Hepatocyte Growth Factor Receptor c-Met Instructs T Cell Cardiotropism and Promotes T Cell Migration to the Heart via Autocrine Chemokine Release

Immunity

Volumn 42, Issue 6, 2015, Pages 1087-1099

  Komarowska, Izabela ^a   Coe, David ^a   Wang, Guosu ^a   Haas, Robert ^a   Mauro, Claudio ^a   Kishore, Madhav ^a   Cooper, Dianne ^a   Nadkarni, Suchita ^a   Fu, Hongmei ^a   Steinbruchel, Daniel A ^b   Pitzalis, Costantino ^a   Anderson, Graham ^c   Bucy, Pat ^d   Lombardi, Giovanna ^e   Breckenridge, Ross ^f   Marelli Berg, Federica M ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b Mental Health Services CPH   (Denmark)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; RANTES; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; STAT3 PROTEIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; 5-((2,6-DICHLOROBENZYL)SULFONYL)-3-((3,5-DIMETHYL-4-((2-(PYRROLIDIN-1-YLMETHYL)PYRROLIDIN-1-YL)CARBONYL)-1H-PYRROL-2-YL)METHYLENE)-1,3-DIHYDRO-2H-INDOL-2-ONE; CCR5 PROTEIN, MOUSE; CHEMOKINE RECEPTOR; HOMING RECEPTOR; INDOLE DERIVATIVE; SMALL INTERFERING RNA; SULFONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CARDIAC GRAFT REJECTION; CARDIOTROPISM; CARDIOVASCULAR FUNCTION; CARDITIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ADHESION; CELL ISOLATION; CELL SURFACE; CELLULAR DISTRIBUTION; CHEMOKINESIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HEART GRAFT; HEART TRANSPLANTATION; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LYMPH NODE; LYMPHOCYTE HOMING; LYMPHOCYTE MIGRATION; LYMPHOCYTE RECIRCULATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKIN ALLOGRAFT; STEADY STATE; SURVIVAL; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TROPISM; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL MOTION; DRUG EFFECTS; GENETICS; GRAFT REJECTION; HEART; IMMUNOLOGICAL MEMORY; LYMPHOCYTE ACTIVATION; METABOLISM; MOLECULARLY TARGETED THERAPY; PHYSIOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; AUTOCRINE COMMUNICATION; CELL MOVEMENT; CELLS, CULTURED; GRAFT REJECTION; HEART; HEART TRANSPLANTATION; HEPATOCYTE GROWTH FACTOR; HUMANS; IMMUNOLOGIC MEMORY; INDOLES; LYMPHOCYTE ACTIVATION; MICE; MICE, SCID; MOLECULAR TARGETED THERAPY; PROTO-ONCOGENE PROTEINS C-MET; RECEPTORS, CCR5; RECEPTORS, CHEMOKINE; RECEPTORS, LYMPHOCYTE HOMING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SULFONES; T-LYMPHOCYTES;

EID: 84937557229     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.05.014     Document Type: Article

References (34)

1. Adams D.H., Harvath L., Bottaro D.P., Interrante R., Catalano G., Tanaka Y., Strain A., Hubscher S.G., Shaw S. Hepatocyte growth factor and macrophage inflammatory protein 1 beta: structurally distinct cytokines that induce rapid cytoskeletal changes and subset-preferential migration in Tcells. Proc. Natl. Acad. Sci. USA 1994, 91:7144-7148.
2. Bao X., Moseman E.A., Saito H., Petryniak B., Thiriot A., Hatakeyama S., Ito Y., Kawashima H., Yamaguchi Y., Lowe J.B., et al. Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes. Immunity 2010, 33:817-829.
3. Campbell D.J., Kim C.H., Butcher E.C. Chemokines in the systemic organization of immunity. Immunol. Rev. 2003, 195:58-71.
4. Casazza J.P., Brenchley J.M., Hill B.J., Ayana R., Ambrozak D., Roederer M., Douek D.C., Betts M.R., Koup R.A. Autocrine production of beta-chemokines protects CMV-specific CD4 Tcells from HIV infection. PLoS Pathog. 2009, 5:e1000646.
5. Garrood T., Blades M., Haskard D.O., Mather S., Pitzalis C. Anovel model for the pre-clinical imaging of inflamed human synovial vasculature. Rheumatology (Oxford) 2009, 48:926-931.
6. Gretz J.E., Norbury C.C., Anderson A.O., Proudfoot A.E., Shaw S. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J.Exp. Med. 2000, 192:1425-1440.
7. Hancock W.W., Gao W., Csizmadia V., Faia K.L., Shemmeri N., Luster A.D. Donor-derived IP-10 initiates development of acute allograft rejection. J.Exp. Med. 2001, 193:975-980.
8. Hartmann G., Prospero T., Brinkmann V., Ozcelik C., Winter G., Hepple J., Batley S., Bladt F., Sachs M., Birchmeier C., et al. Engineered mutants of HGF/SF with reduced binding to heparan sulphate proteoglycans, decreased clearance and enhanced activity invivo. Curr. Biol. 1998, 8:125-134.
9. Honjo K., Yan Xu X., Kapp J.A., Bucy R.P. Evidence for cooperativity in the rejection of cardiac grafts mediated by CD4 TCR Tg Tcells specific for a defined allopeptide. Am. J. Transplant. 2004, 4:1762-1768.
10. Hüser N., Tertilt C., Gerauer K., Maier S., Traeger T., Assfalg V., Reiter R., Heidecke C.D., Pfeffer K. CCR4-deficient mice show prolonged graft survival in a chronic cardiac transplant rejection model. Eur. J. Immunol. 2005, 35:128-138.
11. Kaibori M., Yanagida H., Nakanishi H., Ozaki T., Yoshida H., Matsui K., Hijikawa T., Kamiyama Y., Okumura T. Hepatocyte growth factor stimulates the induction of cytokine-induced neutrophil chemoattractant through the activation of NF-kappaB in rat hepatocytes. J.Surg. Res. 2006, 130:88-93.
12. Khabbazi S., Jacques R.O., Moyano Cardaba C., Mueller A. Janus kinase 2 and signal transducer and activator of transcription 3 activation is not essential for CCL3-, CCL5- or CCL8-induced chemotaxis. Cell Biochem. Funct. 2013, 31:312-318.
13. Kitamura K., Kato J., Kawamoto M., Tanaka M., Chino N., Kangawa K., Eto T. The intermediate form of glycine-extended adrenomedullin is the major circulating molecular form in human plasma. Biochem. Biophys. Res. Commun. 1998, 244:551-555.
14. Lalor P.F., Shields P., Grant A., Adams D.H. Recruitment of lymphocytes to the human liver. Immunol. Cell Biol. 2002, 80:52-64.
15. Lalor P.F., Lai W.K., Curbishley S.M., Shetty S., Adams D.H. Human hepatic sinusoidal endothelial cells can be distinguished by expression of phenotypic markers related to their specialised functions invivo. World J. Gastroenterol. 2006, 12:5429-5439.
16. Leri A., Kajstura J., Anversa P. Cardiac stem cells and mechanisms of myocardial regeneration. Physiol. Rev. 2005, 85:1373-1416.
17. Madonna R., Cevik C., Nasser M., De Caterina R. Hepatocyte growth factor: molecular biomarker and player in cardioprotection and cardiovascular regeneration. Thromb. Haemost. 2012, 107:656-661.
18. Matsuda-Hashii Y., Takai K., Ohta H., Fujisaki H., Tokimasa S., Osugi Y., Ozono K., Matsumoto K., Nakamura T., Hara J. Hepatocyte growth factor plays roles in the induction and autocrine maintenance of bone marrow stromal cell IL-11, SDF-1 alpha, and stem cell factor. Exp. Hematol. 2004, 32:955-961.
19. McCully M.L., Ladell K., Hakobyan S., Mansel R.E., Price D.A., Moser B. Epidermis instructs skin homing receptor expression in human Tcells. Blood 2012, 120:4591-4598.
20. McLoughlin R.M., Jenkins B.J., Grail D., Williams A.S., Fielding C.A., Parker C.R., Ernst M., Topley N., Jones S.A. IL-6 trans-signaling via STAT3 directs Tcell infiltration in acute inflammation. Proc. Natl. Acad. Sci. USA 2005, 102:9589-9594.
21. Mora J.R., von Andrian U.H. T-cell homing specificity and plasticity: new concepts and future challenges. Trends Immunol. 2006, 27:235-243.
22. Okada Y., Morimoto I., Ura K., Nakano Y., Tanaka Y., Nishida S., Nakamura T., Eto S. Short-term treatment of recombinant murine interleukin-4 rapidly inhibits bone formation in normal and ovariectomized mice. Bone 1998, 22:361-365.
23. Ono K., Matsumori A., Shioi T., Furukawa Y., Sasayama S. Enhanced expression of hepatocyte growth factor/c-Met by myocardial ischemia and reperfusion in a rat model. Circulation 1997, 95:2552-2558.
24. Rodig S.J., Shapiro G.I. Crizotinib, a small-molecule dual inhibitor of the c-Met and ALK receptor tyrosine kinases. Curr. Opin. Investig. Drugs 2010, 11:1477-1490.
25. Santiago B., Izquierdo E., Rueda P., Del Rey M.J., Criado G., Usategui A., Arenzana-Seisdedos F., Pablos J.L. CXCL12γ isoform is expressed on endothelial and dendritic cells in rheumatoid arthritis synovium and regulates Tcell activation. Arthritis Rheum. 2012, 64:409-417.
26. Schnickel G.T., Bastani S., Hsieh G.R., Shefizadeh A., Bhatia R., Fishbein M.C., Belperio J., Ardehali A. Combined CXCR3/CCR5 blockade attenuates acute and chronic rejection. J.Immunol. 2008, 180:4714-4721.
27. Sebastiani S., Danelon G., Gerber B., Uguccioni M. CCL22-induced responses are powerfully enhanced by synergy inducing chemokines via CCR4: evidence for the involvement of first beta-strand of chemokine. Eur. J. Immunol. 2005, 35:746-756.
28. Shetty S., Weston C.J., Oo Y.H., Westerlund N., Stamataki Z., Youster J., Hubscher S.G., Salmi M., Jalkanen S., Lalor P.F., Adams D.H. Common lymphatic endothelial and vascular endothelial receptor-1 mediates the transmigration of regulatory Tcells across human hepatic sinusoidal endothelium. J.Immunol. 2011, 186:4147-4155.
29. Tanaka Y., Mine S., Hanagiri T., Hiraga T., Morimoto I., Figdor C.G., van Kooyk Y., Ozawa H., Nakamura T., Yasumoto K., Eto S. Constitutive up-regulation of integrin-mediated adhesion of tumor-infiltrating lymphocytes to osteoblasts and bone marrow-derived stromal cells. Cancer Res. 1998, 58:4138-4145.
30. Trusolino L., Bertotti A., Comoglio P.M. A signaling adapter function for alpha6beta4 integrin in the control of HGF-dependent invasive growth. Cell 2001, 107:643-654.
31. Tsang J.Y., Tanriver Y., Jiang S., Xue S.A., Ratnasothy K., Chen D., Stauss H.J., Bucy R.P., Lombardi G., Lechler R. Conferring indirect allospecificity on CD4+CD25+ Tregs by TCR gene transfer favors transplantation tolerance in mice. J.Clin. Invest. 2008, 118:3619-3628.
32. Tu H., Zhou Z., Liang Q., Li Z., Li D., Qing J., Wang H., Zhang L. CXCR4 and SDF-1 production are stimulated by hepatocyte growth factor and promote glioma cell invasion. Onkologie 2009, 32:331-336.
33. Vischer H.F., Watts A.O., Nijmeijer S., Leurs R. G protein-coupled receptors: walking hand-in-hand, talking hand-in-hand?. Br. J. Pharmacol. 2011, 163:246-260.
34. Zhang Y.W., Vande Woude G.F. HGF/SF-met signaling in the control of branching morphogenesis and invasion. J.Cell. Biochem. 2003, 88:408-417.