Activation of Nrf2 contributes to the protective effect of Exendin-4 against angiotensin II-induced vascular smooth muscle cell senescence

American Journal of Physiology - Cell Physiology

Volumn 311, Issue 4, 2016, Pages C572-C582

  Zhou, Tengfei ^a   Zhang, Mengqian ^a   Zhao, Liang ^a   Li, Aiqin ^a   Qin, Xiaomei ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

Cellular senescence; Glucagon like peptide 1; NF E2 related factor 2; Vascular smooth muscle cells

Indexed keywords

ANGIOTENSIN II; ANTIOXIDANT; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYTOPROTECTIVE AGENT; EXENDIN 4; HEME OXYGENASE 1; HISTONE H2AX; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; GLUCAGON LIKE PEPTIDE 1; NFE2L2 PROTEIN, RAT; OXIDOREDUCTASE; PEPTIDE; PROTECTIVE AGENT; VENOM;

ANIMAL CELL; ARTICLE; CELL AGING; CELL NUCLEUS; CELL PROTECTION; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; DEACETYLATION; DOSE RESPONSE; GENE EXPRESSION; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN EXPRESSION; RAT; SENESCENCE; TRANSACTIVATION; UPREGULATION; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CELL CULTURE; DRUG EFFECT; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; SPRAGUE DAWLEY RAT; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANIMALS; ANTIOXIDANTS; CELLS, CULTURED; CELLULAR SENESCENCE; EXENATIDE; GLUCAGON-LIKE PEPTIDE 1; HEME OXYGENASE-1; MALE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NADH, NADPH OXIDOREDUCTASES; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEPTIDES; PROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; VENOMS;

EID: 84991204026     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00093.2016     Document Type: Article

References (56)

1. Arakawa M, Mita T, Azuma K, Ebato C, Goto H, Nomiyama T, Fujitani Y, Hirose T, Kawamori R, Watada H. Inhibition of monocyte adhesion to endothelial cells and attenuation of atherosclerotic lesion by a glucagon-like peptide-1 receptor agonist, exendin-4. Diabetes 59: 1030–1037, 2010.
2. Bachschmid MM, Schildknecht S, Matsui R, Zee R, Haeussler D, Cohen RA, Pimental D, Loo Bv. Vascular aging: chronic oxidative stress and impairment of redox signaling-consequences for vascular homeostasis and disease. Ann Med 45: 17–36, 2013.
3. Bandyopadhyay D, Okan NA, Bales E, Nascimento L, Cole PA, Medrano EE. Down-regulation of p300/CBP histone acetyltransferase activates a senescence checkpoint in human melanocytes. Cancer Res 62: 6231–6239, 2002.
4. Bedford DC, Brindle PK. Is histone acetylation the most important physiological function for CBP and p300? Aging (Albany NY) 4: 247–255, 2012.
5. Brand S, Amann K, Mandel P, Zimnol A, Schupp N. Oxidative DNA damage in kidneys and heart of hypertensive mice is prevented by blocking angiotensin II and aldosterone receptors. PLoS One 9: e115715, 2014.
6. Brouilette SW, Moore JS, McMahon AD, Thompson JR, Ford I, Shepherd J, Packard CJ, Samani NJ; West of Scotland Coronary Prevention Study Group. Telomere length, risk of coronary heart disease, and statin treatment in the West of Scotland Primary Prevention Study: a nested casecontrol study Lancet 369: 107–114, 2007.
7. Chen YT, Tsai TH, Yang CC, Sun CK, Chang LT, Chen HH, Chang CL, Sung PH, Zhen YY, Leu S, Chang HW, Chen YL, Yip HK. Exendin-4 and sitagliptin protect kidney from ischemia-reperfusion injury through suppressing oxidative stress and inflammatory reaction. J Transl Med 11: 270, 2013.
8. Chung YH, Kim EJ, Shin CM, Joo KM, Kim MJ, Woo HW, Cha CI. Age-related changes in CREB binding protein immunoreactivity in the cerebral cortex and hippocampus of rats. Brain Res 956: 312–318, 2002.
9. Cui G, Sun J, Zhang L, Li R, Wang Y, Cianflone K, Ding H, Wang DW. Lack of causal relationship between leukocyte telomere length and coronary heart disease. Atherosclerosis 233: 375–380, 2014.
10. Dalle S, Burcelin R, Gourdy P. Specific actions of GLP-1 receptor agonists and DPP4 inhibitors for the treatment of pancreatic ˜-cell impairments in type 2 diabetes. Cell Signal 25: 570–579, 2013.
11. Ellehoj H, Bendix L, Osler M. Leucocyte telomere length and risk of cardiovascular disease in a cohort of 1,397 Danish men and women. Cardiology 133: 173–177, 2016.
12. Fernández-Millán E, Martín MA, Goya L, Lizárraga-Mollinedo E, Escrivá F, Ramos S, Álvarez C. Glucagon-like peptide-1 improves beta-cell antioxidant capacity via extracellular regulated kinases pathway and Nrf2 translocation. Free Radic Biol Med 95: 16–26, 2016.
13. Finkel T. Telomeres and mitochondrial function. Circ Res 108: 903–904, 2011.
14. Funakoshi Y, Ichiki T, Takeda K, Tokuno T, Iino N, Takeshita A. Critical role of cAMP-response element-binding protein for angiotensin II-induced hypertrophy of vascular smooth muscle cells. J Biol Chem 277: 18710–18717, 2002.
15. Fyhrquist F, Saijonmaa O, Strandberg T. The roles of senescence and telomere shortening in cardiovascular disease. Nat Rev Cardiol 10: 274–283, 2013.
16. Gorenne I, Kavurma M, Scott S, Bennett M. Vascular smooth muscle cell senescence in atherosclerosis. Cardiovasc Res 72: 9–17, 2006.
17. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413: 179–183, 2001.
18. Kang SJ, You A, Kwak MK. Suppression of Nrf2 signaling by angiotensin II in murine renal epithelial cells. Arch Pharm Res 34: 829–836, 2011.
19. Kasper LH, Lerach S, Wang J, Wu S, Jeevan T, Brindle PK. CBP/ p300 double null cells reveal effect of coactivator level and diversity on CREB transactivation. EMBO J 29: 3660–3672, 2010.
20. Kawai Y, Garduno L, Theodore M, Yang J, Arinze IJ. Acetylationdeacetylation of the transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2) regulates its transcriptional activity and nucleocytoplasmic localization. J Biol Chem 286: 7629–7640, 2011.
21. Kieffer TJ, Habener JF. The glucagon-like peptides. Endocr Rev 20: 876–913, 1999.
22. Kim HJ, Vaziri ND. Contribution of impaired Nrf2-Keap1 pathway to oxidative stress and inflammation in chronic renal failure. Am J Physiol Renal Physiol 298: F662–F671, 2010.
23. Kim SJ, Ao Z, Warnock G, McIntosh CH. Incretin-stimulated interaction between ˜-cell Kv1.5 and Kv˜2 channel proteins involves acetylation/ deacetylation by CBP/SirT1. Biochem J 451: 227–234, 2013.
24. Kobayashi A, Kang MI, Watai Y, Tong KI, Shibata T, Uchida K, Yamamoto M. Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol Cell Biol 26: 221–229, 2006.
25. Kunieda T, Minamino T, Nishi J, Tateno K, Oyama T, Katsuno T, Miyauchi H, Orimo M, Okada S, Takamura M, Nagai T, Kaneko S, Komuro I. Angiotensin II induces premature senescence of vascular smooth muscle cells and accelerates the development of atherosclerosis via a p21-dependent pathway. Circulation 114: 953–960, 2006.
26. Liu X, Wang L, Zhao K, Thompson PR, Hwang Y, Marmorstein R, Cole PA. The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 451: 846–850, 2008.
27. Lorber D. GLP-1 receptor agonists: effects on cardiovascular risk reduction. Cardiovasc Ther 31: 238–249, 2013.
28. Lovshin JA, Drucker DJ. Incretin-based therapies for type 2 diabetes mellitus. Nat Rev Endocrinol 5: 262–269, 2009.
29. Matthews C, Gorenne I, Scott S, Figg N, Kirkpatrick P, Ritchie A, Goddard M, Bennett M. Vascular smooth muscle cells undergo telomere- based senescence in human atherosclerosis: effects of telomerase and oxidative stress. Circ Res 99: 156–164, 2006.
30. Minamino T, Komuro I. Vascular aging: insights from studies on cellular senescence, stem cell aging, and progeroid syndromes. Nat Clin Pract Cardiovasc Med 5: 637–648, 2008.
31. Molnar P, Perrault R, Louis S, Zahradka P. The cyclic AMP response element-binding protein (CREB) mediates smooth muscle cell proliferation in response to angiotensin II. J Cell Commun Signal 8: 29–37, 2014.
32. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10: 549–557, 2004.
33. Niture SK, Khatri R, Jaiswal AK. Regulation of Nrf2-an update. Free Radic Biol Med 66: 36–44, 2014.
34. Noyan-Ashraf MH, Momen MA, Ban K, Sadi AM, Zhou YQ, Riazi AM, Baggio LL, Henkelman RM, Husain M, Drucker DJ. GLP-1R agonist liraglutide activates cytoprotective pathways and improves outcomes after experimental myocardial infarction in mice. Diabetes 58: 975–983, 2009.
35. Oeseburg H, de Boer RA, Buikema H, van der Harst P, van Gilst WH, Silljé HH. Glucagon-Like peptide 1 prevents reactive oxygen speciesinduced endothelial cell senescence through the activation of protein kinase A. Arterioscler Thromb Vasc Biol 30: 1407–1414, 2010.
36. Park SY, Son BG, Park YH, Kim CM, Park G, Choi YW. The neuroprotective effects of —iso-cubebene on dopaminergic cell death: involvement of CREB/Nrf2 signaling. Neurochem Res 39: 1759–1766, 2014.
37. Patel V, Joharapurkar A, Dhanesha N, Kshirsagar S, Detroja J, Patel K, Gandhi T, Patel K, Bahekar R, Jain M. Combination of omeprazole with GLP-1 agonist therapy improves insulin sensitivity and antioxidant activity in liver in type 1 diabetic mice. Pharmacol Rep 65: 927–936, 2013.
38. Puddu A, Sanguineti R, Durante A, Nencioni A, Mach F, Montecucco F, Viviani GL. Glucagon-like peptide-1 triggers protective pathways in pancreatic beta-cells exposed to glycated serum. Mediators Inflamm 2013: 317120, 2013.
39. Pujadas G, De Nigris V, La Sala L, Testa R, Genovese S, Ceriello A. The pivotal role of high glucose-induced overexpression of PKC˜ in the appearance of glucagon-like peptide-1 resistance in endothelial cells. Endocrine. In press.
40. Qin X, Wang X, Wang Y, Tang Z, Cui Q, Xi J, Chien S, Wang N. MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc Natl Acad Sci U S A 107: 3240–3244, 2010.
41. Queisser N, Oteiza PI, Link S, Hey V, Stopper H, Schupp N. Aldosterone activates transcription factor Nrf2 in kidney cells both in vitro and in vivo. Antioxid Redox Signal 21: 2126–2142, 2014.
42. Rodriguez-Brenes IA, Peskin CS. Quantitative theory of telomere length regulation and cellular senescence. Proc Natl Acad Sci U S A 107: 5387–5392, 2010.
43. Rose P, Bond J, Tighe S, Toth MJ, Wellman TL, Briso de Montiano EM, Lewinter MM, Lounsbury KM. Genes overexpressed in cerebral arteries following salt-induced hypertensive disease are regulated by angiotensin II, JunB, and CREB. Am J Physiol Heart Circ Physiol 294: H1075–H1085, 2008.
44. Serrano AL, Andres V. Telomeres and cardiovascular disease: does size matter? Circ Res 94: 575–584, 2004.
45. Shanmugam P, Valente AJ, Prabhu SD, Venkatesan B, Yoshida T, Delafontaine P, Chandrasekar B. Angiotensin-II type 1 receptor and NOX2 mediate TCF/LEF and CREB dependent WISP1 induction and cardiomyocyte hypertrophy. J Mol Cell Cardiol 50: 928–938, 2011.
46. Suh JH, Shenvi SV, Dixon BM, Liu H, Jaiswal AK, Liu RM, Hagen TM. Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proc Natl Acad Sci U S A 101: 3381–3386, 2004a.
47. Sun Z, Chin YE, Zhang DD. Acetylation of Nrf2 by p300/CBP augments promoter-specific DNA binding of Nrf2 during the antioxidant response. Mol Cell Biol 29: 2658–2672, 2009.
48. Ungvari Z, Bailey-Downs L, Sosnowska D, Gautam T, Koncz P, Losonczy G, Ballabh P, de Cabo R, Sonntag WE, Csiszar A. Vascular oxidative stress in aging: a homeostatic failure due to dysregulation of NRF2-mediated antioxidant response. Am J Physiol Heart Circ Physiol 301: H363–H372, 2011.
49. Wang CY, Wang ZY, Xie JW, Wang T, Wang X, Xu Y, Cai JH. Dl-3-n-butylphthalide-induced upregulation of antioxidant defense is involved in the enhancement of cross talk between CREB and Nrf2 in an Alzheimer’s disease mouse model. Neurobiol Aging 38: 32–46, 2016.
50. Wang D, Luo P, Wang Y, Li W, Wang C, Sun D, Zhang R, Su T, Ma X, Zeng C, Wang H, Ren J, Cao F. Glucagon-like peptide-1 protects against cardiac microvascular injury in diabetes via a cAMP/PKA/Rhodependent mechanism. Diabetes 62: 1697–1708, 2013.
51. Willeit P, Willeit J, Brandstter A, Ehrlenbach S, Mayr A, Gasperi A, Weger S, Oberhollenzer F, Reindl M, Kronenberg F, Kiechl S. Cellular aging reflected by leukocyte telomere length predicts advanced atherosclerosis and cardiovascular disease risk. Arterioscler Thromb Vasc Biol 30: 1649–1656, 2010.
52. Woo JS, Kim W, Ha SJ, Kim JB, Kim SJ, Kim WS, Seon HJ, Kim KS. Cardioprotective effects of exenatide in patients with ST-segment-elevation myocardial infarction undergoing primary percutaneous coronary intervention: results of exenatide myocardial protection in revascularization study. Arterioscler Thromb Vasc Biol 33: 2252–2260, 2013.
53. Wu L, Noyan Ashraf MH, Facci M, Wang R, Paterson PG, Ferrie A, Juurlink BH. Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system. Proc Natl Acad Sci U S A 101: 7094–7099, 2004.
54. Zhao L, Li AQ, Zhou TF, Zhang MQ, Qin XM. Exendin-4 alleviates angiotensin II-induced senescence in vascular smooth muscle cells by inhibiting Rac1 activation via a cAMP/PKA-dependent pathway. Am J Physiol Cell Physiol 307: C1130–C1141, 2014.
55. Ziady AG, Sokolow A, Shank S, Corey D, Myers R, Plafker S, Kelley TJ. Interaction with CREB binding protein modulates the activities of Nrf2 and NF-_B in cystic fibrosis airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 302: L1221–L1231, 2012.
56. Younce CW, Burmeister MA, Ayala JE. Exendin-4 attenuates high glucose-induced cardiomyocyte apoptosis via inhibition of endoplasmic reticulum stress and activation of SERCA2a. Am J Physiol Cell Physiol 304: C508–C518, 2013.