Deletion of the activated protein-1 transcription factor JunD induces oxidative stress and accelerates age-related endothelial dysfunction

Circulation

Volumn 127, Issue 11, 2013, Pages 1229-1240

  Paneni, Francesco ^a,b   Osto, Elena ^a   Costantino, Sarah ^a,c   Mateescu, Bogdan ^d   Briand, Sylvie ^a   Coppolino, Giuseppe ^a   Perna, Enrico ^e   Mocharla, Pavani ^a   Akhmedov, Alexander ^a   Kubant, Ruslan ^f   Rohrer, Lucia ^g   Malinski, Tadeusz ^f   Camici, Giovanni G ^a   Matter, Christian M ^a   Mechta Grigoriou, Fatima ^d   Volpe, Massimo ^b,e   Lüscher, Thomas F ^a   Cosentino, Francesco ^a,e  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b IRCCS NEUROMED   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d INSTITUT CURIE   (France)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f OHIO UNIVERSITY   (United States)

^g UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Aging; Endothelial dysfunction; Oxidative stress; Vascular biology

Indexed keywords

ALDEHYDE DEHYDROGENASE ISOENZYME 2; BETA GALACTOSIDASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MANGANESE; NITRIC OXIDE; PROTEIN P16; PROTEIN P47; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SUPEROXIDE DISMUTASE; TELOMERASE; TRANSCRIPTION FACTOR JUND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; UPREGULATION; VASODILATATION;

AGING; ANIMALS; ENDOTHELIUM, VASCULAR; GENE DELETION; HOMEOSTASIS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MODELS, ANIMAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-JUN; REACTIVE OXYGEN SPECIES;

EID: 84875220397     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.112.000826     Document Type: Article

References (46)

1. Sawabe M. Vascular aging: from molecular mechanism to clinical significance. Geriatr Gerontol Int. 2010; (suppl 1):S213-S220.
2. Dai DF, Rabinovitch PS, Ungvari Z. Mitochondria and cardiovascular aging. Circ Res. 2012;110:1109-1124.
3. Cosentino F, Francia P, Camici GG, Pelicci PG, Lüscher TF, Volpe M. Final common molecular pathways of aging and cardiovascular disease: role of the p66Shc protein. Arterioscler Thromb Vasc Biol. 2008;28:622-628.
4. Chen K, Keaney JF Jr. Evolving concepts of oxidative stress and reactive oxygen species in cardiovascular disease. Curr Atheroscler Rep. 2012;14:476-483.
5. van der Loo B, Labugger R, Skepper JN, Bachschmid M, Kilo J, Powell JM, Palacios-Callender M, Erusalimsky JD, Quaschning T, Malinski T, Gygi D, Ullrich V, Lüscher TF. Enhanced peroxynitrite formation is associated with vascular aging. J Exp Med. 2000;192:1731-1744.
6. Cosentino F, Lüscher TF. Tetrahydrobiopterin and endothelial nitric oxide synthase activity. Cardiovasc Res. 1999;43:274-278.
7. Toda N. Age-related changes in endothelial function and blood flow regulation. Pharmacol Ther. 2012;133:159-176.
8. Epstein SE, Lassance-Soares RM, Faber JE, Burnett MS. Effects of aging on the collateral circulation, and therapeutic implications. Circulation. 2012;125:3211-3219.
9. Camici GG, Sudano I, Noll G, Tanner FC, Lüscher TF. Molecular pathways of aging and hypertension. Curr Opin Nephrol Hypertens. 2009;18:134-137.
10. Labunskyy VM, Gladyshev VN. Role of reactive oxygen species-mediated signaling in aging [published online ahead of print September 20, 2012]. Antioxid Redox Signal. doi:10.1089/ars.2012.4891.
11. Hai T, Curran T. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci U S A. 1991;88:3720-3724.
12. Persengiev SP, Green MR. The role of ATF/CREB family members in cell growth, survival and apoptosis. Apoptosis. 2003;8:225-228.
13. Mechta-Grigoriou F, Gerald D, Yaniv M. The mammalian Jun proteins: redundancy and specificity. Oncogene. 2001;20:2378-2389.
14. Thépot D, Weitzman JB, Barra J, Segretain D, Stinnakre MG, Babinet C, Yaniv M. Targeted disruption of the murine junD gene results in multiple defects in male reproductive function. Development. 2000;127:143-153.
15. Laurent G, Solari F, Mateescu B, Karaca M, Castel J, Bourachot B, Magnan C, Billaud M, Mechta-Grigoriou F. Oxidative stress contributes to aging by enhancing pancreatic angiogenesis and insulin signaling. Cell Metab. 2008;7:113-124.
16. Toullec A, Gerald D, Despouy G, Bourachot B, Cardon M, Lefort S, Richardson M, Rigaill G, Parrini MC, Lucchesi C, Bellanger D, Stern MH, Dubois T, Sastre-Garau X, Delattre O, Vincent-Salomon A, Mechta-Grigoriou F. Oxidative stress promotes myofibroblast differentiation and tumour spreading. EMBO Mol Med. 2010;2:211-230.
17. Gerald D, Berra E, Frapart YM, Chan DA, Giaccia AJ, Mansuy D, Pouysségur J, Yaniv M, Mechta-Grigoriou F. JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell. 2004;118:781-794.
18. Zhou H, Gao J, Lu ZY, Lu L, Dai W, Xu M. Role of c-Fos/JunD in protecting stress-induced cell death. Cell Prolif. 2007;40:431-444.
19. Paneni F, Mocharla P, Akhmedov A, Costantino S, Osto E, Volpe M, Lüscher TF, Cosentino F. Gene silencing of the mitochondrial adaptor p66(Shc) suppresses vascular hyperglycemic memory in diabetes. Circ Res. 2012;111:278-289.
20. Erdei N, Tóth A, Pásztor ET, Papp Z, Edes I, Koller A, Bagi Z. High-fat diet-induced reduction in nitric oxide-dependent arteriolar dilation in rats: role of xanthine oxidase-derived superoxide anion. Am J Physiol Heart Circ Physiol. 2006;291:H2107-H2115.
21. Malinski T, Taha Z. Nitric oxide release from a single cell measured in situ by a porphyrinic-based microsensor. Nature. 1992;358:676-678.
22. Borillo GA, Mason M, Quijada P, Völkers M, Cottage C, McGregor M, Din S, Fischer K, Gude N, Avitabile D, Barlow S, Alvarez R, Truffa S, Whittaker R, Glassy MS, Gustafsson AB, Miyamoto S, Glembotski CC, Gottlieb RA, Brown JH, Sussman MA. Pim-1 kinase protects mitochondrial integrity in cardiomyocytes. Circ Res. 2010;106:1265-1274.
23. Santos JH, Mandavilli BS, Van Houten B. Measuring oxidative mtDNA damage and repair using quantitative PCR. Methods Mol Biol. 2002;197:159-176.
24. Kajstura J, Bai Y, Cappetta D, Kim J, Arranto C, Sanada F, D'Amario D, Matsuda A, Bardelli S, Ferreira-Martins J, Hosoda T, Leri A, Rota M, Loscalzo J, Anversa P. Tracking chromatid segregation to identify human cardiac stem cells that regenerate extensively the infarcted myocardium. Circ Res. 2012;111:894-906.
25. Sorrentino SA, Bahlmann FH, Besler C, Müller M, Schulz S, Kirchhoff N, Doerries C, Horváth T, Limbourg A, Limbourg F, Fliser D, Haller H, Drexler H, Landmesser U. Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: restoration by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. Circulation. 2007;116:163-173.
26. Hernandez JM, Floyd DH, Weilbaecher KN, Green PL, Boris-Lawrie K. Multiple facets of junD gene expression are atypical among AP-1 family members. Oncogene. 2008;27:4757-4767.
27. Jochum W, Passegué E, Wagner EF. AP-1 in mouse development and tumorigenesis. Oncogene. 2001;20:2401-2412.
28. Wenzel P, Schuhmacher S, Kienhöfer J, Müller J, Hortmann M, Oelze M, Schulz E, Treiber N, Kawamoto T, Scharffetter-Kochanek K, Münzel T, Bürkle A, Bachschmid MM, Daiber A. Manganese superoxide dismutase and aldehyde dehydrogenase deficiency increase mitochondrial oxidative stress and aggravate age-dependent vascular dysfunction. Cardiovasc Res. 2008;80:280-289.
29. Chen CH, Budas GR, Churchill EN, Disatnik MH, Hurley TD, Mochly-Rosen D. Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science. 2008;321:1493-1495.
30. Koda K, Salazar-Rodriguez M, Corti F, Chan NY, Estephan R, Silver RB, Mochly-Rosen D, Levi R. Aldehyde dehydrogenase activation prevents reperfusion arrhythmias by inhibiting local renin release from cardiac mast cells. Circulation. 2010;122:771-781.
31. Venugopal R, Jaiswal AK. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene. 1998;17:3145-3156.
32. Srinivasan S, Hatley ME, Bolick DT, Palmer LA, Edelstein D, Brownlee M, Hedrick CC. Hyperglycaemia-induced superoxide production decreases eNOS expression via AP-1 activation in aortic endothelial cells. Diabetologia. 2004;47:1727-1734.
33. Ladurner A, Schmitt CA, Schachner D, Atanasov AG, Werner ER, Dirsch VM, Heiss EH. Ascorbate stimulates endothelial nitric oxide synthase enzyme activity by rapid modulation of its phosphorylation status. Free Radic Biol Med. 2012;52:2082-2090.
34. Kovacic JC, Moreno P, Nabel EG, Hachinski V, Fuster V. Cellular senescence, vascular disease, and aging: part 2 of a 2-part review: clinical vascular disease in the elderly. Circulation. 2011;123:1900-1910.
35. Touyz RM, Montezano AC. Vascular Nox4: a multifarious NADPH oxidase. Circ Res. 2012;110:1159-1161.
36. Weyemi U, Lagente-Chevallier O, Boufraqech M, Prenois F, Courtin F, Caillou B, Talbot M, Dardalhon M, Al Ghuzlan A, Bidart JM, Schlumberger M, Dupuy C. ROS-generating NADPH oxidase NOX4 is a critical mediator in oncogenic H-Ras-induced DNA damage and subsequent senescence. Oncogene. 2012;31:1117-1129.
37. Lener B, Kozieł R, Pircher H, Hütter E, Greussing R, Herndler-Brandstet-ter D, Hermann M, Unterluggauer H, Jansen-Dürr P. The NADPH oxidase Nox4 restricts the replicative lifespan of human endothelial cells. Biochem J. 2009;423:363-374.
38. Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res. 2010;106:1253-1264.
39. Craige SM, Chen K, Pei Y, Li C, Huang X, Chen C, Shibata R, Sato K, Walsh K, Keaney JF Jr. NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation. 2011;124:731-740.
40. Schröder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, Kruse C, Luedike P, Michaelis UR, Weissmann N, Dimmeler S, Shah AM, Brandes RP. Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ Res. 2012;110:1217-1225.
41. Francia P, Schiavoni M, Gatti CD, Bachschmid M, Savoia C, Volpe M, Luscher TF, Cosentino F. Deletion of p66shc gene protects against agerelated endothelial dysfunction. Circulation. 2004;108:254-254.
42. Handy DE, Castro R, Loscalzo J. Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation. 2011;123: 2145-2156.
43. Huang J, Gurung B, Wan B, Matkar S, Veniaminova NA, Wan K, Merchant JL, Hua X, Lei M. The same pocket in menin binds both MLL and JUND but has opposite effects on transcription. Nature. 2012;482:542-546.
44. Taddei S, Virdis A, Ghiadoni L, Salvetti G, Bernini G, Magagna A, Salvetti A. Age-related reduction of NO availability and oxidative stress in humans. Hypertension. 2001;38:274-279.
45. Wray DW, Nishiyama SK, Harris RA, Zhao J, McDaniel J, Fjeldstad AS, Witman MA, Ives SJ, Barrett-O'Keefe Z, Richardson RS. Acute reversal of endothelial dysfunction in the elderly after antioxidant consumption. Hypertension. 2012;59:818-824.
46. Ghiadoni L, Faita F, Salvetti M, Cordiano C, Biggi A, Puato M, Di Monaco A, De Siati L, Volpe M, Ambrosio G, Gemignani V, Muiesan ML, Taddei S, Lanza GA, Cosentino F. Assessment of flow-mediated dilation reproducibility: a nationwide multicenter study. J Hypertens. 2012;30:1399-1405.