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Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 6135319, 8 pages
http://dx.doi.org/10.1155/2016/6135319
Research Article

Grape Powder Improves Age-Related Decline in Mitochondrial and Kidney Functions in Fischer 344 Rats

1Heart and Kidney Institute, Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204, USA
2University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA

Received 16 March 2016; Revised 15 June 2016; Accepted 15 June 2016

Academic Editor: Bruno Meloni

Copyright © 2016 Indira Pokkunuri et al. 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. J. R. Weinstein and S. Anderson, “The aging kidney: physiological changes,” Advances in Chronic Kidney Disease, vol. 17, no. 4, pp. 302–307, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Yang and A. B. Fogo, “Cell senescence in the aging kidney,” Journal of the American Society of Nephrology, vol. 21, no. 9, pp. 1436–1439, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Epstein, “Aging and the kidney,” Journal of the American Society of Nephrology, vol. 7, no. 8, pp. 1106–1122, 1996. View at Google Scholar · View at Scopus
  4. R. D. Lindeman and R. Goldman, “Anatomic and physiologic age changes in the kidney,” Experimental Gerontology, vol. 21, no. 4-5, pp. 379–406, 1986. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Melk, W. Kittikowit, I. Sandhu et al., “Cell senescence in rat kidneys in vivo increases with growth and age despite lack of telomere shortening,” Kidney International, vol. 63, no. 6, pp. 2134–2143, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Bratic and N.-G. Larsson, “The role of mitochondria in aging,” The Journal of Clinical Investigation, vol. 123, no. 3, pp. 951–957, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. B. A. I. Payne and P. F. Chinnery, “Mitochondrial dysfunction in aging: Much progress but many unresolved questions,” Biochimica et Biophysica Acta (BBA)—Bioenergetics, vol. 1847, no. 11, pp. 1347–1353, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. C. B. Park and N.-G. Larsson, “Mitochondrial DNA mutations in disease and aging,” The Journal of Cell Biology, vol. 193, no. 5, pp. 809–818, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Dai, Y. Chiao, D. J. Marcinek, H. H. Szeto, and P. S. Rabinovitch, “Mitochondrial oxidative stress in aging and healthspan,” Longevity & Healthspan, vol. 3, no. 1, article 6, 2014. View at Publisher · View at Google Scholar
  10. N. Braidy, G. J. Guillemin, H. Mansour, T. Chan-Ling, A. Poljak, and R. Grant, “Age related changes in NAD+ metabolism oxidative stress and sirt1 activity in wistar rats,” PLoS ONE, vol. 6, no. 4, Article ID e19194, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. K. A. Nath and S. M. Norby, “Reactive oxygen species and acute renal failure,” The American Journal of Medicine, vol. 109, no. 8, pp. 665–678, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Nistala, A. Whaley-Connell, and J. R. Sowers, “Redox control of renal function and hypertension,” Antioxidants and Redox Signaling, vol. 10, no. 12, pp. 2047–2089, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. Z. Zuo, H. Lei, X. Wang, Y. Wang, W. Sonntag, and Z. Sun, “Aging-related kidney damage is associated with a decrease in klotho expression and an increase in superoxide production,” Age, vol. 33, no. 3, pp. 261–274, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Asghar and M. F. Lokhandwala, “Antioxidant supplementation normalizes elevated protein kinase C activity in the proximal tubules of old rats,” Experimental Biology and Medicine, vol. 229, no. 3, pp. 270–275, 2004. View at Google Scholar · View at Scopus
  15. G. Chugh, M. F. Lokhandwala, and M. Asghar, “Oxidative stress alters renal D1 and AT1 receptor functions and increases blood pressure in old rats,” American Journal of Physiology—Renal Physiology, vol. 300, no. 1, pp. F133–F138, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Xu, V. I. Khaoustov, H. U. I. Wang, J. Yu, F. Tabassam, and B. Yoffe, “Freeze-dried grape powder attenuates mitochondria- and oxidative stress-mediated apoptosis in liver cells,” Journal of Agricultural and Food Chemistry, vol. 57, no. 19, pp. 9324–9331, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. 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
  18. F. Allam, A. T. Dao, G. Chugh et al., “Grape powder supplementation prevents oxidative stress-induced anxiety-like behavior, memory impairment, and high blood pressure in rats,” The Journal of Nutrition, vol. 143, no. 6, pp. 835–842, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Chugh, M. F. Lokhandwala, and M. Asghar, “Altered functioning of both renal dopamine D1 and angiotensin II type 1 receptors causes hypertension in old rats,” Hypertension, vol. 59, no. 5, pp. 1029–1036, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Patki, Q. Ali, I. Pokkunuri, M. Asghar, and S. Salim, “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 · View at Scopus
  21. M. Yoshida, M. Takahashi, K. Inoue, D. Nakae, and A. Nishikawa, “Lack of chronic toxicity and carcinogenicity of dietary administrated catechin mixture in Wistar Hannover GALAS rats,” Journal of Toxicological Sciences, vol. 36, no. 3, pp. 297–311, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Morazzoni and E. Bombardelli, “Post-marketing investigation on Tegens® preparation with respect to side effects, 1987 Cited in Vaccinium myrtillus,” Fitoterapia, vol. 67, pp. 3–29, 1996. View at Google Scholar
  23. R. C. Ekeanyanwu and O. U. Njoku, “Acute and subacute oral toxicity study on the flavonoid rich fraction of Monodora tenuifolia seed in albino rats,” Asian Pacific Journal of Tropical Biomedicine, vol. 4, no. 3, pp. 194–202, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. J. A. Crowell, P. J. Korytko, R. L. Morrissey, T. D. Booth, and B. S. Levine, “Resveratrol-associated renal toxicity,” Toxicological Sciences, vol. 82, no. 2, pp. 614–619, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Pokkunuri, G. Chugh, I. Rizvi, and M. Asghar, “Age-related hypertension and salt sensitivity are associated with unique cortico-medullary distribution of D1R, AT1R, and NADPH-oxidase in FBN rats,” Clinical and Experimental Hypertension, vol. 37, no. 1, pp. 1–7, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. L. George, M. F. Lokhandwala, and M. Asghar, “Exercise activates redox-sensitive transcription factors and restores renal D1 receptor function in old rats,” American Journal of Physiology—Renal Physiology, vol. 297, no. 5, pp. F1174–F1180, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Pesta and E. Gnaiger, “High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle,” Methods in Molecular Biology, vol. 810, pp. 25–58, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Hütter, H. Unterluggauer, A. Garedew, P. Jansen-Dürr, and E. Gnaiger, “High-resolution respirometry—a modern tool in aging research,” Experimental Gerontology, vol. 41, no. 1, pp. 103–109, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. I. D. Pokkunuri, G. Chugh, and M. Asghar, “Human kidney-2 cells harbor functional dopamine D1 receptors that require Giα for Gq/11α signaling,” American Journal of Physiology—Renal Physiology, vol. 305, no. 4, pp. F560–F567, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. W. Bors and C. Michel, “Chemistry of the antioxidant effect of polyphenols,” Annals of the New York Academy of Sciences, vol. 957, pp. 57–69, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Hanausek, E. Spears, Z. Walaszek et al., “Inhibition of murine skin carcinogenesis by freeze-dried grape powder and other grape-derived major antioxidants,” Nutrition and Cancer, vol. 63, no. 1, pp. 28–38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. D. A. Chistiakov, I. A. Sobenin, V. V. Revin, A. N. Orekhov, and Y. V. Bobryshev, “Mitochondrial aging and age-related dysfunction of mitochondria,” BioMed Research International, vol. 2014, Article ID 238463, 7 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. E. Lionaki, M. Markaki, K. Palikaras, and N. Tavernarakis, “Mitochondria, autophagy and age-associated neurodegenerative diseases: new insights into a complex interplay,” Biochimica et Biophysica Acta (BBA)—Bioenergetics, vol. 1847, no. 11, pp. 1412–1423, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. R. X. Santos, S. C. Correia, C. Carvalho, S. Cardoso, M. S. Santos, and P. I. Moreira, “Mitophagy in neurodegeneration: an opportunity for therapy?” Current Drug Targets, vol. 12, no. 6, pp. 790–799, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. J. P. Little, A. Safdar, N. Cermak, M. A. Tarnopolsky, and M. J. Gibala, “Acute endurance exercise increases the nuclear abundance of PGC-1α in trained human skeletal muscle,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 298, no. 4, pp. R912–R917, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Ventura-Clapier, A. Garnier, and V. Veksler, “Transcriptional control of mitochondrial biogenesis: the central role of PGC-1α,” Cardiovascular Research, vol. 79, no. 2, pp. 208–217, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. L. Zhu, Q. Wang, L. Zhang et al., “Hypoxia induces PGC-1α expression and mitochondrial biogenesis in the myocardium of TOF patients,” Cell Research, vol. 20, no. 6, pp. 676–687, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. B. N. Chorley, M. R. Campbell, X. Wang et al., “Identification of novel NRF2-regulated genes by ChiP-Seq: influence on retinoid X receptor alpha,” Nucleic Acids Research, vol. 40, no. 15, pp. 7416–7429, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Kovac, P. R. Angelova, K. M. Holmström, Y. Zhang, A. T. Dinkova-Kostova, and A. Y. Abramov, “Nrf2 regulates ROS production by mitochondria and NADPH oxidase,” Biochimica et Biophysica Acta—General Subjects, vol. 1850, no. 4, pp. 794–801, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. K. M. Holmström, L. Baird, Y. Zhang et al., “Nrf2 impacts cellular bioenergetics by controlling substrate availability for mitochondrial respiration,” Biology Open, vol. 2, no. 8, pp. 761–770, 2013. View at Publisher · View at Google Scholar
  41. S. Hogan, C. Canning, S. Sun, X. Sun, H. Kadouh, and K. Zhou, “Dietary supplementation of grape skin extract improves glycemia and inflammation in diet-induced obese mice fed a western high fat diet,” Journal of Agricultural and Food Chemistry, vol. 59, no. 7, pp. 3035–3041, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Agostino, F. Invernizzi, C. Tiveron et al., “Constitutive knockout of Surf1 is associated with high embryonic lethality, mitochondrial disease and cytochrome c oxidase deficiency in mice,” Human Molecular Genetics, vol. 12, no. 4, pp. 399–413, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. M. O. Péquignot, R. Dey, M. Zeviani et al., “Mutations in the SURF1 gene associated with Leigh Syndrome and cytochrome c oxidase deficiency,” Human Mutation, vol. 17, no. 5, pp. 374–381, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Laloi-Michelin, M. Virally, C. Jardel et al., “Kearns Sayre syndrome: an unusual form of mitochondrial diabetes,” Diabetes & Metabolism, vol. 32, no. 2, pp. 182–186, 2006. View at Publisher · View at Google Scholar · View at Scopus