Home LiteratureArticle Details
PMID: 26617609 Published · epublish English Journal Article Review

MIF: Implications in the Pathoetiology of Systemic Lupus Erythematosus.

Frontiers in immunology ·Vol. 6 ·2015-00-00 ·Pages 577

Lang T, Foote A, Lee JP, Morand EF, Harris J

Abstract

Macrophage migration Inhibitory factor (MIF) was one of the earliest pro-inflammatory cytokines to be identified. Increasing interest in this cytokine in recent decades has followed the cloning of human MIF and the generation of Mif(-/-) mice. Deepening understanding of signaling pathways utilized by MIF and putative receptor mechanisms have followed. MIF is distinct from all other cytokines by virtue of its unique induction by and counter regulation of glucocorticoids (GCs). MIF is further differentiated from other cytokines by its structural homology to specific tautomerase and isomerase enzymes and correlative in vitro enzymatic functions. The role of MIF in immune and inflammatory states, including a range of human autoimmune diseases, is now well established, as are the relationships between MIF polymorphisms and a number of inflammatory diseases. Here, we review the known pleiotropic activities of MIF, in addition to novel functions of MIF in processes including autophagy and autophagic cell death. In addition, recent developments in the understanding of the role of MIF in systemic lupus erythematosus (SLE) are reviewed. Finally, we discuss the potential application of anti-MIF strategies to treat human diseases such as SLE, which will require a comprehensive understanding of the unique and complex activities of this ubiquitously expressed cytokine.

Keywords
MIF SLE autophagy innate immunity and responses therapeutics
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lang Tali
Lupus Research Group, Monash Centre for Inflammatory Diseases, School of Clinical Sciences at Monash Health, Faculty of Medicine, Nursing and Health Sciences, Monash Medical Centre , Clayton, VIC , Australia.
Foote Andrew
Lupus Research Group, Monash Centre for Inflammatory Diseases, School of Clinical Sciences at Monash Health, Faculty of Medicine, Nursing and Health Sciences, Monash Medical Centre , Clayton, VIC , Australia.
Lee Jacinta P W
Lupus Research Group, Monash Centre for Inflammatory Diseases, School of Clinical Sciences at Monash Health, Faculty of Medicine, Nursing and Health Sciences, Monash Medical Centre , Clayton, VIC , Australia.
Morand Eric F
Lupus Research Group, Monash Centre for Inflammatory Diseases, School of Clinical Sciences at Monash Health, Faculty of Medicine, Nursing and Health Sciences, Monash Medical Centre , Clayton, VIC , Australia.
Harris James
Lupus Research Group, Monash Centre for Inflammatory Diseases, School of Clinical Sciences at Monash Health, Faculty of Medicine, Nursing and Health Sciences, Monash Medical Centre , Clayton, VIC , Australia.
References (134)
134 references, click to expand
  1. Protection from septic shock by neutralization of macrophage migration inhibitory factor.
    Nat Med. 2000 Feb;6(2):164-70 PMID: 10655104
  2. 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
  3. Autoimmune diseases: MIF as a therapeutic target.
    Expert Opin Ther Targets. 2010 Mar;14(3):253-64 PMID: 20148714
  4. The influence of macrophage migration inhibitory factor gene polymorphisms on outcome from community-acquired pneumonia.
    FASEB J. 2009 Aug;23(8):2403-11 PMID: 19346297
  5. Allosteric inhibition of macrophage migration inhibitory factor revealed by ibudilast.
    Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11313-8 PMID: 20534506
  6. Role of macrophage migration inhibitory factor (MIF) in murine antigen-induced arthritis: interaction with glucocorticoids.
    Clin Exp Immunol. 2001 Feb;123(2):309-14 PMID: 11207663
  7. Receptor-mediated recognition of mycobacterial pathogens.
    Cell Microbiol. 2013 Sep;15(9):1484-95 PMID: 23795683
  8. T lymphocytes from patients with systemic lupus erythematosus are resistant to induction of autophagy.
    FASEB J. 2012 Nov;26(11):4722-32 PMID: 22835828
  9. Induction of macrophage parasiticidal activity by Staphylococcus aureus and exotoxins through the nitric oxide synthesis pathway.
    Immunology. 1993 Apr;78(4):563-7 PMID: 8495974
  10. MIF promotes B cell chemotaxis through the receptors CXCR4 and CD74 and ZAP-70 signaling.
    J Immunol. 2014 Jun 1;192(11):5273-84 PMID: 24760155
  11. Macrophage migration inhibitory factor (MIF) promotes cell survival by activation of the Akt pathway and role for CSN5/JAB1 in the control of autocrine MIF activity.
    Oncogene. 2007 Aug 2;26(35):5046-59 PMID: 17310986
  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 polymorphism in the macrophage migration inhibitory factor gene is involved in the genetic predisposition of Crohn's disease and associated with cumulative steroid doses.
    Hepatogastroenterology. 2007 Apr-May;54(75):784-6 PMID: 17591062
  14. Macrophage migration inhibitory factor (MIF) -173G/C promoter polymorphism influences upper gastrointestinal tract involvement and disease activity in patients with Crohn's disease.
    Inflamm Bowel Dis. 2007 Jan;13(1):71-82 PMID: 17206642
  15. Antirheumatic drug use and the risk of acute myocardial infarction.
    Arthritis Rheum. 2006 Aug 15;55(4):531-6 PMID: 16874796
  16. 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
  17. Macrophage migration inhibitory factor (MIF): genetic evidence for participation in early onset and early stage rheumatoid arthritis.
    Cytokine. 2013 Mar;61(3):759-65 PMID: 23402792
  18. Role of macrophage migration inhibitory factor in the regulatory T cell response of tumor-bearing mice.
    J Immunol. 2012 Oct 15;189(8):3905-13 PMID: 22972922
  19. 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
  20. A novel allosteric inhibitor of macrophage migration inhibitory factor (MIF).
    J Biol Chem. 2012 Aug 31;287(36):30653-63 PMID: 22782901
  21. Association of MIF-173 gene polymorphism with inflammatory bowel disease in Chinese Han population.
    Cytokine. 2008 Jan;41(1):44-7 PMID: 18054247
  22. Racial differences in treatment preferences among lupus patients: a two-site study.
    Clin Exp Rheumatol. 2014 Sep-Oct;32(5):680-8 PMID: 25084365
  23. Pro-inflammatory action of MIF in acute myocardial infarction via activation of peripheral blood mononuclear cells.
    PLoS One. 2013 Oct 01;8(10):e76206 PMID: 24098445
  24. Macrophage migration inhibitory factor deficiency attenuates macrophage recruitment, glomerulonephritis, and lethality in MRL/lpr mice.
    J Immunol. 2006 Oct 15;177(8):5687-96 PMID: 17015758
  25. Influence of MIF, CD40, and CD226 polymorphisms on risk of rheumatoid arthritis.
    Mol Biol Rep. 2012 Jun;39(6):6915-22 PMID: 22302395
  26. Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction.
    Nat Immunol. 2012 Jan 29;13(3):255-63 PMID: 22286270
  27. Discovery of human macrophage migration inhibitory factor (MIF)-CD74 antagonists via virtual screening.
    J Med Chem. 2009 Jan 22;52(2):416-24 PMID: 19090668
  28. Association between functional promoter polymorphisms of macrophage migration inhibitory factor (MIF) gene and ulcerative colitis in Japan.
    Cytokine. 2010 Aug;51(2):173-7 PMID: 20621719
  29. A functional heteromeric MIF receptor formed by CD74 and CXCR4.
    FEBS Lett. 2009 Sep 3;583(17):2749-57 PMID: 19665027
  30. Role of macrophage migration inhibition factor in kidney disease.
    Nephron Exp Nephrol. 2008;109(3):e79-83 PMID: 18663334
  31. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome.
    Nat Immunol. 2011 Mar;12 (3):222-30 PMID: 21151103
  32. Control of fibroblast-like synoviocyte proliferation by macrophage migration inhibitory factor.
    Arthritis Rheum. 2003 Jan;48(1):103-9 PMID: 12528110
  33. Role for macrophage migration inhibitory factor in asthma.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14410-5 PMID: 16186482
  34. How glucocorticoids control their own strength and the balance between pro- and anti-inflammatory mediators.
    Eur J Immunol. 2005 Dec;35(12):3396-9 PMID: 16331703
  35. Endogenous macrophage migration inhibitory factor modulates glucocorticoid sensitivity in macrophages via effects on MAP kinase phosphatase-1 and p38 MAP kinase.
    FEBS Lett. 2006 Feb 6;580(3):974-81 PMID: 16442105
  36. 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
  37. ISO-1 binding to the tautomerase active site of MIF inhibits its pro-inflammatory activity and increases survival in severe sepsis.
    J Biol Chem. 2005 Nov 4;280(44):36541-4 PMID: 16115897
  38. Functional and prognostic relevance of the -173 polymorphism of the macrophage migration inhibitory factor gene in systemic-onset juvenile idiopathic arthritis.
    Arthritis Rheum. 2003 May;48(5):1398-407 PMID: 12746913
  39. MIF: metastasis/MDSC-inducing factor?
    Oncoimmunology. 2013 Mar 1;2(3):e23337 PMID: 23802077
  40. Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2.
    J Immunol. 2006 Dec 1;177(11):8072-9 PMID: 17114481
  41. MIF (macrophage migration inhibitory factor) promoter polymorphisms and susceptibility to severe malarial anemia.
    J Infect Dis. 2009 Aug 15;200(4):629-37 PMID: 19591577
  42. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity.
    Science. 1966 Jul 1;153(3731):80-2 PMID: 5938421
  43. Identification and characterization of novel classes of macrophage migration inhibitory factor (MIF) inhibitors with distinct mechanisms of action.
    J Biol Chem. 2010 Aug 20;285(34):26581-98 PMID: 20516071
  44. Emerging regulation and functions of autophagy.
    Nat Cell Biol. 2013 Jul;15(7):713-20 PMID: 23817233
  45. 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
  46. Macrophage migration inhibitory factor plays a permissive role in the maintenance of cardiac contractile function under starvation through regulation of autophagy.
    Cardiovasc Res. 2013 Aug 1;99(3):412-21 PMID: 23674514
  47. Autophagy and cytokines.
    Cytokine. 2011 Nov;56(2):140-4 PMID: 21889357
  48. D-dopachrome tautomerase (D-DT or MIF-2): doubling the MIF cytokine family.
    Cytokine. 2012 Jul;59(1):10-7 PMID: 22507380
  49. The -173 G/C polymorphism of the MIF gene and inflammatory bowel disease risk: a meta-analysis.
    Int J Mol Sci. 2013 May 28;14(6):11392-401 PMID: 23759989
  50. Macrophage migration inhibitory factor is a neuroendocrine mediator of endotoxaemia.
    Trends Microbiol. 1994 Jun;2(6):198-201 PMID: 8087451
  51. Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion.
    Immunology. 1997 Sep;92(1):131-7 PMID: 9370935
  52. Crystal structure of macrophage migration inhibitory factor from human lymphocyte at 2.1 A resolution.
    FEBS Lett. 1996 Jul 1;389(2):145-8 PMID: 8766818
  53. 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
  54. The macrophage migration inhibitory factor-glucocorticoid dyad: regulation of inflammation and immunity.
    Mol Endocrinol. 2007 Jun;21(6):1267-80 PMID: 17389748
  55. 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
  56. Arachidonic acid activates c-jun N-terminal kinase through NADPH oxidase in rabbit proximal tubular epithelial cells.
    Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3771-6 PMID: 9108053
  57. Macrophage migration inhibitory factor (MIF) gene polymorphism is associated with susceptibility to but not severity of inflammatory polyarthritis.
    Genes Immun. 2003 Oct;4(7):487-91 PMID: 14551601
  58. A functional promoter haplotype of macrophage migration inhibitory factor is linked and associated with juvenile idiopathic arthritis.
    Arthritis Rheum. 2004 May;50(5):1604-10 PMID: 15146431
  59. Macrophage migration inhibitory factor (MIF): a promising biomarker.
    Drug News Perspect. 2010 May;23(4):257-64 PMID: 20520854
  60. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment.
    Nat Med. 2007 May;13(5):587-96 PMID: 17435771
  61. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production.
    Nature. 2008 Nov 13;456(7219):264-8 PMID: 18849965
  62. A small-molecule macrophage migration inhibitory factor antagonist protects against glomerulonephritis in lupus-prone NZB/NZW F1 and MRL/lpr mice.
    J Immunol. 2011 Jan 1;186(1):527-38 PMID: 21106847
  63. Association of the -173 G/C polymorphism of the macrophage migration inhibitory factor gene with ulcerative colitis.
    J Gastroenterol. 2004;39(3):242-6 PMID: 15065001
  64. Autophagy and inflammatory diseases.
    Immunol Cell Biol. 2013 Mar;91(3):250-8 PMID: 23318657
  65. 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
  66. Steroid receptor coactivator 3 regulates autophagy in breast cancer cells through macrophage migration inhibitory factor.
    Cell Res. 2012 Jun;22(6):1003-21 PMID: 22430150
  67. 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
  68. Macrophage migration inhibitory factor (MIF), enzymatic activity and the inflammatory response.
    Biofactors. 2009 Mar-Apr;35(2):165-8 PMID: 19322762
  69. Incidence of systemic lupus erythematosus in Finland, 2000-2007, a nationwide study.
    Clin Exp Rheumatol. 2014 Nov-Dec;32(6):953-5 PMID: 25328038
  70. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway.
    J Biol Chem. 2001 Sep 21;276(38):35243-6 PMID: 11477064
  71. Ibudilast in healthy volunteers: safety, tolerability and pharmacokinetics with single and multiple doses.
    Br J Clin Pharmacol. 2008 Dec;66(6):792-801 PMID: 19032723
  72. Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK) is required for lipopolysaccharide stimulation of tumor necrosis factor alpha (TNF-alpha) translation: glucocorticoids inhibit TNF-alpha translation by blocking JNK/SAPK.
    Mol Cell Biol. 1997 Nov;17(11):6274-82 PMID: 9343388
  73. 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
  74. Macrophage migration inhibitory factor gene polymorphism is associated with psoriasis.
    J Invest Dermatol. 2004 Sep;123(3):484-7 PMID: 15304087
  75. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex.
    Immunity. 2006 Oct;25(4):595-606 PMID: 17045821
  76. Macrophage migration inhibitory factor (MIF) and oligoarticular juvenile idiopathic arthritis (o-JIA): association of MIF promoter polymorphisms with response to intra-articular glucocorticoids.
    Clin Exp Rheumatol. 2007 Sep-Oct;25(5):775-81 PMID: 18078632
  77. 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
  78. Macrophage migration inhibitory factor (MIF) tautomerase inhibitors as potential novel anti-inflammatory agents: current developments.
    Curr Med Chem. 2009;16(9):1091-114 PMID: 19275614
  79. Regulation of p53 by macrophage migration inhibitory factor in inflammatory arthritis.
    Arthritis Rheum. 2003 Jul;48(7):1881-9 PMID: 12847682
  80. Involvement of macrophage migration inhibitory factor gene in celiac disease susceptibility.
    Genes Immun. 2007 Mar;8(2):168-70 PMID: 17215861
  81. 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
  82. Macrophage migration inhibitory factor in systemic lupus erythematosus.
    J Rheumatol. 2004 Feb;31(2):268-73 PMID: 14760795
  83. Contribution of the -173 G/C polymorphism of macrophage migration inhibitory factor gene to the risk of inflammatory bowel diseases.
    Pol Przegl Chir. 2011 Feb;83(2):76-80 PMID: 22166284
  84. Crystal structure of the macrophage migration inhibitory factor from rat liver.
    Nat Struct Biol. 1996 Mar;3(3):259-66 PMID: 8605628
  85. Inhibition of macrophage migration inhibitory factor (MIF) tautomerase and biological activities by acetaminophen metabolites.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):144-9 PMID: 11773615
  86. Macrophage migration inhibitory factor and innate immune responses to bacterial infections.
    Crit Care Med. 2001 Jul;29(7 Suppl):S13-5 PMID: 11445727
  87. 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
  88. Association of MIF-173G/C and MBL2 codon 54 gene polymorphisms with rheumatoid arthritis: a meta-analysis.
    Hum Immunol. 2012 Sep;73(9):966-71 PMID: 22820623
  89. Association of macrophage migration inhibitory factor and mannose-binding lectin-2 gene polymorphisms in acute rheumatic fever.
    Cardiol Young. 2013 Aug;23(4):486-90 PMID: 22813781
  90. Neutralization of macrophage migration inhibitory factor (MIF) by fully human antibodies correlates with their specificity for the β-sheet structure of MIF.
    J Biol Chem. 2012 Mar 2;287(10):7446-55 PMID: 22238348
  91. Antigen and mitogen induced production of macrophage migration inhibitory factor in the mouse.
    Int Arch Allergy Appl Immunol. 1979;60(1):29-43 PMID: 378863
  92. Dual effect of the macrophage migration inhibitory factor gene on the development and severity of human systemic lupus erythematosus.
    Arthritis Rheum. 2011 Dec;63(12):3942-51 PMID: 22127710
  93. Macrophage migration inhibitory factor polymorphism and the risk of ulcerative colitis and Crohn's disease in Asian and European populations: a meta-analysis.
    BMJ Open. 2013 Dec 23;3(12):e003729 PMID: 24366577
  94. Taming lupus-a new understanding of pathogenesis is leading to clinical advances.
    Nat Med. 2012 Jun 06;18(6):871-82 PMID: 22674006
  95. Macrophage migration inhibitory factor gene polymorphisms in inflammatory bowel disease: an association study in New Zealand Caucasians and meta-analysis.
    World J Gastroenterol. 2013 Oct 21;19(39):6656-64 PMID: 24151396
  96. MIF signal transduction initiated by binding to CD74.
    J Exp Med. 2003 Jun 2;197(11):1467-76 PMID: 12782713
  97. Activation of synovial cell p38 MAP kinase by macrophage migration inhibitory factor.
    J Rheumatol. 2004 Jun;31(6):1038-43 PMID: 15170913
  98. The association between the functional PTPN22 1858 C/T and MIF -173 C/G polymorphisms and juvenile idiopathic arthritis: a meta-analysis.
    Inflamm Res. 2012 May;61(5):411-5 PMID: 22327470
  99. Correlation of rheumatoid arthritis severity with the genetic functional variants and circulating levels of macrophage migration inhibitory factor.
    Arthritis Rheum. 2005 Oct;52(10):3020-9 PMID: 16200611
  100. T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis.
    Immunity. 2007 Sep;27(3):505-17 PMID: 17892853
  101. An integrative in silico methodology for the identification of modulators of macrophage migration inhibitory factor (MIF) tautomerase activity.
    Bioorg Med Chem. 2010 Jul 15;18(14):5425-40 PMID: 20639113
  102. Influence of Atg5 mutation in SLE depends on functional IL-10 genotype.
    PLoS One. 2013 Oct 18;8(10 ):e78756 PMID: 24205307
  103. Human single-chain variable fragment antibody inhibits macrophage migration inhibitory factor tautomerase activity.
    Int J Mol Med. 2014 Mar;33(3):515-22 PMID: 24424397
  104. Macrophage migration inhibitory factor polymorphisms do not predict therapeutic response to glucocorticoids or to tumour necrosis factor alpha-neutralising treatments in rheumatoid arthritis.
    Ann Rheum Dis. 2007 Nov;66(11):1525-30 PMID: 17456524
  105. The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase.
    FEBS Lett. 1997 Nov 3;417(1):85-8 PMID: 9395080
  106. Association of macrophage migration inhibitory factor gene -173 G/C polymorphism with prognosis in Turkish children with juvenile rheumatoid arthritis.
    Rheumatol Int. 2006 Jun;26(8):726-31 PMID: 16220288
  107. Reduced arthritis in MIF deficient mice is associated with reduced T cell activation: down-regulation of ERK MAP kinase phosphorylation.
    Clin Exp Immunol. 2008 May;152(2):372-80 PMID: 18341611
  108. Autophagy is activated in systemic lupus erythematosus and required for plasmablast development.
    Ann Rheum Dis. 2015 May;74(5):912-20 PMID: 24419333
  109. Inflammasome-independent modulation of cytokine response by autophagy in human cells.
    PLoS One. 2011 Apr 07;6(4):e18666 PMID: 21490934
  110. 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
  111. Macrophage migration inhibitory factor: association of -794 CATT5-8 and -173 G>C polymorphisms with TNF-α in systemic lupus erythematosus.
    Hum Immunol. 2014 May;75(5):433-9 PMID: 24530749
  112. Autophagy regulates IL-23 secretion and innate T cell responses through effects on IL-1 secretion.
    J Immunol. 2012 Oct 15;189(8):4144-53 PMID: 22972933
  113. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation.
    J Biol Chem. 2011 Mar 18;286(11):9587-97 PMID: 21228274
  114. Macrophage migration inhibitory factor stimulates interleukin-17 expression and production in lymph node cells.
    Immunology. 2009 Jan;126(1):74-83 PMID: 18624729
  115. 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. 2002 Sep;46(9):2402-9 PMID: 12355488
  116. Macrophage migration inhibitory factor deficiency augments doxorubicin-induced cardiomyopathy.
    J Am Heart Assoc. 2013 Dec 12;2(6):e000439 PMID: 24334905
  117. Macrophage migration inhibitory factor promotes innate immune responses by suppressing glucocorticoid-induced expression of mitogen-activated protein kinase phosphatase-1.
    Eur J Immunol. 2005 Dec;35(12):3405-13 PMID: 16224818
  118. Macrophage migration inhibitory factor, Toll-like receptor 4, and CD14 polymorphisms with altered expression levels in patients with ulcerative colitis.
    Hum Immunol. 2012 Feb;73(2):201-5 PMID: 22192785
  119. Role of GILZ in immune regulation, glucocorticoid actions and rheumatoid arthritis.
    Nat Rev Rheumatol. 2011 Jun;7(6):340-8 PMID: 21556028
  120. Macrophage migration inhibitory factor (MIF) is a critical mediator of the innate immune response to Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 2013 Aug 6;110(32):E2997-3006 PMID: 23882081
  121. 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. 2004 May;50(5):1437-47 PMID: 15146413
  122. Evidence of association of macrophage migration inhibitory factor gene polymorphisms with systemic lupus erythematosus.
    Genes Immun. 2006 Jul;7(5):433-6 PMID: 16724072
  123. Macrophage migration inhibitory factor: a regulator of innate immunity.
    Nat Rev Immunol. 2003 Oct;3(10):791-800 PMID: 14502271
  124. A novel, macrophage migration inhibitory factor suicide substrate inhibits motility and growth of lung cancer cells.
    Cancer Res. 2008 Sep 15;68(18):7253-7 PMID: 18794110
  125. 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
  126. Association of MIF promoter polymorphisms with psoriasis in a Han population in northeastern China.
    J Dermatol Sci. 2009 Mar;53(3):212-5 PMID: 19157791
  127. 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
  128. Macroautophagy is deregulated in murine and human lupus T lymphocytes.
    Autophagy. 2012 Jul 1;8(7):1113-23 PMID: 22522825
  129. 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
  130. Macrophage migration inhibitory factor induces autophagy via reactive oxygen species generation.
    PLoS One. 2012;7(5):e37613 PMID: 22629429
  131. Macrophage migration inhibitory factor inhibits the antiinflammatory effects of glucocorticoids via glucocorticoid-induced leucine zipper.
    Arthritis Rheumatol. 2014 Aug;66(8):2059-70 PMID: 24782327
  132. Macrophage migration inhibitory factor deletion exacerbates pressure overload-induced cardiac hypertrophy through mitigating autophagy.
    Hypertension. 2014 Mar;63(3):490-9 PMID: 24366076
  133. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia.
    Nature. 1993 Oct 21;365(6448):756-9 PMID: 8413654
  134. Expression of macrophage migration inhibitory factor in human glomerulonephritis.
    Kidney Int. 2000 Feb;57(2):499-509 PMID: 10652026
Article Info
Journal
Frontiers in immunology
Abbr.
Front Immunol
ISSN
1664-3224
DOI
10.3389/fimmu.2015.00577
Published
2015-00-00
Epub
2015-00-11
Pages
577
Language
English
Region
Switzerland
NLM ID
101560960
PMCID
PMC4641160
External Links
PubMed source DOI: 10.3389/fimmu.2015.00577 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2