Macrophage migration inhibitory factor is critical to interleukin-5-driven eosinophilopoiesis and tissue eosinophilia triggered by Schistosoma mansoni infection

FASEB Journal

Volumn 23, Issue 4, 2009, Pages 1262-1271

  Magalhães, Elizabeth S ^a   Paiva, Claudia N ^a   Souza, Heitor S P ^a   Pyrrho, Alexandre S ^a   Mourão Sá, Diego ^a   Figueiredo, Rodrigo T ^a   Vieira de Abreu, Adriana ^b   Dutra, Helio S ^a   Silveira, Mariana S ^a   Gaspar Elsas, Maria Ignez C ^b   Xavier Elsas, Pedro ^a   Bozza, Patrícia T ^b   Bozza, Marcelo T ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Apoptosis; Granuloma; Inflammation; MIF; Th2 response

Indexed keywords

CASPASE INHIBITOR; CHEMOATTRACTANT; IMMUNOGLOBULIN E; INTERLEUKIN 5; MACROPHAGE MIGRATION INHIBITION FACTOR; RECOMBINANT PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BONE MARROW CULTURE; CELL CULTURE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; EGG; EOSINOPHILIA; FEMALE; GRANULOMA; HUMAN; INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; TH2 CELL; TRANSGENIC MOUSE; WILD TYPE; WORM; ANIMAL; C57BL MOUSE; DRUG EFFECT; EOSINOPHIL; GENETICS; IMMUNOLOGY; INFLAMMATION; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SCHISTOSOMIASIS MANSONI;

CUCURBITA; MUS; MUS MUSCULUS; SCHISTOSOMA MANSONI;

ANIMALS; EOSINOPHILIA; EOSINOPHILS; GRANULOMA; INFLAMMATION; INTERLEUKIN-5; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECOMBINANT PROTEINS; SCHISTOSOMIASIS MANSONI; TH2 CELLS;

EID: 65349084929     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-124248     Document Type: Article

References (54)

1. Flaster, H., Bernhagen, J., Calandra, T., and Bucala, R. (2007) The macrophage migration inhibitory factor-glucocorticoid dyad: regulation of inflammation and immunity. Mol. Endocrinol. 21, 1267-1280 (Pubitemid 46984737)
2. Hudson, J. D., Shoaibi, M. A., Maestro, R., Carnero, A., Hannon, G. J., and Beach, D. H. (1999) A proinflammatory cytokine inhibits p53 tumor suppressor activity. J. Exp. Med. 190, 1375-1382
3. Baumann, R., Casaulta, C., Simon, D., Conus, S., Yousefi, S., and Simon, H. U. (2003) Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway. FASEB J. 17, 2221-2230 (Pubitemid 37509578)
4. Mitchell, R. A., Liao, H., Chesney, J., Fingerle-Rowson, G., Baugh, J., David, J., and Bucala, R. (2002) Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc. Natl. Acad. Sci. U. S. A. 99, 345-350 (Pubitemid 34060365)
5. Bozza, M., Satoskar, A. R., Lin, G., Lu, B., Humbles, A. A., Gerard, C., and David, J. R. (1999) Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J. Exp. Med. 189, 341-346 (Pubitemid 29063255)
6. Satoskar, A. R., Bozza, M., Rodriguez Sosa, M., Lin, G., and David, J. R. (2001) Migration-inhibitory factor gene-deficient mice are susceptible to cutaneous Leishmania major infection. Infect. Immun. 69, 906-911 (Pubitemid 32109555)
7. Bozza, F. A., Gomes, R. N., Japiassu, A. M., Soares, M., Castro-Faria-Neto, H. C., Bozza, P. T., Bozza, M. T. (2004) Macrophage migration inhibitory factor levels correlate with fatal outcome in sepsis. Shock 22, 309-313 (Pubitemid 39480698)
8. Rodriguez-Sosa, M., Rosas, L. E., David, J. R., Bojalil, R., Satoskar, A. R., and Terrazas, L. I. (2003) Macrophage migration inhibitory factor plays a critical role in mediating protection against the helminth parasite Taenia crassiceps. Infect. Immun. 71, 1247-1254 (Pubitemid 36254308)
9. Denkinger, C. M., Metz, C., Fingerle-Rowson, G., Denkinger, M. D., and Forsthuber, T. (2004) Macrophage migration inhibitory factor and its role in autoimmune diseases. Arch. Immunol. Ther. Exp. (Warsz.) 52, 389-400 (Pubitemid 40115973)
10. Powell, N. D., Papenfuss, T. L., McClain, M. A., Gienapp, I. E., Shawler, T. M., Satoskar, A. R., and Whitacre, C. C. (2005) Cutting edge: macrophage migration inhibitory factor is necessary for progression of experimental autoimmune encephalomyelitis. J. Immunol. 175, 5611-5614 (Pubitemid 41508040)
11. Rossi, A. G., Haslett, C., Hirani, N., Greening, A. P., Rahman, I., Metz, C. N., Bucala, R., and Donnelly, S. C. (1998) Human circulating eosinophils secrete macrophage migration inhibitory factor (MIF). Potential role in asthma. J. Clin. Invest. 101, 2869-2874 (Pubitemid 28294596)
12. Yamaguchi, E., Nishihira, J., Shimizu, T., Takahashi, T., Kitashiro, N., Hizawa, N., Kamishima, K., and Kawakami, Y. (2000) Macrophage migration inhibitory factor (MIF) in bronchial asthma. Clin. Exp. Allergy 30, 1244-1249 (Pubitemid 30671250)
13. Bacher, M., Metz, C. N., Calandra, T., Mayer, K., Chesney, J., Lohoff, M., Gemsa, D., Donnelly, T., and Bucala, R. (1996) An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc. Natl. Acad. Sci. U. S. A. 93, 7849-7854 (Pubitemid 26277127)
14. Sabroe, I., Pease, J. E., and Williams, T. J. (2000) Asthma and MIF: innately Th1 and Th2. Clin. Exp. Allergy. 30, 1194-1196 (Pubitemid 30673808)
15. Mizue, Y., Ghani, S., Leng, L., McDonald, C., Kong, P., Baugh, J., Lane, S. J., Craft, J., Nishihira, J., Donnelly, S. C., Zhu, Z., and Bucala, R. (2005) Role for macrophage migration inhibitory factor in asthma. Proc. Natl. Acad. Sci. U. S. A. 102, 14410-14415 (Pubitemid 41429711)
16. Magalhaes, E. S., Mourao-Sa, D. S., Vieira-de-Abreu, A., Figueiredo, R. T., Pires, A. L., Farias-Filho, F. A., Fonseca, B. P., Viola, J. P., Metz, C., Martins, M. A., Castro-Faria-Neto, H. C., Bozza, P. T., and Bozza, M. T. (2007) Macrophage migration inhibitory factor is essential for allergic asthma but not for Th2 differentiation. Eur. J. Immunol. 37, 1097-1106 (Pubitemid 46925345)
17. Amano, T., Nishihira, J., and Miki, I. (2007) Blockade of macrophage migration inhibitory factor (MIF) prevents the antigen-induced response in a murine model of allergic airway inflammation. Inflamm. Res. 56, 24-31 (Pubitemid 46356224)
18. Nakamaru, Y., Oridate, N., Nishihira, J., Takagi, D., Furuta, Y., and Fukuda, S. (2005) Macrophage migration inhibitory factor (MIF) contributes to the development of allergic rhinitis. Cytokine 31, 103-108 (Pubitemid 40910225)
19. Wang, F., Gao, F., and Jing, L. (2005) Is macrophage migration inhibitory factor (MIF) the "control point" of vascular hypo-responsiveness in septic shock? Med. Hypotheses 65, 1082-1087
20. Stavitsky, A. B., Metz, C., Liu, S., Xianli, J., and Bucala, R. (2003) Blockade of macrophage migration inhibitory factor (MIF) in Schistosoma japonicum-infected mice results in an increased adult worm burden and reduced fecundity. Parasite Immunol. 25, 369-374 (Pubitemid 38019280)
21. Rothenberg, M. E., and Hogan, S. P. (2006) The eosinophil. Annu. Rev. Immunol. 24, 147-174
22. Padigel, U. M., Lee, J. J., Nolan, T. J., Schad, G. A., and Abraham, D. (2006) Eosinophils can function as antigen-presenting cells to induce primary and secondary immune responses to Strongyloides stercoralis. Infect. Immun. 74, 3232-3238
23. Kariyawasam, H. H., and Robinson, D. S. (2007) The role of eosinophils in airway tissue remodelling in asthma. Curr. Opin. Immunol.
24. Lee, J. J., Dimina, D., Macias, M. P., Ochkur, S. I., McGarry, M. P., O'Neill, K. R., Protheroe, C., Pero, R., Nguyen, T., Cormier, S. A., Lenkiewicz, E., Colbert, D., Rinaldi, L., Ackerman, S. J., Irvin, C. G., and Lee, N. A. (2004) Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305, 1773-1776 (Pubitemid 39249644)
25. Humbles, A. A., Lloyd, C. M., McMillan, S. J., Friend, D. S., Xanthou, G., McKenna, E. E., Ghiran, S., Gerard, N. P., Yu, C., Orkin, S. H., and Gerard, C. (2004) A critical role for eosinophils in allergic airways remodeling. Science 305, 1776-1779 (Pubitemid 39249645)
26. David, J. R., Butterworth, A. E., and Vadas, M. A. (1980) Mechanism of the interaction mediating killing of Schistosoma mansoni by human eosinophils. Am. J. Trop. Med. Hyg. 29, 842-848
27. Lenzi, H. L., Sobral, A. C., and Lenzi, J. A. (1987) "In vivo" kinetics of eosinophils and mast cells in experimental murine schistosomiasis. Mem. Inst. Oswaldo. Cruz. 82(Suppl. 4), 67-76
28. Sher, A., Coffman, R. L., Hieny, S., Scott, P., and Cheever, A. W. (1990) Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni. Proc. Natl. Acad. Sci. U. S. A. 87, 61-65 (Pubitemid 20033006)
29. Davies, S. J., Smith, S. J., Lim, K. C., Zhang, H., Purchio, A. F., McKerrow, J. H., and West, D. B. (2005) In vivo imaging of tissue eosinophilia and eosinopoietic responses to schistosome worms and eggs. Int. J. Parasitol. 35, 851-859 (Pubitemid 40905202)
30. Reiman, R. M., Thompson, R. W., Feng, C. G., Hari, D., Knight, R., Cheever, A. W., Rosenberg, H. F., and Wynn, T. A. (2006) Interleukin-5 (IL-5) augments the progression of liver fibrosis by regulating IL-13 activity. Infect. Immun. 74, 1471-1479 (Pubitemid 43346779)
31. Swartz, J. M., Dyer, K. D., Cheever, A. W., Ramalingam, T., Pesnicak, L., Domachowske, J. B., Lee, J. J., Lee, N. A., Foster, P. S., Wynn, T. A., and Rosenberg, H. F. (2006) Schistosoma mansoni infection in eosinophil lineage-ablated mice. Blood 108, 2420-2427 (Pubitemid 44497528)
32. Dolber, P. C., and Spach, M. S. (1993) Conventional and confocal fluorescence microscopy of collagen fibers in the heart. J. Histochem. Cytochem. 41, 465-469
33. Wilson, M. S., Mentink-Kane, M. M., Pesce, J. T., Ramalingam, T. R., Thompson, R., and Wynn, T. A. (2007) Immunopathology of schistosomiasis. Immunol. Cell Biol. 85, 148-154
34. Davies, S. J., Lim, K. C., Blank, R. B., Kim, J. H., Lucas, K. D., Hernandez, D. C., Sedgwick, J. D., and McKerrow, J. H. (2004) Involvement of TNF in limiting liver pathology and promoting parasite survival during schistosome infection. Int. J. Parasitol. 34, 27-36
35. Fallon, P. G., Richardson, E. J., McKenzie, G. J., and McKenzie, A. N. (2000) Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J. Immunol. 164, 2585-2591
36. Bernhagen, J., Krohn, R., Lue, H., Gregory, J. L., Zernecke, A., Koenen, R. R., Dewor, M., Georgiev, I., Schober, A., Leng, L., Kooistra, T., Fingerle-Rowson, G., Ghezzi, P., Kleemann, R., McColl, S. R., Bucala, R., Hickey, M. J., and Weber, C. (2007) MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat. Med. 13, 587-596 (Pubitemid 46828480)
37. Gaspar Elsas, M. I., Joseph, D., Elsas, P. X., and Vargaftig, B. B. (1997) Rapid increase in bone-marrow eosinophil production and responses to eosinopoietic interleukins triggered by intranasal allergen challenge. Am. J. Respir. Cell Mol. Biol. 17, 404-413 (Pubitemid 127500973)
38. Falcone, F. H., Loke, P., Zang, X., MacDonald, A. S., Maizels, R. M., and Allen, J. E. (2001) A Brugia malayi homolog of macrophage migration inhibitory factor reveals an important link between macrophages and eosinophil recruitment during nematode infection. J. Immunol. 167, 5348-5354 (Pubitemid 33009774)
39. Vermeire, J. J., Cho, Y., Lolis, E., Bucala, R., and Cappello, M. (2008) Orthologs of macrophage migration inhibitory factor from parasitic nematodes. Trends. Parasitol. 24, 355-363
40. Ohnmacht, C., Pullner, A., van Rooijen, N., and Voehringer, D. (2007) Analysis of eosinophil turnover in vivo reveals their active recruitment to and prolonged survival in the peritoneal cavity. J. Immunol. 179, 4766-4774
41. Hoffmann, K. F., Cheever, A. W., and 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
42. Leeto, M., Herbert, D. R., Marillier, R., Schwegmann, A., Fick, L., and Brombacher, F. (2006) TH1-dominant granulomatous pathology does not inhibit fibrosis or cause lethality during murine schistosomiasis. Am. J. Pathol. 169, 1701-1712 (Pubitemid 351182001)
43. Chiaramonte, M. G., Donaldson, D. D., Cheever, A. W., and Wynn, T. A. (1999) An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J. Clin. Invest. 104, 777-785
44. Her, E., Frazer, J., Austen, K. F., and Owen, W. F., Jr. (1991) Eosinophil hematopoietins antagonize the programmed cell death of eosinophils. Cytokine and glucocorticoid effects on eosinophils maintained by endothelial cell-conditioned medium. J. Clin. Invest. 88, 1982-1987
45. Yamaguchi, Y., Suda, T., Ohta, S., Tominaga, K., Miura, Y., and Kasahara, T. (1991) Analysis of the survival of mature human eosinophils: interleukin-5 prevents apoptosis in mature human eosinophils. Blood 78, 2542-2547
46. Yousefi, S., Blaser, K., and Simon, H. U. (1997) Activation of signaling pathways and prevention of apoptosis by cytokines in eosinophils. Int. Arch. Allergy Immunol. 112, 9-12 (Pubitemid 26418375)
47. Hoontrakoon, R., Chu, H. W., Gardai, S. J., Wenzel, S. E., McDonald, P., Fadok, V. A., Henson, P. M., and Bratton, D. L. (2002) Interleukin-15 inhibits spontaneous apoptosis in human eosinophils via autocrine production of granulocyte macrophage-colony stimulating factor and nuclear factor-kappaB activation. Am. J. Respir. Cell Mol. Biol. 26, 404-412 (Pubitemid 34253924)
48. Farahi, N., Cowburn, A. S., Upton, P. D., Deighton, J., Sobolewski, A., Gherardi, E., Morrell, N. W., and Chilvers, E. R. (2007) Eotaxin-1/CC chemokine ligand 11: a novel eosinophil survival factor secreted by human pulmonary artery endothelial cells. J. Immunol. 179, 1264-1273
49. Nagase, H., Miyamasu, M., Yamaguchi, M., Fujisawa, T., Kawasaki, H., Ohta, K., Yamamoto, K., Morita, Y., and Hirai, K. (2001) Regulation of chemokine receptor expression in eosinophils. Int. Arch. Allergy Immunol. 125(Suppl. 1), 29-32 (Pubitemid 32620157)
50. Lukacs, N. W., Berlin, A., Schols, D., Skerlj, R. T., and Bridger, G. J. (2002) AMD3100, a CxCR4 antagonist, attenuates allergic lung inflammation and airway hyperreactivity. Am. J. Pathol. 160, 1353-1360 (Pubitemid 34411639)
51. Hu, J. S., Freeman, C. M., Stolberg, V. R., Chiu, B. C., Bridger, G. J., Fricker, S. P., Lukacs, N. W., and Chensue, S. W. (2006) AMD3465, a novel CXCR4 receptor antagonist, abrogates schistosomal antigen-elicited (type-2) pulmonary granuloma formation. Am. J. Pathol. 169, 424-432
52. Borchers, M. T., Ansay, T., DeSalle, R., Daugherty, B. L., Shen, H., Metzger, M., Lee, N. A., and Lee, J. J. (2002) In vitro assessment of chemokine receptor-ligand interactions mediating mouse eosinophil migration. J. Leukoc. Biol. 71, 1033-1041
53. Heath, H., Qin, S., Rao, P., Wu, L., LaRosa, G., Kassam, N., Ponath, P. D., and Mackay, C. R. (1997) Chemokine receptor usage by human eosinophils. The importance of CCR3 demonstrated using an antagonistic monoclonal antibody. J. Clin. Invest. 99, 178-184 (Pubitemid 27053460)
54. Petering, H., Gotze, O., Kimmig, D., Smolarski, R., Kapp, A., and Elsner, J. (1999) The biologic role of interleukin-8: functional analysis and expression of CXCR1 and CXCR2 on human eosinophils. Blood 93, 694-702 (Pubitemid 29035752)