Changes in cardiac heparan sulfate proteoglycan expression and streptozotocin-induced diastolic dysfunction in rats

Cardiovascular Diabetology

Volumn 10, Issue , 2011, Pages

  Strunz, Célia M C ^a   Matsuda, Monique ^a   Salemi, Vera M C ^a   Nogueira, Adriana ^a   Mansur, Antonio P ^a   Cestari, Ismar N ^a   Marquezini, Monica V ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Cardiac Muscle; Diabetes; GlypicanSyndecan 4

Indexed keywords

GLYPICAN 1; PROTEOHEPARAN SULFATE; SYNDECAN 4; GLYPICAN; MESSENGER RNA; SDC4 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DISEASE COURSE; ECHOCARDIOGRAPHY; HEART FUNCTION; HEART MUSCLE; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; STREPTOZOCIN DIABETES; WESTERN BLOTTING; ANIMAL; DIASTOLE; ECHOGRAPHY; EXPERIMENTAL DIABETES MELLITUS; GENETICS; HEART LEFT VENTRICLE FUNCTION; HEART VENTRICLE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; TIME; WISTAR RAT;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; DIASTOLE; GLYPICANS; HEART VENTRICLES; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE, SKELETAL; MYOCARDIUM; RATS; RATS, WISTAR; RNA, MESSENGER; SYNDECAN-4; TIME FACTORS; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT;

EID: 79955036703     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-10-35     Document Type: Article

References (60)

1. Donnelly R, Emslie-Smith AM, Gardner ID, Morris AD. ABC of arterial and venous disease: vascular complications of diabetes. BMJ 2000, 320:1052-1066.
2. Scognamiglio R, Avogaro A, Casara D, Crepaldi C, Marin M, Palisi M, Mingardi R, Erle G, Fasoli G, Dalla Volta S. Myocardial dysfunction and adrenergic cardiac innervation in patients with insulin-dependent diabetes mellitus. J Am Coll Cardiol 1998, 3:404-412.
3. Freire CM, Moura AL, Barbosa M de M, Machado LJ, Nogueira AI, Ribeiro-Oliveira A. Left ventricular diastolic dysfunction in diabetes: an update. Arq Bras Endocrinol. Metabol 2007, 51:168-175.
4. Diamant M, Lamb HJ, Groeneveld Y, Endert EL, Smit JW, Bax JJ, Romijn JA, de Roos A, Radder JK. Diastolic dysfunction is associated with altered myocardial metabolism in asymptomatic normotensive patients with well-controlled type 2 diabetes mellitus. J Am Coll Cardiol 2003, 42:328-335. 10.1016/S0735-1097(03)00625-9, 12875772.
5. Aneja A, Tang WHW, Bansilal S, Garcia MJ, Farkouh ME. Diabetic Cardiomyopathy: insights into pathogenesis, diagnostic challenges, and therapeutic options. Am J Med 2008, 121:748-757. 10.1016/j.amjmed.2008.03.046, 18724960.
6. Rossen JD. Abnormal microvascular function in diabetes: relationship to diabetic cardiomyopathy. Coron Artery Dis 1996, 7:133-138. 10.1097/00019501-199602000-00006, 8813444.
7. An D, Rodrigues B. Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 2006, 291:H1489-H1506. 10.1152/ajpheart.00278.2006, 16751293.
8. Tumova S, Woods A, Couchman JR. Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions. Int J Biochem Cell Biol 2000, 32:269-288. 10.1016/S1357-2725(99)00116-8, 10716625.
9. Shriver Z, Liu D, Sasisekharan R. Emerging views of heparan sulfate glycosaminoglycan structure/activity relationships modulating dynamic biological functions. Trends Cardiovasc Med 2002, 12:71-77. 10.1016/S1050-1738(01)00150-5, 11852254.
10. Obunike JC, Pillarisetti S, Paka L, Kako Y, Butteri MJ, Ho YY, Wagner WD, Yamada N, Mazzone T, Deckelbaum RJ, Goldberg IJ. The heparin-binding proteins apolipoprotein E and lipoprotein lipase enhance cellular proteoglycan production. Arterioscler Thromb Vasc Biol 2000, 20:111-118.
11. van den Born J, van Kraats AA, Bakker MA, Assmann KJ, Dijkman HB, van der Laak JA, Berden JH. Reduction of heparan sulphate-associated anionic sites in the glomerular basement membrane of rats with streptozotocin-induced diabetic nephropathy. Diabetologia 1995, 38:1169-1175. 10.1007/BF00422365, 8690168.
12. Redd AS. Prevention of albuminuria by captopril in diabetic rats. Gen Pharmacol 1991, 22:323-328.
13. Jensen T. Pathogenesis of diabetic vascular disease: evidence for the role of reduced heparan sulfate proteoglycan. Diabetes 1997, 46:S98-100.
14. Bollineni JS, Alluru I, Reddi AS. Heparan sulfate proteoglycan synthesis and its expression are decreased in the retina of diabetic rats. Curr Eye Res 1997, 16:127-130. 10.1076/ceyr.16.2.127.5089, 9068943.
15. Morano S, Guidobaldi L, Cipriani R, Gabriele A, Pantellini F, Medici F, D'Erme M, Di Nissen NN, Shankar R, Gamelli RL, Singh A, DiPietro LA. Heparin and heparan sulphate protect basic fibroblast growth factor from non-enzymic glycosylation. Biochem J 1999, 15:637-642.
16. Medina-Sanchez M, Rodriguez-Sanchez C, Vega-Alvarez J, Menedez-Pelaez A, Perez-Casas A. Proximal skeletal muscle alterations in streptozotocin-diabetic rats: a histochemical and morphometric analysis. Am J Anat 1991, 191:48-56. 10.1002/aja.1001910105, 1829578.
17. Klueber KM, Feczko JD. Ultrastructural, histochemical, and morphometric analysis of skeletal muscle in a murine model of type I diabetes. Anat Rec 1994, 239:18-34. 10.1002/ar.1092390104, 8037375.
18. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving Bioscience Research Reporting: The ARRIVE Guidelines for Reporting Animal Research. PLoS Biol 2010, 8(6):e1000412. 10.1371/journal.pbio.1000412, 2893951, 20613859.
19. Schnedl WJ, Ferber S, Johnson JH, Newgard CB. STZ transport and cytotoxicity. Specific enhancement in GLUT2-expressing cells. Diabetes 1994, 43(11):1326-33. 10.2337/diabetes.43.11.1326, 7926307.
20. Salemi VM, Bilate AM, Ramires FJ, Picard MH, Gregio DM, Kalil J, Neto EC, Mady C. Reference values from M-mode and Doppler echocardiography for normal Syrian hamsters. Eur J Echocardiogr 2005, 6:41-46. 10.1016/j.euje.2004.06.001, 15664552.
21. Pires MD, Salemi VM, Cestari IA, Picard MH, Leirner AA, Mady C, Cestari IN. Noninvasive assessment of hemodynamic parameters in experimental stenosis of the ascending aorta. Artif Organs 2003, 27:695-700. 10.1046/j.1525-1594.2003.07276.x, 12911343.
22. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ. 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 2005, 18:1440-1463. 10.1016/j.echo.2005.10.005, 16376782.
23. Bilate AM, Salemi VM, Ramires FJ, de Brito T, Silva AM, Umezawa ES, Mady C, Kalil J, Cunha-Neto E. The Syrian hamster as a model for the dilated cardiomyopathy of Chagas' disease: a quantitative echocardiographical and histopathological analysis. Microbes Infect 2003, 5:1116-1124. 10.1016/j.micinf.2003.07.001, 14554253.
24. Hascall VC, Calabro A, Midura RJ, Yanagishita M. Isolation and characterization of proteoglycans. Methods Enzymol 1994, 230:390-417.
25. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
26. Horowitz A, Simons M. Regulation of syndecan-4 phosphorylation in vivo. J Biol Chem 1998, 273(18):10914-10918. 10.1074/jbc.273.18.10914, 9556568.
27. Chomczynski P. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 1993, 162:156-160.
28. Veugelers M, De Cat B, Ceulemans H, Bruystens AM, Coomans C, Durr J, Vermeesch J, Marynen P, David G. Glypican-6, a new member of the glypican family of cell surface heparan sulfate proteoglycans. J Biol Chem 1999, 274:26968-26977. 10.1074/jbc.274.38.26968, 10480909.
29. Kojima T, Shworak NW, Rosenberg RD. Molecular cloning and expression of two distinct cDNA-encoding heparan sulfate proteoglycan core proteins from a rat endothelial cell line. J Biol Chem 1992, 267:4870-4877.
30. Tokunaga K, Taniguchi H, Yoda K, Shimizu M, Sakiyama S. Nucleotide sequence of a full-length cDNA for mouse cytoskeletal beta-actin mRNA. Nucleic Acids Res 1986, 14:2829. 10.1093/nar/14.6.2829, 339701, 3754329.
31. Sägerstrom CG, Sive HL. RNA blot analysis. In: A Laboratory Guide to RNA: Isolation, Analysis, and Synthesis. 1996, 83-103. Wiley-Liss Inc., New York, NY, P.A. Krieg.
32. Kleeff J, Ishiwata T, Kumbasar A, Friess H, Büchler MW, Lander AD, Korc M. The Cell-surface heparan sulfate proteoglycan glypican-1 regulates growth factor action in pancreatic carcinoma cells and is overexpressed in human pancreatic cancer. J Clin Invest 1998, 102(9):1662-1673. 10.1172/JCI4105, 509114, 9802880.
33. Matsuda K, Maruyama H, Guo F, Kleeff J, Itakura J, Matsumoto Y, Lander AD, Murray K. Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Research 2001, 61:5562-5569.
34. Hamon M, Mbemba E, Charnaux N, Slimani H, Brule S, Saffar L, Vassy R, Prost C, Lievre N, Starzec A, Gattegno L. A syndecan-4/CXCR4 complex expressed on human primary lymphocytes and macrophages and HeLa cell line binds the CXC chemokine stromal cell-derived factor-1 (SDF-1). Glycobiology 2004, 14(4):311-323. 10.1093/glycob/cwh038, 15033938.
35. Braga JCF, Guimarães Filho FV, Padovani CR, Matsubara BB. Disfunção diastólica em pacientes diabéticos normotensos, independente da presença de microangiopatia. Arq Bras Cardiol 2005, 84:461-466. 10.1590/S0066-782X2005000600006, 16007311.
36. van den Brom CE, Huisman MC, Vlasblom R, Boontje NM, Duijst S, Lubberink M, Molthoff CF, Lammertsma AA, van der Velden J, Boer C, Ouwens DM, Diamant M. Altered myocardial substrate metabolism is associated with myocardial dysfunction in early diabetic cardiomyopathy in rats: studies using positron emission tomography. Cardiovasc Diabetol 2009, 8:39. 10.1186/1475-2840-8-39, 2722582, 19624828.
37. van den Brom CE, Bosmans JW, Vlasblom R, Handoko LM, Huisman MC, Lubberink M, Molthoff CF, Lammertsma AA, Ouwens MD, Diamant M, Boer C. Diabetic cardiomyopathy in Zucker diabetic fatty rats: the forgotten right ventricle. Cardiovasc Diabetol 2010, 9:25. 10.1186/1475-2840-9-25, 2898761, 20550678.
38. Pulinilkunnil T, Rodrigues B. Cardiac lipoprotein lipase: metabolic basis for diabetic heart disease. Cardiovasc Res 2006, 69:329-340. 10.1016/j.cardiores.2005.09.017, 16307734.
39. Zhong Y, Ahmed S, Grupp IL, Matlib MA. Altered SR protein expression associated with contractile dysfunction in diabetic rat hearts. Am J Physiol Heart Circ Physiol 2001, 281:H1137-H1147.
40. Wold LE, Ren J. Streptozotocin directly impairs cardiac contractile function in isolated ventricular myocytes via a p38 map kinase-dependent oxidative stress mechanism. Biochem Biophys Res Commun 2004, 318:1066-1071. 10.1016/j.bbrc.2004.04.138, 15147982.
41. Brandan E, Carey DJ, Larrain J, Melo F, Campos A. Synthesis and processing of glypican during differentiation of skeletal muscle cells. Eur J Cell Biol 1996, 71:170-176.
42. Li J, Brown LF, Laham RJ, Volk R, Simons M. Macrophage-dependent regulation of syndecan gene expression. Circ Res 1997, 81:785-796.
43. Asundi VK, Keister BF, Stahl RC, Carey DJ. Developmental and cell-type-specific expression of cell surface heparan sulfate proteoglycans in the rat heart. Exp Cell Res 1997, 230:145-153. 10.1006/excr.1996.3400, 9013716.
44. Cornelison DD, Filla MS, Stanley HM, Rapraeger AC, Olwin BB. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 2001, 239:79-94. 10.1006/dbio.2001.0416, 11784020.
45. vanWinkle WB, Snuggs MB, De Hostos EL, Buja LM, Woods A, Couchman JR. Localization of the transmembrane proteoglycan syndecan-4 and its regulatory kinases in costameres of rat cardiomyocytes: a deconvolution microscopic study. Anat Rec 2002, 268(1):38-46. 10.1002/ar.10130, 12209563.
46. Elenius K, Vainio S, Laato M, Salmivirta M, Thesleff I, Jalkanen M. Induced expression of syndecan in healing wounds. J Cell Biol 1991, 114:585-595. 10.1083/jcb.114.3.585, 2289093, 1860887.
47. Duraisamy Y, Slevin M, Smith N, Bailey J, Zweit J, Smith C, Ahmed N, Gaffney J. Effect of glycation on basic fibroblast growth factor induced angiogenesis and activation of associated signal transduction pathways in vascular endothelial cells: possible relevance to wound healing in diabetes. Angiogenesis 2001, 4:277-288. 10.1023/A:1016068917266, 12197473.
48. Facchiano F, Lentini A, Fogliano V, Mancarella S, Rossi C, Facchiano A, Capogrossil MC. Sugar-induced modification of fibroblast growth factor 2 reduces its angiogenic activity in vivo. Am J Pathol 2002, 161:531-541. 10.1016/S0002-9440(10)64209-5, 1850725, 12163378.
49. Nugent MA, Iozzo RV. Fibroblast growth factor-2. Int J Biochem Cell Biol 2000, 32:115-120. 10.1016/S1357-2725(99)00123-5, 10687947.
50. Clarke MS, Khakee R, McNeil PL. Loss of cytoplasmic basic fibroblast growth factor from physiologically wounded myofibers of normal and dystrophic muscle. J Cell Sci 1993, 106:121-133.
51. Clarke MS, Caldwell RW, Chiao H, Miyake K, McNeil PL. Contraction-induced cell wounding and release of fibroblast growth factor in heart. Circ Res 1995, 76:927-934.
52. Alvarez K, Fadic R, Brandan E. Augmented synthesis and differential localization of heparan sulfate proteoglycans in Duchenne muscular dystrophy. J Cell Biochem 2002, 85:703-713. 10.1002/jcb.10184, 11968010.
53. Liu W, Litwack ED, Stanley MJ, Langford JK, Lander AD, Sanderson RD. Heparan sulfate proteoglycans as adhesive and anti-invasive molecules. Syndecans and glypican have distinct functions. J Biol Chem 1998, 273:22825-22832. 10.1074/jbc.273.35.22825, 9712917.
54. Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 1999, 68:729-77. 10.1146/annurev.biochem.68.1.729, 10872465.
55. Schultz JE, Witt SA, Nieman ML, Reiser PJ, Engle SJ, Zhou M, Pawlowski SA, Lorenz JN, Kimball TR, Doetschman T. Fibroblast growth factor-2 mediates pressure-induced hypertrophic response. J Clin Invest 1999, 104(6):709-719. 10.1172/JCI7315, 408439, 10491406.
56. Pellieux C, Foletti A, Peduto G, Aubert JF, Nussberger J, Beermann F, Brunner HR, Pedrazzini T. Dilated cardiomyopathy and impaired cardiac hypertrophic response to angiotensin II in mice lacking FGF-2. J Clin Invest 2001, 108(12):1843-1851. 209469, 11748268.
57. Bonneh-Barkay D, Shlissel M, Berman B, Shaoul E, Admon A, Vlodavsky I, Carey DJ, Asund VK, Reich-Slotky R, Ron D. Identification of glypican as a dual modulator of the biological activity of fibroblast growth factors. J Biol Chem 1997, 272:12415-12421. 10.1074/jbc.272.19.12415, 9139688.
58. Litwack ED, Ivins JK, Kumbasar A, Paine-Saunders S, Stipp CS, Lander AD. Expression of the heparan sulfate proteoglycan glypican-1 in the developing rodent. Dev Dyn 1998, 211(1):72-87. 10.1002/(SICI)1097-0177(199801)211:1<72::AID-AJA7>3.0.CO;2-4, 9438425.
59. Kardami E, Liu L, Doble BW. Basic fibroblast growth factor in cultured cardiac myocytes. Ann N Y Acad Sci 1991, 638:244-255. 10.1111/j.1749-6632.1991.tb49035.x, 1785804.
60. Jessup JA, Zhang L, Chen AF, Presley TD, Kim-Shapiro DB, Chappell MC, Wang H, Groban L. Neuronal nitric oxide synthase inhibition improves diastolic function and reduces oxidative stress in ovariectomized mRen2.Lewis rats. Menopause 2011,