Soluble receptor for advanced glycation end products mitigates vascular dysfunction in spontaneously hypertensive rats

Molecular and Cellular Biochemistry

Volumn 419, Issue 1-2, 2016, Pages 165-176

  Liu, Yu ^a   Yu, Manli ^b   Zhang, Le ^c   Cao, Qingxin ^d   Song, Ying ^d   Liu, Yuxiu ^a   Gong, Jianbin ^a  

^a NANJING UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

^d The 455th Hospital of PLA   (China)

Author keywords

Inflammation; Oxidative stress; Soluble receptor for advanced glycation end products; Spontaneously hypertensive rats; Vascular dysfunction

Indexed keywords

3 NITROTYROSINE; ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; ALDEHYDE REDUCTASE; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN II; ANGIOTENSIN[1-7]; DIPEPTIDYL CARBOXYPEPTIDASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLYOXALASE; GLYOXALASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; METHYLGLYOXAL; MONOCYTE CHEMOTACTIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; AGER PROTEIN, RAT; ANGIOTENSIN I; ANGIOTENSIN I (1-7); LACTOYLGLUTATHIONE LYASE; PEPTIDE FRAGMENT; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; HEART RATE; HEMODYNAMIC PARAMETERS; HYPERTENSION; HYPERTROPHY; IN VITRO STUDY; INFLAMMATION; MALE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SMOOTH MUSCLE CELL; SPONTANEOUSLY HYPERTENSIVE RAT; SYSTOLIC BLOOD PRESSURE; UPREGULATION; VASCULAR DISEASE; ANIMAL; AORTA; AORTIC DISEASE; BIOSYNTHESIS; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; VASCULAR REMODELING;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; ANGIOTENSIN I; ANIMALS; AORTA; AORTIC DISEASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOSYLATION END PRODUCTS, ADVANCED; LACTOYLGLUTATHIONE LYASE; NF-KAPPA B; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; PPAR GAMMA; RATS; RATS, INBRED SHR; REACTIVE OXYGEN SPECIES; VASCULAR REMODELING;

EID: 84978499135     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-016-2763-5     Document Type: Article

References (44)

1. Perticone F, Ceravolo R, Pujia A, Ventura G, Iacopino S, Scozzafava A, Ferraro A, Chello M, Mastroroberto P, Verdecchia P, Schillaci G (2001) Prognostic significance of endothelial dysfunction in hypertensive patients. Circulation 104:191–196
2. Intengan HD, Schiffrin EL (2001) Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis. Hypertension 38:581–587
3. Park JB, Schiffrin EL (2000) Effects of antihypertensive therapy on hypertensive vascular disease. Curr Hypertens Rep 2:280–288
4. Ramasamy R, Yan SF, Schmidt AM (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 1243:88–102
5. Brownlee M (1995) Advanced protein glycosylation in diabetes and aging. Annu Rev Med 46:223–234
6. Soro-Paavonen A, Watson AM, Li J, Paavonen K, Koitka A, Calkin AC, Barit D, Coughlan MT, Drew BG, Lancaster GI, Thomas M, Forbes JM, Nawroth PP, Bierhaus A, Cooper ME, Jandeleit-Dahm KA (2008) Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes. Diabetes 57:2461–2469
7. −/− mice. J Clin Invest 118:183–194
8. Baumann M (2012) Role of advanced glycation end products in hypertension and cardiovascular risk: human studies. J Am Soc Hypertens 6:427–435
9. Dhar I, Dhar A, Wu L, Desai KM (2013) Increased methylglyoxal formation with upregulation of renin angiotensin system in fructose fed sprague dawley rats. PLoS One 8:e74212
10. Carnevale D, Mascio G, D’Andrea I, Fardella V, Bell RD, Branchi I, Pallante F, Zlokovic B, Yan SS, Lembo G (2012) Hypertension induces brain β-amyloid accumulation, cognitive impairment, and memory deterioration through activation of receptor for advanced glycation end products in brain vasculature. Hypertension 60:188–197
11. Zhu WW, Liu XP, Wu N, Zhao TT, Zhao Y, Zhang J, Shao JH (2007) Beneficial effects of losartan on vascular injury induced by advanced glycosylation end products and their receptors in spontaneous hypertension rats. Mol Cell Biochem 304:35–43
12. Lee TI, Kao YH, Chen YC, Huang JH, Hsu MI, Chen YJ (2013) The dipeptidyl peptidase-4 inhibitor-sitagliptin modulates calcium dysregulation, inflammation, and PPARs in hypertensive cardiomyocytes. Int J Cardiol 168:5390–5395
13. Liu XP, Pang YJ, Zhu WW, Zhao TT, Zheng M, Wang YB, Sun ZJ, Sun SJ (2009) Benazepril, an angiotensin-converting enzyme inhibitor, alleviates renal injury in spontaneously hypertensive rats by inhibiting advanced glycation end-product-mediated pathways. Clin Exp Pharmacol Physiol 36:287–296
14. Yu W, Liu-Bryan R, Stevens S, Damanahalli JK, Terkeltaub R (2012) RAGE signaling mediates post-injury arterial neointima formation by suppression of liver kinase B1 and AMPK activity. Atherosclerosis 222:417–425
15. Koyama H, Yamamoto H, Nishizawa Y (2007) RAGE and soluble RAGE: potential therapeutic targets for cardiovascular diseases. Mol Med 13:625–635
16. Lee D, Lee KH, Park H, Kim SH, Jin T, Cho S, Chung JH, Lim S, Park S (2013) The effect of soluble RAGE on inhibition of angiotensin II-mediated atherosclerosis in apolipoprotein E deficient mice. PLoS One 8:e69669
17. Wu F, Feng JZ, Qiu YH, Yu FB, Zhang JZ, Zhou W, Yu F, Wang GK, An LN, Ni FH, Wu H, Zhao XX, Qin YW, Luo HD (2013) Activation of receptor for advanced glycation end products contributes to aortic remodeling and endothelial dysfunction in sinoaortic denervated rats. Atherosclerosis 229:287–294
18. Kajikawa M, Nakashima A, Fujimura N, Maruhashi T, Iwamoto Y, Iwamoto A, Matsumoto T, Oda N, Hidaka T, Kihara Y, Chayama K, Goto C, Aibara Y, Noma K, Takeuchi M, Matsui T, Yamagishi S, Higashi Y (2015) Ratio of serum levels of AGEs to soluble form of RAGE is a predictor of endothelial function. Diabetes Care 38:119–125
19. Heijnen BF, Van Essen H, Schalkwijk CG, Janssen BJ, Struijker-Boudier HA (2014) Renal inflammatory markers during the onset of hypertension in spontaneously hypertensive rats. Hypertens Res 37:100–109
20. Yoo SM, Choi SH, Jung MD, Lim SC, Baek SH (2015) Short-term use of telmisartan attenuates oxidation and improves Prdx2 expression more than antioxidant β-blockers in the cardiovascular systems of spontaneously hypertensive rats. Hypertens Res 38:106–115
21. Farmer DG, Ewart MA, Mair KM, Kennedy S (2014) Soluble receptor for advanced glycation end products (sRAGE) attenuates haemodynamic changes to chronic hypoxia in the mouse. Pulm Pharmacol Ther 29:7–14
22. Wang K, Zhou Z, Zhang M, Fan L, Forudi F, Zhou X, Qu W, Lincoff AM, Schmidt AM, Topol EJ, Penn MS (2006) Peroxisome proliferator-activated receptor gamma down-regulates receptor for advanced glycation end products and inhibits smooth muscle cell proliferation in a diabetic and nondiabetic rat carotid artery injury model. J Pharmacol Exp Ther 317:37–43
23. Durante P, Chávez M, Pérez M, Romero F, Rivera F (2010) Effect of uric acid on hypertension progression in spontaneously hypertensive rats. Life Sci 86:957–964
24. Kaiserova K, Srivastava S, Hoetker JD, Awe SO, Tang XL, Cai J, Bhatnagar A (2006) Redox activation of aldose reductase in the ischemic heart. J Biol Chem 281:15110–15120
25. McLellan AC, Phillips SA, Thornalley PJ (1993) The assay of S-d-lactoylglutathione in biological systems. Anal Biochem 211:37–43
26. Untereiner AA, Dhar A, Liu J, Wu L (2011) Increased renal methylglyoxal formation with down-regulation of PGC-1α-FBPase pathway in cystathionine γ-lyase knockout mice. PLoS One 6:e29592
27. Elks CM, Mariappan N, Haque M, Guggilam A, Majid DS, Francis J (2009) Chronic NF-kB blockade reduces cytosolic and mitochondrial oxidative stress and attenuates renal injury and hypertension in SHR. Am J Physiol Renal Physiol 296:F298–F305
28. Wang X, Jia X, Chang T, Desai K, Wu L (2008) Attenuation of hypertension development by scavenging methylglyoxal in fructose-treated rats. J Hypertens 26:765–772
29. Li YL, Gao L, Zucker IH, Schultz HD (2007) NADPH oxidase-derived superoxide anion mediates angiotensin II-enhanced carotid body chemoreceptor sensitivity in heart failure rabbits. Cardiovasc Res 75:546–554
30. Zheng H, Yu YS (2012) Chronic hydrogen-rich saline treatment attenuates vascular dysfunction in spontaneous hypertensive rats. Biochem Pharmacol 83:1269–1277
31. Marin-Castano ME, Schanstra JP, Neau E, Praddaude F, Pecher C, Ader JL, Girolami JP, Bascands JL (2002) Induction of functional bradykinin b(1)-receptors in normotensive rats and mice under chronic angiotensin converting enzyme inhibitor treatment. Circulation 105:627–632
32. Lal S, Szwergold BS, Taylor AH, Randall WC, Kappler F, Wells-Knecht K, Baynes JW, Brown TR (1995) Metabolism of fructose-3-phosphate in the diabetic rat lens. Arch Biochem Biophys 318:191–199
33. Thornalley PJ (2003) Glyoxalase 1-structure, function and a critical role in the enzymatic defence against glycation. Biochem Soc Trans 31:1343–1348
34. Sarkar R, Meinberg EG, Stanley JC, Gordon D, Webb RC (1996) Nitric oxide reversibly inhibits the migration of cultured vascular smooth muscle cells. Circ Res 78:225–230
35. Gao X, Zhang H, Schmidt AM, Zhang C (2008) AGE/RAGE produces endothelial dysfunction in coronary arterioles in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 295:H491–H498
36. Coughlan MT, Thorburn DR, Penfold SA, Laskowski A, Harcourt BE, Sourris KC, Tan AL, Fukami K, Thallas-Bonke V, Nawroth PP, Brownlee M, Bierhaus A, Cooper ME, Forbes JM (2009) RAGE-induced cytosolic ROS promote mitochondrial superoxide generation in diabetes. J Am Soc Nephrol 20:742–752
37. Bierhaus A, Stern DM, Nawroth PP (2006) RAGE in inflammation: a new therapeutic target? Curr Opin Investig Drugs 7:985–991
38. Cheng CL, Tang Y, Zheng Z, Liu X, Ye ZC, Wang C, Lou TQ (2012) Advanced glycation end-products activate the renin-angiotensin system through the RAGE/PI3-K signaling pathway in podocytes. Clin Invest Med 35:E282
39. Rentzsch B, Todiras M, Iliescu R, Popova E, Campos LA, Oliveira ML, Baltatu OC, Santos RA, Bader M (2008) Transgenic angiotensin-converting enzyme 2 overexpression in vessels of SHRSP rats reduces blood pressure and improves endothelial function. Hypertension 52:967–973
40. Marchesi C, Rehman A, Rautureau Y, Kasal DA, Briet M, Leibowitz A, Simeone SM, Ebrahimian T, Neves MF, Offermanns S, Gonzalez FJ, Paradis P, Schiffrin EL (2013) Protective role of vascular smooth muscle cell PPARγ in angiotensin II-induced vascular disease. Cardiovasc Res 97:562–570
41. Bijli KM, Kleinhenz JM, Murphy TC, Kang BY, Adesina SE, Sutliff RL, Hart CM (2015) Peroxisome proliferator-activated receptor gamma depletion stimulates Nox4 expression and human pulmonary artery smooth muscle cell proliferation. Free Radic Biol Med 80:111–120
42. Chen YJ, Sheu ML, Tsai KS, Yang RS, Liu SH (2013) Advanced glycation end products induce peroxisome proliferator-activated receptor γ down-regulation-related inflammatory signals in human chondrocytes via Toll-like receptor-4 and receptor for advanced glycation end products. PLoS One 8:e66611
43. Kaji Y, Usui T, Ishida S, Yamashiro K, Moore TC, Moore J, Yamamoto Y, Yamamoto H, Adamis AP (2007) Inhibition of diabetic leukostasis and blood-retinal barrier breakdown with a soluble form of a receptor for advanced glycation end products. Invest Ophthalmol Vis Sci 48:858–865
44. Lalla E, Lamster IB, Feit M, Huang L, Spessot A, Qu W, Kislinger T, Lu Y, Stern DM, Schmidt AM (2000) Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. J Clin Invest 105:1117–1124