EXERCISE AND THE AGEING IMMUNE SYSTEM

Authors

  • Nina Mohorko University of Primorska, Faculty of Health Sciences
  • Ana Petelin University of Primorska, Faculty of Health Sciences

Abstract

Life expectancy in the developed world has increased exponentially over the last century. There is now a strong body of evidence demonstrating that aging is accompanied by severe alterations in the immune system, a process known as “immunosenescence”, commonly defined as the functional decline of the adaptive immune system with age. Inflamm-aging, a chronic progressive increase in the inflammatory status has attracted great attention in recent years in age-related research field. This process plays an important role in the age-related diseases, such as heart disease, atherosclerosis, Alzheimer’s disease, type II diabetes, among others. Exercise impacts immune function both acutely and chronically. This article describes how exercise activates the release of hormones, myokines and cytokines, as well as modulates the expression of various immune-reactive molecules, which all contribute to anti-inflammatory effects and possible attenuation of immunosenescence.

References

Arnold, C. R., Wolf, J., Brunner, S., Herndler-Brandstetter, D., & Grubeck-Loebenstein, B. (2011). Gain and loss of T cell subsets in old age--age-related reshaping of the T cell repertoire. Journal of Clinical Immunology, 31(2), 137-146. doi 10.1007/s10875-010-9499-x.

Brown, B. M., Peiffer, J. J., Taddei, K., Lui, J. K., Laws, S. M., Gupta, V. B., … Martins, R. N. (2013). Physical activity and amyloid-β plasma and brain levels: results from the Australian Imaging, Biomarkers and Lifestyle Study of Ageing. Molecular Psychiatry, 18(8), 875-881. doi:10.1038/mp.2012.107.

Bruunsgaard, H. (2006). The clinical impact of systemic low-level inflammation in elderly populations. With special reference to cardiovascular disease, dementia and mortality. Danish Medical Bulletin, 53(3), 285-309.

Calder, P. C., Ahluwalia, N., Brouns, F., Buetler, T., Clement, K., Cunningham, K., … Winklhofer-Roob, B. M. (2011). Dietary factors and low-grade inflammation in relation to overweight and obesity. British Journal of Nutrition, 106(3), S5-S78. doi: 10.1017/S0007114511005460.

Cannizzo, E. S., Clement, C. C., Sahu, R., Follo, C., & Santambrogio, L. (2011). Oxidative stress, inflamm-aging and immunosenescence. Journal of Proteomics, 74(11), 2313-2323. doi: 10.1016/j.jprot.2011.06.005.

Carter, C. S., Hofer, T., Seo, A. Y., & Leeuwenburgh, C. (2007). Molecular mechanisms of life- and health-span extension: role of calorie restriction and exercise intervention. Applied Physiology, Nutrition and Metabolism, 32(5), 954-966. doi: 10.1139/H07-085.

Chung, H. Y., Cesari, M., Anton, S., Marzetti, E., Giovannini, S., Seo, A. Y., ... Leeuwenburgh, C. (2009). Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Research Reviews, 8(1), 18-30. doi: 10.1016/j.arr.2008.07.002.

Colbert, L. H., Visser, M., Simonsick, E. M., Tracy, R. P., Newman, A. B., Kritchevsky, S. B., … Harris, T. B. (2004). Physical activity, exercise, and inflammatory markers in older adults: findings from the Health, Aging and Body Composition Study. Journal of the American Geriatric Society, 52(7), 1098-1104. doi: 10.1111/j.1532-5415.2004.52307.x.

Cross, C. E., Hasegawa, G., Reddy, K. A., & Omaye, S. T. (1977). Enhanced lung toxicity of O2 in selenium-deficient rats. Research Communications in Chemical Pathology and Pharmacology, 16(4), 695-706.

De Martinis, M., Franceschi, C., Monti, D., & Ginaldi, L. (2005). Inflamm-ageing and lifelong antigenic load as major determinants of ageing rate and longevity. FEBS Letters, 579(10), 2035-2039. doi: 10.1016/j.febslet.2005.02.055.

Engelhart, M. J., Geerlings, M. I., Meijer, J., Kiliaan, A., Ruitenberg, A., van Swieten, J. C., ... Breteler, M. M. B. (2004). Inflammatory proteins in plasma and the risk of dementia: the rotterdam study. Archives of Neurology, 61(5), 668-672. doi:10.1001/archneur.61.5.668.

Franceschi, C., Bonafè, M., & Valensin, S. (2000). Human immunosenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space. Vaccine, 18(16), 1717-1720. doi: 10.1016/S0264-410X(99)00513-7.

Fried, L. P., Tangen, C. M., Walston, J., Newman, A. B., Hirsch, C., Gottdiener, J., ... McBurnie, M. A. (2001). Frailty in older adults: evidence for a phenotype. The journals of gerontology. Series A, Biological sciences and medical sciences, 56(3). M146-m157. doi: 10.1093/gerona/56.3.M146.

Gill, R., Tsung, A., & Billiar, T. (2010). Linking oxidative stress to inflammation: Toll-like receptors. Free Radical Biology and Medicine, 48(9), 1121-1132. doi: 10.1016/j.freeradbiomed.2010.01.006.

Gleeson, M., Bishop, N. C., Stensel, D. J., Lindley, M. R., Mastana, S. S., & Nimmo, M. A. (2011). The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nature Reviews Immunology, 11(9), 607-615. doi:10.1038/nri3041.

Gruver, A. L., Hudson, L. L., & Sempowski, G. D. (2007). Immunosenescence of ageing. The Journal of Pathology, 211(2), 144-156. doi: 10.1002/path.2104.

Head, D., Bugg, J. M., Goate, A. M., Fagan, A. M., Mintun, M. A., Benzinger, T., ... Morris, J. C. (2012). Exercise engagement as a moderator of the effects of APOE genotype on amyloid deposition. Archives of Neurology, 69(5), 636-643. doi:10.1001/archneurol.2011.845.

Hubbard, R. E., O'Mahony, M. S., Savva, G. M., Calver, B. L., & Woodhouse, K. W. (2009). Inflammation and frailty measures in older people. Journal of Cellular and Molecular Medicine, 13(9B), 3103-3109. doi: 10.1111/j.1582-4934.2009.00733.x.

Jurdana, M., Jenko-Pražnikar, Z., Mohorko, N., Petelin, A., Jakus, T., Šimunič, B., Pišot, R. (2015). Impact of 14-day bed rest on serum adipokines and low-grade inflammation in younger and older adults. Age, 37(6), 116. doi: 10.1007/s11357-015-9848-z.

Jylhä, M., Paavilainen, P., Lehtimäki, T., Goebeler, S., Karhunen, P. J., Hervonen, A., & Hurme, M. (2007). Interleukin-1 receptor antagonist, interleukin-6, and C-reactive protein as predictors of mortality in nonagenarians: the vitality 90+ study. The journals of gerontology. Series A, Biological sciences and medical sciences, 62(9), 1016-1021. doi: 10.1093/gerona/62.9.1016.

Knight, J. A. (2011). Diseases and disorders associated with excess body weight. Annals of Clinical & Laboratory Science, 41(2), 107-121.

Kohut, M. L., & Senchina, D. S. (2004). Reversing age-associated immunosenescence via exercise. Exercise Immunology Review, 10, 6-41.

Kregel, K. C., & Zhang, H. J. (2007). An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. American Journal of Physiology, Regulatory, Integrative and Comparative Physiology, 292(1), R18-R36. doi: 10.1152/ajpregu.00327.2006.

Lang, T., Streeper, T., Cawthon, P., Baldwin, K., Taaffe, D. R., & Harris, T. B. (2010). Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporosis International, 21(4), 543-559. doi: 10.1007/s00198-009-1059-y.

Liang, K. Y., Mintun, M. A., Fagan, A. M., Goate, A. M., Bugg, J. M., Holtzman, D. M., … Head, D. (2010). Exercise and Alzheimer's disease biomarkers in cognitively normal older adults. Annals of Neurology, 68(3), 311-318. doi: 10.1002/ana.22096.

Luck, T., Riedel-Heller, S. G., Luppa, M., Wiese, B., Köhler, M., Jessen, F., ... Maier, W. (2013). Apolipoprotein E epsilon 4 genotype and a physically active lifestyle in late life: analysis of gene-environment interaction for the risk of dementia and Alzheimer's disease dementia. Psychological Medicine, 44(6), 1319-1329. doi: 10.1017/S0033291713001918.

Lykkesfeldt, J., Hagen, T. M., Vinarsky, V., & Ames, B. N. (1998). Age-associated decline in ascorbic acid concentration, recycling, and biosynthesis in rat hepatocytes--reversal with (R)-alpha-lipoic acid supplementation. FASEB Journal, 12(12), 1183-1189.

Mota, M. P., Peixoto, F. M., Soares, J. F., Figueiredo, P. A., Leitão, J. C., Gaivão, I., & Duarte, J. A. (2010). Influence of aerobic fitness on age-related lymphocyte DNA damage in humans: relationship with mitochondria respiratory chain and hydrogen peroxide production. Age, 32(3), 337-346. doi 10.1007/s11357-010-9138-8.

Müller, L., & Pawelec, G. (2014). Aging and immunity - Impact of behavioral intervention. Brain Behavour and Immunity, 39, 8-22. doi: 10.1016/j.bbi.2013.11.015.

Nguyen, V., Mendelsohn, A., & Larrick, J. W. (2017). Interleukin-7 and Immunosenescence. Journal of Immunology Research, 2017:4807853. doi: 10.1155/2017/4807853.

Nicklas, B. J., Hsu, F. C., Brinkley, T. J., Church, T., Goodpaster, B. H., Kritchevsky, S. B., & Pahor, M. (2008). Exercise training and plasma C-reactive protein and interleukin-6 in elderly people. Journal of the American Geriatric Society, 56(11), 2045-2052. doi: 10.1111/j.1532-5415.2008.01994.x.

Ouchi, N., Parker, J. L., Lugus, J. J., & Walsh, K. (2011). Adipokines in inflammation and metabolic disease. Nature Reviews Immunology, 11(2), 85-97. doi:10.1038/nri2921.

Pedersen, B. K., & Bruunsgaard, H. (2003). Possible beneficial role of exercise in modulating low-grade inflammation in the elderly. Scandinavian Journal of Medicine & Science in Sports, 13(1), 56-62. doi: 10.1034/j.1600-0838.2003.20218.x.

Pedersen, B. K., & Febbraio, M. A. (2008). Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiological Review, 88(4), 1379-1406. doi: 10.1152/physrev.90100.2007.

Phillips, M. D., Flynn, M. G., McFarlin, B. K., Stewart, L. K., & Timmerman, K. L. (2010). Resistance training at eight-repetition maximum reduces the inflammatory milieu in elderly women. Medicine and Science in Sports & Exercise, 42(2), 314-325. doi: 10.1249/MSS.0b013e3181b11ab7.

Shimizu, K., Kimura, F., Akimoto, T., Akama, T., Tanabe, K., Nishijima, T., … Kono, I. (2008). Effect of moderate exercise training on T-helper cell subpopulations in elderly people. Exercise Immunology Review, 14, 24-37.

Shimizu, K., Suzuki, N,. Imai, T., Aizawa, K., Nanba, H., Hanaoka, Y., … Akama, T. (2011). Monocyte and T-cell responses to exercise training in elderly subjects. The Journal of Strength & Conditioning Research, 25(9), 2565-2572. doi: 10.1519/JSC.0b013e3181fc5e67.

Simpson, R. J., & Guy, K. (2010). Coupling aging immunity with a sedentary lifestyle: has the damage already been done? Gerontology, 56(5), 449-458. doi: 10.1159/000270905.

Singh, T., & Newman, A. B. (2011). Inflammatory markers in population studies of aging. Ageing Research Reviews, 10(3), 319-329. doi: 10.1016/j.arr.2010.11.002.

Starkie, R., Ostrowski, S. R., Jauffred, S., Febbraio, M., & Pedersen, B. K. (2003). Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB Journal, 17(8), 884-886. doi: 10.1096/fj.02-0670fje.

Thomas, J. L. (2013). Helpful or harmful? Potential effects of exercise on select inflammatory conditions. Physician Sportsmed, 41(4), 93-100. doi: 10.3810/psm.2013.11.2040.

van der Geest, K. S. M., Wang, Q., Eijsvogels, T. M. H., Koenen, H. J. P., Joosten, I., Brouwer, E., … Boots, A. M. H. (2017). Changes in peripheral immune cell numbers and functions in octogenarian walkers - an acute exercise study. Immunity & ageing. 14(5). doi: 10.1186/s12979-017-0087-2.

Vasto, S., Candore, G., Balistreri, C. R., Caruso, M., Colonna-Romano, G., Grimaldi, M. P., … Caruso, C. (2007). Inflammatory networks in ageing, age-related diseases and longevity. Mechanism of Ageing and Development, 128(1), 83-91. doi: 10.1016/j.mad.2006.11.015.

Visser, M., Pahor, M., Taaffe, D. R., Goodpaster, B. H., Simonsick, E. M., Newman, A. B., … Harris, T. B. (2002). Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. The journals of gerontology. Series A, Biological sciences and medical sciences, 57(5), M326-332. doi: 10.1093/gerona/57.5.M326.

Voss, M. W., Vivar, C., Kramer, A. F., & van Praag, H. (2013). Bridging animal and human models of exercise-induced brain plasticity. Trends in Cognitive Sciences, 17(10), 525-544. doi: 10.1016/j.tics.2013.08.001.

Woods, J. A., Keylock, K. T., Lowder, T., Vieira, V. J., Zelkovich, W., Dumich, S., … McAuley, E. (2009). Cardiovascular exercise training extends influenza vaccine seroprotection in sedentary older adults: the immune function intervention trial. Journal of the American Geriatric Society, 57(12), 2183-2191. doi: 10.1111/j.1532-5415.2009.02563.x.

Woods, J. A., Wilund, K. R., Martin, S. A., & Kistler, B. M. (2012). Exercise, inflammation and aging. Aging and Disease, 3(1), 130-140.

Yaffe, K., Lindquist, K., Penninx, B. W., Simonsick, E. M., Pahor, M., Kritchevsky, S., … Harris, T. (2003). Inflammatory markers and cognition in well-functioning African-American and white elders. Neurology, 61(1), 76-80. doi: 10.1212/01.WNL.0000073620.42047.D7.

Xia, S., Zhang, X., Zheng, S., Khanabdali, R., Kalionis, B., Wu, J., … Tai, X. (2016). An update on inflamm-aging: mechanisms, prevention, and treatment. Journal of Immunology Research, 2016:8426874. doi: 10.1155/2016/8426874.

Downloads

Additional Files

Published

24-10-2017

How to Cite

Mohorko, N., & Petelin, A. (2017). EXERCISE AND THE AGEING IMMUNE SYSTEM. Annales Kinesiologiae, 8(1), 23–32. Retrieved from http://ojs.zrs-kp.si/index.php/AK/article/view/136

Issue

Section

Articles