Matricellular signaling molecule CCN1 attenuates experimental autoimmune myocarditis by acting as a novel immune cell migration modulator

Circulation

Volumn 122, Issue 25, 2010, Pages 2688-2698

  Rother, Madlen ^a   Krohn, Stefanie ^a   Kania, Gabriela ^a   Vanhoutte, Davy ^d   Eisenreich, Andreas ^a   Wang, Xiaomin ^a   Westermann, Dirk ^a   Savvatis, Kostas ^a   Dannemann, Nadine ^c   Skurk, Carsten ^a   Hilfiker Kleiner, Denise ^b   Cathomen, Toni ^c   Fechner, Henry ^a   Rauch, Ursula ^a   Schultheiss, Heinz Peter ^a   Heymans, Stephane ^e   Eriksson, Urs ^a   Scheibenbogen, Carmen ^a   Poller, Wolfgang ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

cardiomyopathy; chemotaxis; immunomodulation; inflammation; migration

Indexed keywords

CHEMOKINE; CYSTEINE RICH PROTEIN 61; CYTOKINE; HEMAGGLUTININ; MACROPHAGE INFLAMMATORY PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 1; STROMAL CELL DERIVED FACTOR 1ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL MIGRATION; CONTROLLED STUDY; DRUG MECHANISM; EXPERIMENTAL AUTOIMMUNE MYOCARDITIS; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; MYOCARDITIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION;

ADULT; ANIMALS; AUTOIMMUNE DISEASES; BIOMIMETICS; CELL MOVEMENT; CELLS, CULTURED; CYSTEINE-RICH PROTEIN 61; DISEASE MODELS, ANIMAL; FEMALE; GENE TRANSFER TECHNIQUES; HUMANS; LEUKOCYTES, MONONUCLEAR; LIVER; MALE; MICE; MICE, INBRED BALB C; MIDDLE AGED; MONOCYTES; MYOCARDITIS; PEPTIDES, CYCLIC; RECOMBINANT PROTEINS; SPLEEN;

EID: 78650704018     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.110.945261     Document Type: Article

References (48)

1. Wittchen F, Suckau L, Witt H, Skurk C, Lassner D, Fechner H, Sipo I, Ungethum U, Ruiz P, Pauschinger M, Tschope C, Rauch U, Kuhl U, Schultheiss HP, Poller W. Genomic expression profiling of human inflammatory cardiomyopathy (DCMi) suggests novel therapeutic targets. J Mol Med. 2007;85:257-271.
2. Chaqour B, Goppelt-Struebe M. Mechanical regulation of the Cyr61/CCN1 and CTGF/CCN2 proteins. FEBS J. 2006;273:3639-3649.
3. Colston JT, de la Rosa SD, Koehler M, Gonzales K, Mestril R, Freeman GL, Bailey SR, Chandrasekar B. Wnt-induced secreted protein-1 is a prohypertrophic and profibrotic growth factor. Am J Physiol Heart Circ Physiol. 2007;293:H1839-H1846.
4. Frangogiannis NG, Ren G, Dewald O, Zymek P, Haudek S, Koerting A, Winkelmann K, Michael LH, Lawler J, Entman ML. Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts. Circulation. 2005;111:2935-2942.
5. 1 Integrins modulate /3-adrenergic receptor-stimulated cardiac myocyte apoptosis and myocardial remodeling. Hypertension. 2007;49:865-872.
6. 3, independent of its carboxyl-terminal domain. J Biol Chem. 2001;276:21943-21950
7. 2 binding site in CCN1 (CYR61), a matricellular protein expressed in healing wounds and atherosclerotic lesions. J Biol Chem. 2003;278:25808-25815.
8. 2 as an adhesion receptor on peripheral blood monocytes for Cyr61 (CCN1) and connective tissue growth factor (CCN2): immediate-early gene products expressed in atherosclerotic lesions. Blood. 2002;99:4457-4465.
9. 3 binding site in CCN1 (CYR61) critical for pro-angiogenic activities in vascular endothelial cells. J Biol Chem. 2004;279: 44166-44176.
10. 1 and cell surface heparan sulfate proteoglycans. Endocrinology. 2002;143:1441-1450.
11. Leu SJ, Chen N, Chen CC, Todorovic V, Bai T, Juric V, Liu Y, Yan G, Lam SC, Lau LF. Targeted mutagenesis of the angiogenic protein CCN1 (CYR61). Selective inactivation of integrin a-heparan sulfate proteoglycan coreceptor-mediated cellular functions. J Biol Chem. 2004;279: 44177-44187.
12. Xie D, Yin D, Tong X, O'Kelly J, Mori A, Miller C, Black K, Gui D, Said JW, Koeffler HP. Cyr61 is overexpressed in gliomas and involved in integrin-linked kinase-mediated Akt and /3-catenin-TCF/Lef signaling pathways. Cancer Res. 2004;64:1987-1996.
13. Si W, Kang Q, Luu HH, Park JK, Luo Q, Song WX, Jiang W, Luo X, Li X, Yin H, Montag AG, Haydon RC, He TC. CCN1/Cyr61 is regulated by the canonical Wnt signal and plays an important role in Wnt3A-induced osteoblast differentiation of mesenchymal stem cells. Mol Cell Biol. 2006;26:2955-2964.
14. Hilfiker-Kleiner D, Kaminski K, Kaminska A, Fuchs M, Klein G, Podewski E, Grote K, Kiian I, Wollert KC, Hilfiker A, Drexler H. Regulation of proangiogenic factor CCN1 in cardiac muscle: impact of ischemia, pressure overload, and neurohumoral activation. Circulation. 2004;109:2227-2233.
15. Chen CC, Mo FE, Lau LF. The angiogenic factor Cyr61 activates a genetic program for wound healing in human skin fibroblasts. J Biol Chem. 2001;276:47329-47337.
16. + monocytes abrogate Th17 CD4+ T cell-mediated experimental autoimmune myocarditis. J Immunol. 2008;180:2686-2695.
17. + bone marrow-derived heart-resident cells suppress experimental autoimmune myocarditis. Cardiovasc Res. 2008;80:236-245.
18. Marty RR, Dirnhofer S, Mauermann N, Schweikert S, Akira S, Hunziker L, Penninger JM, Eriksson U. MyD88 signaling controls autoimmune myocarditis induction. Circulation. 2006;113:258-265.
19. Rangachari M, Mauermann N, Marty RR, Dirnhofer S, Kurrer MO, Komnenovic V, Penninger JM, Eriksson U. T-bet negatively regulates autoimmune myocarditis by suppressing local production of interleukin 17. J Exp Med. 2006;203:2009-2019.
20. Eriksson U, Ricci R, Hunziker L, Kurrer MO, Oudit GY, Watts TH, Sonderegger I, Bachmaier K, Kopf M, Penninger JM. Dendritic cell-induced autoimmune heart failure requires cooperation between adaptive and innate immunity. Nat Med. 2003;9:1484-1490.
21. Goser S, Ottl R, Brodner A, Dengler TJ, Torzewski J, Egashira K, Rose NR, Katus HA, Kaya Z. Critical role for monocyte chemoattractant protein-1 and macrophage inflammatory protein-1alpha in induction of experimental autoimmune myocarditis and effective anti-monocyte chemoattractant protein-1 gene therapy. Circulation. 2005;112:3400-3407.
22. Suckau L, Fechner H, Chemaly E, Krohn S, Hadri L, Kockskamper J, Westermann D, Bisping E, Ly H, Wang X, Kawase Y, Chen J, Liang L, Sipo I, Vetter R, Weger S, Kurreck J, Erdmann V, Tschope C, Pieske B, Lebeche D, Schultheiss H, Hajjar R, Poller W. Chronic cardiac-targeted RNA interference for the treatment of heart failure restores cardiac function and reduces pathological hypertrophy. Circulation. 2009;119: 1241-1252.
23. Fechner H, Noutsias M, Tschoepe C, Hinze K, Wang X, Escher F, Pauschinger M, Dekkers D, Vetter R, Paul M, Lamers J, Schultheiss HP, Poller W. Induction of coxsackievirus-adenovirus-receptor expression during myocardial tissue formation and remodeling: identification of a cell-to-cell contact-dependent regulatory mechanism. Circulation. 2003; 107:876-882.
24. Colantonio DA, Dunkinson C, Bovenkamp DE, Van Eyk JE. Effective removal of albumin from serum. Proteomics. 2005;5:3831-3835.
25. Schellings MW, Vanhoutte D, Swinnen M, Cleutjens JP, Debets J, Van Leeuwen RE, d'Hooge J, Van de Werf F, Carmeliet P, Pinto YM, Sage EH, Heymans S. Absence of SPARC results in increased cardiac rupture and dysfunction after acute myocardial infarction. J Exp Med. 2009;206: 113-123.
26. Kireeva ML, Latinkic BV, Kolesnikova TV, Chen CC, Yang GP, Abler AS, Lau LF. Cyr61 and Fisp12 are both ECM-associated signaling molecules: activities, metabolism, and localization during development. Exp Cell Res. 1997;233:63-77.
27. + progenitor cells: potential role in angiogenesis and endothelial regeneration. Blood. 2007;110:877-885.
28. Pendurthi UR, Tran TT, Post M, Rao LV. Proteolysis of CCN1 by plasmin: functional implications. Cancer Res. 2005;65:9705-9711.
29. Hehlgans S, Haase M, Cordes N. Signalling via integrins: implications for cell survival and anticancer strategies. Biochim Biophys Acta. 2007;1775: 163-180.
30. Camps M, Ruckle T, Ji H, Ardissone V, Rintelen F, Shaw J, Ferrandi C, Chabert C, Gillieron C, Francon B, Martin T, Gretener D, Perrin D, Leroy D, Vitte PA, Hirsch E, Wymann MP, Cirillo R, Schwarz MK, Rommel C. Blockade of PI3K-y suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat Med. 2005;11:936-943.
31. Arefieva TI, Kukhtina NB, Antonova OA, Krasnikova TL. MCP-1-stimulated chemotaxis of monocytic and endothelial cells is dependent on activation of different signaling cascades. Cytokine. 2005;31:439-446.
32. Dieterle A, Orth R, Daubrawa M, Grotemeier A, Alers S, Ullrich S, Lammers R, Wesselborg S, Stork B. The Akt inhibitor triciribine sensitizes prostate carcinoma cells to TRAIL-induced apoptosis. Int J Cancer. 2009;125:932-941.
33. Menschikowski M, Hagelgans A, Heyne B, Hempel U, Neumeister V, Goez P, Jaross W, Siegert G. Statins potentiate the IFN-y-induced upregulation of group IIA phospholipase A2 in human aortic smooth muscle cells and HepG2 hepatoma cells. Biochim Biophys Acta. 2005; 1733:157-171.
34. Holbourn KP, Acharya KR, Perbal B. The CCN family of proteins: structure-function relationships. Trends Biochem Sci. 2008;33:461-473.
35. Desnoyers L. Structural basis and therapeutic implication of the interaction of CCN proteins with glycoconjugates. Curr Pharm Des. 2004; 10:3913-3928.
36. Reynolds AR, Hart IR, Watson AR, Welti JC, Silva RG, Robinson SD, Da Violante G, Gourlaouen M, Salih M, Jones MC, Jones DT, Saunders G, Kostourou V, Perron-Sierra F, Norman JC, Tucker GC, Hodivala-Dilke KM. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat Med. 2009; 15:392-400.
37. Mo FE, Muntean AG, Chen CC, Stolz DB, Watkins SC, Lau LF. CYR61 (CCN1) is essential for placental development and vascular integrity. Mol Cell Biol. 2002;22:8709-8720.
38. Lake AC, Bialik A, Walsh K, Castellot JJ Jr. CCN5 is a growth arrest-specific gene that regulates smooth muscle cell proliferation and motility. Am J Pathol. 2003;162:219-231.
39. Friedl P, Weigelin B. Interstitial leukocyte migration and immune function. Nat Immunol. 2008;9:960-969.
40. Wong CH, Heit B, Kubes P. Molecular regulators of leucocyte che-motaxis during inflammation. Cardiovasc Res. 2010;86:183-191.
41. Bishop JR, Schuksz M, Esko JD. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature. 2007;446:1030-1037.
42. Horuk R. Chemokine receptor antagonists: overcoming developmental hurdles. Nat Rev Drug Discov. 2009;8:23-33.
43. Mackay CR. Moving targets: cell migration inhibitors as new anti-inflammatory therapies. Nat Immunol. 2008;9:988-998.
44. Morimoto H, Takahashi M, Izawa A, Ise H, Hongo M, Kolattukudy PE, Ikeda U. Cardiac overexpression of monocyte chemoattractant protein-1 in transgenic mice prevents cardiac dysfunction and remodeling after myocardial infarction. Circ Res. 2006;99:891-899.
45. Dewald O, Zymek P, Winkelmann K, Koerting A, Ren G, Abou-Khamis T, Michael LH, Rollins BJ, Entman ML, Frangogiannis NG. CCL2/monocyte chemoattractant protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res. 2005;96: 881-889
46. Frangogiannis NG, Dewald O, Xia Y, Ren G, Haudek S, Leucker T, Kraemer D, Taffet G, Rollins BJ, Entman ML. Critical role of monocyte chemoattractant protein-1/CC chemokine ligand 2 in the pathogenesis of ischemic cardiomyopathy. Circulation. 2007;115:584-592.
47. Barber DF, Bartolome A, Hernandez C, Flores JM, Redondo C, Fernandez-Arias C, Camps M, Ruckle T, Schwarz MK, Rodriguez S, Martinez AC, Balomenos D, Rommel C, Carrera AC. PI3K-y inhibition blocks glomerulonephritis and extends lifespan in a mouse model of systemic lupus. Nat Med. 2005;11:933-935.
48. Plump AS, Lum PY. Genomics and cardiovascular drug development. J Am Coll Cardiol. 2009;53:1089-1100.