Migration inhibitory factor (MIF) released by macrophages upon recognition of immune complexes is critical to inflammation in Arthus reaction

Journal of Leukocyte Biology

Volumn 85, Issue 5, 2009, Pages 855-861

  Paiva, Claudia N ^a   Arras, Rosa H ^a   Magalhães, Elisabeth S ^a   Alves, Letícia S ^a   Lessa, Luiz Paulo ^a   Silva, Maria Helena ^a   Ejzemberg, Regina ^a   Canetti, Cláudio ^a   Bozza, Marcelo T ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Cytokines; Fc receptors; Monocytes

Indexed keywords

IMMUNOGLOBULIN G; KERATINOCYTE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 2; MIGRATION INHIBITION FACTOR; TUMOR NECROSIS FACTOR; FC RECEPTOR; ISOMERASE; MACROPHAGE MIGRATION INHIBITION FACTOR; MIF PROTEIN, HUMAN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANTIGEN ANTIBODY COMPLEX; ANTIGEN RECOGNITION; ARTHUS PHENOMENON; ARTICLE; BLOOD VESSEL PERMEABILITY; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ERYTHROCYTE; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLAMMATION; LEUKOCYTE COUNT; LUNG; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; OPSONIZATION; PERITONEUM; PRIORITY JOURNAL; PROTEIN FUNCTION; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHAGOCYTOSIS;

MUS;

ADOPTIVE TRANSFER; ANIMALS; ANTIGEN-ANTIBODY COMPLEX; ARTHUS REACTION; CELLS, CULTURED; FEMALE; HUMANS; INFLAMMATION; INTRAMOLECULAR OXIDOREDUCTASES; LUNG; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHAGOCYTOSIS; RECEPTORS, IGG; TUMOR NECROSIS FACTORS;

EID: 65549101058     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0108009     Document Type: Article

References (52)

1. Calandra, T., Roger, T. (2003) Macrophage migration inhibitory factor: a regulator of innate immunity. Nat. Rev. Immunol. 3, 791-800. (Pubitemid 37328657)
2. Calandra, T., Froidevaux, C., Martin, C., Roger, T. (2003) Macrophage migration inhibitory factor and host innate immune defenses against bacterial sepsis. J. Infect. Dis. 187 (Suppl. 2), S385-S390. (Pubitemid 36724512)
3. Baugh, J. A., Bucala, R. (2002) Macrophage migration inhibitory factor. Crit. Care Med. 30, S27-S35.
4. Bernhagen, J., Calandra, T., Bucala, R. (1994) The emerging role of MIF in septic shock and infection. Biotherapy 8, 123-127. (Pubitemid 26014886)
5. Mitchell, R. A., Metz, C. N., Peng, T., Bucala, R. (1999) Sustained mitogenactivated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid action. J. Biol. Chem. 274, 18100-18106. (Pubitemid 129519178)
6. Leng, L., Metz, C. N., Fang, Y., Xu, J., Donnelly, S., Baugh, J., Delohery, T., Chen, Y., Mitchell, R. A., Bucala, R. (2003) MIF signal transduction initiated by binding to CD74. J. Exp. Med. 197, 1467-1476. (Pubitemid 36686708)
7. Bozza, M., Satoskar, A. R., Lin, G., Lu, B., Humbles, A. A., Gerard, C., 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)
8. Calandra, T., Echtenacher, B., Roy, D. L., Pugin, J., Metz, C. N., Hultner, L., Heumann, D., Mannel, D., Bucala, R., Glauser, M. P. (2000) Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat. Med. 6, 164-170. (Pubitemid 30082360)
9. Lan, H. Y., Bacher, M., Yang, N., Mu, W., Nikolic-Paterson, D. J., Metz, C., Meinhardt, A., Bucala, R., Atkins, R. C. (1997) The pathogenic role of macrophage migration inhibitory factor in immunologically induced kidney disease in the rat. J. Exp. Med. 185, 1455-1465. (Pubitemid 27187602)
10. De Jong, Y. P., Abadia-Molina, A. C., Satoskar, A. R., Clarke, K., Rietdijk, S. T., Faubion, W. A., Mizoguchi, E., Metz, C. N., Alsahli, M., ten Hove, T., Keates, A. C., Lubetsky, J. B., Farrell, R. J., Michetti, P., van Deventer, S. J., Lolis, E., David, J. R., Bhan, A. K., Terhorst, C. (2001) Development of chronic colitis is dependent on the cytokine MIF. Nat. Immunol. 2, 1061-1066.
11. Denkinger, C. M., Denkinger, M., Kort, J. J., Metz, C., Forsthuber, T. G. (2003) In vivo blockade of macrophage migration inhibitory factor ameliorates acute experimental autoimmune encephalomyelitis by impairing the homing of encephalitogenic T cells to the central nervous system. J. Immunol. 170, 1274-1282. (Pubitemid 36139493)
12. Satoskar, A. R., Bozza, M., Rodriguez Sosa, M., Lin, G., David, J. R. (2001) Migration-inhibitory factor gene-deficient mice are susceptible to cutaneous Leishmania major infection. Infect. Immun. 69, 906-911. (Pubitemid 32109555)
13. Pan, J. H., Sukhova, G. K., Yang, J. T., Wang, B., Xie, T., Fu, H., Zhang, Y., Satoskar, A. R., David, J. R., Metz, C. N., Bucala, R., Fang, K., Simon, D. I., Chapman, H. A., Libby, P., Shi, G. P. (2004) Macrophage migration inhibitory factor deficiency impairs atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 109, 3149-3153.
14. Lehmann, L. E., Novender, U., Schroeder, S., Pietsch, T., von Spiegel, T., Putensen, C., Hoeft, A., Stuber, F. (2001) Plasma levels of macrophage migration inhibitory factor are elevated in patients with severe sepsis. Intensive Care Med. 27, 1412-1415. (Pubitemid 32758941)
15. 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)
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., 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. Mikulowska, A., Metz, C. N., Bucala, R., Holmdahl, R. (1997) Macrophage migration inhibitory factor is involved in the pathogenesis of collagen type II-induced arthritis in mice. J. Immunol. 158, 5514-5517. (Pubitemid 127681261)
18. Leech, M., Metz, C., Hall, P., Hutchinson, P., Gianis, K., Smith, M., Weedon, H., Holdsworth, S. R., Bucala, R., Morand, E. F. (1999) Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of pro-inflammatory function and regulation by glucocorticoids. Arthritis Rheum. 42, 1601-1608. (Pubitemid 30263626)
19. Onodera, S., Kaneda, K., Mizue, Y., Koyama, Y., Fujinaga, M., Nishihira, J. (2000) Macrophage migration inhibitory factor up-regulates expression of matrix metalloproteinases in synovial fibroblasts of rheumatoid arthritis. J. Biol. Chem. 275, 444-450. (Pubitemid 30039004)
20. Kim, H. R., Park, M. K., Cho, M. L., Yoon, C. H., Lee, S. H., Park, S. H., Leng, L., Bucala, R., Kang, I., Choe, J., Kim, H. Y. (2007) Macrophage migration inhibitory factor upregulates angiogenic factors and correlates with clinical measures in rheumatoid arthritis. J. Rheumatol. 34, 927-936. (Pubitemid 46774834)
21. Morand, E. F. (2005) New therapeutic target in inflammatory disease: macrophage migration inhibitory factor. Intern. Med. J. 35, 419-426. (Pubitemid 40917441)
22. Suzuki, Y., Gomez-Guerrero, C., Shirato, I., Lopez-Franco, O., Gallego- Delgado, J., Sanjuan, G., Lazaro, A., Hernandez-Vargas, P., Okumura, K., Tomino, Y., Ra, C., Egido, J. (2003) Pre-existing glomerular immune complexes induce polymorphonuclear cell recruitment through an Fc receptor-dependent respiratory burst: potential role in the perpetuation of immune nephritis. J. Immunol. 170, 3243-3253. (Pubitemid 36302202)
23. Bergtold, A., Gavhane, A., D'Agati, V., Madaio, M., Clynes, R. (2006) FcR-bearing myeloid cells are responsible for triggering murine lupus nephritis. J. Immunol. 177, 7287-7895. (Pubitemid 44715098)
24. Van Lent, P. L., Grevers, L., Lubberts, E., de Vries, T. J., Nabbe, K. C., Verbeek, S., Oppers, B., Sloetjes, A., Blom, A. B., van den Berg, W. B. (2006) Fcγ receptors directly mediate cartilage, but not bone, destruction in murine antigen-induced arthritis: uncoupling of cartilage damage from bone erosion and joint inflammation. Arthritis Rheum. 54, 3868-3877. (Pubitemid 44955889)
25. Bao, L., Quigg, R. J. (2007) Complement in lupus nephritis: the good, the bad, and the unknown. Semin. Nephrol. 27, 69-80. (Pubitemid 46320752)
26. Okroj, M., Heinegård, D., Holmdahl, R., Blom, A. M. (2007) Rheumatoid arthritis and the complement system. Ann. Med. 39, 517-530.
27. Weissmann, G. (2006) The pathogenesis of rheumatoid arthritis. Bull. NYU Hosp. Jt. Dis. 64, 12-15.
28. Kohl, J., Gessner, J. E. (1999) On the role of complement and Fc γ-receptors in the Arthus reaction. Mol. Immunol. 36, 893-903. (Pubitemid 30100842)
29. Skokowa, J., Ali, S. R., Felda, O., Kumar, V., Konrad, S., Shushakova, N., Schmidt, R. E., Piekorz, R. P., Nurnberg, B., Spicher, K., Birnbaumer, L., Zwirner, J., Claassens, J. W., Verbeek, J. S., van Rooijen, N., Köhl, J., Gessner, J. E. (2005) Macrophages induce the inflammatory response in the pulmonary Arthus reaction through G α i2 activation that controls C5aR and Fc receptor cooperation. J. Immunol. 174, 3041-3050. (Pubitemid 40279725)
30. Chouchakova, N., Skokowa, J., Baumann, U., Tschernig, T., Philippens, K. M., Nieswandt, B., Schmidt, R. E., Gessner, J. E. (2001) Fc γ RIIImediated production of TNF-α induces immune complex alveolitis independently of CXC chemokine generation. J. Immunol. 166, 5193-5200. (Pubitemid 32280735)
31. Issekutz, A. C., Meager, A., Otterness, I., Issekutz, T. B. (1994) The role of tumor necrosis factor- and IL-1 in polymorphonuclear leucocyte and T lymphocyte recruitment to joint inflammation in adjuvant arthritis. Clin. Exp. Immunol. 97, 26-32. (Pubitemid 24244050)
32. Calandra, T., Bernhagen, J., Mitchell, R. A., Bucala, R. (1994) The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J. Exp. Med. 179, 1895-1902. (Pubitemid 24155670)
33. Juttner, S., Bernhagen, J., Metz, C. N., Rollinghoff, M., Bucala, R., Gessner, A. (1998) Migration inhibitory factor induces killing of Leishmania major by macrophages: dependence on reactive nitrogen intermediates and endogenous TNF-α. J. Immunol. 161, 2383-2390. (Pubitemid 28397052)
34. Nakamaru, Y., Oridate, N., Nishihira, J., Takagi, D., Furuta, Y., Fukuda, S. (2005) Macrophage migration inhibitory factor (MIF) contributes to the development of allergic rhinitis. Cytokine 31, 103-108. (Pubitemid 40910225)
35. Matsui, Y., Okamoto, H., Jia, N., Akino, M., Uede, T., Kitabatake, A., Nishihira, J. (2004) Blockade of macrophage migration inhibitory factor ameliorates experimental autoimmune myocarditis. J. Mol. Cell. Cardiol. 37, 557-566. (Pubitemid 38953383)
36. Powell, N. D., Papenfuss, T. L., McClain, M. A., Gienapp, I. E., Shawler, T. M., Satoskar, A. R., 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)
37. Paiva, C. N., Arras, R. H., Lessa, L. P., Gibaldi, D., Alves, L., Metz, C. N., Gazzinelli, R., Pyrrho, A. S., Lannes-Vieira, J., Bozza, M. T. (2007) Unraveling the lethal synergism between Trypanosoma cruzi infection and LPS: a role for increased macrophage reactivity. Eur. J. Immunol. 37, 1355-1364. (Pubitemid 46925319)
38. Al-Abed, Y., Dabideen, D., Aljabari, B., Valster, A., Messmer, D., Ochani, M., Tanovic, M., Ochani, K., Bacher, M., Nicoletti, F., Metz, C., Pavlov, V. A., Miller, E. J., Tracey, K. J. (2005) ISO-1 binding to the tautomerase active site of MIF inhibits its pro inflammatory activity and increases survival in severe sepsis. J. Biol. Chem. 280, 36541-36544. (Pubitemid 41587728)
39. Roger, T., Froidevaux, C., Martin, C., Calandra, T. (2003) Macrophage migration inhibitory factor (MIF) regulates host responses to endotoxin through modulation of Toll like receptor 4 (TLR4). J. Endotoxin Res. 9, 119-123. (Pubitemid 36603687)
40. Roger, T., David, J., Glauser, M. P., Calandra, T. (2001) MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature 414, 920-924. (Pubitemid 34024744)
41. Makita, H., Nishimura, M., Miyamoto, K., Nakano, T., Tanino, Y., Hirokawa, J., Nishihira, J., Kawakami, Y. (1998) Effect of anti-macrophage migration inhibitory factor antibody on lipopolysaccharide-induced pulmonary neutrophil accumulation. Am. J. Respir. Crit. Care Med. 158, 573-579. (Pubitemid 28378189)
42. Gao, H., Neff, T., Ward, P. A. (2006) Regulation of lung inflammation in the model of IgG immune-complex injury. Annu. Rev. Pathol. 1, 215-242.
43. Heller, T., Gessner, J. E., Schmidt, R. E., Klos, A., Bautsch, W., Kohl, J. (1999) Cutting edge: Fc receptor type I for IgG on macrophages and complement mediate the inflammatory response in immune complex peritonitis. J. Immunol. 162, 5657-5661. (Pubitemid 29314912)
44. Amin, M. A., Haas, C. S., Zhu, K., Mansfield, P. J., Kim, M. J., Lackowski, N. P., Koch, A. E. (2006) Migration inhibitory factor up-regulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 via Src, PI3 kinase, and NFκB. Blood 107, 2252-2261. (Pubitemid 43345542)
45. 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., 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)
46. Magalhães, E. S., Paiva, C. N., Souza, H. S. P., Pyrrho, A. S., Mourão-Sá, D., Figueiredo, R. T., Vieira-de-Abreu, A., Dutra, H. S., Silveira, M. S., Gaspar-Elsas, M. I., Xavier-Elsas, P., Bozza, P. T., Bozza, M. T. (2008) Macrophage migration inhibitory factor is critical to interleukin-5-driven eosinophilopoiesis and tissue eosinophilia triggered by Schistosoma mansoni infection. FASEB J., Epub ahead of print.
47. Zhang, Y., Ramos, B. F., Jakschik, B. A. (1991) Augmentation of reverse Arthus reaction by mast cells in mice. J. Clin. Invest. 88, 841-846.
48. Baumann, U., Kohl, J., Tschernig, T., Schwerter-Strumpf, K., Verbeek, J. S., Schmidt, R. E., Gessner, J. E. (2000) A codominant role of Fc γ RI/III and C5aR in the reverse Arthus reaction. J. Immunol. 164, 1065-1070. (Pubitemid 30043735)
49. Clynes, R., Maizes, J. S., Guinamard, R., Ono, M., Takai, T., Ravetch, J. V. (1999) Modulation of immune complex-induced inflammation in vivo by the coordinate expression of activation and inhibitory Fc receptors. J. Exp. Med. 189, 179-185. (Pubitemid 29047037)
50. Daryadel, A., Grifone, R. F., Simon, H. U., Yousefi, S. (2006) Apoptotic neutrophils release macrophage migration inhibitory factor upon stimulation with tumor necrosis factor-α. J. Biol. Chem. 281, 27653-27661. (Pubitemid 44401790)
51. Riedemann, N. C., Guo, R. F., Gao, H., Sun, L., Hoesel, M., Hollmann, T. J., Wetsel, R. A., Zetoune, F. S., Ward, P. A. (2004) Regulatory role of C5a on macrophage migration inhibitory factor release from neutrophils. J. Immunol. 173, 1355-1359. (Pubitemid 38924315)
52. Hoi, A. Y., Hickey, M. J., Hall, P., Yamana, J., O'Sullivan, K. M., Santos, L. L., James, W. G., Kitching, A. R., Morand, E. F. (2006) Macrophage migration inhibitory factor deficiency attenuates macrophage recruitment, glomerulonephritis, and lethality in MRL/lpr mice. J. Immunol. 177, 5687-5696. (Pubitemid 44527645)