The role of glycosaminoglycans in blood pressure regulation.
blood pressure
glycocalyx
glycosaminoglycan
hypertension
sodium deposition
Journal
Microcirculation (New York, N.Y. : 1994)
ISSN: 1549-8719
Titre abrégé: Microcirculation
Pays: United States
ID NLM: 9434935
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
06
05
2023
received:
01
02
2023
accepted:
23
09
2023
medline:
9
11
2023
pubmed:
5
10
2023
entrez:
5
10
2023
Statut:
ppublish
Résumé
Essential hypertension (HT) is the global health problem and is a major risk factor for the development of cardiovascular and kidney disease. High salt intake has been associated with HT and impaired kidney sodium excretion is considered to be a major mechanism for the development of HT. Although kidney has a very important role in regulation of BP, this traditional view of BP regulation was challenged by recent findings suggesting that nonosmotic tissue sodium deposition is very important for BP regulation. This new paradigm indicates that sodium can be stored and deposited nonosmotically in the interstitium without water retention and without increased BP. One of the major determinants of this deposition is glycosaminoglycans (GAGs). By binding to GAGs found in the endothelial surface layer (ESL) which contains glycocalyx, sodium is osmotically inactivated and not induce concurrent water retention. Thus, GAGs has important function for homeostatic BP and sodium regulation. In the current review, we summarized the role of GAGs in ESL and BP regulation.
Substances chimiques
Glycosaminoglycans
0
Sodium
9NEZ333N27
Water
059QF0KO0R
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12832Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Kanbay M, Demiray A, Afsar B, et al. Role of klotho in the development of essential hypertension. Hypertension. 2021;77:740-750.
Afsar B, Kuwabara M, Ortiz A, et al. Salt intake and immunity. Hypertension. 2018;72:19-23.
Olde Engberink RHG, Selvarajah V, Vogt L. Clinical impact of tissue sodium storage. Pediatr Nephrol. 2020;35:1373-1380.
Heer M, Baisch F, Kropp J, Gerzer R, Drummer C. High dietary sodium chloride consumption may not induce body fluid retention in humans. Am J Physiol Renal Physiol. 2000;278:F585-F595.
Titze J, Shakibaei M, Schafflhuber M, et al. Glycosaminoglycan polymerization may enable osmotically inactive Na+ storage in the skin. Am J Physiol Heart Circ Physiol. 2004;287:H203-H208.
Sugár D, Agócs R, Tatár E, et al. The contribution of skin glycosaminoglycans to the regulation of sodium homeostasis in rats. Physiol Res. 2018;67:777-785.
Bernfield M, Götte M, Park PW, et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 1999;68:729-777.
Rienks M, Papageorgiou AP, Frangogiannis NG, Heymans S. Myocardial extracellular matrix: an ever-changing and diverse entity. Circ Res. 2014;114:872-888.
Cadaval RA, Kohlman O, Michelacci YM. Urinary excretion of glycosaminoglycans and albumin in experimental diabetes mellitus. Glycobiology. 2000;10:185-192.
Yang R, Chen M, Zheng J, Li X, Zhang X. The role of heparin and glycocalyx in blood-brain barrier dysfunction. Front Immunol. 2021;12:754141.
Yilmaz O, Afsar B, Ortiz A, Kanbay M. The role of endothelial glycocalyx in health and disease. Clin Kidney J. 2019;12:611-619.
Stanimirovic DB, Friedman A. Pathophysiology of the neurovascular unit: disease cause or consequence? J Cereb Blood Flow Metab. 2012;32:1207-1221.
Filmus J, Capurro M, Rast J. Glypicans. Genome Biol. 2008;9:224.
Lunde IG, Herum KM, Carlson CC, Christensen G. Syndecans in heart fibrosis. Cell Tissue Res. 2016;365:539-552.
Becker BF, Jacob M, Leipert S, Salmon AH, Chappell D. Degradation of the endothelial glycocalyx in clinical settings: searching for the sheddases. Br J Clin Pharmacol. 2015;80:389-402.
Boels MG, Lee DH, van den Berg BM, Dane MJ, van der Vlag J, Rabelink TJ. The endothelial glycocalyx as a potential modifier of the hemolytic uremic syndrome. Eur J Intern Med. 2013;24:503-509.
Wilsie LC, Orlando RA. The low density lipoprotein receptor-related protein complexes with cell surface heparan sulfate proteoglycans to regulate proteoglycan-mediated lipoprotein catabolism. J Biol Chem. 2003;278:15758-15764.
Lin X. Functions of heparan sulfate proteoglycans in cell signaling during development. Development. 2004;131:6009-6021.
Olde Engberink RH, Rorije NM, van der Heide JJ H, van den Born BJ, Vogt L. Role of the vascular wall in sodium homeostasis and salt sensitivity. J Am Soc Nephrol. 2015;26:777-783.
Nieuwdorp M, Mooij HL, Kroon J, et al. Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes. Diabetes. 2006;55:1127-1132.
Padberg JS, Wiesinger A, di Marco GS, et al. Damage of the endothelial glycocalyx in chronic kidney disease. Atherosclerosis. 2014;234:335-343.
Vlahu CA, Lemkes BA, Struijk DG, Koopman MG, Krediet RT, Vink H. Damage of the endothelial glycocalyx in dialysis patients. J Am Soc Nephrol. 2012;23:1900-1908.
Wouda RD, Dekker SEI, Reijm J, Olde Engberink RHG, Vogt L. Effects of water loading on observed and predicted plasma sodium, and fluid and urine cation excretion in healthy individuals. Am J Kidney Dis. 2019;74:320-327.
Kopp C, Linz P, Hammon M, et al. Seeing the sodium in a patient with hypernatremia. Kidney Int. 2012;82:1343-1344.
Titze J, Lang R, Ilies C, et al. Osmotically inactive skin Na+ storage in rats. Am J Physiol Renal Physiol. 2003;285:F1108-F1117.
Hijmans RS, Shrestha P, Sarpong KA, et al. High sodium diet converts renal proteoglycans into pro-inflammatory mediators in rats. PloS One. 2017;12:e0178940.
Hofmeister LH, Perisic S, Titze J. Tissue sodium storage: evidence for kidney-like extrarenal countercurrent systems? Pflugers Arch. 2015;467:551-558.
Wiig H, Luft FC, Titze JM. The interstitium conducts extrarenal storage of sodium and represents a third compartment essential for extracellular volume and blood pressure homeostasis. Acta Physiol (Oxf). 2018;222:e13006.
Chachaj A, Szuba A. Skin lymphatic system in the pathogenesis of arterial hypertension - review and critique. Lymphology. 2020;53:99-108.
Titze J, Machnik A. Sodium sensing in the interstitium and relationship to hypertension. Curr Opin Nephrol Hypertens. 2010;19:385-392.
Titze J, Bauer K, Schafflhuber M, et al. Internal sodium balance in DOCA-salt rats: a body composition study. Am J Physiol Renal Physiol. 2005;289:F793-F802.
Machnik A, Neuhofer W, Jantsch J, et al. Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat Med. 2009;15:545-552.
Dahlmann A, Dörfelt K, Eicher F, et al. Magnetic resonance-determined sodium removal from tissue stores in hemodialysis patients. Kidney Int. 2015;87:434-441.
Foster RR, Armstrong L, Baker S, et al. Glycosaminoglycan regulation by VEGFA and VEGFC of the glomerular microvascular endothelial cell glycocalyx in vitro. Am J Pathol. 2013;183:604-616.
Heer M, Frings-Meuthen P, Titze J, et al. Increasing sodium intake from a previous low or high intake affects water, electrolyte and acid-base balance differently. Br J Nutr. 2009;101:1286-1294.
Schafflhuber M, Volpi N, Dahlmann A, et al. Mobilization of osmotically inactive Na+ by growth and by dietary salt restriction in rats. Am J Physiol Renal Physiol. 2007;292:F1490-F1500.
Oberleithner H, Peters W, Kusche-Vihrog K, et al. Salt overload damages the glycocalyx sodium barrier of vascular endothelium. Pflugers Arch. 2011;462:519-528.
Bkaily G, Simon Y, Menkovic I, Bkaily C, Jacques D. High salt-induced hypertrophy of human vascular smooth muscle cells associated with a decrease in glycocalyx. J Mol Cell Cardiol. 2018;125:1-5.
Fronius M. Epithelial Na+ channel and the glycocalyx: a sweet and salty relationship for arterial shear stress sensing. Curr Opin Nephrol Hypertens. 2022;31:142-150.
Oberleithner H, Callies C, Kusche-Vihrog K, et al. Potassium softens vascular endothelium and increases nitric oxide release. Proc Natl Acad Sci U S A. 2009;106:2829-2834.
Meneton P, Jeunemaitre X, de Wardener HE, MacGregor GA. Links between dietary salt intake, renal salt handling, blood pressure, and cardiovascular diseases. Physiol Rev. 2005;85:679-715.
Singh A, Satchell SC, Neal CR, McKenzie EA, Tooke JE, Mathieson PW. Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol. 2007;18:2885-2893.
Weinbaum S, Zhang X, Han Y, Vink H, Cowin SC. Mechanotransduction and flow across the endothelial glycocalyx. Proc Natl Acad Sci U S A. 2003;100:7988-7995.
Nieuwdorp M, Meuwese MC, Vink H, Hoekstra JB, Kastelein JJ, Stroes ES. The endothelial glycocalyx: a potential barrier between health and vascular disease. Curr Opin Lipidol. 2005;16:507-511.
Agócs R, Pap D, Sugár D, et al. Cyclooxygenase-2 modulates glycosaminoglycan production in the skin during salt overload. Front Physiol. 2020;11:561722.
Carroll BJ, Piazza G, Goldhaber SZ. Sulodexide in venous disease. J Thromb Haemost. 2019;17:31-38.
Gambaro G, Kinalska I, Oksa A, et al. Oral sulodexide reduces albuminuria in microalbuminuric and macroalbuminuric type 1 and type 2 diabetic patients: the Di.N.A.S. Randomized trial. J Am Soc Nephrol. 2002;13:1615-1625.
Heerspink HL, Greene T, Lewis JB, et al. Effects of sulodexide in patients with type 2 diabetes and persistent albuminuria. Nephrol Dial Transplant. 2008;23:1946-1954.
Packham DK, Wolfe R, Reutens AT, et al. Sulodexide fails to demonstrate renoprotection in overt type 2 diabetic nephropathy. J Am Soc Nephrol. 2012;23:123-130.
Bang K, Chin HJ, Chae DW, et al. Anti-proteinuric effect of sulodexide in immunoglobulin a nephropathy. Yonsei Med J. 2011;52:588-594.
Solini A, Vergnani L, Ricci F, Crepaldi G. Glycosaminoglycans delay the progression of nephropathy in NIDDM. Diabetes Care. 1997;20:819-823.
Olde Engberink RH, Rorije NM, Lambers Heerspink HJ, De Zeeuw D, van den Born BJ, Vogt L. The blood pressure lowering potential of sulodexide-a systematic review and meta-analysis. Br J Clin Pharmacol. 2015;80:1245-1253.
Olde Engberink RH, Heerspink HJ, de Zeeuw D, Vogt L. Blood pressure-lowering effects of sulodexide depend on albuminuria severity: post hoc analysis of the sulodexide microalbuminuria and macroalbuminuria studies. Br J Clin Pharmacol. 2016;82:1351-1357.
Salmon AH, Ferguson JK, Burford JL, et al. Loss of the endothelial glycocalyx links albuminuria and vascular dysfunction. J Am Soc Nephrol. 2012;23:1339-1350.
Li P, Ma LL, Xie RJ, et al. Treatment of 5/6 nephrectomy rats with sulodexide: a novel therapy for chronic renal failure. Acta Pharmacol Sin. 2012;33:644-651.
Bilinska M, Wolszakiewicz J, Duda M, Janas J, Beresewicz A, Piotrowicz R. Antioxidative activity of sulodexide, a glycosaminoglycan, in patients with stable coronary artery disease: a pilot study. Med Sci Monit. 2009;15:Cr618-Cr623.
Coccheri S, Mannello F. Development and use of sulodexide in vascular diseases: implications for treatment. Drug Des Devel Ther. 2013;8:49-65.
van den Born J, Salmivirta K, Henttinen T, et al. Novel heparan sulfate structures revealed by monoclonal antibodies. J Biol Chem. 2005;280:20516-20523.
Celie JW, Keuning ED, Beelen RH, et al. Identification of L-selectin binding heparan sulfates attached to collagen type XVIII. J Biol Chem. 2005;280:26965-26973.
Adepu S, Katta K, Tietge UJ, et al. Hepatic syndecan-1 changes associate with dyslipidemia after renal transplantation. Am J Transplant. 2014;14:2328-2338.
Lee RM, Richardson M, McKenzie R. Vascular changes associated with deoxycorticosterone-NaCl-induced hypertension. Blood Vessels. 1989;26:137-156.
Jyothirmayi GN, Alluru L, Fine JM, Reddi AS. Sodium depletion prevents albuminuria in hypertensive rats. Res Commun Mol Pathol Pharmacol. 1995;90:115-124.
Pourzitaki C, Tsaousi G, Manthou ME, Karakiulakis G, Kouvelas D, Papakonstantinou E. Furosemide modifies heart hypertrophy and glycosaminoglycan myocardium content in a rat model of neurogenic hypertension. Eur J Pharmacol. 2016;784:155-163.
Heintz B, Stöcker G, Mrowka C, et al. Decreased glomerular basement membrane heparan sulfate proteoglycan in essential hypertension. Hypertension. 1995;25:399-407.
Yavuz D, Toprak A, Budak Y, et al. Urinary glycosaminoglycan excretion in newly diagnosed essential hypertensive patients. Clin Chem. 2000;46:299-301.
Baker AB, Ettenson DS, Jonas M, Nugent MA, Iozzo RV, Edelman ER. Endothelial cells provide feedback control for vascular remodeling through a mechanosensitive autocrine TGF-beta signaling pathway. Circ Res. 2008;103:289-297.
Lemarié CA, Tharaux PL, Lehoux S. Extracellular matrix alterations in hypertensive vascular remodeling. J Mol Cell Cardiol. 2010;48:433-439.
Mitchell GF. Arterial stiffness and hypertension. Hypertension. 2014;64:13-18.
Liu L, Kashyap S, Murphy B, et al. GPER activation ameliorates aortic remodeling induced by salt-sensitive hypertension. Am J Physiol Heart Circ Physiol. 2016;310:H953-H961.
Olde Engberink RHG, de Vos J, van Weert A, et al. Abnormal sodium and water homeostasis in mice with defective heparan sulfate polymerization. PloS One. 2019;14:e0220333.
Drobnik J, Dabrowski R, Szczepanowska A, Giernat L, Lorenc J. Response of aorta connective tissue matrix to injury caused by vassopressin-induced hypertension or hypercholesterolemia. J Physiol Pharmacol. 2000;51:521-533.
Weissgerber TL, Garcia-Valencia O, Milic NM, et al. Early onset preeclampsia is associated with glycocalyx degradation and reduced microvascular perfusion. J Am Heart Assoc. 2019;8:e010647.
Linhardt RJ, Dordick JS, Deangelis PL, Liu J. Enzymatic synthesis of glycosaminoglycan heparin. Semin Thromb Hemost. 2007;33:453-465.
Susic D, Mandal AK, Kentera D. Heparin lowers the blood pressure in hypertensive rats. Hypertension. 1982;4:681-685.
Wilson SK, Solez K, Boitnott JK, Heptinstall RH. The effects of heparin treatment on hypertension and vascular lesions in stroke-prone spontaneously hypertensive rats. Am J Pathol. 1981;102:62-71.
Olson JL. Role of heparin as a protective agent following reduction of renal mass. Kidney Int. 1984;25:376-382.
Benchetrit S, Mandelbaum A, Bernheim J, et al. Altered vascular reactivity following partial nephrectomy in the rat: a possible mechanism of the blood-pressure-lowering effect of heparin. Nephrol Dial Transplant. 1999;14:64-69.
Vasdev S, Ford CA, Longerich L, Barrett B, Parai S, Campbell N. Oral treatment with low molecular weight heparin normalizes blood pressure in hypertensive rats. Artery. 1994;21:1-28.
Mandal AK, Lyden TW, Saklayen MG. Heparin lowers blood pressure: biological and clinical perspectives. Kidney Int. 1995;47:1017-1022.
Zaragoza R, Battle-Tracy KM, Owen NE. Heparin inhibits Na(+)-H+ exchange in vascular smooth muscle cells. Am J Phys. 1990;258:C46-C53.
Castellot JJ Jr, Wright TC, Karnovsky MJ. Regulation of vascular smooth muscle cell growth by heparin and heparan sulfates. Semin Thromb Hemost. 1987;13:489-503.
Lindner V, Olson NE, Clowes AW, Reidy MA. Inhibition of smooth muscle cell proliferation in injured rat arteries. Interaction of heparin with basic fibroblast growth factor. J Clin Invest. 1992;90:2044-2049.
Grainger DJ, Witchell CM, Watson JV, Metcalfe JC, Weissberg PL. Heparin decreases the rate of proliferation of rat vascular smooth muscle cells by releasing transforming growth factor beta-like activity from serum. Cardiovasc Res. 1993;27:2238-2247.
Dilley RJ, Nataatmadja MI. Heparin inhibits mesenteric vascular hypertrophy in angiotensin II-infusion hypertension in rats. Cardiovasc Res. 1998;38:247-255.
Reynertson RH, Parmley RT, Rodén L, Oparil S. Proteoglycans and hypertension. I. A biochemical and ultrastructural study of aorta glycosaminoglycans in spontaneously hypertensive rats. Coll Relat Res. 1986;6:77-101.
Kotlo K, Bhattacharyya S, Yang B, et al. Impact of salt exposure on N-acetylgalactosamine-4-sulfatase (arylsulfatase B) activity, glycosaminoglycans, kininogen, and bradykinin. Glycoconj J. 2013;30:667-676.
Schnabelrauch M, Scharnweber D, Schiller J. Sulfated glycosaminoglycans as promising artificial extracellular matrix components to improve the regeneration of tissues. Curr Med Chem. 2013;20:2501-2523.
Nagy N, Freudenberger T, Melchior-Becker A, et al. Inhibition of hyaluronan synthesis accelerates murine atherosclerosis: novel insights into the role of hyaluronan synthesis. Circulation. 2010;122:2313-2322.
Stridh S, Palm F, Hansell P. Inhibition of hyaluronan synthesis in rats reduces renal ability to excrete fluid and electrolytes during acute hydration. Ups J Med Sci. 2013;118:217-221.
Bai F, Pang XF, Zhang LH, et al. Angiotensin II AT1 receptor alters ACE2 activity, eNOS expression and CD44-hyaluronan interaction in rats with hypertension and myocardial fibrosis. Life Sci. 2016;153:141-152.
Jakob A, Bohlig S, König M, et al. Kawasaki disease and increased cardiovascular risk: is there a link to circulating glycocalyx biomarkers? Microvasc Res. 2022;140:104269.
Watanabe K, Okamoto T, Saitou T, et al. Increased urinary albumin leakage is related to injuries of glomerular glycocalyx and podocytes, and associated with tubular dysfunction in preeclampsia. Pregnancy Hypertens. 2023;32:1-6.
Machin DR, Trott DW, Gogulamudi VR, et al. Glycocalyx-targeted therapy ameliorates age-related arterial dysfunction. Geroscience. 2023. [online ahead of print]
Tkachenko E, Rhodes JM, Simons M. Syndecans: new kids on the signaling block. Circ Res. 2005;96:488-500.
De Luca M, Bryan DR, Hunter GR. Serum syndecan-4 correlates with blood pressure and cardiovascular parameters but not proinflammatory markers in healthy older women. Aging Clin Exp Res. 2022;34:2541-2545.
De Luca M, Bryan DR, Hunter GR. Circulating levels of the heparan sulfate proteoglycan Syndecan-4 positively associate with blood pressure in healthy premenopausal women. Biomol Ther. 2021;11:342.
Lipphardt M, Dihazi H, Maas JH, et al. Syndecan-4 as a marker of endothelial dysfunction in patients with resistant hypertension. J Clin Med. 2020;9:3051.
Simon G, Abraham G, Altman S. Stimulation of vascular glycosaminoglycan synthesis by subpressor angiotensin II in rats. Hypertension. 1994;23:I148-I151.
Simon G. Increased vascular wall sodium in hypertension: where is it, how does it get there and what does it do there? Clin Sci (Lond). 1990;78:533-540.
Nikpey E, Karlsen TV, Rakova N, Titze JM, Tenstad O, Wiig H. High-salt diet causes osmotic gradients and hyperosmolality in skin without affecting interstitial fluid and lymph. Hypertension. 2017;69:660-668.
Warner RR, Myers MC, Taylor DA. Electron probe analysis of human skin: element concentration profiles. J Invest Dermatol. 1988;90:78-85.
Wenstedt EFE, Olde Engberink RHG, Vogt L. Sodium handling by the blood Vessel Wall: critical for hypertension development. Hypertension. 2018;71:990-996.
Steyers CM 3rd, Miller FJ Jr. Endothelial dysfunction in chronic inflammatory diseases. Int J Mol Sci. 2014;15:11324-11349.
Laffer CL, Scott RC 3rd, Titze JM, Luft FC, Elijovich F. Hemodynamics and salt-and-water balance link sodium storage and vascular dysfunction in salt-sensitive subjects. Hypertension. 2016;68:195-203.
Hammon M, Grossmann S, Linz P, et al. 23Na magnetic resonance imaging of the lower leg of acute heart failure patients during diuretic treatment. PloS One. 2015;10:e0141336.
Kopp C, Linz P, Dahlmann A, et al. 23Na magnetic resonance imaging-determined tissue sodium in healthy subjects and hypertensive patients. Hypertension. 2013;61:635-640.
Hunter GK. Chondroitin sulfate-derivatized agarose beads: a new system for studying cation binding to glycosaminoglycans. Anal Biochem. 1987;165:435-441.
Faller CE, Guvench O. Sulfation and cation effects on the conformational properties of the glycan backbone of chondroitin sulfate disaccharides. J Phys Chem B. 2015;119:6063-6073.
McNally RJ, Morselli F, Farukh B, Chowienczyk PJ, Faconti L. A pilot study to evaluate the erythrocyte glycocalyx sensitivity to sodium as a marker for cellular salt sensitivity in hypertension. J Hum Hypertens. 2023;37:286-291.
Masenga SK, Pilic L, Malumani M, Hamooya BM. Erythrocyte sodium buffering capacity status correlates with self-reported salt intake in a population from Livingstone, Zambia. PloS One. 2022;17:e0264650.
Ikonomidis I, Voumvourakis A, Makavos G, et al. Association of impaired endothelial glycocalyx with arterial stiffness, coronary microcirculatory dysfunction, and abnormal myocardial deformation in untreated hypertensives. J Clin Hypertens (Greenwich). 2018;20:672-679.
Ikonomidis I, Frogoudaki A, Vrettou AR, et al. Impaired arterial elastic properties and endothelial glycocalyx in patients with embolic stroke of undetermined source. Thromb Haemost. 2019;119:1860-1868.
Valerio L, Peters RJ, Zwinderman AH, Pinto-Sietsma SJ. Sublingual endothelial glycocalyx and atherosclerosis. A cross-sectional study. PloS One. 2019;14:e0213097.
Nijst P, Verbrugge FH, Grieten L, et al. The pathophysiological role of interstitial sodium in heart failure. J Am Coll Cardiol. 2015;65:378-388.
Suzuki A, Tomita H, Okada H. Form follows function: the endothelial glycocalyx. Transl Res. 2022;247:158-167.
Solak Y, Afsar B, Vaziri ND, et al. Hypertension as an autoimmune and inflammatory disease. Hypertens Res. 2016;39:567-573.
Harwani SC. Macrophages under pressure: the role of macrophage polarization in hypertension. Transl Res. 2018;191:45-63.
Vinaiphat A, Pazhanchamy K, JebaMercy G, et al. Endothelial damage arising from high salt hypertension is elucidated by vascular bed systematic profiling. Arterioscler Thromb Vasc Biol. 2023;43:427-442.
Abassi Z, Armaly Z, Heyman SN. Glycocalyx degradation in ischemia-reperfusion injury. Am J Pathol. 2020;190:752-767.
Nassar M, Nso N, Lakhdar S, et al. New onset hypertension after transplantation. World J Transplant. 2022;12:42-54.
Yoneda H, Ueta K, Nagasaki M, Arakawa K. Involvement of heparan sulfate in the renoprotective effects of imidapril, an angiotensin-converting enzyme inhibitor, in diabetic db/db mice. J Recept Signal Transduct Res. 2014;34:21-25.
Brinkkoetter PT, Holtgrefe S, van der Woude FJ, Yard BA. Angiotensin II type 1-receptor mediated changes in heparan sulfate proteoglycans in human SV40 transformed podocytes. J Am Soc Nephrol. 2004;15:33-40.
van Det NF, Tamsma JT, van den Born J, et al. Differential effects of angiotensin II and transforming growth factor beta on the production of heparan sulfate proteoglycan by mesangial cells in vitro. J Am Soc Nephrol. 1996;7:1015-1023.
Wapstra FH, Navis GJ, van Goor H, et al. ACE inhibition preserves heparan sulfate proteoglycans in the glomerular basement membrane of rats with established adriamycin nephropathy. Exp Nephrol. 2001;9:21-27.
Shimizu-Hirota R, Sasamura H, Mifune M, et al. Regulation of vascular proteoglycan synthesis by angiotensin II type 1 and type 2 receptors. J Am Soc Nephrol. 2001;12:2609-2615.
Sasamura H, Shimizu-Hirota R, Nakaya H, Saruta T. Effects of AT1 receptor antagonist on proteoglycan gene expression in hypertensive rats. Hypertens Res. 2001;24:165-172.
Mennander AA, Shalaby A, Oksala N, et al. Diazoxide may protect endothelial glycocalyx integrity during coronary artery bypass grafting. Scand Cardiovasc J. 2012;46:339-344.
Gohda T, Murakoshi M. Sodium-glucose cotransporter-2 inhibitors-miracle drugs for the treatment of chronic kidney disease irrespective of the diabetes status: lessons from the dedicated kidney disease-focused CREDENCE and DAPA-CKD trials. Int J Mol Sci. 2022;23:13749.
Hallow KM, Greasley PJ, Helmlinger G, Chu L, Heerspink HJ, Boulton DW. Evaluation of renal and cardiovascular protection mechanisms of SGLT2 inhibitors: model-based analysis of clinical data. Am J Physiol Renal Physiol. 2018;315:F1295-F1306.
Wilcox CS, Shen W, Boulton DW, Leslie BR, Griffen SC. Interaction between the sodium-glucose-linked transporter 2 inhibitor dapagliflozin and the loop diuretic bumetanide in normal human subjects. J Am Heart Assoc. 2018;7:e007046.
Karg MV, Bosch A, Kannenkeril D, et al. SGLT-2-inhibition with dapagliflozin reduces tissue sodium content: a randomised controlled trial. Cardiovasc Diabetol. 2018;17:5.
Ikonomidis I, Pavlidis G, Thymis J, et al. Effects of glucagon-like Peptide-1 receptor agonists, sodium-glucose cotransporter-2 inhibitors, and their combination on endothelial glycocalyx, arterial function, and myocardial work index in patients with type 2 diabetes mellitus after 12-month treatment. J Am Heart Assoc. 2020;9:e015716.
Broekhuizen LN, Lemkes BA, Mooij HL, et al. Effect of sulodexide on endothelial glycocalyx and vascular permeability in patients with type 2 diabetes mellitus. Diabetologia. 2010;53:2646-2655.
Waanders F, de Vries LV, van Goor H, et al. Aldosterone, from (patho)physiology to treatment in cardiovascular and renal damage. Curr Vasc Pharmacol. 2011;9:594-605.