Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 6236309, 12 pages
http://dx.doi.org/10.1155/2016/6236309
Review Article

Ageing-Associated Oxidative Stress and Inflammation Are Alleviated by Products from Grapes

Department of Physiological Sciences, Stellenbosch University, Stellenbosch 7600, South Africa

Received 23 October 2015; Revised 3 February 2016; Accepted 7 February 2016

Academic Editor: Hesham A. El Enshasy

Copyright © 2016 K. S. Petersen and C. Smith. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. WHO, WHO Fact Sheet, WHO, 2015, http://www.who.int.
  2. B. F. Oliveira, J. A. Nogueira-Machado, and M. M. Chaves, “The role of oxidative stress in the aging process,” TheScientificWorldJOURNAL, vol. 10, pp. 1121–1128, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. D. P. Jones, V. C. Mody Jr., J. L. Carlson, M. J. Lynn, and P. Sternberg Jr., “Redox analysis of human plasma allows separation of pro-oxidant events of aging from decline in antioxidant defenses,” Free Radical Biology & Medicine, vol. 33, no. 9, pp. 1290–1300, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. W. MacNee, R. A. Rabinovich, and G. Choudhury, “Ageing and the border between health and disease,” The European Respiratory Journal, vol. 44, no. 5, pp. 1332–1352, 2014. View at Publisher · View at Google Scholar
  5. E. Ekblom-Bak, B. Ekblom, M. Vikström, U. De Faire, and M.-L. Hellénius, “The importance of non-exercise physical activity for cardiovascular health and longevity,” British Journal of Sports Medicine, vol. 48, no. 3, pp. 233–238, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Smith and M. F. Essop, “Gender differences in metabolic risk factor prevalence in a South African student population,” Cardiovascular Journal of Africa, vol. 20, no. 3, pp. 178–182, 2009. View at Google Scholar · View at Scopus
  7. C. E. Ottobelli, W. M. De Souza, T. Paz da Silva, R. N. Moresco, and M. B. Moretto, “Adipocytokines, inflammatory and oxidative stress markers of clinical relevance altered in young overweight/obese subjects,” Clinical Biochemistry, 2016. View at Publisher · View at Google Scholar
  8. K. Venkataraman, S. Khurana, and T. C. Tai, “Oxidative stress in aging-matters of the heart and mind,” International Journal of Molecular Sciences, vol. 14, no. 9, pp. 17897–17925, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Harman, “Aging: a theory based on free radical and radiation chemistry,” Journal of gerontology, vol. 11, no. 3, pp. 298–300, 1956. View at Publisher · View at Google Scholar · View at Scopus
  10. J. M. McCord and I. Fridovich, “Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein),” The Journal of Biological Chemistry, vol. 244, no. 22, pp. 6049–6055, 1969. View at Google Scholar · View at Scopus
  11. B. Schöttker, H. Brenner, E. Jansen et al., “Evidence for the free radical/oxidative stress theory of ageing from the CHANCES consortium: a meta-analysis of individual participant data,” BMC Medicine, vol. 13, no. 300, 15 pages, 2015. View at Publisher · View at Google Scholar
  12. B. A. I. Payne and P. F. Chinnery, “Mitochondrial dysfunction in aging: much progress but many unresolved questions,” Biochimica et Biophysica Acta, vol. 1847, no. 11, pp. 1347–1353, 2015. View at Publisher · View at Google Scholar
  13. L. Hayflick, “The limited in vitro lifetime of human diploid cell strains,” Experimental Cell Research, vol. 37, no. 3, pp. 614–636, 1965. View at Publisher · View at Google Scholar · View at Scopus
  14. T. von Zglinicki, V. Serra, M. Lorenz et al., “Short telomeres in patients with vascular dementia: an indicator of low antioxidative capacity and a possible risk factor?” Laboratory Investigation, vol. 80, no. 11, pp. 1739–1747, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Venkatesan, A. T. Natarajan, and M. P. Hande, “Chromosomal instability—mechanisms and consequences,” Mutation Research/Genetic Toxicology and Environmental Mutagenesis, vol. 793, pp. 176–184, 2015. View at Publisher · View at Google Scholar
  16. N. Khansari, Y. Shakiba, and M. Mahmoudi, “Chronic inflammation and oxidative stress as a major cause of age-related diseases and cancer,” Recent Patents on Inflammation & Allergy Drug Discovery, vol. 3, no. 1, pp. 73–80, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Nagai, T. Betsuyaku, T. Kondo, Y. Nasuhara, and M. Nishimura, “Long term smoking with age builds up excessive oxidative stress in bronchoalveolar lavage fluid,” Thorax, vol. 61, no. 6, pp. 496–502, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Sherwood, Human Physiology: From Cells to Systems, Brooks/Cole, 7th edition, 2010.
  19. M. E. Kotas and R. Medzhitov, “Homeostasis, inflammation, and disease susceptibility,” Cell, vol. 160, no. 5, pp. 816–827, 2015. View at Publisher · View at Google Scholar
  20. J. G. Tidball, “Inflammatory processes in muscle injury and repair,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 288, no. 2, pp. R345–R353, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Smith, M. J. Kruger, R. M. Smith, and K. H. Myburgh, “The inflammatory response to skeletal muscle injury: illuminating complexities,” Sports Medicine, vol. 38, no. 11, pp. 947–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Panda, A. Arjona, E. Sapey et al., “Human innate immunosenescence: causes and consequences for immunity in old age,” Trends in Immunology, vol. 30, no. 7, pp. 325–333, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Fulop, A. Larbi, N. Douziech et al., “Signal transduction and functional changes in neutrophils with aging,” Aging Cell, vol. 3, no. 4, pp. 217–226, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Beerman, D. Bhattacharya, S. Zandi et al., “Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 12, pp. 5465–5470, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Li, S. Chen, T. Feng, J. Dong, Y. Li, and H. Li, “Rutin protects against aging-related metabolic dysfunction,” Food & Function, 2016. View at Publisher · View at Google Scholar
  26. A. A. Hill, E. K. Anderson-Baucum, A. J. Kennedy et al., “Activation of NF-κB drives the enhanced survival of adipose tissue macrophages in an obesogenic environment,” Molecular Metabolism, vol. 4, no. 10, pp. 665–677, 2015. View at Publisher · View at Google Scholar
  27. J. Y. Huh, Y. J. Park, M. Ham, and J. B. Kim, “Crosstalk between adipocytes and immune cells in adipose tissue inflammation and metabolic dysregulation in obesity,” Molecules and Cells, vol. 37, no. 5, pp. 365–371, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante Jr., “Obesity is associated with macrophage accumulation in adipose tissue,” The Journal of Clinical Investigation, vol. 112, no. 12, pp. 1796–1808, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. D. C. K. Borato, G. C. Parabocz, J. T. Ribas et al., “Biomarkers in obesity: serum myeloperoxidase and traditional cardiac risk parameters,” Experimental and Clinical Endocrinology & Diabetes, vol. 124, no. 1, pp. 49–54, 2016. View at Publisher · View at Google Scholar
  30. H. Khodabandehloo, S. Gorgani-Firuzjaee, G. Panahi, and R. Meshkani, “Molecular and cellular mechanisms linking inflammation to insulin resistance and β-cell dysfunction,” Translational Research, vol. 167, no. 1, pp. 228–256, 2016. View at Publisher · View at Google Scholar
  31. M. Maes, C. Song, A. Lin et al., “The effects of psychological stress on humans: increased production of pro-inflammatory cytokines and a Th1-like response in stress-induced anxiety,” Cytokine, vol. 10, no. 4, pp. 313–318, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Bruunsgaard, “The clinical impact of systemic low-level inflammation in elderly populations,” Danish Medical Bulletin, vol. 53, no. 3, pp. 285–309, 2006. View at Google Scholar
  33. N. Sallam and I. Laher, “Exercise modulates oxidative stress and inflammation in aging and cardiovascular diseases,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 7239639, 32 pages, 2016. View at Publisher · View at Google Scholar
  34. C. Wenisch, S. Patruta, F. Daxböck, R. Krause, and W. Hörl, “Effect of age on human neutrophil function,” Journal of Leukocyte Biology, vol. 67, no. 1, pp. 40–45, 2000. View at Google Scholar · View at Scopus
  35. B. Weinberger, D. Herndler-Brandstetter, A. Schwanninger, D. Weiskopf, and B. Grubeck-Loebenstein, “Biology of immune responses to vaccines in elderly persons,” Clinical Infectious Diseases, vol. 46, no. 7, pp. 1078–1084, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Baëhl, H. Garneau, A. Le Page et al., “Altered neutrophil functions in elderly patients during a 6-month follow-up period after a hip fracture,” Experimental Gerontology, vol. 65, pp. 58–68, 2015. View at Publisher · View at Google Scholar
  37. P. H. Naccache and J. S. Lefebvre, “A straight neutrophil path to healthy aging?” Blood, vol. 123, no. 2, pp. 154–156, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Mittal, M. R. Siddiqui, K. Tran, S. P. Reddy, and A. B. Malik, “Reactive oxygen species in inflammation and tissue injury,” Antioxidants & Redox Signaling, vol. 20, no. 7, pp. 1126–1167, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Kim, J.-S. Hwang, C.-H. Woo et al., “TNF-α-induced up-regulation of intercellular adhesion molecule-1 is regulated by a Rac-ROS-dependent cascade in human airway epithelial cells,” Experimental and Molecular Medicine, vol. 40, no. 2, pp. 167–175, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Zhang, Y. Park, J. Wu et al., “Role of TNF-α in vascular dysfunction,” Clinical Science, vol. 116, no. 3, pp. 219–230, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. M. J. Morgan and Z.-G. Liu, “Crosstalk of reactive oxygen species and NF-κB signaling,” Cell Research, vol. 21, no. 1, pp. 103–115, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Finkel and N. J. Holbrook, “Oxidants, oxidative stress and the biology of ageing,” Nature, vol. 408, no. 6809, pp. 239–247, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Bedard and K.-H. Krause, “The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology,” Physiological Reviews, vol. 87, no. 1, pp. 245–313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. A. P. Levine, M. R. Duchen, S. de Villiers, P. R. Rich, A. W. Segal, and A. Gaggar, “Alkalinity of neutrophil phagocytic vacuoles is modulated by HVCN1 and has consequences for myeloperoxidase activity,” PLoS ONE, vol. 10, no. 4, Article ID e0125906, pp. 1–20, 2015. View at Publisher · View at Google Scholar
  45. M. J. Berridge, “Module 11: cell stress, inflammatory responses and cell death,” Cell Signalling Biology, 2014. View at Publisher · View at Google Scholar
  46. R. Zhang, M.-L. Brennan, X. Fu et al., “Association between myeloperoxidase levels and risk of coronary artery disease,” The Journal of the American Medical Association, vol. 286, no. 17, pp. 2136–2142, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Salminen, K. Kaarniranta, and A. Kauppinen, “Crosstalk between oxidative stress and SIRT1: impact on the aging process,” International Journal of Molecular Sciences, vol. 14, no. 2, pp. 3834–3859, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Poulose and R. Raju, “Sirtuin regulation in aging and injury,” Biochimica et Biophysica Acta (BBA)—Molecular Basis of Disease, vol. 1852, no. 11, pp. 2442–2455, 2015. View at Publisher · View at Google Scholar
  49. E. Sapey, H. Greenwood, G. Walton et al., “Phosphoinositide 3-kinase inhibition restores neutrophil accuracy in the elderly: toward targeted treatments for immunosenescence,” Blood, vol. 123, no. 2, pp. 239–248, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. M. J. Kruger and C. Smith, “Postcontusion polyphenol treatment alters inflammation and muscle regeneration,” Medicine and Science in Sports and Exercise, vol. 44, no. 5, pp. 872–880, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Carrera-Quintanar, L. Funes, N. Vicente-Salar et al., “Effect of polyphenol supplements on redox status of blood cells: a randomized controlled exercise training trial,” European Journal of Nutrition, vol. 54, no. 7, pp. 1081–1093, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. M. R. De Oliveira, S. F. Nabavi, A. Manayi, M. Daglia, Z. Hajheydari, and S. M. Nabavi, “Resveratrol and the mitochondria: from triggering the intrinsic apoptotic pathway to inducing mitochondrial biogenesis, a mechanistic view,” Biochimica et Biophysica Acta—General Subjects, vol. 1860, no. 4, pp. 727–745, 2016. View at Publisher · View at Google Scholar
  53. W. Pan, H. Yu, S. Huang, P. Zhu, and A. Kumar, “Resveratrol protects against TNF-α-induced injury in human umbilical endothelial cells through promoting sirtuin-1-induced repression of NF-KB and p38 MAPK,” PLOS ONE, vol. 11, no. 1, Article ID e0147034, 2016. View at Publisher · View at Google Scholar
  54. P. Kotora, F. Šeršeň, J. Filo, D. Loos, J. Gregáň, and F. Gregáň, “The scavenging of DPPH, galvinoxyl and ABTS radicals by imine analogs of resveratrol,” Molecules, vol. 21, no. 2, 2016. View at Publisher · View at Google Scholar
  55. G. F. Balata, E. A. Essa, H. A. Shamardl, S. Zidan, and M. Abdo Rehab, “Self-emulsifying drug delivery systems as a tool to improve solubility and bioavailability of resveratrol,” Drug Design, Development and Therapy, vol. 10, pp. 117–128, 2016. View at Publisher · View at Google Scholar
  56. D. R. Valenzano, E. Terzibasi, T. Genade, A. Cattaneo, L. Domenici, and A. Cellerino, “Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate,” Current Biology, vol. 16, no. 3, pp. 296–300, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. E. M. Hernández-Hernández, C. Serrano-García, R. A. Vázquez-Roque et al., “Chronic administration of resveratrol prevents morphological changes in prefrontal cortex and hippocampus of aged rats,” Synapse, 2016. View at Publisher · View at Google Scholar
  58. B. Shukitt-Hale, A. Carey, L. Simon, D. A. Mark, and J. A. Joseph, “Effects of Concord grape juice on cognitive and motor deficits in aging,” Nutrition, vol. 22, no. 3, pp. 295–302, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. E. P. Cherniack, “A berry thought-provoking idea: the potential role of plant polyphenols in the treatment of age-related cognitive disorders,” The British Journal of Nutrition, vol. 108, no. 5, pp. 794–800, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. Y.-J. Wang, P. Thomas, J.-H. Zhong et al., “Consumption of grape seed extract prevents amyloid-β deposition and attenuates inflammation in brain of an Alzheimer's disease mouse,” Neurotoxicity Research, vol. 15, no. 1, pp. 3–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. M. C. Kizilarslanoglu, Ö. Kara, Y. Yesil et al., “Alzheimer disease, inflammation, and novel inflammatory marker: resistin,” Turkish Journal of Medical Sciences, vol. 45, pp. 1040–1046, 2015. View at Publisher · View at Google Scholar
  62. M. Awasthi, S. Singh, V. P. Pandey, and U. N. Dwivedi, “Alzheimer's disease: an overview of amyloid beta dependent pathogenesis and its therapeutic implications along with in silico approaches emphasizing the role of natural products,” Journal of the Neurological Sciences, vol. 361, pp. 256–271, 2016. View at Publisher · View at Google Scholar
  63. F. Cacciapuoti, “Opposite effects of metabolic syndrome and calorie restriction on thrombotic disease: heads and tails of the same coin—resveratrol's role,” Metabolic Syndrome and Related Disorders, vol. 7, no. 5, pp. 397–400, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. L. D. Africa and C. Smith, “Using a simulated blood-brain barrier to investigate potential modulators of HIV-1-associated neuro-inflammatory processes in vitro,” Journal of Research in Biology, vol. 5, pp. 5–20, 2015. View at Google Scholar
  65. M. J. Kruger, K. H. Myburgh, and C. Smith, “Contusion injury with chronic in vivo polyphenol supplementation: leukocyte responses,” Medicine & Science in Sports and Exercise, vol. 46, no. 2, pp. 225–231, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. G. D. Noratto, G. Angel-Morales, S. T. Talcott, and S. U. Mertens-Talcott, “Polyphenolics from Açaí (Euterpe oleracea Mart.) and red muscadine grape (Vitis rotundifolia) protect human umbilical vascular endothelial cells (HUVEC) from glucose- and lipopolysaccharide (LPS)-induced inflammation and target microRNA-126,” Journal of Agricultural and Food Chemistry, vol. 59, no. 14, pp. 7999–8012, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. C.-F. Tsai, K.-T. Wang, L.-G. Chen, C.-J. Lee, S.-H. Tseng, and C.-C. Wang, “Anti-inflammatory effects of Vitis thunbergii var. taiwaniana on knee damage associated with arthritis,” Journal of Medicinal Food, vol. 17, no. 4, pp. 479–486, 2014. View at Publisher · View at Google Scholar · View at Scopus
  68. G. Kuroyanagi, T. Otsuka, N. Yamamoto, R. Matsushima-Nishiwaki, O. Kozawa, and H. Tokuda, “Resveratrol suppresses TGF-β-induced VEGF synthesis in osteoblasts: inhibition of the p44/p42 MAPKs and SAPK/JNK pathways,” Experimental and Therapeutic Medicine, vol. 9, no. 6, pp. 2303–2310, 2015. View at Publisher · View at Google Scholar
  69. J. G. Wood, B. Rogina, S. Lavu et al., “Sirtuin activators mimic caloric restriction and delay ageing in metazoans,” Nature, vol. 430, no. 7000, pp. 686–689, 2004. View at Publisher · View at Google Scholar
  70. K. T. Howitz, K. J. Bitterman, H. Y. Cohen et al., “Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan,” Nature, vol. 425, no. 6954, pp. 191–196, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. L. Zhao, Y. Yagiz, C. Xu, J. Lu, S. Chung, and M. R. Marshall, “Muscadine grape seed oil as a novel source of tocotrienols to reduce adipogenesis and adipocyte inflammation,” Food & Function, vol. 6, no. 7, pp. 2293–2302, 2015. View at Publisher · View at Google Scholar
  72. H. Fujii, T. Yokozawa, Y. A. Kim, C. Tohda, and G.-I. Nonaka, “Protective effect of grape seed polyphenols against high glucose-induced oxidative stress,” Bioscience, Biotechnology, and Biochemistry, vol. 70, no. 9, pp. 2104–2111, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. L. Younes-Sakr, P. Senesse, C. Laurent et al., “Validation of a surgical technique for rat intestinal irradiation: potential Side effects prevention by dietary grape phenolics,” Digestive Diseases and Sciences, vol. 57, no. 10, pp. 2562–2570, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. V. Pallarès, A. Fernández-Iglesias, L. Cedó et al., “Grape seed procyanidin extract reduces the endotoxic effects induced by lipopolysaccharide in rats,” Free Radical Biology & Medicine, vol. 60, pp. 107–114, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. K. H. Myburgh, M. J. Kruger, and C. Smith, “Accelerated skeletal muscle recovery after in vivo polyphenol administration,” Journal of Nutritional Biochemistry, vol. 23, no. 9, pp. 1072–1079, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. G. Patki, Q. Ali, I. Pokkunuri et al., “Grape powder treatment prevents anxiety-like behavior in a rat model of aging,” Nutrition Research, vol. 35, no. 6, pp. 504–511, 2015. View at Publisher · View at Google Scholar
  77. W. Yin, B. Li, X. Li et al., “Anti-inflammatory effects of grape seed procyanidin B2 on a diabetic pancreas,” Food & Function, vol. 6, no. 9, pp. 3065–3071, 2015. View at Publisher · View at Google Scholar
  78. J. A. Baur, K. J. Pearson, N. L. Price et al., “Resveratrol improves health and survival of mice on a high-calorie diet,” Nature, vol. 444, no. 7117, pp. 337–342, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. D. Impellizzeri, E. Talero, R. Siracusa et al., “Protective effect of polyphenols in an inflammatory process associated with experimental pulmonary fibrosis in mice,” The British Journal of Nutrition, vol. 114, no. 6, pp. 853–865, 2015. View at Publisher · View at Google Scholar
  80. A. G. Janiques, V. d. Leal, M. B. Stockler-Pinto, N. X. Moreira, and D. Mafra, “Effects of grape powder supplementation on inflammatory and antioxidant markers in hemodialysis patients: a randomized double-blind study,” Jornal Brasileiro de Nefrologia, vol. 36, no. 4, pp. 496–501, 2014. View at Publisher · View at Google Scholar
  81. I. Urquiaga, S. D’Acuña, D. Pérez et al., “Wine grape pomace flour improves blood pressure, fasting glucose and protein damage in humans: a randomized controlled trial,” Biological Research, vol. 48, article 49, 2015. View at Publisher · View at Google Scholar
  82. J. Tomé-Carneiro, M. Larrosa, M. J. Yáñez-Gascón et al., “One-year supplementation with a grape extract containing resveratrol modulates inflammatory-related microRNAs and cytokines expression in peripheral blood mononuclear cells of type 2 diabetes and hypertensive patients with coronary artery disease,” Pharmacological Research, vol. 72, pp. 69–82, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Zamboni, G. Mazzali, F. Fantin, A. Rossi, and V. Di Francesco, “Sarcopenic obesity: a new category of obesity in the elderly,” Nutrition, Metabolism & Cardiovascular Diseases, vol. 18, no. 5, pp. 388–395, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. K. Lambert, M. Coisy-Quivy, C. Bisbal et al., “Grape polyphenols supplementation reduces muscle atrophy in a mouse model of chronic inflammation,” Nutrition, vol. 31, no. 10, pp. 1275–1283, 2015. View at Publisher · View at Google Scholar
  85. S. W. Lee, G. Dai, Z. Hu, X. Wang, J. Du, and W. E. Mitch, “Regulation of muscle protein degradation: coordinated control of apoptotic and ubiquitin-proteasome systems by phosphatidylinositol 3 kinase,” Journal of the American Society of Nephrology, vol. 15, no. 6, pp. 1537–1545, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. Z. C. Xu, J. Yin, B. Zhou et al., “Grape seed proanthocyanidin protects liver against ischemia/reperfusion injury by attenuating endoplasmic reticulum stress,” World Journal of Gastroenterology, vol. 21, no. 24, pp. 7468–7477, 2015. View at Publisher · View at Google Scholar
  87. D. E. Roopchand, R. N. Carmody, P. Kuhn et al., “Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high-fat diet-induced metabolic syndrome,” Diabetes, vol. 64, no. 8, pp. 2847–2858, 2015. View at Publisher · View at Google Scholar