Prevention of age-related endothelial dysfunction by habitual aerobic exercise in healthy humans: Possible role of nuclear factor κB

Clinical Science

Volumn 127, Issue 11, 2014, Pages 645-654

  Walker, Ashley E ^a   Kaplon, Rachelle E ^a   Pierce, Gary L ^a   Nowlan, Molly J ^a   Seals, Douglas R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Aging; Endothelium dependent dilation (EDD); Exercise; Flow mediated dilation (FMD); Nuclear factor B (NF B); Oxidative stress

Indexed keywords

3 NITROTYROSINE; ASCORBIC ACID; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SALSALATE; TRIACYLGLYCEROL;

ADULT; AEROBIC EXERCISE; AGED; ARTICLE; BODY FAT; BRACHIAL ARTERY; CHOLESTEROL BLOOD LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DRUG BLOOD LEVEL; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; EVENING DOSAGE; FEMALE; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN EXPERIMENT; MALE; MORNING DOSAGE; NORMAL HUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESTING HEART RATE; SIGNAL TRANSDUCTION; SYSTOLIC BLOOD PRESSURE; TRIACYLGLYCEROL BLOOD LEVEL; VASODILATATION; WAIST HIP RATIO; X RAY SYSTEM;

ADULT; AGE FACTORS; AGED; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BRACHIAL ARTERY; ENDOTHELIUM; EXERCISE; FEMALE; HABITS; HUMANS; MALE; MIDDLE AGED; NF-KAPPA B; REGIONAL BLOOD FLOW; SALICYLATES; SEDENTARY LIFESTYLE; SIGNAL TRANSDUCTION; TYROSINE; VASODILATION;

EID: 84905899086     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20140030     Document Type: Article

References (39)

1. Rossi, R., Nuzzo, A., Origliani, G. and Modena, M. G. (2008) Prognostic role of flow-mediated dilation and cardiac risk factors in post-menopausal women. J. Am. Coll. Cardiol. 51, 997-1002
2. Yeboah, J., Crouse, J. R., Hsu, F. C., Burke, G. L. and Herrington, D. M. (2007) Brachial flow-mediated dilation predicts incident cardiovascular events in older adults: the cardiovascular health study. Circulation 115, 2390-2397
3. Yeboah, J., Folsom, A. R., Burke, G. L., Johnson, C., Polak, J. F., Post, W., Lima, J. A., Crouse, J. R. and Herrington, D. M. (2009) Predictive value of brachial flow-mediated dilation for incident cardiovascular events in a population-based study: the multi-ethnic study of atherosclerosis. Circulation 120, 502-509
4. Celermajer, D. S., Sorensen, K. E., Spiegelhalter, D. J., Georgakopoulos, D., Robinson, J. and Deanfield, J. E. (1994) Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J. Am. Coll. Cardiol. 24, 471-476
5. Eskurza, I., Monahan, K., Robinson, J. and Seals, D. (2004) Effect of acute and chronic ascorbic acid augmentation on flow-mediated dilation with physically active and sedentary aging. J. Physiol. 556, 215-224 CrossRef
6. Rinder, M. R., Spina, R. J. and Ehsani, A. A. (2000) Enhanced endothelium-dependent vasodilation in older endurance-trained men. J. Appl. Physiol. 88, 761-766
7. Pierce, G. L., Eskurza, I., Walker, A. E., Fay, T. N. and Seals, D. R. (2011) Sex-specific effects of habitual aerobic exercise on brachial artery flow-mediated dilation in middle-aged and older adults. Clin. Sci. 120, 13-23
8. Gielen, S., Walther, C., Schuler, G. and Hambrecht, R. (2005) Anti-inflammatory effects of physical exercise. A new mechanism to explain the benefits of cardiac rehabilitation? J. Cardiopulm. Rehabil. 25, 339-342
9. Bruunsgaard, H., Skinhoj, P., Pedersen, A. N., Schroll, M. and Pedersen, B. K. (2000) Ageing, tumour necrosis factor-a (TNF-a) and atherosclerosis. Clin. Exp. Immunol. 121, 255-260
10. Read, M. A., Whitley, M. Z., Williams, A. J. and Collins, T. (1994) NF-κB and IκBα: an inducible regulatory system in endothelial activation. J. Exp. Med. 179, 503-512
11. Donato, A. J., Black, A. D., Jablonski, K. L., Gano, L. B. and Seals, D. R. (2008) Aging is associated with greater nuclear NF-κB, reduced IκBα, and increased expression of proinflammatory cytokines in vascular endothelial cells of healthy humans. Aging Cell 7, 805-812
12. Donato, A. J., Eskurza, I., Silver, A. E., Levy, A. S., Pierce, G. L., Gates, P. E. and Seals, D. R. (2007) Direct evidence of endothelial oxidative stress with aging in humans: relation to impaired endothelium-dependent dilation and upregulation of nuclear factor-?B. Circ. Res. 100, 1659-1666
13. Pierce, G. L., Donato, A. J., LaRocca, T. J., Eskurza, I., Silver, A. E. and Seals, D. R. (2011) Habitually exercising older men do not demonstrate age-associated vascular endothelial oxidative stress. Aging Cell 10, 1032-1037
14. Kopp, E. and Ghosh, S. (1994) Inhibition of NF-κB by sodium salicylate and aspirin. Science 265, 956-959
15. Yin, M. J., Yamamoto, Y. and Gaynor, R. B. (1998) The anti-inflammatory agents aspirin and salicylate inhibit the activity of IκB kinase-β. Nature 396, 77-80
16. Pierce, G. L., Lesniewski, L. A., Lawson, B. R., Beske, S. D. and Seals, D. R. (2009) Nuclear factor-?B activation contributes to vascular endothelial dysfunction via oxidative stress in overweight/obese middle-aged and older humans. Circulation 119, 1284-1292
17. Lesniewski, L. A., Durrant, J. R., Connell, M. L., Folian, B. J., Donato, A. J. and Seals, D. R. (2011) Salicylate treatment improves age-associated vascular endothelial dysfunction: potential role of nuclear factor κB and forkhead Box O phosphorylation. J. Gerontol. A Biol. Sci. Med. Sci. 66, 409-418
18. Manea, A., Manea, S. A., Gafencu, A. V. and Raicu, M. (2007) Regulation of NADPH oxidase subunit p22(phox) by NF-κB in human aortic smooth muscle cells. Arch. Physiol. Biochem. 113, 163-172
19. Anrather, J., Racchumi, G. and Iadecola, C. (2006) NF-?B regulates phagocytic NADPH oxidase by inducing the expression of gp91phox. J. Biol. Chem. 281, 5657-5667
20. DeSouza, C. A., Shapiro, L. F., Clevenger, C. M., Dinenno, F. A., Monahan, K. D., Tanaka, H. and Seals, D. R. (2000) Regular aerobic exercise prevents and restores age-related declines in endothelium-dependent vasodilation in healthy men. Circulation 102, 1351-1357
21. Eskurza, I., Myerburgh, L. A., Kahn, Z. D. and Seals, D. R. (2005) Tetrahydrobiopterin augments endothelium-dependent dilatation in sedentary but not in habitually exercising older adults. J. Physiol. 568, 1057-1065
22. Donald, A. E., Halcox, J. P., Charakida, M., Storry, C., Wallace, S. M., Cole, T. J., Friberg, P. and Deanfield, J. E. (2008) Methodological approaches to optimize reproducibility and power in clinical studies of flow-mediated dilation. J. Am. Coll. Cardiol. 51, 1959-1964
23. Donato, A. J., Pierce, G. L., Lesniewski, L. A. and Seals, D. R. (2009) Role of NF?B in age-related vascular endothelial dysfunction in humans. Aging 1, 678-680
24. Silver, A. E., Christou, D. D., Donato, A. J., Beske, S. D., Moreau, K. L., Magerko, K. A. and Seals, D. R. (2010) Protein expression in vascular endothelial cells obtained from human peripheral arteries and veins. J. Vasc. Res. 47, 1-8
25. Hawley, S. A., Fullerton, M. D., Ross, F. A., Schertzer, J. D., Chevtzoff, C., Walker, K. J., Peggie, M. W., Zibrova, D., Green, K. A., Mustard, K. J. et al. (2012) The ancient drug salicylate directly activates AMP-activated protein kinase. Science 336, 918-922
26. Jung, T. W., Choi, H. Y., Lee, S. Y., Hong, H. C., Yang, S. J., Yoo, H. J., Youn, B. S., Baik, S. H. and Choi, K. M. (2013) Salsalate and adiponectin improve palmitate-induced insulin resistance via inhibition of selenoprotein P through the AMPK-FOXO1a pathway. PLoS ONE 8, e66529
27. Krabbe, K. S., Pedersen, M. and Bruunsgaard, H. (2004) Inflammatory mediators in the elderly. Exp. Gerontol. 39, 687-699
28. Hasegawa, Y., Saito, T., Ogihara, T., Ishigaki, Y., Yamada, T., Imai, J., Uno, K., Gao, J., Kaneko, K., Shimosawa, T. et al. (2012) Blockade of the nuclear factor-?B pathway in the endothelium prevents insulin resistance and prolongs life spans. Circulation 125, 1122-1133
29. Rywik, T. M., Blackman, M. R., Yataco, A. R., Vaitkevicius, P. V., Zink, R. C., Cottrell, E. H., Wright, J. G., Katzel, L. I. and Fleg, J. L. (1999) Enhanced endothelial vasoreactivity in endurancetrained older men. J. Appl. Physiol. 87, 2136-2142
30. Goldfine, A. B., Buck, J. S., Desouza, C., Fonseca, V., Chen, Y. D., Shoelson, S. E., Jablonski, K. A. and Creager, M. A. (2013) Targeting inflammation using salsalate in patients with type 2 diabetes: effects on flow-mediated dilation (TINSAL-FMD). Diabetes Care 36, 4132-4139
31. Gupta, S. K., Johnson, R. M., Saha, C., Mather, K. J., Greenwald, M. L., Waltz, J. S., Rehman, J. and Dube, M. P. (2008) Improvement in HIV-related endothelial dysfunction using the anti-inflammatory agent salsalate: a pilot study. AIDS 22, 653-655
32. Goldfine, A. B., Fonseca, V., Jablonski, K. A., Chen, Y. D., Tipton, L., Staten, M. A. and Shoelson, S. E. (2013) Salicylate (salsalate) in patients with type 2 diabetes: a randomized trial. Ann. Intern. Med. 159, 1-12
33. Walker, A. E., Eskurza, I., Pierce, G. L., Gates, P. E. and Seals, D. R. (2009) Modulation of vascular endothelial function by low-density lipoprotein cholesterol with aging: influence of habitual exercise. Am. J. Hypertens. 22, 250-256
34. Taddei, S., Virdis, A., Ghiadoni, L., Salvetti, G., Bernini, G., Magagna, A. and Salvetti, A. (2001) Age-related reduction of NO availability and oxidative stress in humans. Hypertension 38, 274-279
35. Lassegue, B. and Griendling, K. K. (2010) NADPH oxidases: functions and pathologies in the vasculature. Arterioscler. Thromb. Vasc. Biol. 30, 653-661
36. Durrant, J. R., Seals, D. R., Connell, M. L., Russell, M. J., Lawson, B. R., Folian, B. J., Donato, A. J. and Lesniewski, L. A. (2009) 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. 587, 3271-3285
37. Tabit, C. E., Holbrook, M., Shenouda, S. M., Dohadwala, M. M., Widlansky, M. E., Frame, A. A., Kim, B. H., Duess, M. A., Kluge, M. A., Levit, A. et al. (2012) Effect of sulfasalazine on inflammation and endothelial function in patients with established coronary artery disease. Vasc. Med. 17, 101-107
38. Wu, K. K. (2000) Aspirin and salicylate: an old remedy with a new twist. Circulation 102, 2022-2023
39. Awtry, E. H. and Loscalzo, J. (2000) Aspirin. Circulation 101, 1206-1218