Home LiteratureArticle Details
PMID: 14502271 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Macrophage migration inhibitory factor: a regulator of innate immunity.

Nature reviews. Immunology ·Vol. 3 ·No. 10 ·2003-10-00 ·Pages 791-800

Calandra T, Roger T

Abstract

For more than a quarter of a century, macrophage migration inhibitory factor (MIF) has been a mysterious cytokine. In recent years, MIF has assumed an important role as a pivotal regulator of innate immunity. MIF is an integral component of the host antimicrobial alarm system and stress response that promotes the pro-inflammatory functions of immune cells. A rapidly increasing amount of literature indicates that MIF is implicated in the pathogenesis of sepsis, and inflammatory and autoimmune diseases, suggesting that MIF-directed therapies might offer new treatment opportunities for human diseases in the future.

MeSH Terms
Animals Autoimmune Diseases/etiology,immunology Humans Immunity, Innate/genetics,immunology Inflammation/etiology,immunology Macrophage Migration-Inhibitory Factors/genetics,immunology Macrophages/immunology Sepsis/etiology,immunology
Chemicals
Macrophage Migration-Inhibitory Factors
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Calandra Thierry
Division of Infectious Diseases, Department of Internal Medicine, Centre Hospitalier Universitaire Vaudois, CH-1011 Lausanne, Switzerland. Thierry.Calandra@hospvd.ch
Roger Thierry
References (119)
119 references, click to expand
  1. Amelioration of dextran sulfate sodium-induced colitis by anti-macrophage migration inhibitory factor antibody in mice.
    Gastroenterology. 2002 Jul;123(1):256-70 PMID: 12105854
  2. Early endosomal regulation of Smad-dependent signaling in endothelial cells.
    J Biol Chem. 2002 May 17;277(20):18046-52 PMID: 11877415
  3. Innate immune sensing and its roots: the story of endotoxin.
    Nat Rev Immunol. 2003 Feb;3(2):169-76 PMID: 12563300
  4. Elevated serum content of macrophage migration inhibitory factor in patients with type 2 diabetes.
    Diabetes Care. 2000 Feb;23(2):256-8 PMID: 10868843
  5. Elevated levels of serum macrophage migration inhibitory factor in patients with pulmonary tuberculosis.
    Clin Immunol. 2002 Aug;104(2):123-7 PMID: 12165273
  6. Macrophage migration inhibitory factor (MIF) modulates innate immune responses induced by endotoxin and Gram-negative bacteria.
    J Endotoxin Res. 2001;7(6):456-60 PMID: 11753217
  7. 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. 2002 Jan 8;99(1):345-50 PMID: 11756671
  8. The cytokine macrophage migration inhibitory factor reduces pro-oxidative stress-induced apoptosis.
    J Immunol. 2003 Mar 15;170(6):3337-47 PMID: 12626594
  9. Migration-inhibitory factor gene-deficient mice are susceptible to cutaneous Leishmania major infection.
    Infect Immun. 2001 Feb;69(2):906-11 PMID: 11159984
  10. Macrophage migration inhibitory factor expression in human renal allograft rejection.
    Transplantation. 1998 Dec 15;66(11):1465-71 PMID: 9869087
  11. Enzymatically inactive macrophage migration inhibitory factor inhibits monocyte chemotaxis and random migration.
    Biochemistry. 1999 Sep 28;38(39):12841-9 PMID: 10504254
  12. Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase.
    J Mol Biol. 1998 Jul 3;280(1):85-102 PMID: 9653033
  13. A novel 5'-flanking region polymorphism of macrophage migration inhibitory factor is associated with systemic-onset juvenile idiopathic arthritis.
    Arthritis Rheum. 2001 Aug;44(8):1782-5 PMID: 11508429
  14. Expression of macrophage migration inhibitory factor in human glomerulonephritis.
    Kidney Int. 2000 Feb;57(2):499-509 PMID: 10652026
  15. Macrophage migration inhibitory factor (MIF) in bronchial asthma.
    Clin Exp Allergy. 2000 Sep;30(9):1244-9 PMID: 10971470
  16. Increase of macrophage migration inhibitory factor in sera of patients with iridocyclitis.
    Br J Ophthalmol. 2000 Dec;84(12):1423-5 PMID: 11090487
  17. Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids.
    Arthritis Rheum. 1999 Aug;42(8):1601-8 PMID: 10446857
  18. Biochemical basis of antigen-specific suppressor T cell factors: controversies and possible answers.
    Adv Immunol. 2000;74:1-60 PMID: 10605603
  19. Conservation of long-range synteny and microsynteny between the genomes of two distantly related nematodes.
    Genome Biol. 2002 Sep 26;3(10):RESEARCH0057 PMID: 12372145
  20. Macrophage migration inhibitory factor antagonizes hydrocortisone-induced increases in cytosolic IkappaBalpha.
    Am J Physiol Regul Integr Comp Physiol. 2000 Sep;279(3):R1043-9 PMID: 10956264
  21. TNF-alpha up-regulates renal MIF expression in rat crescentic glomerulonephritis.
    Mol Med. 1997 Feb;3(2):136-44 PMID: 9085256
  22. The pathogenic role of macrophage migration inhibitory factor in immunologically induced kidney disease in the rat.
    J Exp Med. 1997 Apr 21;185(8):1455-65 PMID: 9126926
  23. Macrophage migration inhibitory factor is a critical mediator of systemic inflammatory response syndrome.
    Intensive Care Med. 2001 Jul;27(7):1187-93 PMID: 11534567
  24. The staphylococcal enterotoxins and their relatives.
    Science. 1990 May 11;248(4956):705-11 PMID: 2185544
  25. Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11383-8 PMID: 9736745
  26. Effect of anti-macrophage migration inhibitory factor antibody on lipopolysaccharide-induced pulmonary neutrophil accumulation.
    Am J Respir Crit Care Med. 1998 Aug;158(2):573-9 PMID: 9700137
  27. Macrophage migration inhibitory factor in the cerebrospinal fluid of patients with conventional and optic-spinal forms of multiple sclerosis and neuro-Behçet's disease.
    J Neurol Sci. 2000 Oct 1;179(S 1-2):127-31 PMID: 11054496
  28. The evolution and genetics of innate immunity.
    Nat Rev Genet. 2001 Apr;2(4):256-67 PMID: 11283698
  29. Role of macrophage migration inhibitory factor in otitis media with effusion in adults.
    Clin Diagn Lab Immunol. 2003 May;10(3):417-22 PMID: 12738641
  30. Genomic cloning of mouse MIF (macrophage inhibitory factor) and genetic mapping of the human and mouse expressed gene and nine mouse pseudogenes.
    Genomics. 1995 Jun 10;27(3):405-11 PMID: 7558020
  31. Macrophage migration inhibitory factor.
    Expert Opin Ther Targets. 2003 Apr;7(2):153-64 PMID: 12667094
  32. Identification and characterization of a homologue of the pro-inflammatory cytokine Macrophage Migration Inhibitory Factor in the tick, Amblyomma americanum.
    Insect Mol Biol. 2001 Aug;10(4):323-31 PMID: 11520355
  33. Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor.
    Infect Immun. 1998 Dec;66(12):5955-63 PMID: 9826378
  34. Macrophage migration inhibitory factor deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation.
    J Biol Chem. 2003 Mar 28;278(13):11078-85 PMID: 12538581
  35. Macrophage migration inhibitory factor (MIF) plays a pivotal role in immunity against Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13681-6 PMID: 12271144
  36. Conserved gene structure and genomic linkage for D-dopachrome tautomerase (DDT) and MIF.
    Mamm Genome. 1998 Sep;9(9):753-7 PMID: 9716662
  37. Mechanisms of TGF-beta signaling from cell membrane to the nucleus.
    Cell. 2003 Jun 13;113(6):685-700 PMID: 12809600
  38. Characterization of catalytic centre mutants of macrophage migration inhibitory factor (MIF) and comparison to Cys81Ser MIF.
    Eur J Biochem. 1999 May;261(3):753-66 PMID: 10215893
  39. Phylogenetic perspectives in innate immunity.
    Science. 1999 May 21;284(5418):1313-8 PMID: 10334979
  40. Enzymatic ketonization of 2-hydroxymuconate: specificity and mechanism investigated by the crystal structures of two isomerases.
    Biochemistry. 1996 Jan 23;35(3):792-802 PMID: 8547259
  41. Macrophage migration inhibitory factor is a critical mediator of severe acute pancreatitis.
    Gastroenterology. 2003 Mar;124(3):725-36 PMID: 12612911
  42. Regulation of the CTL response by macrophage migration inhibitory factor.
    J Immunol. 2001 Jan 15;166(2):747-53 PMID: 11145646
  43. Pathogenesis of sepsis: new concepts and implications for future treatment.
    BMJ. 2003 Feb 1;326(7383):262-6 PMID: 12560281
  44. Macrophage migration inhibitory factor in patients with juvenile idiopathic arthritis.
    Arthritis Rheum. 2002 Jan;46(1):232-7 PMID: 11817596
  45. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7849-54 PMID: 8755565
  46. Signal transduction. A most interesting factor.
    Nature. 2000 Nov 9;408(6809):146-7 PMID: 11089953
  47. Cloning the human gene for macrophage migration inhibitory factor (MIF).
    Genomics. 1994 Jan 1;19(1):48-51 PMID: 8188240
  48. Regulation of macrophage migration inhibitory factor expression by glucocorticoids in vivo.
    Am J Pathol. 2003 Jan;162(1):47-56 PMID: 12507889
  49. Macrophage migration inhibitory factor plays a critical role in mediating protection against the helminth parasite Taenia crassiceps.
    Infect Immun. 2003 Mar;71(3):1247-54 PMID: 12595439
  50. Innate immune recognition.
    Annu Rev Immunol. 2002;20:197-216 PMID: 11861602
  51. Immunity to placental malaria. IV. Placental malaria is associated with up-regulation of macrophage migration inhibitory factor in intervillous blood.
    J Infect Dis. 2002 Nov 1;186(9):1371-5 PMID: 12402212
  52. Macrophage migration inhibitory factor release by macrophages after ingestion of Plasmodium chabaudi-infected erythrocytes: possible role in the pathogenesis of malarial anemia.
    Infect Immun. 2000 Apr;68(4):2259-67 PMID: 10722628
  53. High expression of macrophage migration inhibitory factor in the synovial tissues of rheumatoid joints.
    Cytokine. 1999 Feb;11(2):163-7 PMID: 10089139
  54. MIF as a glucocorticoid-induced modulator of cytokine production.
    Nature. 1995 Sep 7;377(6544):68-71 PMID: 7659164
  55. 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. 2003 Feb 1;170(3):1274-82 PMID: 12538686
  56. Protection from septic shock by neutralization of macrophage migration inhibitory factor.
    Nat Med. 2000 Feb;6(2):164-70 PMID: 10655104
  57. Development of chronic colitis is dependent on the cytokine MIF.
    Nat Immunol. 2001 Nov;2(11):1061-6 PMID: 11668338
  58. Human circulating eosinophils secrete macrophage migration inhibitory factor (MIF). Potential role in asthma.
    J Clin Invest. 1998 Jun 15;101(12):2869-74 PMID: 9637721
  59. SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor.
    Cell. 1998 Dec 11;95(6):779-91 PMID: 9865696
  60. The tautomerase active site of macrophage migration inhibitory factor is a potential target for discovery of novel anti-inflammatory agents.
    J Biol Chem. 2002 Jul 12;277(28):24976-82 PMID: 11997397
  61. Serum level of macrophage migration inhibitory factor as a useful parameter of clinical course in patients with Wegener's granulomatosis and relapsing polychondritis.
    Ann Otol Rhinol Laryngol. 2001 Nov;110(11):1035-40 PMID: 11713914
  62. Plasma levels of macrophage migration inhibitory factor are elevated in patients with severe sepsis.
    Intensive Care Med. 2001 Aug;27(8):1412-5 PMID: 11511957
  63. Regulatory role for macrophage migration inhibitory factor in acute respiratory distress syndrome.
    Nat Med. 1997 Mar;3(3):320-3 PMID: 9055860
  64. Reversal of established rat crescentic glomerulonephritis by blockade of macrophage migration inhibitory factor (MIF): potential role of MIF in regulating glucocorticoid production.
    Mol Med. 1998 Jun;4(6):413-24 PMID: 10780884
  65. Macrophage migration inhibitory factor: cytokine, hormone, or enzyme?
    Rev Physiol Biochem Pharmacol. 1999;139:1-32 PMID: 10453691
  66. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity.
    Science. 1966 Jul 1;153(3731):80-2 PMID: 5938421
  67. De novo expression of macrophage migration inhibitory factor in atherogenesis in rabbits.
    Circ Res. 2000 Dec 8;87(12):1202-8 PMID: 11110779
  68. Macrophage migration inhibitory factor is an essential immunoregulatory cytokine in atopic dermatitis.
    Biochem Biophys Res Commun. 1997 Nov 7;240(1):173-8 PMID: 9367905
  69. Induction of human interleukin-1 by a product of Staphylococcus aureus associated with toxic shock syndrome.
    J Clin Invest. 1984 May;73(5):1312-20 PMID: 6609169
  70. Structural characterization and chromosomal location of the mouse macrophage migration inhibitory factor gene and pseudogenes.
    Genomics. 1995 Jun 10;27(3):412-9 PMID: 7558021
  71. Crystal structure of human D-dopachrome tautomerase, a homologue of macrophage migration inhibitory factor, at 1.54 A resolution.
    Biochemistry. 1999 Mar 16;38(11):3268-79 PMID: 10079069
  72. A proinflammatory cytokine inhibits p53 tumor suppressor activity.
    J Exp Med. 1999 Nov 15;190(10):1375-82 PMID: 10562313
  73. Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor.
    Proc Natl Acad Sci U S A. 1996 May 28;93(11):5191-6 PMID: 8643551
  74. Inhibition of experimental autoimmune uveoretinitis with anti-macrophage migration inhibitory factor antibodies.
    Curr Eye Res. 2000 Feb;20(2):109-14 PMID: 10617911
  75. A macrophage migration inhibitory factor is expressed in the differentiating cells of the eye lens.
    Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1272-5 PMID: 7679497
  76. The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase.
    FEBS Lett. 1997 Nov 3;417(1):85-8 PMID: 9395080
  77. 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. 1999 Jun 18;274(25):18100-6 PMID: 10364264
  78. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis.
    J Exp Med. 1999 Jan 18;189(2):341-6 PMID: 9892616
  79. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia.
    Nature. 1993 Oct 21;365(6448):756-9 PMID: 8413654
  80. Prominent increase of macrophage migration inhibitory factor in the sera of patients with uveitis.
    Invest Ophthalmol Vis Sci. 1999 Jan;40(1):247-50 PMID: 9888451
  81. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction.
    Proc Natl Acad Sci U S A. 1966 Jul;56(1):72-7 PMID: 5229858
  82. The epidemiology of sepsis in the United States from 1979 through 2000.
    N Engl J Med. 2003 Apr 17;348(16):1546-54 PMID: 12700374
  83. An essential role for macrophage migration inhibitory factor in the tuberculin delayed-type hypersensitivity reaction.
    J Exp Med. 1996 Jan 1;183(1):277-82 PMID: 8551232
  84. AP-1 as a regulator of cell life and death.
    Nat Cell Biol. 2002 May;4(5):E131-6 PMID: 11988758
  85. Macrophage migration inhibitory factor.
    Crit Care Med. 2002 Jan;30(1 Suppl):S27-35 PMID: 11782558
  86. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor.
    J Exp Med. 1994 Jun 1;179(6):1895-902 PMID: 8195715
  87. Dissection of the enzymatic and immunologic functions of macrophage migration inhibitory factor. Full immunologic activity of N-terminally truncated mutants.
    Eur J Biochem. 2000 Dec;267(24):7183-93 PMID: 11106430
  88. Trauma patients with positive cultures have higher levels of circulating macrophage migration inhibitory factor (MIF).
    Res Commun Mol Pathol Pharmacol. 2000;107(1-2):13-20 PMID: 11334363
  89. Role for macrophage migration inhibitory factor in acute respiratory distress syndrome.
    J Pathol. 2003 Apr;199(4):496-508 PMID: 12635141
  90. Evidence for a role of macrophage migration inhibitory factor in psoriatic skin disease.
    Br J Dermatol. 1999 Dec;141(6):1061-6 PMID: 10606853
  91. Migration inhibitory factor expression in experimentally induced endotoxemia.
    Am J Pathol. 1997 Jan;150(1):235-46 PMID: 9006339
  92. Macrophage migration inhibitory factor is involved in the pathogenesis of collagen type II-induced arthritis in mice.
    J Immunol. 1997 Jun 1;158(11):5514-7 PMID: 9164975
  93. Regulation of macrophage migration inhibitory factor by endogenous glucocorticoids in rat adjuvant-induced arthritis.
    Arthritis Rheum. 2000 Apr;43(4):827-33 PMID: 10765927
  94. Up-regulation of macrophage migration inhibitory factor in acute renal allograft rejection in the rat.
    Clin Exp Immunol. 1999 Nov;118(2):329-36 PMID: 10540199
  95. Migration inhibitory factor induces killing of Leishmania major by macrophages: dependence on reactive nitrogen intermediates and endogenous TNF-alpha.
    J Immunol. 1998 Sep 1;161(5):2383-90 PMID: 9725234
  96. MIF signal transduction initiated by binding to CD74.
    J Exp Med. 2003 Jun 2;197(11):1467-76 PMID: 12782713
  97. Expression of macrophage migration inhibitory factor in different stages of human atherosclerosis.
    Circulation. 2002 Apr 2;105(13):1561-6 PMID: 11927523
  98. Molecular cloning of a cDNA encoding a human macrophage migration inhibitory factor.
    Proc Natl Acad Sci U S A. 1989 Oct;86(19):7522-6 PMID: 2552447
  99. Deficiency of the macrophage migration inhibitory factor gene has no significant effect on endotoxaemia.
    Immunology. 2000 May;100(1):84-90 PMID: 10809963
  100. Biochemical and mutational investigations of the enzymatic activity of macrophage migration inhibitory factor.
    Biochemistry. 1997 Dec 9;36(49):15356-62 PMID: 9398265
  101. Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration inhibitory factor (MIF).
    Biochemistry. 1994 Nov 29;33(47):14144-55 PMID: 7947826
  102. Macrophage migration inhibitory factor in rheumatoid arthritis: clinical correlations.
    Rheumatology (Oxford). 2002 May;41(5):558-62 PMID: 12011381
  103. De Novo renal expression of macrophage migration inhibitory factor during the development of rat crescentic glomerulonephritis.
    Am J Pathol. 1996 Oct;149(4):1119-27 PMID: 8863661
  104. Tumor growth-promoting properties of macrophage migration inhibitory factor (MIF).
    Semin Cancer Biol. 2000 Oct;10(5):359-66 PMID: 11100884
  105. The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction.
    Mol Med. 1996 Jan;2(1):143-9 PMID: 8900542
  106. Macrophage migration inhibitory factor is an important mediator in the pathogenesis of gastric inflammation in rats.
    Gastroenterology. 2001 Sep;121(3):619-30 PMID: 11522746
  107. Macrophage migration inhibitory factor (MIF) regulates host responses to endotoxin through modulation of Toll-like receptor 4 (TLR4).
    J Endotoxin Res. 2003;9(2):119-23 PMID: 12803886
  108. Expression of macrophage migration inhibitory factor in diffuse systemic sclerosis.
    Ann Rheum Dis. 2003 May;62(5):460-4 PMID: 12695161
  109. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1.
    Nature. 2000 Nov 9;408(6809):211-6 PMID: 11089976
  110. Macrophage migration inhibitory factor in the sera and at the colonic mucosa in patients with ulcerative colitis: clinical implications and pathogenic significance.
    Eur J Clin Invest. 2001 Apr;31(4):337-43 PMID: 11298781
  111. Macrophage migration inhibitory factor (MIF) of jawed and jawless fishes: implications for its evolutionary origin.
    Dev Comp Immunol. 2003 May;27(5):401-12 PMID: 12631522
  112. Macrophage migration inhibitory factor and hypothalamo-pituitary-adrenal function during critical illness.
    J Clin Endocrinol Metab. 2001 Jun;86(6):2811-6 PMID: 11397892
  113. Involvement of macrophage migration inhibitory factor in the evolution of rat adjuvant arthritis.
    Arthritis Rheum. 1998 May;41(5):910-7 PMID: 9588744
  114. Increased production of macrophage migration inhibitory factor by T cells in patients with IgA nephropathy.
    Am J Nephrol. 2001 Nov-Dec;21(6):455-64 PMID: 11799262
  115. Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease.
    Microbes Infect. 2002 Apr;4(4):449-60 PMID: 11932196
  116. Crystal structure of the macrophage migration inhibitory factor from rat liver.
    Nat Struct Biol. 1996 Mar;3(3):259-66 PMID: 8605628
  117. MIF regulates innate immune responses through modulation of Toll-like receptor 4.
    Nature. 2001 Dec 20-27;414(6866):920-4 PMID: 11780066
  118. Macrophage migration inhibitory factor up-regulates matrix metalloproteinase-9 and -13 in rat osteoblasts. Relevance to intracellular signaling pathways.
    J Biol Chem. 2002 Mar 8;277(10):7865-74 PMID: 11751895
  119. A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis.
    Genes Immun. 2002 May;3(3):170-6 PMID: 12070782
Article Info
Journal
Nature reviews. Immunology
Abbr.
Nat Rev Immunol
ISSN
1474-1733
Published
2003-10-00
Pages
791-800
Language
English
Region
England
NLM ID
101124169
PMCID
PMC7097468
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com