Proinflammatory signature of the dysfunctional endothelium in pulmonary hypertension role of the macrophage migration inhibitory factor/CD74 complex

American Journal of Respiratory and Critical Care Medicine

Volumn 192, Issue 8, 2015, Pages 983-997

  Le Hiress, Morane ^a,b   Tu, Ly ^a,b   Ricard, Nicolas ^a,b   Phan, Carole ^a,b   Thuillet, Raphael ^a,b   Fadel, Elie ^a,b   Dorfmuller, Peter ^a,b   Montani, David ^a,b,c   De Man, Frances ^d   Humbert, Marc ^a,b,c   Huertas, Alice ^a,b,c   Guignabert, Christophe ^a,b  

^a CENTRE CHIRURGICAL MARIE LANNELONGUE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c BICÊTRE HOSPITAL   (France)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Adhesion molecules; CD74 signaling pathway; Endothelial dysfunction; Macrophage migration inhibitory factor; Pulmonary hypertension

Indexed keywords

1 (2 BROMOPHENYL) 3 (2 HYDROXY 4 NITROPHENYL)UREA; CD3 ANTIGEN; CD45 ANTIGEN; CD68 ANTIGEN; CD74 ANTIGEN; CHEMOKINE RECEPTOR CXCR2; CHEMOKINE RECEPTOR CXCR4; DOPACHROME TAUTOMERASE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 12; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE MIGRATION INHIBITION FACTOR; MONOCROTALINE; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTRALIZING ANTIBODY; PADGEM PROTEIN; PLERIXAFOR; VASCULAR CELL ADHESION MOLECULE 1; B LYMPHOCYTE ANTIGEN; HLA ANTIGEN CLASS 2; INVARIANT CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CARDIOVASCULAR DISEASE; CELL INFILTRATION; CELL ISOLATION; CELL SURFACE; COMPARATIVE STUDY; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; EPITHELIUM CELL; HEART MUSCLE FIBROSIS; HEART OUTPUT; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; LUNG ARTERY PRESSURE; LUNG HOMOGENATE; LUNG VASCULAR RESISTANCE; LYMPHOCYTE COUNT; MACROPHAGE; MONOCROTALINE-INDUCED PULMONARY HYPERTENSION; MONOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN SECRETION; PULMONARY HYPERTENSION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEADY STATE; T LYMPHOCYTE; UPREGULATION; WESTERN BLOTTING; ADULT; ANIMAL; CASE CONTROL STUDY; CELL CULTURE; DISEASE MODEL; FEMALE; IMMUNOLOGY; INFLAMMATION; MALE; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; PATHOPHYSIOLOGY; PULMONARY ARTERY; VASCULAR ENDOTHELIUM;

ADULT; ANIMALS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; CASE-CONTROL STUDIES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; E-SELECTIN; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FAMILIAL PRIMARY PULMONARY HYPERTENSION; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IN VITRO TECHNIQUES; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; LEUKOCYTES, MONONUCLEAR; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MALE; MIDDLE AGED; PULMONARY ARTERY; RATS; SIGNAL TRANSDUCTION; UP-REGULATION; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84945539939     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201402-0322OC     Document Type: Article

References (42)

1. Humbert M, Sitbon O, Chaouat A, Bertocchi M, Habib G, Gressin V, Yäci A, Weitzenblum E, Cordier JF, Chabot F, et al. Survival in patients with idiopathic, familial, and anorexigen-associated pulmonary arterial hypertension in the modern management era. Circulation 2010;122: 156-163.
2. Voelkel NF, Gomez-Arroyo J, Abbate A, Bogaard HJ, Nicolls MR. Pathobiology of pulmonary arterial hypertension and right ventricular failure. Eur Respir J 2012;40:1555-1565.
3. Huertas A, Perros F, Tu L, Cohen-Kaminsky S, Montani D, Dorfmuller P, Guignabert C, Humbert M. Immune dysregulation and endothelial dysfunction in pulmonary arterial hypertension: a complex interplay. Circulation 2014;129:1332-1340.
4. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R. MIF signal transduction initiated by binding to CD74. J Exp Med 2003;197:1467-1476.
5. Tillmann S, Bernhagen J, Noels H. Arrest functions of the MIF ligand/receptor axes in atherogenesis. Front Immunol 2013;4: 115.
6. Gregory JL, Morand EF, McKeown SJ, Ralph JA, Hall P, Yang YH, McColl SR, Hickey MJ. Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2. J Immunol 2006;177:8072-8079.
7. Fan H, Hall P, Santos LL, Gregory JL, Fingerle-Rowson G, Bucala R, Morand EF, Hickey MJ. Macrophage migration inhibitory factor and CD74 regulate macrophage chemotactic responses via MAPK and Rho GTPase. J Immunol 2011;186:4915-4924.
8. Miller EJ, Li J, Leng L, McDonald C, Atsumi T, Bucala R, Young LH. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature 2008;451:578-582.
9. Bernhagen J, Krohn R, Lue H, Gregory JL, Zernecke A, Koenen RR, Dewor M, Georgiev I, Schober A, Leng L, et al. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 2007;13:587-596.
10. Damico R, Simms T, Kim BS, Tekeste Z, Amankwan H, Damarla M, Hassoun PM. p53 mediates cigarette smoke-induced apoptosis of pulmonary endothelial cells: inhibitory effects of macrophage migration inhibitor factor. Am J Respir Cell Mol Biol 2011;44:323-332.
11. Lue H, Thiele M, Franz J, Dahl E, Speckgens S, Leng L, Fingerle-Rowson G, Bucala R, Luscher B, Bernhagen J. 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;26:5046-5059.
12. Takahashi K, Koga K, Linge HM, Zhang Y, Lin X, Metz CN, Al-Abed Y, Ojamaa K, Miller EJ. Macrophage CD74 contributes to MIF-induced pulmonary inflammation. Respir Res 2009;10:33.
13. Gore Y, Starlets D, Maharshak N, Becker-Herman S, Kaneyuki U, Leng L, Bucala R, Shachar I. Macrophage migration inhibitory factor induces B cell survival by activation of a CD74-CD44 receptor complex. J Biol Chem 2008;283:2784-2792.
14. Richard V, Kindt N, Decaestecker C, Gabius HJ, Laurent G, Noel JC, Saussez S. Involvement of macrophage migration inhibitory factor and its receptor (CD74) in human breast cancer. Oncol Rep 2014;32: 523-529.
15. de Man FS, Tu L, Handoko ML, Rain S, Ruiter G, François C, Schalij I, Dorfmuller P, Simonneau G, Fadel E, et al. Dysregulated reninangiotensin-aldosterone system contributes to pulmonary arterial hypertension. Am J Respir Crit Care Med 2012;186:780-789.
16. Guignabert C, Tu L, Izikki M, Dewachter L, Zadigue P, Humbert M, Adnot S, Fadel E, Eddahibi S. Dichloroacetate treatment partially regresses established pulmonary hypertension in mice with SM22atargeted overexpression of the serotonin transporter. FASEB J 2009; 23:4135-4147.
17. Huertas A, Tu L, Gambaryan N, Girerd B, Perros F, Montani D, Fabre D, Fadel E, Eddahibi S, Cohen-Kaminsky S, et al. Leptin and regulatory T-lymphocytes in idiopathic pulmonary arterial hypertension. Eur Respir J 2012;40:895-904.
18. Ricard N, Tu L, Le Hiress M, Huertas A, Phan C, Thuillet R, Sattler C, Fadel E, Seferian A, Montani D, et al. Increased pericyte coverage mediated by endothelial-derived fibroblast growth factor-2 and interleukin-6 is a source of smooth muscle-like cells in pulmonary hypertension. Circulation 2014;129:1586-1597.
19. Tu L, De Man FS, Girerd B, Huertas A, Chaumais MC, Lecerf F, François C, Perros F, Dorfmuller P, Fadel E, et al. A critical role for p130Cas in the progression of pulmonary hypertension in humans and rodents. Am J Respir Crit Care Med 2012;186: 666-676.
20. Tu L, Dewachter L, Gore B, Fadel E, Dartevelle P, Simonneau G, Humbert M, Eddahibi S, Guignabert C. Autocrine fibroblast growth factor-2 signaling contributes to altered endothelial phenotype in pulmonary hypertension. Am J Respir Cell Mol Biol 2011;45:311-322.
21. Binsky I, Haran M, Starlets D, Gore Y, Lantner F, Harpaz N, Leng L, Goldenberg DM, Shvidel L, Berrebi A, et al. IL-8 secreted in a macrophage migration-inhibitory factor-and CD74-dependent manner regulates B cell chronic lymphocytic leukemia survival. Proc Natl Acad Sci USA 2007;104:13408-13413.
22. Guignabert C, Raffestin B, Benferhat R, Raoul W, Zadigue P, Rideau D, Hamon M, Adnot S, Eddahibi S. Serotonin transporter inhibition prevents and reverses monocrotaline-induced pulmonary hypertension in rats. Circulation 2005;111:2812-2819.
23. El-Bizri N, Guignabert C, Wang L, Cheng A, Stankunas K, Chang CP, Mishina Y, Rabinovitch M. SM22a-targeted deletion of bone morphogenetic protein receptor 1A in mice impairs cardiac and vascular development, and influences organogenesis. Development 2008;135:2981-2991.
24. Guignabert C, Alvira CM, Alastalo TP, Sawada H, Hansmann G, Zhao M, Wang L, El-Bizri N, Rabinovitch M. Tie2-mediated loss of peroxisome proliferator-activated receptor-g in mice causes PDGF receptor-b-dependent pulmonary arterial muscularization. Am J Physiol Lung Cell Mol Physiol 2009;297: L1082-L1090.
25. Badve S, Deshpande C, Hua Z, Logdberg L. Expression of invariant chain (CD 74) and major histocompatibility complex (MHC) class II antigens in the human fetus. J Histochem Cytochem 2002;50:473-482.
26. Pyrz M, Wang B, Wabl M, Pedersen FS. A retroviral mutagenesis screen identifies Cd74 as a common insertion site in murine B-lymphomas and reveals the existence of a novel IFNg-inducible Cd74 isoform. Mol Cancer 2010;9:86.
27. Eriksson EE. Mechanisms of leukocyte recruitment to atherosclerotic lesions: future prospects. Curr Opin Lipidol 2004;15:553-558.
28. Davis BB, Shen YH, Tancredi DJ, Flores V, Davis RP, Pinkerton KE. Leukocytes are recruited through the bronchial circulation to the lung in a spontaneously hypertensive rat model of COPD. PLoS One 2012;7:e33304.
29. Stacher E, Graham BB, Hunt JM, Gandjeva A, Groshong SD, McLaughlin VV, Jessup M, Grizzle WE, Aldred MA, Cool CD, et al. Modern age pathology of pulmonary arterial hypertension. Am J Respir Crit Care Med 2012;186:261-272.
30. Vera PL, Wang X, Bucala RJ, Meyer-Siegler KL. Intraluminal blockade of cell-surface CD74 and glucose regulated protein 78 prevents substance P-induced bladder inflammatory changes in the rat. PLoS One 2009;4:e5835.
31. Cracowski JL, Chabot F, Labarè re J, Faure P, Degano B, Schwebel C, Chaouat A, Reynaud-Gaubert M, Cracowski C, Sitbon O, et al. Proinflammatory cytokine levels are linked to death in pulmonary arterial hypertension. Eur Respir J 2014;43:915-917.
32. Soon E, Holmes AM, Treacy CM, Doughty NJ, Southgate L, Machado RD, Trembath RC, Jennings S, Barker L, Nicklin P, et al. Elevated levels of inflammatory cytokines predict survival in idiopathic and familial pulmonary arterial hypertension. Circulation 2010;122:920-927.
33. Rabinovitch M, Guignabert C, Humbert M, Nicolls MR. Inflammation and immunity in the pathogenesis of pulmonary arterial hypertension. Circ Res 2014;115:165-175.
34. Sorescu GP, Sykes M, Weiss D, Platt MO, Saha A, Hwang J, Boyd N, Boo YC, Vega JD, Taylor WR, et al. Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress stimulates an inflammatory response. J Biol Chem 2003;278:31128-31135.
35. Csiszar A, Ahmad M, Smith KE, Labinskyy N, Gao Q, Kaley G, Edwards JG, Wolin MS, Ungvari Z. Bone morphogenetic protein-2 induces proinflammatory endothelial phenotype. Am J Pathol 2006;168: 629-638.
36. Davies RJ, Holmes AM, Deighton J, Long L, Yang X, Barker L, Walker C, Budd DC, Upton PD, Morrell NW. BMP type II receptor deficiency confers resistance to growth inhibition by TGF-b in pulmonary artery smooth muscle cells: role of proinflammatory cytokines. Am J Physiol Lung Cell Mol Physiol 2012;302:L604-L615.
37. Helbing T, Rothweiler R, Ketterer E, Goetz L, Heinke J, Grundmann S, Duerschmied D, Patterson C, Bode C, Moser M. BMP activity controlled by BMPER regulates the proinflammatory phenotype of endothelium. Blood 2011;118:5040-5049.
38. Zhang B, Shen M, Xu M, Liu LL, Luo Y, Xu DQ, Wang YX, Liu ML, Liu Y, Dong HY, et al. Role of macrophage migration inhibitory factor in the proliferation of smooth muscle cell in pulmonary hypertension. Mediators Inflamm 2012;2012:840737.
39. Zhang Y, Talwar A, Tsang D, Bruchfeld A, Sadoughi A, Hu M, Omonuwa K, Cheng KF, Al-Abed Y, Miller EJ. Macrophage migration inhibitory factor mediates hypoxia-induced pulmonary hypertension. Mol Med 2012;18:215-223.
40. Gambaryan N, Perros F, Montani D, Cohen-Kaminsky S, Mazmanian M, Renaud JF, Simonneau G, Lombet A, Humbert M. Targeting of c-kit1 haematopoietic progenitor cells prevents hypoxic pulmonary hypertension. Eur Respir J 2011;37:1392-1399.
41. Koga K, Kenessey A, Ojamaa K. Macrophage migration inhibitory factor antagonizes pressure overload-induced cardiac hypertrophy. Am J Physiol Heart Circ Physiol 2013;304:H282-H293.
42. Schober A, Bernhagen J, Thiele M, Zeiffer U, Knarren S, Roller M, Bucala R, Weber C. Stabilization of atherosclerotic plaques by blockade of macrophage migration inhibitory factor after vascular injury in apolipoprotein E-deficient mice. Circulation 2004;109:380-385.