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Thromb Haemost 2013; 109(03): 391-398
DOI: 10.1160/TH12-11-0831
Theme Issue Article
Schattauer GmbH

The vascular biology of macrophage migration inhibitory factor (MIF)

Expression and effects in inflammation, atherogenesis and angiogenesis
Yaw Asare
1   Institute of Biochemistry and Molecular Cell Biology, RWTH Aachen University, Aachen, Germany
,
Martin Schmitt
2   Institute of Molecular Cardiovascular Research (IMCAR), RWTH Aachen University, Aachen, Germany
3   Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, The Netherlands
,
Jürgen Bernhagen
1   Institute of Biochemistry and Molecular Cell Biology, RWTH Aachen University, Aachen, Germany
› Institutsangaben
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Publikationsverlauf

Received: 18. November 2012

Accepted after minor revision: 03. Januar 2012

Publikationsdatum:
29. November 2017 (online)

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Summary

Macrophage migration inhibitory factor (MIF) is a pleiotropic cytokine with chemokine-like functions. MIF is a critical mediator of the host immune and inflammatory response. Dysregulated MIF expression has been demonstrated to contribute to various acute and chronic inflammatory conditions as well as cancer development. More recently, MIF has been identified as an important pro-atherogenic factor. Its blockade could even aid plaque regression in advanced atherosclerosis. Promotion of atherogenic leukocyte recruitment processes has been recognised as a major underlying mechanism of MIF in vascular pathology. However, MIF’s role in vascular biology is not limited to immune cell recruitment as recent evidence also points to a role for this mediator in neo-angiogenesis / vasculogenesis by endothelial cell activation and endothelial progenitor cell recruitment. On the basis of introducing MIF’s chemokine-like functions, the current article focusses on MIF’s role in vascular biology and pathology.

Keywords

Chemokine - monocyte/macrophage - cardiovascular disease - atherosclerosis - (neo-)angiogenesis/vasculogenesis
 

  • References

  • 1 Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 2006; 354: 610-621.
    CrossrefPubMedGoogle Scholar
  • 2 Laudanna C, Alon R. Right on the spot. Chemokine triggering of integrin-mediated arrest of rolling leukocytes. Thromb Haemost 2006; 95: 5-11.
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 3 Weber C, Schober A, Zernecke A. Chemokines: key regulators of mononuclear cell recruitment in atherosclerotic vascular disease. Arterioscler Thromb Vasc Biol 2004; 24: 1997-2008.
    CrossrefPubMedGoogle Scholar
  • 4 Murphy PM, Baggiolini M, Charo IF. et al. International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol Rev 2000; 52: 145-176.
    PubMedGoogle Scholar
  • 5 Koenen RR, Weber C. Chemokines: established and novel targets in atherosclerosis. EMBO Mol Med 2011; 3: 713-725.
    CrossrefPubMedGoogle Scholar
  • 6 Weber C. Chemokines take centre stage in vascular biology. Thromb Haemost 2007; 97: 685-687.
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 7 Humbert M, Morrell NW, Archer SL. et al. Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 2004; 43: 13S-24S.
    CrossrefPubMedGoogle Scholar
  • 8 Murdoch C, Finn A. Chemokine receptors and their role in vascular biology. J Vasc Res 2000; 37: 1-7.
    PubMedGoogle Scholar
  • 9 Thelen M. Dancing to the tune of chemokines. Nat Immunol 2001; 2: 129-134.
    CrossrefPubMedGoogle Scholar
  • 10 von Hundelshausen P, Koenen RR, Sack M. et al. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005; 105: 924-930.
    PubMedGoogle Scholar
  • 11 Koenen RR, von Hundelshausen P, Nesmelova IV. et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009; 15: 97-103.
    CrossrefPubMedGoogle Scholar
  • 12 Moore BB, Arenberg DA, Addison CL. et al. CXC chemokines mechanism of action in regulating tumour angiogenesis. Angiogenesis 1998; 2: 123-134.
    CrossrefPubMedGoogle Scholar
  • 13 Strieter RM, Polverini PJ, Kunkel SL. et al. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J Biol Chem 1995; 270: 27348-27357.
    CrossrefPubMedGoogle Scholar
  • 14 Belperio JA, Keane MP, Arenberg DA. et al. CXC chemokines in angiogenesis. J Leukoc Biol 2000; 68: 1-8.
    PubMedGoogle Scholar
  • 15 Arenberg DA, Kunkel SL, Polverini PJ. et al. Inhibition of interleukin-8 reduces tumourigenesis of human non-small cell lung cancer in SCID mice. J Clin Invest 1996; 97: 2792-2802.
    CrossrefPubMedGoogle Scholar
  • 16 Takamori H, Oades ZG, Hoch OC. et al. Autocrine growth effect of IL-8 and GROalpha on a human pancreatic cancer cell line, Capan-1. Pancreas 2000; 21: 52-56.
    CrossrefPubMedGoogle Scholar
  • 17 Yoneda J, Kuniyasu H, Crispens MA. et al. Expression of angiogenesis-related genes and progression of human ovarian carcinomas in nude mice. J Natl Cancer Inst 1998; 90: 447-454.
    CrossrefPubMedGoogle Scholar
  • 18 Simonini A, Moscucci M, Muller DW. et al. IL-8 is an angiogenic factor in human coronary atherectomy tissue. Circulation 2000; 101: 1519-1526.
    CrossrefPubMedGoogle Scholar
  • 19 Peeters W, Hellings WE, de Kleijn DP. et al. Carotid atherosclerotic plaques stabilize after stroke: insights into the natural process of atherosclerotic plaque stabilisation. Arterioscler Thromb Vasc Biol 2009; 29: 128-133.
    CrossrefPubMedGoogle Scholar
  • 20 Gerszten RE, Garcia-Zepeda EA, Lim YC. et al. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 1999; 398: 718-723.
    CrossrefPubMedGoogle Scholar
  • 21 Weber KS, von Hundelshausen P, Clark-Lewis I. et al. Differential immobilisation and hierarchical involvement of chemokines in monocyte arrest and transmigration on inflamed endothelium in shear flow. Eur J Immunol 1999; 29: 700-712.
    CrossrefPubMedGoogle Scholar
  • 22 Gu L, Okada Y, Clinton SK. et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 1998; 2: 275-281.
    CrossrefPubMedGoogle Scholar
  • 23 Boring L, Gosling J, Cleary M. et al. Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 1998; 394: 894-897.
    CrossrefPubMedGoogle Scholar
  • 24 Wakasugi K, Schimmel P. Two distinct cytokines released from a human aminoacyl-tRNA synthetase. Science 1999; 284: 147-151.
    CrossrefPubMedGoogle Scholar
  • 25 Wakasugi K, Slike BM, Hood J. et al. Induction of angiogenesis by a fragment of human tyrosyl-tRNA synthetase. J Biol Chem 2002; 277: 20124-20126.
    CrossrefPubMedGoogle Scholar
  • 26 Yang XL, Skene RJ, McRee DE. et al. Crystal structure of a human aminoacyl-tRNA synthetase cytokine. Proc Natl Acad Sci U S A 2002; 99: 15369-15374.
    CrossrefPubMedGoogle Scholar
  • 27 Howard OM, Dong HF, Yang D. et al. Histidyl-tRNA synthetase and asparaginyl-tRNA synthetase, autoantigens in myositis, activate chemokine receptors on T lymphocytes and immature dendritic cells. J Exp Med 2002; 196: 781-791.
    CrossrefPubMedGoogle Scholar
  • 28 Yang D, Chertov O, Bykovskaia SN. et al. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 1999; 286: 525-528.
    CrossrefPubMedGoogle Scholar
  • 29 Alcami A. Viral mimicry of cytokines, chemokines and their receptors. Nat Rev Immunol 2003; 3: 36-50.
    CrossrefPubMedGoogle Scholar
  • 30 Noels H, Bernhagen J, Weber C. Macrophage migration inhibitory factor: a noncanonical chemokine important in atherosclerosis. Trends Cardiovasc Med 2009; 19: 76-86.
    CrossrefPubMedGoogle Scholar
  • 31 Murphy PM. Viral exploitation and subversion of the immune system through chemokine mimicry. Nat Immunol 2001; 2: 116-122.
    CrossrefPubMedGoogle Scholar
  • 32 Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 2011; 29: 139-162.
    CrossrefPubMedGoogle Scholar
  • 33 Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5: 331-342.
    CrossrefPubMedGoogle Scholar
  • 34 Schiraldi M, Raucci A, Munoz LM. et al. HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signalling via CXCR4. J Exp Med 2012; 209: 551-563.
    CrossrefPubMedGoogle Scholar
  • 35 David JR. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci USA 1966; 56: 72-77.
    CrossrefPubMedGoogle Scholar
  • 36 Degryse B, de Virgilio M. The nuclear protein HMGB1, a new kind of chemokine?. FEBS Lett 2003; 553: 11-17.
    CrossrefPubMedGoogle Scholar
  • 37 Calandra T, Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 2003; 3: 791-800.
    CrossrefPubMedGoogle Scholar
  • 38 Morand EF, Leech M, Bernhagen J. MIF: a new cytokine link between rheumatoid arthritis and atherosclerosis. Nat Rev Drug Discov 2006; 5: 399-410.
    CrossrefPubMedGoogle Scholar
  • 39 Noels H, Bernhagen J, Weber C. MIF in atherosclerosis. In Bucala R editor.. The MIF Handbook. World Scientific Publishing; Hongkong: 2012
    Google Scholar
  • 40 Leng L, Metz CN, Fang Y. et al. MIF signal transduction initiated by binding to CD7. J Exp Med 2003; 197: 1467-1476.
    CrossrefPubMedGoogle Scholar
  • 41 Shi X, Leng L, Wang T. et al. CD44 is the signalling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 2006; 25: 595-606.
    CrossrefPubMedGoogle Scholar
  • 42 Bernhagen J, Krohn R, Lue H. et al. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 2007; 13: 587-596.
    CrossrefPubMedGoogle Scholar
  • 43 Schwartz V, Lue H, Kraemer S. et al. A functional heteromeric MIF receptor formed by CD74 and CXCR4. FEBS Lett 2009; 583: 2749-2757.
    CrossrefPubMedGoogle Scholar
  • 44 Liu Y, Shaw SK, Ma S. et al. Regulation of leukocyte transmigration: cell surface interactions and signalling events. J Immunol 2004; 172: 7-13.
    CrossrefPubMedGoogle Scholar
  • 45 Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 2007; 7: 803-815.
    CrossrefPubMedGoogle Scholar
  • 46 Danese S, Dejana E, Fiocchi C. Immune regulation by microvascular endothelial cells: directing innate and adaptive immunity, coagulation, and inflammation. J Immunol 2007; 178: 6017-6022.
    CrossrefPubMedGoogle Scholar
  • 47 Donnelly SC, Bucala R. Macrophage migration inhibitory factor: a regulator of glucocorticoid activity with a critical role in inflammatory disease. Mol Med Today 1997; 3: 502-507.
    CrossrefPubMedGoogle Scholar
  • 48 Lolis E, Bucala R. Therapeutic approaches to innate immunity: severe sepsis and septic shock. Nat Rev Drug Discov 2003; 2: 635-645.
    CrossrefPubMedGoogle Scholar
  • 49 Mitchell RA, Bucala R. Tumour growth-promoting properties of macrophage migration inhibitory factor. Semin Cancer Biol 2000; 10: 359-366.
    CrossrefPubMedGoogle Scholar
  • 50 Bernhagen J, Calandra T, Mitchell RA. et al. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 1993; 365: 756-759.
    CrossrefPubMedGoogle Scholar
  • 51 Calandra T, Spiegel LA, Metz CN. et al. Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria. Proc Natl Acad Sci USA 1998; 95: 11383-11388.
    CrossrefPubMedGoogle Scholar
  • 52 Bozza M, Satoskar AR, Lin G. et al. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 1999; 189: 341-346.
    CrossrefPubMedGoogle Scholar
  • 53 Calandra T, Echtenacher B, Roy DL. et al. Protection from septic shock by neutralisation of macrophage migration inhibitory factor. Nat Med 2000; 6: 164-170.
    CrossrefPubMedGoogle Scholar
  • 54 Veillat V, Carli C, Metz CN. et al. Macrophage migration inhibitory factor elicits an angiogenic phenotype in human ectopic endometrial cells and triggers the production of major angiogenic factors via CD44, CD74, and MAPK signalling pathways. J Clin Endocrinol Metab 2010; 95: E403-412.
    CrossrefPubMedGoogle Scholar
  • 55 Baugh JA, Chitnis S, Donnelly SC. et al. A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun 2002; 3: 170-176.
    Google Scholar
  • 56 Burger-Kentischer A, Goebel H, Seiler R. et al. Expression of macrophage migration inhibitory factor in different stages of human atherosclerosis. Circulation 2002; 105: 1561-1566.
    CrossrefPubMedGoogle Scholar
  • 57 Shimizu T, Nishihira J, Watanabe H. et al. Macrophage migration inhibitory factor is induced by thrombin and factor Xa in endothelial cells. J Biol Chem 2004; 279: 13729-13737.
    CrossrefPubMedGoogle Scholar
  • 58 Schober A, Bernhagen J, Thiele M. et al. Stabilisation of atherosclerotic plaques by blockade of macrophage migration inhibitory factor after vascular injury in apolipoprotein E-deficient mice. Circulation 2004; 109: 380-385.
    CrossrefPubMedGoogle Scholar
  • 59 Simons D, Grieb G, Hristov M. et al. Hypoxia-induced endothelial secretion of macrophage migration inhibitory factor and role in endothelial progenitor cell recruitment. J Cell Mol Med 2011; 15: 668-678.
    CrossrefPubMedGoogle Scholar
  • 60 Chen L, Yang G, Zhang X. et al. Induction of MIF expression by oxidized LDL via activation of NF-κB in vascular smooth muscle cells. Atherosclerosis 2009; 207: 428-433.
    CrossrefPubMedGoogle Scholar
  • 61 Schrans-Stassen BH, Lue H, Sonnemans DG. et al. Stimulation of vascular smooth muscle cell migration by macrophage migration inhibitory factor. Antioxid Redox Signal 2005; 7: 1211-1216.
    CrossrefPubMedGoogle Scholar
  • 62 Lin SG, Yu XY, Chen YX. et al. De novo expression of macrophage migration inhibitory factor in atherogenesis in rabbits. Circ Res 2000; 87: 1202-1208.
    CrossrefPubMedGoogle Scholar
  • 63 Cheng Q, McKeown SJ, Santos L. et al. Macrophage migration inhibitory factor increases leukocyte-endothelial interactions in human endothelial cells via promotion of expression of adhesion molecules. J Immunol 2010; 185: 1238-1247.
    CrossrefPubMedGoogle Scholar
  • 64 Amin MA, Haas CS, Zhu K. et al. Migration inhibitory factor up-regulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 via Src, PI3 kinase, and NFkappaB. Blood 2006; 107: 2252-2261.
    CrossrefPubMedGoogle Scholar
  • 65 Chen Z, Sakuma M, Zago AC. et al. Evidence for a role of macrophage migration inhibitory factor in vascular disease. Arterioscler Thromb Vasc Biol 2004; 24: 709-714.
    CrossrefPubMedGoogle Scholar
  • 66 Libby P. Inflammation in atherosclerosis. Nature 2002; 420: 868-874.
    CrossrefPubMedGoogle Scholar
  • 67 Schmeisser A, Marquetant R, Illmer T. et al. The expression of macrophage migration inhibitory factor 1alpha (MIF 1alpha) in human atherosclerotic plaques is induced by different proatherogenic stimuli and associated with plaque instability. Atherosclerosis 2005; 178: 83-94.
    CrossrefPubMedGoogle Scholar
  • 68 de Winther MP, Kanters E, Kraal G. et al. Nuclear factor kappaB signalling in atherogenesis. Arterioscler Thromb Vasc Biol 2005; 25: 904-914.
    CrossrefPubMedGoogle Scholar
  • 69 Schweitzer K, Bozko PM, Dubiel W. et al. CSN controls NF-kappaB by deubiquitinylation of IkappaBalpha. Embo J 2007; 26: 1532-1541.
    CrossrefPubMedGoogle Scholar
  • 70 Kleemann R, Hausser A, Geiger G. et al. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 2000; 408: 211-216.
    CrossrefPubMedGoogle Scholar
  • 71 Pan JH, Sukhova GK, Yang JT. et al. Macrophage migration inhibitory factor deficiency impairs atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 2004; 109: 3149-3153.
    CrossrefPubMedGoogle Scholar
  • 72 Burger-Kentischer A, Gobel H, Kleemann R. et al. Reduction of the aortic inflammatory response in spontaneous atherosclerosis by blockade of macrophage migration inhibitory factor (MIF). Atherosclerosis 2006; 184: 28-38.
    CrossrefPubMedGoogle Scholar
  • 73 Kraemer S, Lue H, Zernecke A. et al. MIF-chemokine receptor interactions in atherogenesis are dependent on an N-loop-based 2-site binding mechanism. FASEB J 2011; 25: 894-906.
    CrossrefPubMedGoogle Scholar
  • 74 Herder C, Illig T, Baumert J. et al. Macrophage migration inhibitory factor (MIF) and risk for coronary heart disease: results from the MONICA/KORA Augsburg case-cohort study, 1984-2002. Atherosclerosis 2008; 200: 380-388.
    CrossrefPubMedGoogle Scholar
  • 75 Tereshchenko IP, Petrkova J, Mrazek F. et al. The macrophage migration inhibitory factor (MIF) gene polymorphism in Czech and Russian patients with myocardial infarction. Clin Chim Acta 2009; 402: 199-202.
    CrossrefPubMedGoogle Scholar
  • 76 Makino A, Nakamura T, Hirano M. et al. High plasma levels of macrophage migration inhibitory factor are associated with adverse long-term outcome in patients with stable coronary artery disease and impaired glucose tolerance or type 2 diabetes mellitus. Atherosclerosis 2010; 213: 573-578.
    CrossrefPubMedGoogle Scholar
  • 77 Muller II, Muller KA, Schonleber H. et al. Macrophage migration inhibitory factor is enhanced in acute coronary syndromes and is associated with the inflammatory response. PLoS One 2012; 7: e38376.
    CrossrefPubMedGoogle Scholar
  • 78 Conway EM, Collen D, Carmeliet P. Molecular mechanisms of blood vessel growth. Cardiovasc Res 2001; 49: 507-521.
    CrossrefPubMedGoogle Scholar
  • 79 Buschmann I, Schaper W. Arteriogenesis versus angiogenesis: two mechanisms of vessel growth. News Physiol Sci 1999; 14: 121-125.
    PubMedGoogle Scholar
  • 80 Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 1995; 11: 73-91.
    CrossrefPubMedGoogle Scholar
  • 81 Asahara T, Murohara T, Sullivan A. et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275: 964-967.
    CrossrefPubMedGoogle Scholar
  • 82 Ingram DA, Caplice NM, Yoder MC. Unresolved questions, changing definitions, and novel paradigms for defining endothelial progenitor cells. Blood 2005; 106: 1525-1531.
    CrossrefPubMedGoogle Scholar
  • 83 Ingram DA, Mead LE, Tanaka H. et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 2004; 104: 2752-2760.
    CrossrefPubMedGoogle Scholar
  • 84 Rehman J, Li J, Orschell CM. et al. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 2003; 107: 1164-1169.
    CrossrefPubMedGoogle Scholar
  • 85 Simons M, Ware JA. Therapeutic angiogenesis in cardiovascular disease. Nat Rev Drug Discov 2003; 2: 863-871.
    CrossrefPubMedGoogle Scholar
  • 86 Tuchscheerer N. The ligands of CXCR4 in vascularisation. [Dissertation thesis]. Aachen: RWTH Aachen University; 2012
    Google Scholar
  • 87 Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011; 473: 298-307.
    CrossrefPubMedGoogle Scholar
  • 88 Yancopoulos GD, Davis S, Gale NW. et al. Vascular-specific growth factors and blood vessel formation. Nature 2000; 407: 242-248.
    CrossrefPubMedGoogle Scholar
  • 89 Chesney J, Metz C, Bacher M. et al. An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol Med 1999; 5: 181-191.
    PubMedGoogle Scholar
  • 90 Wilson JM, Coletta PL, Cuthbert RJ. et al. Macrophage migration inhibitory factor promotes intestinal tumourigenesis. Gastroenterology 2005; 129: 1485-1503.
    CrossrefPubMedGoogle Scholar
  • 91 Winner M, Meier J, Zierow S. et al. A novel, macrophage migration inhibitory factor suicide substrate inhibits motility and growth of lung cancer cells. Cancer Res 2008; 68: 7253-7257.
    CrossrefPubMedGoogle Scholar
  • 92 Rendon BE, Roger T, Teneng I. et al. Regulation of human lung adenocarcinoma cell migration and invasion by macrophage migration inhibitory factor. J Biol Chem 2007; 282: 29910-29918.
    CrossrefPubMedGoogle Scholar
  • 93 Brock SE, Rendon BE, Yaddanapudi K. et al. Negative Regulation of AMP-activated Protein Kinase (AMPK) Activity by Macrophage Migration Inhibitory Factor (MIF) Family Members in Non-small Cell Lung Carcinomas. J Biol Chem 2012; 287: 37917-37925.
    CrossrefPubMedGoogle Scholar
  • 94 Rendon BE, Willer SS, Zundel W. et al. Mechanisms of macrophage migration inhibitory factor (MIF)-dependent tumour microenvironmental adaptation. Exp Mol Pathol 2009; 86: 180-185.
    CrossrefPubMedGoogle Scholar
  • 95 Coleman AM, Rendon BE, Zhao M. et al. Cooperative regulation of non-small cell lung carcinoma angiogenic potential by macrophage migration inhibitory factor and its homolog, D-dopachrome tautomerase. J Immunol 2008; 181: 2330-2337.
    CrossrefPubMedGoogle Scholar
  • 96 Baugh JA, Gantier M, Li L. et al. Dual regulation of macrophage migration inhibitory factor (MIF) expression in hypoxia by CREB and HIF-1. Biochem Biophys Res Commun 2006; 347: 895-903.
    CrossrefPubMedGoogle Scholar
  • 97 Copple BL, Bai S, Burgoon LD. et al. Hypoxia-inducible factor-1alpha regulates the expression of genes in hypoxic hepatic stellate cells important for collagen deposition and angiogenesis. Liver Int 2011; 31: 230-244.
    CrossrefPubMedGoogle Scholar
  • 98 Fu H, Luo F, Yang L. et al. Hypoxia stimulates the expression of macrophage migration inhibitory factor in human vascular smooth muscle cells via HIF-1alpha dependent pathway. BMC Cell Biol 2010; 11: 66.
    CrossrefPubMedGoogle Scholar
  • 99 Amin MA, Volpert OV, Woods JM. et al. Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase. Circ Res 2003; 93: 321-329.
    CrossrefPubMedGoogle Scholar
  • 100 Lue H, Kapurniotu A, Fingerle-Rowson G. 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 2006; 18: 688-703.
    CrossrefPubMedGoogle Scholar
  • 101 Mitchell RA, Metz CN, Peng T. et al. 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; 274: 18100-18106.
    CrossrefPubMedGoogle Scholar
  • 102 Liehn EA, Merx MW, Postea O. et al. Ccr1 deficiency reduces inflammatory remodelling and preserves left ventricular function after myocardial infarction. J Cell Mol Med 2008; 12: 496-506.
    CrossrefPubMedGoogle Scholar
  • 103 Liehn EA, Tuchscheerer N, Kanzler I. et al. Double-edged role of the CXCL12/CXCR4 axis in experimental myocardial infarction. J Am Coll Cardiol 2011; 58: 2415-2423.
    CrossrefPubMedGoogle Scholar
  • 104 Koga K, Kenessey A, Powell S. et al. Macrophage migration inhibitory factor provides cardioprotection during ischaemia/reperfusion by reducing oxidative stress. Antioxid Redox Signal 2010; 14: 1191-1202.
    PubMedGoogle Scholar
  • 105 Miller EJ, Li J, Leng L. et al. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature 2008; 451: 578-582.
    CrossrefPubMedGoogle Scholar
  • 106 Qi D, Hu X, Wu X. et al. Cardiac macrophage migration inhibitory factor inhibits JNK pathway activation and injury during ischaemia/reperfusion. J Clin Invest 2009; 119: 3807-3816.
    CrossrefPubMedGoogle Scholar
  • 107 Luedike P, Hendgen-Cotta UB, Sobierajski J. et al. Cardioprotection through S-nitros(yl)ation of macrophage migration inhibitory factor. Circulation 2012; 125: 1880-1889.
    CrossrefPubMedGoogle Scholar
  • 108 Ceradini DJ, Gurtner GC. Homing to hypoxia: HIF-1 as a mediator of progenitor cell recruitment to injured tissue. Trends Cardiovasc Med 2005; 15: 57-63.
    CrossrefPubMedGoogle Scholar
  • 109 Ceradini DJ, Kulkarni AR, Callaghan MJ. et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004; 10: 858-864.
    CrossrefPubMedGoogle Scholar
  • 110 Grieb G, Piatkowski A, Simons D. et al. Macrophage migration inhibitory factor is a potential inducer of endothelial progenitor cell mobilisation after flap operation. Surgery 2012; 151: 268-277.
    CrossrefPubMedGoogle Scholar
  • 111 Kupatt C, Bock-Marquette I, Boekstegers P. Embryonic endothelial progenitor cell-mediated cardioprotection requires Thymosin beta4. Trends Cardiovasc Med 2008; 18: 205-210.
    CrossrefPubMedGoogle Scholar
  • 112 Kupatt C, Horstkotte J, Vlastos GA. et al. Embryonic endothelial progenitor cells expressing a broad range of proangiogenic and remodelling factors enhance vascularisation and tissue recovery in acute and chronic ischaemia. Faseb J 2005; 19: 1576-1578.
    CrossrefPubMedGoogle Scholar
  • 113 Kanzler I, Tuchscheerer N, Steffens G. et al. Differential roles of angiogenic chemokines in endothelial progenitor cell-induced angiogenesis. Basic Res Cardiol 2013; 108: 310-323.
    CrossrefPubMedGoogle Scholar