primary granuloma formation induced by eggs of Schistosoma mansoni. J. Immunol. 151, 1430-1440.
7. Chiu, B. C., Freeman, C. M., Stolberg, V. R., Komuniecki, E., Lincoln, P. M., Kunkel, S. L., Chensue, S. W. (2003) Cytokine-chemokine networks in experimental mycobacterial and schistosomal pulmonary granuloma formation. Am. J. Respir. Cell Mol. Biol. 29, 106-116.
8. Hoffmann, K. F., Cheever, A. W., Wynn, T. A. (2000) IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J. Immunol. 164, 6406-6416.
9. Brunet, L. R., Finkelman, F. D., Cheever, A. W., Kopf, M. A., Pearce, E. J. (1997) IL-4 protects against TNF-α-mediated cachexia and death during acute schistosomiasis. J. Immunol. 159, 777-785.
10. Herbert, D. R., Holscher, C., Mohrs, M., Arendse, B., Schwegmann, A., Radwanska, M., Leeto, M., Kirsch, R., Hall, P., Mossmann, H., Claussen, B., Förster, I., Brombacher, F. (2004) Alternative macrophage activation is essential for survival during schistosomiasis and down modulates T helper 1 responses and immunopathology. Immunity 20, 623-635.
11. Chiu, B. C., Chensue, S. W. (2002) Chemokine responses in schistosomal antigen-elicited granuloma formation. Parasite Immunol. 24, 285-294.
12. Jakubzick, C., Wen, H., Matsukawa, A., Keller, M., Kunkel, S. L., Hogaboam, C. M. (2004) Role of CCR4 ligands, CCL17 and CCL22, during Schistosoma mansoni egg-induced pulmonary granuloma formation in mice. Am. J. Pathol. 165, 1211-1221.
13. Katakura, T., Miyazaki, M., Kobayashi, M., Herndon, D. N., Suzuki, F. (2004) CCL17 and IL-10 as effectors that enable alternatively activated macrophages to inhibit the generation of classically activated macrophages. J. Immunol. 172, 1407-1413.
14. Lukacs, N. W., Strieter, R. M., Shaklee, C. L., Chensue, S. W., Kunkel, S. L. (1995) Macrophage inflammatory protein-1 α influences eosinophil recruitment in antigen-specific airway inflammation. Eur. J. Immunol. 25, 245-251.
15. Chensue, S. W., Ruth, J. H., Warmington, K., Lincoln, P., Kunkel, S. L. (1995) In vivo regulation of macrophage IL-12 production during type 1 and type 2 cytokine-mediated granuloma formation. J. Immunol. 155, 3546-3551.
16. Lukacs, N. W., Strieter, R. M., Lincoln, P. M., Brownell, E., Pullen, D. M., Schock, H. J., Chensue, S. W., Taub, D. D., Kunkel, S. L. (1996) Stem cell factor (c-kit ligand) influences eosinophil recruitment and histamine levels in allergic airway inflammation. J. Immunol. 156, 3945-3951.
17. Hesse, M., Modolell, M., La Flamme, A. C., Schito, M., Fuentes, J. M., Cheever, A. W., Pearce, E. J., Wynn, T. A. (2001) Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol. 167, 6533-6544.
18. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686.
19. Gordon, S. (2003) Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23-35.
20. Kondo, M., Scherer, D. C., Miyamoto, T., King, A. G., Akashi, K., Sugamura, K., Weissman, I. L. (2000) Cell-fate conversion of lymphoid-committed progenitors by instructive actions of cytokines. Nature 407, 383-386.
21. Erwig, L. P., Kluth, D. C., Walsh, G. M., Rees, A. J. (1998) Initial cytokine exposure determines function of macrophages and renders them unresponsive to other cytokines. J. Immunol. 161, 1983-1988.
22. Stout, R. D., Jiang, C., Matta, B., Tietzel, I., Watkins, S. K., Suttles, J. (2005) Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J. Immunol. 175, 342-349.
23. Wood, L. J., Inman, M. D., Watson, R. M., Foley, R., Denburg, J. A., O'Byrne, P. M. (1998) Changes in bone marrow inflammatory cell progenitors after inhaled allergen in asthmatic subjects. Am. J. Respir. Crit. Care Med. 157, 99-105.
24. Redente, E. F., Orlicky, D. J., Bouchard, R. J., Malkinson, A. M. (2007) Tumor signaling to the bone marrow changes the phenotype of monocytes and pulmonary macrophages during urethane-induced primary lung tumorigenesis in A/J mice. Am. J. Pathol. 170, 693-708.
25. Souza, A. L., Roffe, E., Pinho, V., Souza, D. G., Silva, A. F., Russo, R. C., Guabiraba, R., Pereira, C. A., Carvalho, F. M., Barsante, M. M., Correa-Oliveira, R., Fraga, L. A., Negrão-Correa, D., Teixeira, M. M. (2005) Potential role of the chemokine macrophage inflammatory protein 1α in human and experimental schistosomiasis. Infect. Immun. 73, 2515-2523.
26. Pearce, E. J., M. Cane, C., Sun, J., J. Taylor, J., McKee, A. S., Cervi, L. (2004) Th2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunol. Rev. 201, 117-126.
27. Pearce, E. J. (2005) Priming of the immune response by schistosome eggs. Parasite Immunol. 27, 265-270.
28. Lukacs, N. W., Strieter, R. M., Warmington, K., Lincoln, P., Chensue, S. W., Kunkel, S. L. (1997) Differential recruitment of leukocyte populations and alteration of airway hyperreactivity by C-C family chemokines in allergic airway inflammation. J. Immunol. 158, 4398-4404.
29. Lukacs, N. W., Kunkel, S. L., Strieter, R. M., Warmington, K., Chensue, S. W. (1993) The role of macrophage inflammatory protein 1 α in Schistosoma mansoni egg-induced granulomatous inflammation. J. Exp. Med. 177, 1551-1559.
30. Swanson, M. S., Isberg, R. R. (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63, 3609-3620.
31. Alberti-Segui, C., Goeden, K. R., Higgins, D. E. (2007) Differential function of Listeria monocytogenes listeriolysin O and phospholipases C in vacuolar dissolution following cell-to-cell spread. Cell. Microbiol. 9, 179-195.
32. Ness, T. L., Ewing, J. L., Hogaboam, C. M., Kunkel, S. L. (2006) CCR4 is a key modulator of innate immune responses. J. Immunol. 177, 7531-7539.
33. Boonstra, A., Rajsbaum, R., Holman, M., Marques, R., Asselin-Paturel, C., Pereira, J. P., Bates, E. E., Akira, S., Vieira, P., Liu, Y. J., Trinchieri, G., O'Garra, A. (2006) Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce IL-10 in response to MyD88- and TRIF-dependent TLR signals, and TLR-independent signals. J. Immunol. 177, 7551-7558.
34. Kobayashi, K., Hernandez, L. D., Galan, J. E., Janeway Jr., C. A., Medzhitov, R., Flavell, R. A. (2002) IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110, 191-202.
35. Zouain, C. S., Gustavson, S., Silva-Teixeira, D. N., Contigli, C., Rodriques, V., Leite, M. F., Goes, A. M. (2002) Human immune response in schistosomiasis: the role of P24 in the modulation of cellular activity to Schistosoma mansoni antigens. Hum. Immunol. 63, 647-656.
36. Ness, T. L., Carpenter, K. J., Ewing, J. L., Gerard, C. J., Hogaboam, C. M., Kunkel, S. L. (2004) CCR1 and CC chemokine ligand 5 interactions exacerbate innate immune responses during sepsis. J. Immunol. 173, 6938-6948.
37. Trajkovic, V., Sweet, M. J., Xu, D. (2004) T1/ST2 - an IL-1 receptor-like modulator of immune responses. Cytokine Growth Factor Rev. 15, 87-95.
38. Pasare, C., Medzhitov, R. (2005) Toll-like receptors: linking innate and adaptive immunity. Adv. Exp. Med. Biol. 560, 11-18.
39. Kaisho, T., Akira, S. (2006) Toll-like receptor function and signaling. J. Allergy Clin. Immunol. 117, 979-987.
40. Wilson, M. S., Mentink-Kane, M. M., Pesce, J. T., Ramalingam, T. R., Thompson, R., Wynn, T. A. (2007) Immunopathology of schistosomiasis. Immunol. Cell Biol. 85, 148-154.
41. Nair, M. G., Guild, K. J., Artis, D. (2006) Novel effector molecules in type 2 inflammation: lessons drawn from helminth infection and allergy. J. Immunol. 177, 1393-1399.
42. Nair, M. G., Cochrane, D. W., Allen, J. E. (2003) Macrophages in chronic type 2 inflammation have a novel phenotype characterized by the abundant expression of Ym1 and Fizz1 that can be partly replicated in vitro. Immunol. Lett. 85, 173-180.
43. Linehan, S. A., Coulson, P. S., Wilson, R. A., Mountford, A. P., Brombacher, F., Martinez-Pomares, L., Gordon, S. (2003) IL-4 receptor signaling is required for mannose receptor expression by macrophages recruited to granulomata but not resident cells in mice infected with Schistosoma mansoni. Lab. Invest. 83, 1223-1231.
44. Rauh, M. J., Sly, L. M., Kalesnikoff, J., Hughes, M. R., Cao, L. P., Lam, V., Krystal, G. (2004) The role of SHIP1 in macrophage programming and activation. Biochem. Soc. Trans. 32, 785-788.
45. Rauh, M. J., Ho, V., Pereira, C., Sham, A., Sly, L. M., Lam, V., Huxham, L., Minchinton, A. I., Mui, A., Krystal, G. (2005) SHIP represses the generation of alternatively activated macrophages. Immunity 23, 361-374.
46. Hogaboam, C. M., Bone-Larson, C. L., Lipinski, S., Lukacs, N. W., Chensue, S. W., Strieter, R. M., Kunkel, S. L. (1999) Differential monocyte chemoattractant protein-1 and chemokine receptor 2 expression by murine lung fibroblasts derived from Th1- and Th2-type pulmonary granuloma models. J. Immunol. 163, 2193-2201.
47. Mohammad, M. K., Morran, M., Slotterbeck, B., Leaman, D. W., Sun, Y., von Grafenstein, H., Hong, S. C., McInerney, M. F. (2006) Dysregulated Toll-like receptor expression and signaling in bone marrow-derived macrophages at the onset of diabetes in the non-obese diabetic mouse. Int. Immunol. 18, 1101-1113.
48. Babu, S., Blauvelt, C. P., Kumaraswami, V., Nutman, T. B. (2006) Cutting edge: diminished T cell TLR expression and function modulates the immune response in human filarial infection. J. Immunol. 176, 3885-3889.
49. Pearce, E. J., Kane, C. M., Sun, J. (2006) Regulation of dendritic cell function by pathogen-derived molecules plays a key role in dictating the outcome of the adaptive immune response. Chem. Immunol. Allergy 90, 82-90.
50. Kane, C. M., Cervi, L., Sun, J., McKee, A. S., Masek, K. S., Shapira, S., Hunter, C. A., Pearce, E. J. (2004) Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 173, 7454-7461.
51. Babu, S., Blauvelt, C. P., Kumaraswami, V., Nutman, T. B. (2005) Diminished expression and function of TLR in lymphatic filariasis: a novel mechanism of immune dysregulation. J. Immunol. 175, 1170-1176.
52. Van der Kleij, D., van den Biggelaar, A. H., Kruize, Y. C., Retra, K., Fillie, Y., Schmitz, M., Kremsner, P. G., Tielens, A. G., Yazdanbakhsh, M. (2004) Responses to Toll-like receptor ligands in children living in areas where schistosome infections are endemic. J. Infect. Dis. 189, 1044-1051.
53. Aksoy, E., Zouain, C. S., Vanhoutte, F., Fontaine, J., Pavelka, N., Thieblemont, N., Willems, F., Ricciardi-Castagnoli, P., Goldman, M., Capron, M., Ryffel, B., Trottein, F. (2005) Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J. Biol. Chem. 280, 277-283.
54. Jenkins, S. J., Hewitson, J. P., Ferret-Bernard, S., Mountford, A. P. (2005) Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int. Immunol. 17, 1409-1418.
55. Goodridge, H. S., Marshall, F. A., Else, K. J., Houston, K. M., Egan, C., Al-Riyami, L., Liew, F. Y., Harnett, W., Harnett, M. M. (2005) Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. J. Immunol. 174, 284 -293.