The role of macrophage migration inhibitory factor in the inflammatory immune response and rheumatoid arthritis

Wiener Medizinische Wochenschrift

Volumn 156, Issue 1-2, 2006, Pages 11-18

  Santos, Leilani L ^a   Morand, Eric F ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Arthritis; Glucocorticoids; Immune response; MIF; Signal transduction

Indexed keywords

B7 ANTIGEN; CD3 ANTIBODY; CD40 ANTIGEN; CD86 ANTIGEN; CYCLOOXYGENASE 2; CYTOKINE; ENDOTOXIN; EXOTOXIN; GAMMA INTERFERON; GLUCOCORTICOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MACROPHAGE MIGRATION INHIBITION FACTOR; MATRIX METALLOPROTEINASE; MESSENGER RNA; NITRIC OXIDE; PHOSPHOLIPASE A2; PROTEIN P53; RECOMBINANT CYTOKINE; TUMOR NECROSIS FACTOR;

APOPTOSIS; CELL HYPERPLASIA; CELL PROLIFERATION; DISEASE ACTIVITY; DISEASE SEVERITY; DRUG INHIBITION; DRUG MECHANISM; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYNOVIAL FLUID; T LYMPHOCYTE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; DISEASE MODELS, ANIMAL; GLUCOCORTICOIDS; HUMANS; HYPERPLASIA; MACROPHAGE MIGRATION-INHIBITORY FACTORS; SIGNAL TRANSDUCTION; SYNOVIAL MEMBRANE;

EID: 32544451352     PISSN: 00435341     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10354-005-0243-8     Document Type: Review

References (79)

1. Bloom BR, Bennett B (1966) Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 153: 80-82
2. Calandra T, Bernhagen J, Mitchell RA, Bucala R (1994) The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 179: 1895-1902
3. Onodera S, Suzuki K, Matsuno T, Kaneda K, Takagi M, Nishihira J (1997) Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion. Immunology 92: 131-137
4. Froidevaux C, Roger T, Martin C, Glauser MP, Calandra T (2001) Macrophage migration inhibitory factor and innate immune responses to bacterial infections. Crit Care Med 29: S13-15
5. Cunha FQ, Weiser WY, David JR, Moss DW, Moncada S, Liew FY (1993) Recombinant migration inhibitory factor induces nitric oxide synthase in murine macrophages. J Immunol 150: 1908-1912
6. Bernhagen J, Mitchell RA, Calandra T, Voelter W, Cerami A, Bucala R (1994) Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration inhibitory factor (MIF). Biochemistry 33: 14144-14155
7. Gregory JL, Leech MT, David JR, Yang YH, Dacumos A, Hickey MJ (2004) Reduced leukocyte-endothelial cell interactions in the inflamed microcirculation of macrophage migration inhibitory factor-deficient mice. Arthritis Rheum 50: 3023-3034
8. Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, Manogue KR, Cerami A, Bucala R (1993) MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 365: 756-759
9. Bozza M, Satoskar AR, Lin G, Lu B, Humbles AA, Gerard C, David JR (1999) Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 189: 341-346
10. Roger T, David J, Glauser MP, Calandra T (2001) MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature 414: 920-924
11. Bacher M, Meinhardt A, Lan HY, Mu W, Metz CN, Chesney JA, Calandra T, Gemsa D, Donnelly T, Atkins RC, Bucala R (1997) Migration inhibitory factor expression in experimentally induced endotoxemia. Am J Pathol 150: 235-246
12. David JR (1966) Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci USA 56: 72-77
13. Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, Gemsa D, Donnelly T, 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
14. Altboum I, Pick E (1979) Antigen and mitogen induced production of macrophage migration inhibitory factor in the mouse. Int Arch Allergy Appl Immunol 60: 29-43
15. Bernhagen J, Bacher M, Calandra T, Metz CN, Doty SB, Donnelly T, Bucala R (1996) An essential role for macrophage migration inhibitory factor in the tuberculin delayed-type hypersensitivity reaction. J Exp Med 183: 277-282
16. Zaitseva MB, Mojcik CF, Salomon DR, Shevach EM, Golding H (1998) Co-ligation of alpha4beta1 integrin and TCR rescues human thymocytes from steroid-induced apoptosis. Int Immunol 10: 1551-1561
17. Santos L, Hall P, Metz C, Bucala R, Morand EF (2001) Role of macrophage migration inhibitory factor (MIF) in murine antigen-induced arthritis: interaction with glucocorticoids. Clin Exp Immunol 123: 309-314
18. Stavitsky AB, Xianli J (2002) In vitro and in vivo regulation by macrophage migration inhibitory factor (MIF) of expression of MHC-II, costimulatory, adhesion, receptor, and cytokine molecules. Cell Immunol 217: 95-104
19. Kitaichi N, Ogasawara K, Iwabuchi K, Nishihira J, Namba K, Onoe K, Konishi J, Kotake S, Matsuda H. Different influence of macrophage migration inhibitory factor (MIF) in signal transduction pathway of various T cell subsets. Immunobiology (2000) 201: 356-367
20. Shimizu T, Abe R, Nishihira J, Shibaki A, Watanabe H, Nakayama T, Taniguchi M, Ishibashi T, Shimizu H (2003) Impaired contact hypersensitivity in macrophage migration inhibitory factor-deficient mice. Eur J Immunol 33: 1478-1487
21. Denkinger CM, Denkinger M, Kort JJ, Metz C, Forsthuber TG (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
22. Abe R, Peng T, Sailors J, Bucala R, Metz CN (2001) Regulation of the CTL response by macrophage migration inhibitory factor. J Immunol 166: 747-753
23. Xu D, McSorley SJ, Tetley L, Chatfield S, Dougan G, Chan WL, Satoskar A, David JR, Liew FY (1998) Protective effect on Leishmania major infection of migration inhibitory factor, TNF-alpha, and IFN-gamma administered orally via attenuated Salmonella typhimurium. J Immunol 160: 1285-1289
24. de Jong YP, Abadia-Molina AC, Satoskar AR, Clarke K, Rietdijk ST, Faubion WA, Mizoguchi E, Metz CN, Alsahli M, ten Hove T, Keates AC, Lubetsky JB, Farrell RJ, Michetti P, van Deventer SJ, Lolis E, David JR, Bhan AK, Terhorst C (2001) Development of chronic colitis is dependent on the cytokine MIF. Nat Immunol 2: 1061-1066
25. Wu J, Cunha FQ, Liew FY, Weiser WY (1993) IL-10 inhibits the synthesis of migration inhibitory factor and migration inhibitory factor-mediated macrophage activation. J Immunol 151: 4325-4332
26. Mikulowska A, Metz CN, 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
27. Leech M, Metz C, Santos L, Peng T, Holdsworth SR, Bucala R, Morand EF (1998) Involvement of macrophage migration inhibitory factor in the evolution of rat adjuvant arthritis. Arthritis Rheum 41: 910-917
28. Leech M, Metz C, Bucala R, Morand EF (2000) Regulation of macrophage migration inhibitory factor by endogenous glucocorticoids in rat adjuvant-induced arthritis. Arthritis Rheum 43: 827-833
29. Leech M, Lacey D, Xue JR, Santos L, Hutchinson P, Wolvetang E, David JR, Bucala R, Morand EF (2003) Regulation of p53 by macrophage migration inhibitory factor in inflammatory arthritis. Arthritis Rheum 48: 1881-1889
30. Ichiyama H, Onodera S, Nishihira J, Ishibashi T, Nakayama T, Minami A, Yasuda K, Tohyama H (2004) Inhibition of joint inflammation and destruction induced by antitype II collagen antibody/lipopolysaccharide (LPS)-induced arthritis in mice due to deletion of macrophage migration inhibitory factor (MIF). Cytokine 26: 187-194
31. Onodera S, Nishihira J, Iwabuchi K, Koyama Y, Yoshida K, Tanaka S, Minami A (2002) Macrophage migration inhibitory factor up-regulates matrix metalloproteinase-9 and -13 in rat osteoblasts. Relevance to intracellular signaling pathways. J Biol Chem 277: 7865-7874
32. Leech M, Metz C, Hall P, Hutchinson P, Gianis K, Smith M, Weedon H, Holdsworth SR, Bucala R, Morand EF (1999) Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids. Arthritis Rheum 42: 1601-1608
33. Onodera S, Tanji H, Suzuki K, Kaneda K, Mizue Y, Sagawa A, Nishihira J (1999) High expression of macrophage migration inhibitory factor in the synovial tissues of rheumatoid joints. Cytokine 11: 163-167
34. Lacey D, Sampey A, Mitchell R, Bucala R, Santos L, Leech M, Morand E (2003) Control of fibroblast-like synoviocyte proliferation by macrophage migration inhibitory factor. Arthritis Rheum 48: 103-109
35. Sampey AV, Hall PH, Mitchell RA, Metz CN, Morand EF (2001) Regulation of synoviocyte phospholipase A2 and cyclooxygenase 2 by macrophage migration inhibitory factor. Arthritis Rheum 44: 1273-1280
36. Onodera S, Nishihira J, Koyama Y, Majima T, Aoki Y, Ichiyama H, Ishibashi T, Minami A (2004) Macrophage migration inhibitory factor up-regulates the expression of interleukin-8 messenger RNA in synovial fibroblasts of rheumatoid arthritis patients: common transcriptional regulatory mechanism between interleukin-8 and interleukin-1beta. Arthritis Rheum 50: 1437-1447
37. Santos LL, Lacey D, Yang Y, Leech M, Morand EF (2004) Activation of synovial cell p38 MAP kinase by macrophage migration inhibitory factor. J Rheumatol 31: 1038-1043
38. 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
39. Morand EF, Leech M, Weedon H, Metz C, Bucala R, Smith MD (2002) Macrophage migration inhibitory factor in rheumatoid arthritis: clinical correlations. Rheumatology (Oxford) 41: 558-562
40. Baugh JA, Chitnis S, Donnelly SC, Monteiro J, Lin X, Plant BJ, Wolfe F, Gregersen PK, Bucala R (2002) A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun 3: 170-176
41. Donn RP, Shelley E, Ollier WE, Thomson W (2001) A novel 5′-flanking region polymorphism of macrophage migration inhibitory factor is associated with systemic-onset juvenile idiopathic arthritis. Arthritis Rheum 44: 1782-1785
42. Donn R, Alourfi Z, De Benedetti F, Meazza C, Zeggini E, Lunt M, Stevens A, Shelley E, Lamb R, Ollier WE, Thomson W, Ray D (2002) Mutation screening of the macrophage migration inhibitory factor gene: positive association of a functional polymorphism of macrophage migration inhibitory factor with juvenile idiopathic arthritis. Arthritis Rheum 46: 2402-2409
43. Donn R, Alourfi Z, Zeggini E, Lamb R, Jury F, Lunt M, Meazza C, De Benedetti F, Thomson W, Ray D (2004) A functional promoter haplotype of macrophage migration inhibitory factor is linked and associated with juvenile idiopathic arthritis. Arthritis Rheum 50: 1604-1610
44. De Benedetti F, Meazza C, Vivarelli M, Rossi F, Pistorio A, Lamb R, Lunt M, Thomson W, Ravelli A, Donn R, Martini A (2003) Functional and prognostic relevance of the -173 polymorphism of the macrophage migration inhibitory factor gene in systemic-onset juvenile idiopathic arthritis. Arthritis Rheum 48: 1398-1407
45. Amoli MM, Garcia-Porrua C, Ollier WE, Gonzalez-Gay MA (2005) Lack of association between macrophage migration inhibitory factor gene polymorphism and giant cell arteritis. J Rheumatol 32: 74-76
46. Nohara H, Okayama N, Inoue N, Koike Y, Fujimura K, Suehiro Y, Hamanaka Y, Higaki S, Yanai H, Yoshida T, Hibi T, Okita K, Hinoda Y (2004) Association of the -173 G/C polymorphism of the macrophage migration inhibitory factor gene with ulcerative colitis. J Gastroenterol 39: 242-246
47. Gregersen PK, Bucala R (2003) Macrophage migration inhibitory factor, MIF alleles, and the genetics of inflammatory disorders: incorporating disease outcome into the definition of phenotype. Arthritis Rheum 48: 1171-1176
48. Radstake TR, Sweep FC, Welsing P, Franke B, Vermeulen SH, Geurts-Moespot A, Calandra T, Donn R, van Riel PL (2005) Correlation of rheumatoid arthritis severity with the genetic functional variants and circulating levels of macrophage migration inhibitory factor. Arthritis Rheum 52: 3020-3029
49. Bucala R (2000) Signal transduction. A most interesting factor. Nature 408: 146-147
50. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R (2003) MIF signal transduction initiated by binding to CD74. J Exp Med 197: 1467-1476
51. Firestein GS, Manning AM (1999) Signal transduction and transcription factors in rheumatic disease. Arthritis Rheum 42: 609-621
52. Kyriakis JM, Avruch J (1996) Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays 18: 567-577
53. Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, 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 USA 99: 345-350
54. Ren Y, Chan HM, Li Z, Lin C, Nicholls J, Chen CF, Lee PY, Lui V, Bacher M, Tam PK (2004) Upregulation of macrophage migration inhibitory factor contributes to induced N-Myc expression by the activation of ERK signaling pathway and increased expression of interleukin-8 and VEGF in neuroblastoma. Oncogene 23: 4146-4154
55. Sun B, Nishihira J, Suzuki M, Fukushima N, Ishibashi T, Kondo M, Sato Y, Todo S (2003) Induction of macrophage migration inhibitory factor by lysophosphatidic acid: relevance to tumor growth and angiogenesis. Int J Mol Med 12: 633-641
56. Watanabe H, Shimizu T, Nishihira J, Abe R, Nakayama T, Taniguchi M, Sabe H, Ishibashi T, Shimizu H (2004) Ultraviolet A-induced production of matrix metalloproteinase-1 is mediated by macrophage migration inhibitory factor (MIF) in human dermal fibroblasts. J Biol Chem 279: 1676-1683
57. Amin MA, Volpert OV, Woods JM, Kumar P, Harlow LA, Koch AE (2003) Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase. Circ Res 93: 321-329
58. Barnes PJ, Karin M (1997) Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 336: 1066-1071
59. Cao WG, Morin M, Metz C, Maheux R, Akoum A (2005) Stimulation of Macrophage Migration Inhibitory Factor Expression in Endometrial Stromal Cells by Interleukin 1,{beta} Involving the Nuclear Transcription Factor NF{kappa}B. Biol Reprod 73: 565-570
60. Kleemann R, Hausser A, Geiger G, Mischke R, Burger-Kentischer A, Flieger O, Johannes FJ, Roger T, Calandra T, Kapurniotu A, Grell M, Finkelmeier D, Brunner H, Bernhagen J (2005) Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 408: 211-216
61. Rehli M, Poltorak A, Schwarzfischer L, Krause SW, Andreesen R, Beutler B (2000) PU.1 and interferon consensus sequence-binding protein regulate the myeloid expression of the human Toll-like receptor 4 gene. J Biol Chem 275: 9773-9781
62. Kleemann R, Grell M, Mischke R, Zimmermann G, Bernhagen J (2002) Receptor binding and cellular uptake studies of macrophage migration inhibitory factor (MIF): use of biologically active labeled MIF derivatives. J Interferon Cytokine Res 22: 351-363
63. Stephanou A, Sarlis NJ, Knight RA, Lightman SL, Chowdrey HS (1992) Glucocorticoid-mediated responses of plasma ACTH and anterior pituitary pro-opiomelanocortin, growth hormone and prolactin mRNAs during adjuvant-induced arthritis in the rat. J Mol Endocrinol 9: 273-281
64. Harbuz MS, Stephanou A, Sarlis N, Lightman SL (1992) The effects of recombinant human interleukin (IL)-1 alpha, IL-1 beta or IL-6 on hypothalamo-pituitary-adrenal axis activation. J Endocrinol 133: 349-355
65. Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A, Bucala R (1995) MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377: 68-71
66. Vedder H, Krieg JC, Gerlach B, Gemsa D, Bacher M (2000) Expression and glucocorticoid regulation of macrophage migration inhibitory factor (MIF) in hippocampal and neocortical rat brain cells in culture. Brain Res 869: 25-30
67. Delbrouck C, Gabius HJ, Vandenhoven G, Kiss R, Hassid S (2004) Budesonide-dependent modulation of expression of macrophage migration inhibitory factor in a polyposis model: evidence for differential regulation in surface and glandular epithelia. Ann Otol Rhinol Laryngol 113: 544-551
68. Tierney T, Patel R, Stead CA, Leng L, Bucala R, Buckingham JC (2005) Macrophage migration inhibitory factor is released from pituitary folliculo-stellate-like cells by endotoxin and dexamethasone and attenuates the steroid-induced inhibition of interleukin 6 release. Endocrinology 146: 35-43
69. Fingerle-Rowson G, Koch P, Bikoff R, Lin X, Metz CN, Dhabhar FS, Meinhardt A, Bucala R (2003) Regulation of macrophage migration inhibitory factor expression by glucocorticoids in vivo. Am J Pathol 162: 47-56
70. Kitaichi N, Kotake S, Mizue Y, Sasamoto Y, Goda C, Iwabuchi K, Onoe K, Matsuda H, Nishihira J (2000) High-dose corticosteroid administration induces increase of serum macrophage migration inhibitory factor in patients with Vogt-Koyanagi-Harada's disease. Microbiol Immunol 44: 1075-1077
71. Foote A, Briganti EM, Kipen Y, Santos L, Leech M, Morand EF (2004) Macrophage migration inhibitory factor in systemic lupus erythematosus. J Rheumatol 31: 268-273
72. Calandra T, Bucala R (1997) Macrophage migration inhibitory factor (MIF): a glucocorticoid counter-regulator within the immune system. Crit Rev Immunol 17: 77-88
73. Donnelly SC, Haslett C, Reid PT, Grant IS, Wallace WA, Metz CN, Bruce LJ, Bucala R (1997) Regulatory role for macrophage migration inhibitory factor in acute respiratory distress syndrome. Nat Med 3: 320-323
74. Daun JM, Cannon JG (2000) Macrophage migration inhibitory factor antagonizes hydrocortisone-induced increases in cytosolic IkappaBalpha. Am J Physiol Regul Integr Comp Physiol 279: R1043-1049
75. Slack DN, Seternes OM, Gabrielsen M, Keyse SM (2001) Distinct binding determinants for ERK2/p38alpha and JNK map kinases mediate catalytic activation and substrate selectivity of map kinase phosphatase-1. J Biol Chem 276: 16491-16500
76. Bresnihan B, Alvaro-Gracia JM, Cobby M, Doherty M, Domljan Z, Emery P, Nuki G, Pavelka K, Rau R, Rozman B, Watt I, Williams B, Aitchison R, McCabe D, Musikic P (1998) Treatment of rheumatoid arthritis with recombinant human interleukin-1 receptor antagonist. Arthritis Rheum 41: 2196-2204
77. Moreland LW, Schiff MH, Baumgartner SW, Tindall EA, Fleischmann RM, Bulpitt KJ, Weaver AL, Keystone EC, Furst DE, Mease PJ, Ruderman EM, Horwitz DA, Arkfeld DG, Garrison L, Burge DJ, Blosch CM, Lange ML, McDonnell ND, Weinblatt ME (1999) Etanercept therapy in rheumatoid arthritis. A randomized, controlled trial. Ann Intern Med 130: 478-486
78. Targan SR, Hanauer SB, van Deventer SJ, Mayer L, Present DH, Braakman T, DeWoody KL, Schaible TF, Rutgeerts PJ (1997) A short-term study of chimeric monoclonal antibody cA2 to tumor necrosis factor alpha for Crohn's disease. Crohn's Disease cA2 Study Group. N Engl J Med 337: 1029-1035
79. Maini R, St Clair, EW Breedveld F, Furst D, Kalden J, Weisman M, Smolen J, Emery P, Harriman G, Feldmann M, Lipsky P (1999) Infliximab (chimeric anti-tumour necrosis factor alpha monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: a randomised phase III trial. ATTRACT Study Group. Lancet 354: 1932-1939