Home LiteratureArticle Details
PMID: 25617421 Published · epublish English Journal Article

Macrophage migration inhibitory factor induces vascular leakage via autophagy.

Biology open ·Vol. 4 ·No. 2 ·2015-01-23 ·Pages 244-52

Chen HR, Chuang YC, Chao CH, Yeh TM

Abstract

Vascular leakage is an important feature of acute inflammatory shock, which currently has no effective treatment. Macrophage migration inhibitory factor (MIF) is a pro-inflammatory cytokine that can induce vascular leakage and plays an important role in the pathogenesis of shock. However, the mechanism of MIF-induced vascular leakage is still unclear. In this study, using recombinant MIF (rMIF), we demonstrated that MIF induced disorganization and degradation of junction proteins and increased the permeability of human endothelial cells in vitro. Western blotting analysis showed that rMIF treatment induced LC3 conversion and p62 degradation. Inhibition of autophagy with a PI3K inhibitor (3-MA), a ROS scavenger (NAC) or autophagosomal-lysosomal fusion inhibitors (bafilomycin A1 and chloroquine) rescued rMIF-induced vascular leakage, suggesting that autophagy mediates MIF-induced vascular leakage. The potential involvement of other signaling pathways was also studied using different inhibitors, and the results suggested that MIF-induced vascular leakage may occur through the ERK pathway. In conclusion, we showed that MIF triggered autophagic degradation of endothelial cells, resulting in vascular leakage. Inhibition of MIF-induced autophagy may provide therapeutic targets against vascular leakage in inflammatory shock.

Keywords
Autophagy Cytokine Endothelial cells MIF Shock
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chen Hong-Ru
The Institute of Basic Medical Sciences, Medical College, National Cheng Kung University, Tainan, Taiwan.
Chuang Yung-Chun
Department of Medical Laboratory Science and Biotechnology, Medical College, National Cheng Kung University, Tainan, Taiwan.
Chao Chiao-Hsuan
Department of Medical Laboratory Science and Biotechnology, Medical College, National Cheng Kung University, Tainan, Taiwan.
Yeh Trai-Ming
The Institute of Basic Medical Sciences, Medical College, National Cheng Kung University, Tainan, Taiwan Department of Medical Laboratory Science and Biotechnology, Medical College, National Cheng Kung University, Tainan, Taiwan today@mail.ncku.edu.tw.
References (57)
57 references, click to expand
  1. Endotoxin-induced myocardial dysfunction: effects of macrophage migration inhibitory factor neutralization.
    Circ Res. 2005 May 27;96(10):1095-102 PMID: 15879312
  2. Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization.
    Arterioscler Thromb Vasc Biol. 1996 Mar;16(3):488-96 PMID: 8630677
  3. The permeability of the blood-brain barrier in mice suffering from fatal lymphocytic choriomeningitis virus infection.
    Acta Neuropathol. 1984;63(3):229-39 PMID: 6464679
  4. 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 Nov 2;287(45):37917-25 PMID: 22988252
  5. 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
  6. Tissue inhibitor of metalloproteinase-2 regulates matrix metalloproteinase-2-mediated endothelial barrier dysfunction and breast cancer cell transmigration through lung microvascular endothelial cells.
    Mol Cancer Res. 2010 Jul;8(7):939-51 PMID: 20571065
  7. A functional heteromeric MIF receptor formed by CD74 and CXCR4.
    FEBS Lett. 2009 Sep 3;583(17):2749-57 PMID: 19665027
  8. Autophagy regulates lipid metabolism.
    Nature. 2009 Apr 30;458(7242):1131-5 PMID: 19339967
  9. 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
  10. Vascular reactions to histamine, histamine-liberator and leukotaxine in the skin of guinea-pigs.
    J Physiol. 1952 Oct;118(2):228-57 PMID: 13000707
  11. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin.
    Nat Cell Biol. 2006 Nov;8(11):1223-34 PMID: 17060906
  12. HMGB1 induces human lung endothelial cell cytoskeletal rearrangement and barrier disruption.
    Microvasc Res. 2011 Mar;81(2):189-97 PMID: 21146549
  13. Autophagy and cytokines.
    Cytokine. 2011 Nov;56(2):140-4 PMID: 21889357
  14. Egr-1 regulates autophagy in cigarette smoke-induced chronic obstructive pulmonary disease.
    PLoS One. 2008 Oct 02;3(10):e3316 PMID: 18830406
  15. Molecular basis of endothelial dysfunction in sepsis.
    Cardiovasc Res. 2003 Oct 15;60(1):49-57 PMID: 14522406
  16. Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever-dengue shock syndrome (DHF/DSS).
    Immunol Cell Biol. 2007 Jan;85(1):43-5 PMID: 17130899
  17. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast.
    J Biol Chem. 1998 Feb 13;273(7):3963-6 PMID: 9461583
  18. Autophagy promotes hepatocellular carcinoma cell invasion through activation of epithelial-mesenchymal transition.
    Carcinogenesis. 2013 Jun;34(6):1343-51 PMID: 23430956
  19. RhoA/ROCK signaling is essential for multiple aspects of VEGF-mediated angiogenesis.
    FASEB J. 2010 Sep;24(9):3186-95 PMID: 20400538
  20. Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases.
    Circ Res. 2000 Aug 18;87(4):335-40 PMID: 10948069
  21. 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
  22. Human fatal zaire ebola virus infection is associated with an aberrant innate immunity and with massive lymphocyte apoptosis.
    PLoS Negl Trop Dis. 2010 Oct 05;4(10):null PMID: 20957152
  23. Autophagy is involved in nanoalumina-induced cerebrovascular toxicity.
    Nanomedicine. 2013 Feb;9(2):212-21 PMID: 22687898
  24. Contribution of macrophage migration inhibitory factor to the pathogenesis of dengue virus infection.
    FASEB J. 2010 Jan;24(1):218-28 PMID: 19776337
  25. KDR stimulates endothelial cell migration through heterotrimeric G protein Gq/11-mediated activation of a small GTPase RhoA.
    J Biol Chem. 2002 Nov 29;277(48):46791-8 PMID: 12244099
  26. A matrix metalloprotease-PAR1 system regulates vascular integrity, systemic inflammation and death in sepsis.
    EMBO Mol Med. 2011 Jul;3(7):370-84 PMID: 21591259
  27. mTOR: from growth signal integration to cancer, diabetes and ageing.
    Nat Rev Mol Cell Biol. 2011 Jan;12(1):21-35 PMID: 21157483
  28. Thrombin-induced autophagy: a potential role in intracerebral hemorrhage.
    Brain Res. 2011 Nov 18;1424:60-6 PMID: 22015349
  29. TNF-α signals through PKCζ/NF-κB to alter the tight junction complex and increase retinal endothelial cell permeability.
    Diabetes. 2010 Nov;59(11):2872-82 PMID: 20693346
  30. Macrophage migration inhibitory factor in cardiovascular disease.
    Circulation. 2008 Mar 25;117(12):1594-602 PMID: 18362243
  31. 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
  32. Role of the endothelial actin filament cytoskeleton in rheology and permeability.
    Z Kardiol. 1989;78 Suppl 6:1-4 PMID: 2618125
  33. Novel strategies for the treatment of sepsis.
    Nat Med. 2003 May;9(5):517-24 PMID: 12724763
  34. 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 May;18(5):688-703 PMID: 16122907
  35. The emerging role of MIF in septic shock and infection.
    Biotherapy. 1994;8(2):123-7 PMID: 8924353
  36. Endogenous HMGB1 regulates autophagy.
    J Cell Biol. 2010 Sep 6;190(5):881-92 PMID: 20819940
  37. Macrophage migration inhibitory factor is enhanced in acute coronary syndromes and is associated with the inflammatory response.
    PLoS One. 2012;7(6):e38376 PMID: 22693633
  38. Interleukin receptor activates a MYD88-ARNO-ARF6 cascade to disrupt vascular stability.
    Nature. 2012 Dec 13;492(7428):252-5 PMID: 23143332
  39. Limiting cardiac ischemic injury by pharmacological augmentation of macrophage migration inhibitory factor-AMP-activated protein kinase signal transduction.
    Circulation. 2013 Jul 16;128(3):225-36 PMID: 23753877
  40. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling.
    J Cell Biol. 2012 Mar 5;196(5):641-52 PMID: 22391038
  41. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3.
    Autophagy. 2007 Sep-Oct;3(5):452-60 PMID: 17534139
  42. The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis.
    Nat Med. 2012 Aug;18(8):1217-23 PMID: 22820644
  43. Atg1-mediated myosin II activation regulates autophagosome formation during starvation-induced autophagy.
    EMBO J. 2011 Feb 16;30(4):636-51 PMID: 21169990
  44. Macrophage migration inhibitory factor induced by dengue virus infection increases vascular permeability.
    Cytokine. 2011 May;54(2):222-31 PMID: 21320786
  45. Autophagosomes induced by a bacterial Beclin 1 binding protein facilitate obligatory intracellular infection.
    Proc Natl Acad Sci U S A. 2012 Dec 18;109 (51):20800-7 PMID: 23197835
  46. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice.
    Nature. 2006 Jun 15;441(7095):885-9 PMID: 16625204
  47. The tumour necrosis factor-alpha induced vascular permeability is associated with a reduction of VE-cadherin expression.
    Eur J Med Res. 2002 Apr 30;7(4):171-6 PMID: 12010652
  48. Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication.
    J Biol Chem. 2011 Jun 24;286(25):22147-59 PMID: 21511946
  49. Tight junctions and the modulation of barrier function in disease.
    Histochem Cell Biol. 2008 Jul;130(1):55-70 PMID: 18415116
  50. Macrophage migration inhibitory factor (MIF): a key player in protozoan infections.
    Int J Biol Sci. 2011;7(9):1239-56 PMID: 22110378
  51. Role of GTPases in control of microvascular permeability.
    Cardiovasc Res. 2010 Jul 15;87(2):243-53 PMID: 20299335
  52. Erk1/2-dependent phosphorylation of Galpha-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells.
    J Biol Chem. 2000 Dec 15;275(50):39090-5 PMID: 10993892
  53. In vitro production of choleragen and vascular permeability factor by Vibrio cholerae.
    J Bacteriol. 1968 Jul;96(1):126-30 PMID: 5663564
  54. Macrophage migration inhibitory factor (MIF) exerts antifibrotic effects in experimental liver fibrosis via CD74.
    Proc Natl Acad Sci U S A. 2011 Oct 18;108(42):17444-9 PMID: 21969590
  55. Hypothetical pathophysiology of acute encephalopathy and encephalitis related to influenza virus infection and hypothermia therapy.
    Pediatr Int. 2000 Apr;42(2):197-203 PMID: 10804742
  56. Increased macrophage migration inhibitory factor (MIF) plasma levels in acute HIV-1 infection.
    Cytokine. 2012 Nov;60(2):338-40 PMID: 22898393
  57. Macrophage migration inhibitory factor induces autophagy via reactive oxygen species generation.
    PLoS One. 2012;7(5):e37613 PMID: 22629429
Article Info
Journal
Biology open
Abbr.
Biol Open
ISSN
2046-6390
Published
2015-01-23
Epub
2015-00-23
Pages
244-52
Language
English
Region
England
NLM ID
101578018
PMCID
PMC4365493
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