Salicylate treatment improves age-associated vascular endothelial dysfunction: Potential role of nuclear factor κb and forkhead box o phosphorylation

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 66 A, Issue 4, 2011, Pages 409-418

  Lesniewski, Lisa A ^a   Durrant, Jessica R ^a   Connell, Melanie L ^a   Folian, Brian J ^a   Donate, Anthony J ^a   Seals, Douglas R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

EDD; NADPH oxidase; SOD

Indexed keywords

MUS;

3 NITROTYROSINE; 3-NITROTYROSINE; CYTOKINE; DRUG DERIVATIVE; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, MOUSE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NONSTEROID ANTIINFLAMMATORY AGENT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SALICYLIC ACID DERIVATIVE; SUPEROXIDE DISMUTASE; TYROSINE;

AGING; ANIMAL; AORTA; ARTICLE; BIOSYNTHESIS; DRUG ANTAGONISM; DRUG EFFECT; MALE; METABOLISM; MOUSE; OXIDATIVE STRESS; PHOSPHORYLATION; PHYSIOLOGY; VASCULAR ENDOTHELIUM; VASODILATATION;

AGING; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; AORTA; CYTOKINES; ENDOTHELIUM, VASCULAR; FORKHEAD TRANSCRIPTION FACTORS; I-KAPPA B KINASE; MALE; MICE; NADPH OXIDASE; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS; PHOSPHORYLATION; SALICYLATES; SUPEROXIDE DISMUTASE; TYROSINE; VASODILATION;

EID: 79957794634     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glq233     Document Type: Article

References (54)

1. Lakatta E, Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: part I: aging arteries: a "set up" for vascular disease. Circulation. 2003;107:139-146. (Pubitemid 36070946)
2. Delp MD, Brown M, Laughlin MH, Hasser EM. Rat aortic vasoreac-tivity is altered by old age and hindlimb unloading. J Appl Physiol. 1995;78:2079-2086.
3. Taddei S, Virdis A, Ghiadoni L, et al. Menopause is associated with endothelial dysfunction in women. Hypertension. 1996;28:576-582. (Pubitemid 26327952)
4. Koga T, Takata Y, Kobayashi K, Takishita S, Yamashita Y, Fujishima M. Ageing suppresses endothelium-dependent relaxation and generates contraction mediated by the muscarinic receptors in vascular smooth muscle of normotensive Wistar-Kyoto and spontaneously hypertensive rats. J Hypertens Suppl. 1988;6:S243-S245. (Pubitemid 19067449)
5. Lesniewski LA, Connell ML, Durrant JR, et al. B6D2F1 Mice are a suitable model of oxidative stress-mediated impaired endothelium-dependent dilation with aging. J Gerontol A Biol Sci Med Sci. 2009;64:9-20.
6. Luscher TF, Barton M. Biology of the endothelium. Clin Cardiol. 1997;20(suppl 2):II-3-10.
7. Csiszar A, Ungvari Z, Edwards JG, et al. Aging-induced phenotypic changes and oxidative stress impair coronary arteriolar function. Circ Res. 2002;90:1159-1166. (Pubitemid 34786900)
8. Donato AJ, Eskurza I, Silver AE, et al. Direct evidence of endothelial oxidative stress with aging in humans: relation to impaired endothe-lium- dependent dilation and upregulation of nuclear factor-kappaB. Circ Res. 2007;100:1659-1666. (Pubitemid 46897269)
9. Ballou SP, Lozanski FB, Hodder S, et al. Quantitative and qualitative alterations of acute-phase proteins in healthy elderly persons. Age Ageing. 1996;25:224-230. (Pubitemid 26152041)
10. Bruunsgaard H, Pedersen M, Pedersen BK. Aging and proinflamma-tory cytokines. Curr Opin Hematol. 2001;8:131-136.
11. Donato AJ, Black AD, Jablonski KL, Gano LB, Seals DR. Aging is associated with greater nuclear NFkappaB, reduced IkappaBalpha, and increased expression of proinflammatory cytokines in vascular endothelial cells of healthy humans. Aging Cell. 2008;7:805-812. (Pubitemid 352749435)
12. Csiszar A, Ungvari Z, Koller A, Edwards JG, Kaley G. Proinflamma-tory phenotype of coronary arteries promotes endothelial apoptosis in aging. Physiol Genomics. 2004;17:21-30. (Pubitemid 38924147)
13. Ungvari Z, Orosz Z, Labinskyy N, et al. Increased mitochondrial H2O2 production promotes endothelial NF-kappaB activation in aged rat arteries. Am J Physiol Heart Circ Physiol. 2007;293:H37-H47. (Pubitemid 47108162)
14. Zou Y, Yoon S, Jung KJ, et al. Upregulation of aortic adhesion molecules during aging. J Gerontol A Biol Sci Med Sci. 2006;61:232-244.
15. Vila E, Salaices M. Cytokines and vascular reactivity in resistance arteries. Am J Physiol Heart Circ Physiol. 2005;288:H1016-H1021. (Pubitemid 40270001)
16. Delhalle S, Blasius R, Dicato M, Diederich M. A beginner's guide to NF-kappaB signaling pathways. Ann N Y Acad Sci. 2004;1030:1-13. (Pubitemid 40378891)
17. Karin M. The beginning of the end: IkappaB kinase (IKK) and NF-kappaB activation. J Biol Chem. 1999;274:27339-27342.
18. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene. 1999;18:6853-6866.
19. Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol. 2004;24:816-823. (Pubitemid 38620857)
20. Manea A, Manea SA, Gafencu AV, Raicu M. Regulation of NADPH oxidase subunit p22(phox) by NF-kB in human aortic smooth muscle cells. Arch Physiol Biochem. 2007;113:163-172.
21. Anrather J, Racchumi G, Iadecola C. NF-kappaB regulates phagocytic NADPH oxidase by inducing the expression of gp91phox. J Biol Chem. 2006;281:5657-5667. (Pubitemid 43847663)
22. Papanicolaou KN, Izumiya Y, Walsh K. Forkhead transcription factors and cardiovascular biology. Circ Res. 2008;102:16-31.
23. Weitzel RP, Lesniewski ML, Haviernik P, et al. microRNA 184 regulates expression of NFAT1 in umbilical cord blood CD4+ T cells. Blood. 2009;113:6648-6657.
24. Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci. 2007;120(Pt 15):2479-2487. (Pubitemid 47323857)
25. Salminen A, Ojala J, Huuskonen J, Kauppinen A, Suuronen T, Kaarniranta K. Interaction of aging-associated signaling cascades: inhibition of NF-kappaB signaling by longevity factors FoxOs and SIRT1. Cell Mol Life Sci. 2008;65:1049-1058.
26. Cronstein BN, Montesinos MC, Weissmann G. Salicylates and sul-fasalazine, but not glucocorticoids, inhibit leukocyte accumulation by an adenosine-dependent mechanism that is independent of inhibition of prostaglandin synthesis and p105 of NFkappaB. Proc Natl Acad Sci U S A. 1999;96:6377-6381. (Pubitemid 29256673)
27. Yin MJ, Yamamoto Y, Gaynor RB. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta. Nature. 1998;396:77-80. (Pubitemid 28520452)
28. Pierce JW, Read MA, Ding H, Luscinskas FW, Collins T. Salicylates inhibit I kappa B-alpha phosphorylation, endothelial-leukocyte adhesion molecule expression, and neutrophil transmigration. J Immunol. 1996;156:3961-3969. (Pubitemid 26137683)
29. Kopp E, Ghosh S. Inhibition of NF-kappa B by sodium salicylate and aspirin. Science. 1994;265:956-959.
30. Wu KK. Aspirin and salicylate: an old remedy with a new twist. Circulation. 2000;102:2022-2023.
31. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest. 2006;116:1793-1801. (Pubitemid 44033299)
32. Awtry EH, Loscalzo J. Aspirin. Circulation. 2000;101:1206-1218.
33. Pierce GL, Lesniewski LA, Lawson BR, Beske SD, Seals DR. Nuclear factor-{kappa}B activation contributes to vascular endothelial dysfunction via oxidative stress in overweight/obese middle-aged and older humans. Circulation. 2009;119:1284-1292.
34. Durrant JR, Seals DR, Connell ML, et al. Voluntary wheel running restores endothelial function in conduit arteries of old mice: direct evidence for reduced oxidative stress, increased superoxide dismutase activity and down-regulation of NADPH oxidase. J Physiol. 2009; 587(Pt 13):3271-3285.
35. Didion SP, Ryan MJ, Baumbach GL, Sigmund CD, Faraci FM. Superoxide contributes to vascular dysfunction in mice that express human renin and angiotensinogen. Am J Physiol Heart Circ Physiol. 2002;283: H1569-H1576.
36. d'Uscio LV, Smith LA, Santhanam AV, Richardson D, Nath KA, Katusic ZS. Essential role of endothelial nitric oxide synthase in vascular effects of erythropoietin. Hypertension. 2007;49:1142-1148. (Pubitemid 351664320)
37. Reiter CD, Teng RJ, Beckman JS. Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite. J Biol Chem. 2000;275:32460-32466.
38. van den Berg R, Haenen GR, van den Berg H, Bast A. Transcription factor NF-kappaB as a potential biomarker for oxidative stress. Br J Nutr. 2001;86(suppl 1):S121-S12-7.
39. Donato AJ, Gano LB, Eskurza I, et al. Vascular endothelial dysfunction with aging: endothelin-1 and endothelial nitric oxide synthase. Am J Physiol Heart Circ Physiol. 2009;297:H425-H432.
40. Torella D, Leosco D, Indolfi C, et al. Aging exacerbates negative remodeling and impairs endothelial regeneration after balloon injury. Am J Physiol Heart Circ Physiol. 2004;287:H2850-H2860.
41. Csiszar A, Ungvari Z, Koller A, Edwards JG, Kaley G. Aging-induced proinflammatory shift in cytokine expression profile in coronary arteries. Faseb J. 2003;17:1183-1185.
42. Belmin J, Bernard C, Corman B, Merval R, Esposito B, Tedgui A. Increased production of tumor necrosis factor and interleukin-6 by arterial wall of aged rats. Am J Physiol. 1995;268(Pt 2):H2288-H2293.
43. Lernbecher T, Muller U, Wirth T. Distinct NF-kappa B/Rel transcription factors are responsible for tissue-specific and inducible gene activation. Nature. 1993;365:767-770. (Pubitemid 23339886)
44. Frey RS, Rahman A, Kefer JC, Minshall RD, Malik AB. PKCzeta regulates TNF-alpha-induced activation of NADPH oxidase in endo-thelial cells. Circ Res. 2002;90:1012-1019. (Pubitemid 34633868)
45. Brunet A, Sweeney LB, Sturgill JF, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004;303:2011-2015.
46. Yamakura F, Taka H, Fujimura T, Murayama K. Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosine. J Biol Chem. 1998;273: 14085-14089.
47. Strong R, Miller RA, Astle CM, et al. Nordihydroguaiaretic acid and aspirin increase lifespan of genetically heterogeneous male mice. Aging Cell. 2008;7:641-650.
48. Arranz L, Caamano JH, Lord JM, De la Fuente M. Preserved immune functions and controlled leukocyte oxidative stress in naturally long-lived mice: possible role of nuclear factor kappa B. J Gerontol A Biol Sci Med Sci. 2010;65:941-950.
49. Buford TW, Cooke MB, Manini TM, Leeuwenburgh C, Willoughby DS. Effects of age and sedentary lifestyle on skeletal muscle NF-kappaB signaling in men. J Gerontol A Biol Sci Med Sci. 2010; 65:532-537.
50. Massie HR, Williams TR, Iodice AA. Influence of anti-inflammatory agents on the survival of Drosophila. J Gerontol. 1985;40:257-260. (Pubitemid 15010343)
51. Flurkey K, Astle CM, Harrison DE. Life extension by diet restriction and N-acetyl-L-cysteine in genetically heterogeneous mice. J Geron-tol A Biol Sci Med Sci. 2010;6:1275-1284.
52. Zollei I, Szabo A, Kaszaki J, Tiszlavicz L, Ghyczy M, Boros M. Betaine-palmitate reduces acetylsalicylic acid-induced gastric damage in rats. Scand J Gastroenterol. 2001;36:811-816. (Pubitemid 32656555)
53. Mitchell JA, Akarasereenont P, Thiemermann C, Flower RJ, Vane JR. Selectivity of nonsteroidal antiinflammatory drugs as inhibitors of constitutive and inducible cyclooxygenase. Proc Natl Acad Sci U S A. 1993;90:11693-11697.
54. Pierce JW, Schoenleber R, Jesmok G, et al. Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem. 1997;272:21096-21103. (Pubitemid 27373968)