Innate immune signaling induces expression and shedding of the heparan sulfate proteoglycan syndecan-4 in cardiac fibroblasts and myocytes, affecting inflammation in the pressure-overloaded heart

FEBS Journal

Volumn 280, Issue 10, 2013, Pages 2228-2247

  Strand, Mari E ^a,b   Herum, Kate M ^a,b   Rana, Zaheer A ^a,b   Skrbic, Biljana ^a,b   Askevold, Erik T ^b,c   Dahl, Christen P ^b,c   Vistnes, Maria ^a,b   Hasic, Almira ^a,b   Kvaløy, Heidi ^a,b   Sjaastad, Ivar ^a,b   Carlson, Cathrine R ^a,b   Tønnessen, Theis ^a,b   Gullestad, Lars ^b,c   Christensen, Geir ^a,b   Lunde, Ida G ^a,b  

^a ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

heart failure; heparan sulfate; inflammation; proteoglycan; shedding

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MESSENGER RNA; PROTEOHEPARAN SULFATE; SYNDECAN 4; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FIBROBLAST; FOCAL ADHESION; GENETIC TRANSFECTION; HEART MUSCLE; HEART MUSCLE CELL; HEART VENTRICLE OVERLOAD; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INNATE IMMUNITY; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ADULT; ANIMALS; ANIMALS, NEWBORN; BENZAMIDES; CELL ADHESION; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; FOCAL ADHESIONS; HEART FAILURE; HEK293 CELLS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MYOCARDIUM; MYOCYTES, CARDIAC; NF-KAPPA B; PRIMARY CELL CULTURE; RATS; RATS, WISTAR; RNA, MESSENGER; SYNDECAN-4; T-LYMPHOCYTES; THIAZOLES; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; VENTRICULAR REMODELING;

EID: 84877711612     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12161     Document Type: Article

References (53)

1. Cohn JN, Ferrari R, &, Sharpe N, (2000) Cardiac remodeling-concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. J Am Coll Cardiol 35, 569-582. (Pubitemid 30167013)
2. Bui AL, Horwich TB, &, Fonarow GC, (2011) Epidemiology and risk profile of heart failure. Nat Rev Cardiol 8, 30-41.
3. McMurray JJ, Petrie MC, Murdoch DR, &, Davie AP, (1998) Clinical epidemiology of heart failure: public and private health burden. Eur Heart J 19 (Suppl P), P9-P16. (Pubitemid 28556634)
4. Finsen AV, Woldbaek PR, Li J, Wu J, Lyberg T, Tonnessen T, &, Christensen G, (2004) Increased syndecan expression following myocardial infarction indicates a role in cardiac remodeling. Physiol Genom 16, 301-308. (Pubitemid 38420048)
5. Alexopoulou AN, Multhaupt HAB, &, Couchman JR, (2007) Syndecans in wound healing, inflammation and vascular biology. Int J Biochem Cell Biol 39, 505-528. (Pubitemid 46099032)
6. VanWinkle WB, Snuggs MB, De Hostos EL, Buja LM, Woods A, &, Couchman JR, (2002) Localization of the transmembrane proteoglycan syndecan-4 and its regulatory kinases in costameres of rat cardiomyocytes: a deconvolution microscopic study. Anat Rec 268, 38-46. (Pubitemid 34983296)
7. Finsen AV, Lunde IG, Sjaastad I, Østli EK, Lyngra M, Jarstadmarken HO, Hasic A, Nygård S, Wilcox-Adelman SA, Goetinck PF, et al,. (2011) Syndecan-4 is essential for development of concentric myocardial hypertrophy via stretch-induced activation of the calcineurin-NFAT pathway. PLoS One 6, e28302.
8. Herum KM, Lunde IG, Skrbic B, Florholmen G, Behmen D, Sjaastad I, Carlson CR, Gomez MF, &, Christensen G, (2013) Syndecan-4 signaling via NFAT regulates extracellular matrix production and cardiac myofibroblast differentiation in response to mechanical stress. J Mol Cell Cardiol 54, 73-81.
9. Matsui Y, Ikesue M, Danzaki K, Morimoto J, Sato M, Tanaka S, Kojima T, Tsutsui H, &, Uede T, (2011) Syndecan-4 prevents cardiac rupture and dysfunction after myocardial infarction. Circ Res 108, 1328-1339.
10. Echtermeyer F, Harendza T, Hubrich S, Lorenz A, Herzog C, Mueller M, Schmitz M, Grund A, Larmann J, Stypmann J, et al,. (2011) Syndecan-4 signalling inhibits apoptosis and controls NFAT activity during myocardial damage and remodelling. Cardiovasc Res 92, 123-131.
11. Götte M, (2003) Syndecans in inflammation. FASEB J 17, 575-591. (Pubitemid 37221142)
12. Parish CR, (2006) The role of heparan sulphate in inflammation. Nat Rev Immunol 6, 633-643. (Pubitemid 44298213)
13. Yu Q, Vazquez R, Zabadi S, Watson RR, &, Larson DF, (2010) T-lymphocytes mediate left ventricular fibrillar collagen cross-linking and diastolic dysfunction in mice. Matrix Biol 29, 511-518.
14. Hofmann U, Beyersdorf N, Weirather J, Podolskaya A, Bauersachs J, Ertl G, Kerkau T, &, Frantz S, (2012) Activation of CD4+ T lymphocytes improves wound healing and survival after experimental myocardial infarction in mice. Circulation 125, 1652-1663.
15. Yu Q, Horak K, &, Larson DF, (2006) Role of T lymphocytes in hypertension-induced cardiac extracellular matrix remodeling. Hypertension 48, 98-104. (Pubitemid 44297530)
16. Poltorak A, He X, Smirnova I, Liu M-Y, Huffel CV, Du X, Birdwell D, Alejos E, Silva M, Galanos C, et al,. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in tlr4 gene. Science 282, 2085-2088. (Pubitemid 29001265)
17. Kawai T, &, Akira S, (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11, 373-384.
18. Louch WE, Sheehan KA, &, Wolska BM, (2011) Methods in cardiomyocyte isolation, culture, and gene transfer. J Mol Cell Cardiol 51, 288-298.
19. Wilkins BJ, &, Molkentin JD, (2004) Calcium-calcineurin signaling in the regulation of cardiac hypertrophy. Biochem Biophys Res Commun 322, 1178-1191. (Pubitemid 39164648)
20. Molkentin JD, Lu J-R, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, &, Olson EN, (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228. (Pubitemid 28180855)
21. Wilkins BJ, Dai Y-S, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, &, Molkentin JD, (2004) Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 94, 110-118. (Pubitemid 38064105)
22. Manon-Jensen T, Itoh Y, &, Couchman JR, (2010) Proteoglycans in health and disease: the multiple roles of syndecan shedding. FEBS J 277, 3876-3889.
23. Ramani VC, Pruett PS, Thompson CA, DeLucas LD, &, Sanderson RD, (2012) Heparan sulfate chains of syndecan-1 regulate ectodomain shedding. J Biol Chem 287, 9952-9961.
24. Woods A, &, Couchman JR, (1994) Syndecan-4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol Biol Cell 5, 183-192. (Pubitemid 24108464)
25. Saoncella S, Echtermeyer F, Denhez F, Nowlen JK, Mosher DF, Robinson SD, Hynes RO, &, Goetinck PF, (1999) Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc Natl Acad Sci 96, 2805-2810. (Pubitemid 29148799)
26. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Tsuzuki S, Nakamura E, Kusugami K, Saito H, &, Muramatsu T, (2000) Syndecan-4 deficiency impairs focal adhesion formation only under restricted conditions. J Biol Chem 275, 5249-5252. (Pubitemid 30115150)
27. Couchman JR, (2010) Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol 26, 89-114. doi: 10.1146/annurev-cellbio-100109-104126.
28. Yndestad A, Damås J, Øie E, Ueland T, Gullestad L, &, Aukrust P, (2007) Role of inflammation in the progression of heart failure. Curr Cardiol Rep 9, 236-241. (Pubitemid 46784419)
29. Mann DL, (2003) Stress-activated cytokines and the heart: from adaptation to maladaptation. Ann Rev Physiol 65, 81-101. (Pubitemid 38249148)
30. Frantz S, Ertl G, &, Bauersachs J, (2007) Mechanisms of disease: toll-like receptors in cardiovascular disease. Nat Clin Pract Cardiovasc Med 4, 444-454. (Pubitemid 47180328)
31. Ha T, Li Y, Hua F, Ma J, Gao X, Kelley J, Zhao A, Haddad G, Williams D, Browder I, et al,. (2005) Reduced cardiac hypertrophy in toll-like receptor 4-deficient mice following pressure overload. Cardiovasc Res 68, 224-234. (Pubitemid 41428419)
32. Frantz S, Kobzik L, Kim Y-D, Fukazawa R, Medzhitov R, Lee RT, &, Kelly RA, (1999) Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J Clin Invest 104, 271-280.
33. Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, &, Zako M, (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68, 729-777. (Pubitemid 29449208)
34. Echtermeyer F, Streit M, Wilcox-Adelman S, Saoncella S, Denhez F, Detmar M, &, Goetinck PF, (2001) Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J Clin Invest 107, R9-R14. (Pubitemid 32096841)
35. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Iwase M, Yoshikai Y, Yanada M, Yamamoto K, Matsushita T, Nishimura M, et al,. (2001) Syndecan-4 deficiency leads to high mortality of lipopolysaccharide-injected mice. J Biol Chem 276, 47483-47488.
36. Ishiguro K, Kojima T, &, Muramatsu T, (2002) Syndecan-4 as a molecule involved in defense mechanisms: special issue on proteoglycans: genetic manipulation in intact organisms-on the road to function. Glycoconjugate J 19, 315-318.
37. Xie J, Wang J, Li R, Dai Q, Yong Y, Zong B, Xu Y, Li E, Ferro A, &, Xu B, (2012) Syndecan-4 over-expression preserves cardiac function in a rat model of myocardial infarction. J Mol Cell Cardiol 53, 250-258.
38. Rodríguez-Manzaneque JC, Carpizo D, Plaza-Calonge MdC, Torres-Collado AX, Thai SNM, Simons M, Horowitz A, &, Iruela-Arispe ML, (2009) Cleavage of syndecan-4 by ADAMTS1 provokes defects in adhesion. Int J Biochem Cell Biol 41, 800-810.
39. Choi S, Lee H, Choi JR, &, Oh ES, (2010) Shedding; towards a new paradigm of syndecan function in cancer. BMB Rep 43, 305-310.
40. Theocharis AD, Skandalis SS, Tzanakakis GN, &, Karamanos NK, (2010) Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS J 277, 3904-3923.
41. Kojima T, Takagi A, Maeda M, Segawa T, Shimizu A, Yamamoto K, Matsushita T, &, Saito H, (2001) Plasma levels of syndecan-4 (ryudocan) are elevated in patients with acute myocardial infarction. Thromb Haemost 85, 793-799. (Pubitemid 32421810)
42. Takahashi R, Negishi K, Watanabe A, Arai M, Naganuma F, Ohyama Y, &, Kurabayashi M, (2011) Serum syndecan-4 is a novel biomarker for patients with chronic heart failure. J Cardiol 57, 325-332.
43. Wang J, Markova D, Anderson DG, Zheng Z, Shapiro IM, &, Risbud MV, (2011) TNF-α and IL-1β promote a disintegrin-like and metalloprotease with thrombospondin type I motifs(ADAMTS) -5 mediated aggrecan degradation through syndecan-4 in intervertebral disc. J Biol Chem 286, 39738-39749.
44. Smith MF, Novotny J, Carl VS, &, Comeau LD, (2006) Helicobacter pylori and toll-like receptor agonists induce syndecan-4 expression in an NF-κB-dependent manner. Glycobiology 16, 221-229. (Pubitemid 43264688)
45. Tan X, Khalil N, Tesarik C, Vanapalli K, Yaputra V, Alkhouri H, Oliver BGG, Armour CL, &, Hughes JM, (2012) Th1 cytokine-induced syndecan-4 shedding by airway smooth muscle cells is dependent on mitogen-activated protein kinases. Am J Physiol-Lung C 302, L700-L710.
46. Li Y, Ha T, Gao X, Kelley J, Williams DL, Browder IW, Kao RL, &, Li C, (2004) NF-κB activation is required for the development of cardiac hypertrophy in vivo. Am J Physiol-Heart C 287, H1712-H1720. (Pubitemid 39313278)
47. Heymans S, Hirsch E, Anker SD, Aukrust P, Balligand J-L, Cohen-Tervaert JW, Drexler H, Filippatos G, Felix SB, Gullestad L, et al,. (2009) Inflammation as a therapeutic target in heart failure? A scientific statement from the Translational Research Committee of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Failure 11, 119-129.
48. Lunde IG, Kvaløy H, Austbo B, Christensen G, &, Carlson CR, (2011) Angiotensin II and norepinephrine activate specific calcineurin-dependent NFAT transcription factor isoforms in cardiomyocytes. J Appl Physiol 111, 1278-1289.
49. Rasheed S, Nelson-Rees WA, Toth EM, Arnstein P, &, Gardner MB, (1974) Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 33, 1027-1033.
50. Claycomb WC, Lanson NA, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, &, Izzo NJ, (1998) HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 95, 2979-2984. (Pubitemid 28135840)
51. Brattelid T, Winer LH, Levy FO, Liestør K, Sejersted OM, &, Andersson KB, (2010) Reference gene alternatives to Gapdh in rodent and human heart failure gene expression studies. BMC Mol Biol 11, 22.
52. Burbach BJ, Friedl A, Mundhenke C, &, Rapraeger AC, (2003) Syndecan-1 accumulates in lysosomes of poorly differentiated breast carcinoma cells. Matrix Biol 22, 163-177. (Pubitemid 36627474)
53. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, et al,. (2005) Recommendations for chamber quantification: a report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18, 1440-1463. (Pubitemid 41821197)