MIF: a new cytokine link between rheumatoid arthritis and atherosclerosis (original) (raw)
Charo, I. F. & Ransohoff, R. M. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med.354, 610–621 (2006). ArticleCASPubMed Google Scholar
David, J. R. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc. Natl Acad. Sci. USA56, 72–77 (1966). ArticleCASPubMedPubMed Central Google Scholar
Sorg, C. Characterization of murine macrophage migration inhibitory activities (MIF) released by concanavalin A stimulated thymus or spleen cells. Mol. Immunol.17, 565–569 (1980). ArticleCASPubMed Google Scholar
Smolen, J. S. & Steiner, G. Therapeutic strategies for rheumatoid arthritis. Nature Rev. Drug Discov.2, 473–488 (2003). ArticleCAS Google Scholar
Mikulowska, A., Metz, C. N., Bucala, R. & Holmdahl, R. Macrophage migration inhibitory factor is involved in the pathogenesis of collagen type II-induced arthritis in mice. J. Immunol.158, 5514–5517 (1997). The first report of the participation of MIF in an animal model of RA. CASPubMed Google Scholar
Leech, M. et al. Involvement of macrophage migration inhibitory factor in the evolution of rat adjuvant arthritis. Arthritis Rheum.41, 910–917 (1998). ArticleCASPubMed Google Scholar
Leech, M., Metz, C., Bucala, R. & Morand, E. F. Regulation of macrophage migration inhibitory factor by endogenous glucocorticoids in rat adjuvant-induced arthritis. Arthritis Rheum.43, 827–833 (2000). ArticleCASPubMed Google Scholar
Santos, L. L., Hall, P., Metz, C. N., Bucala, R. & Morand, E. F. Role of macrophage migration inhibitory factor (MIF) in murine antigen-induced arthritis: interaction with glucocorticoids. Clin. Exp. Immunol.123, 309–314 (2001). ArticleCASPubMedPubMed Central Google Scholar
Bernhagen, J. et al. An essential role for macrophage migration inhibitory factor in the tuberculin delayed-type hypersensitivity reaction. J. Exp. Med.183, 277–282 (1996). ArticleCASPubMed Google Scholar
Onodera, S. et al. 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-1β. Arthritis Rheum.50, 1437–1447 (2004). ArticleCASPubMed Google Scholar
Ichiyama, H. et al. Inhibition of joint inflammation and destruction induced by anti-type II collagen antibody/lipopolysaccharide (LPS)-induced arthritis in mice due to deletion of macrophage migration inhibitory factor (MIF). Cytokine26, 187–194 (2004). ArticleCASPubMed Google Scholar
Leech, M. et al. Regulation of p53 by macrophage migration inhibitory factor (MIF) in inflammatory arthritis. Arthritis Rheum.48, 1881–1889 (2003). The firstin vivodemonstration of the regulatory effect of MIF on p53 and apoptosis, which was confirmedin vitroin human RA cells. ArticleCASPubMed Google Scholar
Gregory, J. L. et al. Reduced leukocyte–endothelial cell interactions in the inflamed microcirculation of macrophage migration inhibitory factor-deficient mice. Arthritis Rheum.50, 3023–3034 (2004). ArticleCASPubMed Google Scholar
Leech, M. et al. Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids. Arthritis Rheum.42, 1601–1608 (1999). ArticleCASPubMed Google Scholar
Onodera, S. et al. High expression of macrophage migration inhibitory factor in the synovial tissues of rheumatoid joints. Cytokine11, 163–167 (1999). ArticleCASPubMed Google Scholar
Morand, E. F. et al. Macrophage migration inhibitory factor in rheumatoid arthritis: clinical correlations. Rheumatology (Oxford)41, 558–562 (2002). ArticleCAS Google Scholar
Sampey, A. V., Hall, P. H., Mitchell, R. A., Metz, C. N. & Morand, E. F. Regulation of synoviocyte phospholipase A2 and cyclooxygenase 2 by macrophage migration inhibitory factor. Arthritis Rheum.44, 1273–1280 (2001). ArticleCASPubMed Google Scholar
Santos, L., Lacey, D. C., Yang, Y., Leech, M. & Morand, E. F. Activation of synovial cell p38 MAP kinase by macrophage migration inhibitory factor (MIF). J. Rheumatol.31, 1038–1043 (2004). CASPubMed Google Scholar
Onodera, S. et al. Macrophage migration inhibitory factor up-regulates expression of matrix metalloproteinases in synovial fibroblasts of rheumatoid arthritis. J. Biol. Chem.275, 444–450 (2000). ArticleCASPubMed Google Scholar
Onodera, S. et al. 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 (2002). ArticleCASPubMed Google Scholar
Lacey, D. et al. Control of fibroblast-like synoviocyte proliferation by macrophage migration inhibitory factor. Arthritis Rheum.48, 103–109 (2003). ArticleCASPubMed Google Scholar
Mitchell, R. A. et al. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc. Natl Acad. Sci. USA99, 345–350 (2002). ArticleCASPubMed Google Scholar
Baugh, J. A. et al. A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun.3, 170–176 (2002). ArticleCASPubMed Google Scholar
Radstake, T. R. et al. Correlation of rheumatoid arthritis severity with the genetic functional variants and circulating levels of macrophage migration inhibitory factor. Arthritis Rheum.52, 3020–3029 (2005). ArticleCASPubMed Google Scholar
Donn, R. et al. A functional promoter haplotype of macrophage migration inhibitory factor is linked and associated with juvenile idiopathic arthritis. Arthritis Rheum.50, 1604–1610 (2004). ArticlePubMed Google Scholar
Donn, R. P. et al. Macrophage migration inhibitory factor gene polymorphism is associated with psoriasis. J. Invest. Dermatol.123, 484–487 (2004). ArticleCASPubMed Google Scholar
Amoli, M. M. et al. Macrophage migration inhibitory factor gene polymorphism is associated with sarcoidosis in biopsy proven erythema nodosum. J. Rheumatol.29, 1671–1673 (2002). CASPubMed Google Scholar
Nohara, H. et al. Association of the −173 G/C polymorphism of the macrophage migration inhibitory factor gene with ulcerative colitis. J. Gastroenterol.39, 242–246 (2004). ArticleCASPubMed Google Scholar
Nissen, S. E. et al. Statin therapy, LDL cholesterol, C-reactive protein, and coronary artery disease. N. Engl. J. Med.352, 29–38 (2005). ArticleCASPubMed Google Scholar
Hansson, G. K., Libby, P., Schonbeck, U. & Yan, Z. Q. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ. Res.91, 281–291 (2002). ArticleCASPubMed Google Scholar
Schober, A. & Weber, C. Mechanisms of monocyte recruitment in vascular repair after injury. Antioxid. Redox Signal.7, 1249–1257 (2005). ArticleCASPubMed Google Scholar
Burger-Kentischer, A. et al. Expression of macrophage migration inhibitory factor in different stages of human atherosclerosis. Circulation105, 1561–1566 (2002). ArticleCASPubMed Google Scholar
Burger-Kentischer, A. et al. Reduction of the aortic inflammatory response in spontaneous atherosclerosis by blockade of macrophage migration inhibitory factor (MIF). Atherosclerosis184, 28–38 (2006). ArticleCASPubMed Google Scholar
Lin, S. G. et al. De novo expression of macrophage migration inhibitory factor in atherogenesis in rabbits. Circ. Res.87, 1202–1208 (2000). ArticleCASPubMed Google Scholar
Pan, J. H. et al. Macrophage migration inhibitory factor deficiency impairs atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation109, 3149–3153 (2004). ArticleCASPubMed Google Scholar
Ip, J. H. et al. Syndromes of accelerated atherosclerosis: role of vascular injury and smooth muscle cell proliferation. J. Am. Coll. Cardiol.15, 1667–1687 (1990). ArticleCASPubMed Google Scholar
Shah, P. K. Inflammation, neointimal hyperplasia, and restenosis: as the leukocytes roll, the arteries thicken. Circulation107, 2175–2177 (2003). ArticlePubMed Google Scholar
Chen, Z. et al. Evidence for a role of macrophage migration inhibitory factor in vascular disease. Arterioscler. Thromb. Vasc. Biol.24, 709–714 (2004). ArticleCASPubMed Google Scholar
Schober, A. et al. Stabilization of atherosclerotic plaques by blockade of macrophage migration inhibitory factor after vascular injury in apolipoprotein E-deficient mice. Circulation109, 380–385 (2004). ArticleCASPubMed Google Scholar
Pan, J. H. et al. Macrophage migration inhibitory factor is associated with aneurysmal expansion. J. Vasc. Surg.37, 628–635 (2003). ArticleCASPubMed Google Scholar
Atsumi, T., Nishihira, J., Makita, Z. & Koike, T. Enhancement of oxidised low-density lipoprotein uptake by macrophages in response to macrophage migration inhibitory factor. Cytokine12, 1553–1556 (2000). ArticleCASPubMed Google Scholar
Verschuren, L. et al. Up-regulation and coexpression of MIF and matrix metalloproteinases in human abdominal aortic aneurysms. Antioxid. Redox Signal.7, 1195–1202 (2005). ArticleCASPubMed Google Scholar
Kong, Y. Z. et al. Macrophage migration inhibitory factor induces MMP-9 expression: implications for destabilization of human atherosclerotic plaques. Atherosclerosis178, 207–215 (2005). ArticleCASPubMed Google Scholar
Kong, Y. Z. et al. Evidence for vascular macrophage migration inhibitory factor in destabilization of human atherosclerotic plaques. Cardiovasc. Res.65, 272–282 (2005). ArticleCASPubMed Google Scholar
Kusuhara, M., Chait, A., Cader, A. & Berk, B. C. Oxidized LDL stimulates mitogen-activated protein kinases in smooth muscle cells and macrophages. Arterioscler. Thromb. Vasc. Biol.17, 141–148 (1997). ArticleCASPubMed Google Scholar
Hudson, J. D. et al. A proinflammatory cytokine inhibits p53 tumor suppressor activity. J. Exp. Med.190, 1375–1382 (1999). The first report of the unique inhibitory effect of MIF on p53 activity. ArticleCASPubMedPubMed Central Google Scholar
Mitchell, R. A. et al. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc. Natl Acad. Sci. USA99, 345–350 (2002). Demonstration that the inhibitory effects of MIF on p53 are mediated via downregulation of p53 protein and involve cyclooxygenase 2. ArticleCASPubMed Google Scholar
Simelyte, E. et al. Regulation of arthritis by p53: critical role of adaptive immunity. Arthritis Rheum.52, 1876–1884 (2005). ArticleCASPubMed Google Scholar
Mercer, J., Figg, N., Stoneman, V., Braganza, D. & Bennett, M. R. Endogenous p53 protects vascular smooth muscle cells from apoptosis and reduces atherosclerosis in ApoE knockout mice. Circ. Res.96, 667–674 (2005). Describes the role of p53 in atherosclerosis in a model of atheroma. ArticleCASPubMed Google Scholar
Asanuma, Y. et al. Premature coronary-artery atherosclerosis in systemic lupus erythematosus. N. Engl. J. Med.349, 2407–2415 (2003). ArticleCASPubMed Google Scholar
Roman, M. J. et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N. Engl. J. Med.349, 2399–2406 (2003). ArticleCASPubMed Google Scholar
Van Doornum, S., McColl, G. & Wicks, I. P. Accelerated atherosclerosis: an extraarticular feature of rheumatoid arthritis? Arthritis Rheum.46, 862–873 (2002). ArticleCASPubMed Google Scholar
del Rincon, I. D., Williams, K., Stern, M. P., Freeman, G. L. & Escalante, A. High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum.44, 2737–2745 (2001). ArticleCASPubMed Google Scholar
Foote, A. et al. Macrophage migration inhibitory factor in systemic lupus erythematosus. J. Rheumatol.31, 268–273 (2004). CASPubMed Google Scholar
Walsh, L. J., Wong, C. A., Pringle, M. & Tattersfield, A. E. Use of oral corticosteroids in the community and the prevention of secondary osteoporosis: a cross sectional study. Brit. Med. J.313, 344–346 (1996). ArticleCASPubMedPubMed Central Google Scholar
Genovese, M. C. et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor α inhibition. N. Engl. J. Med.353, 1114–1123 (2005). ArticleCASPubMed Google Scholar
Yang, Y. et al. Modulation of inflammation and response to dexamethasone by annexin-1 in antigen-induced arthritis. Arthritis Rheum.50, 976–984 (2004). ArticleCASPubMed Google Scholar
Auphan, N., DiDonato, J. A., Rosette, C., Helmberg, A. & Karin, M. Immunosuppression by glucocorticoids: inhibition of NF-κB activity through induction of IκB synthesis. Science270, 286–290 (1995). ArticleCASPubMed Google Scholar
Ito, K. et al. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-κB suppression. J. Exp. Med.203, 7–13 (2006). ArticleCASPubMedPubMed Central Google Scholar
Choi, J. H. et al. Trichostatin A exacerbates atherosclerosis in low density lipoprotein receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol.25, 2404–2409 (2005). ArticleCASPubMed Google Scholar
Wiley, R. E. et al. Transient corticosteroid treatment permanently amplifies the Th2 response in a murine model of asthma. J. Immunol.172, 4995–5005 (2004). ArticleCASPubMed Google Scholar
Calandra, T. et al. MIF as a glucocorticoid-induced modulator of cytokine production. Nature377, 68–71 (1995). The first report of the unique relationship between MIF and glucocorticoids. ArticleCASPubMed Google Scholar
Roger, T., Chanson, A. L., Knaup-Reymond, M. & Calandra, T. Macrophage migration inhibitory factor promotes innate immune responses by suppressing glucocorticoid-induced expression of mitogen-activated protein kinase phosphatase-1. Eur. J. Immunol.35, 3405–3413 (2005). Describes the mechanism of MIF-mediated reversal of the anti-inflammatory effects of glucocorticoids, which involves MAP kinase phosphatase 1. ArticleCASPubMed Google Scholar
Aeberli, D. et al. Endogenous macrophage migration inhibitory factor modulates glucocorticoid sensitivity in macrophages via effects on MAP kinase phosphatase-1 and p38 MAP kinase. FEBS Lett.580, 974–981 (2006). Reports that cells obtained from MIF-deficient mice have increased sensitivity to glucocorticoids. ArticleCASPubMed Google Scholar
Sapolsky, R. M., Romero, L. M. & Munck, A. U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev.21, 55–89 (2000). CASPubMed Google Scholar
Munck, A., Guyre, P. M. & Holbrook, N. J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev.5, 25–44 (1984). ArticleCASPubMed Google Scholar
Dhabhar, F. S. & McEwen, B. S. Enhancing versus suppressive effects of stress hormones on skin immune function. Proc. Natl Acad. Sci. USA96, 1059–1064 (1999). ArticleCASPubMedPubMed Central Google Scholar
Galon, J. et al. Gene profiling reveals unknown enhancing and suppressive actions of glucocorticoids on immune cells. FASEB J.16, 61–71 (2002). ArticleCASPubMed Google Scholar
Barnes, P. J. Anti-inflammatory actions of glucocorticoids — molecular mechanisms. Clin. Sci.94, 557–572 (1998). ArticleCAS Google Scholar
Faggiano, A. et al. Cardiovascular risk factors and common carotid artery caliber and stiffness in patients with Cushing's disease during active disease and 1 year after disease remission. J. Clin. Endocrinol. Metab.88, 2527–2533 (2003). ArticleCASPubMed Google Scholar
Colao, A. et al. Persistence of increased cardiovascular risk in patients with Cushing's disease after five years of successful cure. J. Clin. Endocrinol. Metab.84, 2664–2672 (1999). CASPubMed Google Scholar
Pivonello, R., Faggiano, A., Lombardi, G. & Colao, A. The metabolic syndrome and cardiovascular risk in Cushing's syndrome. Endocrinol. Metab. Clin. North Am.34, 327–339, viii (2005). ArticleCASPubMed Google Scholar
Kirilov, G. et al. Elevated plasma endothelin as an additional cardiovascular risk factor in patients with Cushing's syndrome. Eur. J. Endocrinol.149, 549–553 (2003). ArticleCASPubMed Google Scholar
Hurwitz Eller, N., Netterstrom, B. & Hansen, A. M. Cortisol in urine and saliva: relations to the intima media thickness, IMT. Atherosclerosis159, 175–185 (2001). ArticleCASPubMed Google Scholar
Maddali, K. K., Korzick, D. H., Turk, J. R. & Bowles, D. K. Isoform-specific modulation of coronary artery PKC by glucocorticoids. Vascul. Pharmacol.42, 153–162 (2005). ArticleCASPubMed Google Scholar
Hermanowski-Vosatka, A. et al. 11β-HSD1 inhibition ameliorates metabolic syndrome and prevents progression of atherosclerosis in mice. J. Exp. Med.202, 517–527 (2005). Reports the role of glucocorticoids in accelerating atherosclerosis. ArticleCASPubMedPubMed Central Google Scholar
Feldmann, M. et al. Future prospects for anti-cytokine treatment. Ann. Rheum. Dis.59 (Suppl. 1), 119–122 (2000). Article Google Scholar
Taylor, P. C., Williams, R. O. & Feldmann, M. Tumour necrosis factor α as a therapeutic target for immune-mediated inflammatory diseases. Curr. Opin. Biotechnol.15, 557–563 (2004). ArticleCASPubMed Google Scholar
Thomson, A. W. The Cytokine Handbook (Academic, New York, 2003). Google Scholar
Pugsley, M. K. Etanercept. Immunex. Curr. Opin. Investig. Drugs2, 1725–1731 (2001). CASPubMed Google Scholar
Toussirot, E. & Wendling, D. The use of TNF-α blocking agents in rheumatoid arthritis: an overview. Expert Opin. Pharmacother.5, 581–594 (2004). ArticleCASPubMed Google Scholar
Braddock, M. & Quinn, A. Targeting IL-1 in inflammatory disease: new opportunities for therapeutic intervention. Nature Rev. Drug Discov.3, 330–339 (2004). ArticleCAS Google Scholar
Calandra, T. et al. Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nature Med.6, 164–170 (2000). ArticleCASPubMed Google Scholar
Bernhagen, J. et al. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature365, 756–759 (1993). ArticleCASPubMed Google Scholar
Sakai, Y. et al. Macrophage migration inhibitory factor is a critical mediator of severe acute pancreatitis. Gastroenterology124, 725–736 (2003). ArticleCASPubMed Google Scholar
Meyer-Siegler, K. L., Leifheit, E. C. & Vera, P. L. Inhibition of macrophage migration inhibitory factor decreases proliferation and cytokine expression in bladder cancer cells. BMC Cancer4, 34 (2004). ArticlePubMedPubMed CentralCAS Google Scholar
Palladino, M. A., Bahjat, F. R., Theodorakis, E. A. & Moldawer, L. L. Anti-TNF-α therapies: the next generation. Nature Rev. Drug Discov.2, 736–746 (2003). ArticleCAS Google Scholar
Thiele, M. & Bernhagen, J. Link between macrophage migration inhibitory factor and cellular redox regulation. Antioxid. Redox Signal.7, 1234–1248 (2005). ArticleCASPubMed Google Scholar
Kleemann, R. et al. Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as a thiol-protein oxidoreductase. J. Mol. Biol.280, 85–102 (1998). ArticleCASPubMed Google Scholar
Rosengren, E. et al. The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction. Mol. Med.2, 143–149 (1996). The first demonstration that human MIF has enzymatic activity. ArticleCASPubMedPubMed Central Google Scholar
Rosengren, E. et al. The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase. FEBS Lett.417, 85–88 (1997). ArticleCASPubMed Google Scholar
Swope, M., Sun, H.-W., Blake, P. R. & Lolis, E. Direct link between cytokine activity and a catalytic site for macrophage migration inhibitory factor. EMBO J.1, 3534–3541 (1998). Article Google Scholar
Bendrat, K. et al. Biochemical and mutational investigations of the enzymatic activity of macrophage migration inhibitory factor. Biochemistry36, 15356–15362 (1997). ArticleCASPubMed Google Scholar
Hermanowski-Vosatka, A. et al. Enzymatically inactive macrophage migration inhibitory factor inhibits monocyte chemotaxis and random migration. Biochemistry38, 12841–12849 (1999). ArticleCASPubMed Google Scholar
Kleemann, R., Kapurniotu, A., Mischke, R., Held, J. & Bernhagen, J. Characterization of catalytic centre mutants of macrophage migration inhibitory factor (MIF) and comparison to Cys81Ser MIF. Eur. J. Biochem.261, 753–766 (1999). ArticleCASPubMed Google Scholar
Kleemann, R. et al. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature408, 211–216 (2000). ArticleCASPubMed Google Scholar
Stamps, S. L., Fitzgerald, M. C. & Whitman, C. P. Characterization of the role of the amino-terminal proline in the enzymatic activity catalyzed by macrophage migration inhibitory factor. Biochemistry37, 10195–10202 (1998). Describes the structural characterization of the MIF catalytic pocket. ArticleCASPubMed Google Scholar
Lubetsky, J. B., Swope, M., Dealwis, C., Blake, P. & Lolis, E. Pro-1 of macrophage migration inhibitory factor functions as a catalytic base in the phenylpyruvate tautomerase activity. Biochemistry38, 7346–7354 (1999). ArticleCASPubMed Google Scholar
Philo, J. S., Yang, T. H. & LaBarre, M. Re-examining the oligomerization state of macrophage migration inhibitory factor (MIF) in solution. Biophys. Chem.108, 77–87 (2004). ArticleCASPubMed Google Scholar
Jasanoff, A., Wagner, G. & Wiley, D. C. Structure of a trimeric domain of the MHC class II-associated chaperonin and targeting protein Ii. EMBO J.17, 6812–6818 (1998). ArticleCASPubMedPubMed Central Google Scholar
Taylor, A. B. et al. Crystal structure of macrophage migration inhibitory factor complexed with (E)-2-fluoro-_p_-hydroxycinnamate at 1.8 Å resolution: implications for enzymatic catalysis and inhibition. Biochemistry38, 7444–7452 (1999). ArticleCASPubMed Google Scholar
Orita, M., Yamamoto, S., Katayama, N. & Fujita, S. Macrophage migration inhibitory factor and the discovery of tautomerase inhibitors. Curr. Pharm. Des.8, 1297–1317 (2002). ArticleCASPubMed Google Scholar
Morand, E. F., Leech, M. & Iskander, M. Therapeutic opportunities for antagonism of macrophage migration inhibitory factor. Expert Opin. Ther. Patents8, 1189–1212 (2003). Article Google Scholar
Dios, A. et al. Inhibition of MIF bioactivity by rational design of pharmacological inhibitors of MIF tautomerase activity. J. Med. Chem.45, 2410–2416 (2002). ArticleCASPubMed Google Scholar
Lubetsky, J. B. et al. The tautomerase activity of MIF is a potential target for discovery of novel anti-inflammatory agents. J. Biol. Chem.277, 24976–24982 (2002). ArticleCASPubMed Google Scholar
Senter, P. D. et al. Inhibition of macrophage migration inhibitory factor (MIF) tautomerase and biological activities by acetaminophen metabolites. Proc. Natl Acad. Sci. USA99, 144–149 (2002). ArticleCASPubMedPubMed Central Google Scholar
Zhuang, S. et al. Some insights into the stereochemistry of inhibition of macrophage migration inhibitory factor with 2-fluoro-_p_-hydroxycinnamate and its analogues from molecular dynamics simulations. J. Med. Chem.48, 7208–7214 (2005). ArticleCASPubMed Google Scholar
Nguyen, M. T. et al. A sixteen residue peptide fragment of macrophage migration inhibitory factor, MIF(50–65), exhibits redox activity and has MIF-like biological functions. J. Biol. Chem.278, 33654–33671 (2003). ArticleCASPubMed Google Scholar
Petrenko, O., Fingerle-Rowson, G., Peng, T., Mitchell, R. A. & Metz, C. N. MIF-deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation. J. Biol. Chem.278, 11078–11085 (2003). ArticleCASPubMed Google Scholar
Petrenko, O. & Moll, U. M. Macrophage migration inhibitory factor MIF interferes with the Rb-E2F pathway. Mol. Cell17, 225–236 (2005). ArticleCASPubMed Google Scholar
Nguyen, M. T. et al. The cytokine macrophage migration inhibitory factor reduces pro-oxidative stress-induced apoptosis. J. Immunol.170, 3337–3347 (2003). ArticleCASPubMed Google Scholar
Wadgaonkar, R. et al. Intracellular interaction of myosin light chain kinase with macrophage migration inhibition factor (MIF) in endothelium. J. Cell. Biochem.95, 849–858 (2005). ArticleCASPubMed Google Scholar
Swant, J. D., Rendon, B. E., Symons, M. & Mitchell, R. A. Rho GTPase-dependent signaling is required for MIF-mediated expression of cyclin D1. J. Biol. Chem.280, 23066–23072 (2005). ArticleCASPubMed Google Scholar
Jung, H., Kim, T., Chae, H. Z., Kim, K. T. & Ha, H. Regulation of macrophage migration inhibitory factor and thiol-specific antioxidant protein PAG by direct interaction. J. Biol. Chem.276, 15504–15510 (2001). ArticleCASPubMed Google Scholar
Lue, H. et al. Rapid and transient activation of the ERK MAPK signalling pathway by macrophage migration inhibitory factor (MIF) and dependence on JAB1/CSN5 and Src kinase activity. Cell Signal.18, 688–703 (2006). ArticleCASPubMed Google Scholar
Kleemann, R. et al. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature408, 211–216 (2000). ArticleCASPubMed Google Scholar
Roger, T., David, J., Glauser, M. & Calandra, T. MIF regulates innate immune responses through modulation of Toll-like receptor-4. Nature414, 920–924 (2001). ArticleCASPubMed Google Scholar
Al-Abed, Y. et al. 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 (2005). The firstin vivodemonstration of the beneficial effects of small-molecule MIF antagonists. ArticleCASPubMed Google Scholar
Cvetkovic, I. et al. Critical role of macrophage migration inhibitory factor (MIF) activity in experimental autoimmune diabetes. Endocrinology146, 2942–2951 (2005). ArticleCASPubMed Google Scholar
Bacher, M. et al. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc. Natl Acad. Sci. USA93, 7849–7854 (1996). ArticleCASPubMedPubMed Central Google Scholar
Calandra, T., Bernhagen, J., Mitchell, R. A. & Bucala, R. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J. Exp. Med.179, 1895–1902 (1994). ArticleCASPubMed Google Scholar
Mitchell, R. A., Metz, C. N., Peng, T. & Bucala, R. Sustained mitogen-activated 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 (1999). ArticleCASPubMed Google Scholar
Chesney, J. et al. An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol. Med.5, 181–191 (1999). ArticleCASPubMedPubMed Central Google Scholar
Lacey, D. C. et al. Control of fibroblast-like synoviocyte proliferation by macrophage migration inhibitory factor (MIF). Arthritis Rheum.48, 103–109 (2003). ArticleCASPubMed Google Scholar