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Journal of Diabetes Research
Volume 2015, Article ID 485759, 9 pages
http://dx.doi.org/10.1155/2015/485759
Research Article

Avocado Oil Improves Mitochondrial Function and Decreases Oxidative Stress in Brain of Diabetic Rats

1Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, 58030 Morelia, MICH, Mexico
2Facultad de Químico Farmacobiología, Universidad Michoacana de San Nicolás de Hidalgo, 58240 Morelia, MICH, Mexico
3Facultad de Ciencias Médicas y Biológicas “Dr. Ignacio Chávez”, Universidad Michoacana de San Nicolás de Hidalgo, 58020 Morelia, MICH, Mexico

Received 25 March 2015; Revised 13 May 2015; Accepted 18 May 2015

Academic Editor: Mark A. Yorek

Copyright © 2015 Omar Ortiz-Avila 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. K. G. Alberti and P. Z. Zimmet, “Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation,” Diabetic Medicine, vol. 15, no. 7, pp. 539–553, 1998. View at Google Scholar
  2. P. I. Moreira, M. S. Santos, A. M. Moreno, T. Proença, R. Seiça, and C. R. de Oliveira, “Effect of streptozotocin-induced diabetes on rat brain mitochondria,” Journal of Neuroendocrinology, vol. 16, no. 1, pp. 32–38, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. M. S. Ola, A. M. Aleisa, S. S. Al-Rejaie et al., “Flavonoid, morin inhibits oxidative stress, inflammation and enhances neurotrophic support in the brain of streptozotocin-induced diabetic rats,” Neurological Sciences, vol. 35, no. 7, pp. 1003–1008, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. A. M. Vincent, L. L. McLean, C. Backus, and E. L. Feldman, “Short-term hyperglycemia produces oxidative damage and apoptosis in neurons,” The FASEB Journal, vol. 19, no. 6, pp. 638–640, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. L. B. Ceretta, G. Z. Réus, G. T. Rezin, G. Scaini, E. L. Streck, and J. Quevedo, “Brain energy metabolism parameters in an animal model of diabetes,” Metabolic Brain Disease, vol. 25, no. 4, pp. 391–396, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. P. I. Moreira and C. R. Oliveira, “Mitochondria as potential targets in antidiabetic therapy,” in Diabetes—Perspectives in Drug Therapy, vol. 203 of Handbook of Experimental Pharmacology, pp. 331–356, Springer, Berlin, Germany, 2011. View at Publisher · View at Google Scholar
  7. C. Toth, “Diabetes and neurodegeneration in the brain,” in Diabetes and the Nervous System, vol. 126 of Handbook of Clinical Neurology, pp. 489–511, Elsevier, New York, NY, USA, 2014. View at Publisher · View at Google Scholar
  8. P. I. Moreira, M. S. Santos, A. M. Moreno, R. Seiça, and C. R. Oliveira, “Increased vulnerability of brain mitochondria in diabetic (Goto-Kakizaki) rats with aging and amyloid-β exposure,” Diabetes, vol. 52, no. 6, pp. 1449–1456, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. J. L. Edwards, A. Quattrini, S. I. Lentz et al., “Diabetes regulates mitochondrial biogenesis and fission in mouse neurons,” Diabetologia, vol. 53, no. 1, pp. 160–169, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Acar, E. Akil, H. Alp et al., “Oxidative damage is ameliorated by curcumin treatment in brain and sciatic nerve of diabetic rats,” International Journal of Neuroscience, vol. 122, no. 7, pp. 367–372, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. L. B. Ceretta, G. Z. Réus, H. M. Abelaira et al., “Increased oxidative stress and imbalance in antioxidant enzymes in the brains of alloxan-induced diabetic rats,” Experimental Diabetes Research, vol. 2012, Article ID 302682, 8 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. F. del Chierico, P. Vernocchi, B. Dallapiccola, and L. Putignani, “Mediterranean diet and health: food effects on gut microbiota and disease control,” International Journal of Molecular Sciences, vol. 15, no. 7, pp. 11678–11699, 2014. View at Google Scholar
  13. M. P. Riya, K. A. Antu, S. Pal, A. K. Srivastava, S. Sharma, and K. G. Raghu, “Nutraceutical potential of Aerva lanata (L.) Juss. ex Schult ameliorates secondary complications in streptozotocin-induced diabetic rats,” Food & Function, vol. 5, no. 9, pp. 2086–2095, 2014. View at Publisher · View at Google Scholar
  14. S. S. Anusree, A. Priyanka, V. M. Nisha, A. A. Das, and K. G. Raghu, “An in vitro study reveals the nutraceutical potential of punicic acid relevant to diabetes via enhanced GLUT4 expression and adiponectin secretion,” Food & Function, vol. 5, no. 10, pp. 2590–2601, 2014. View at Publisher · View at Google Scholar
  15. M. L. Dreher and A. J. Davenport, “Hass avocado composition and potential health effects,” Critical Reviews in Food Science and Nutrition, vol. 53, no. 7, pp. 738–750, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Carranza-Madrigal, M. Alvizouri-Muñoz, J. E. Herrera-Abarca, and F. Chávez-Carbajal, “Efectos del aguacate como fuente de ácidos grasos monoinsaturados en lípidos séricos, metabolismo de la glucosa y reología en pacientes con diabetes tipo 2,” Medicina Interna de México, vol. 24, no. 4, pp. 267–272, 2008. View at Google Scholar
  17. O. Ortiz-Avila, C. A. Sámano-García, E. Calderón-Cortés et al., “Dietary avocado oil supplementation attenuates the alterations induced by type I diabetes and oxidative stress in electron transfer at the complex II-complex III segment of the electron transport chain in rat kidney mitochondria,” Journal of Bioenergetics and Biomembranes, vol. 45, no. 3, pp. 271–287, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. N. R. Sims, “Rapid isolation of metabolically active mitochondria from rat brain and subregions using percoll density gradient centrifugation,” Journal of Neurochemistry, vol. 55, no. 2, pp. 698–707, 1990. View at Publisher · View at Google Scholar · View at Scopus
  19. A. G. Gornall, C. J. Bardawill, and M. M. David, “Determination of serum proteins by means of the biuret reaction,” The Journal of Biological Chemistry, vol. 177, no. 2, pp. 751–766, 1949. View at Google Scholar · View at Scopus
  20. R. Colonna, S. Massari, G. F. Azzone, B. Ziche, and P. Veronese, “The problem of cation-binding sites in the energized membrane of intact mitochondria,” European Journal of Biochemistry, vol. 34, no. 3, pp. 577–585, 1973. View at Publisher · View at Google Scholar
  21. J. A. Buege and S. D. Aust, “Microsomal lipid peroxidation,” Methods in Enzymology, vol. 52, pp. 302–310, 1978. View at Publisher · View at Google Scholar · View at Scopus
  22. E. M. Hallberg, Y. Shu, and R. L. Hallberg, “Loss of mitochondrial hsp60 function: nonequivalent effects on matrix—targeted and intermembrane-targeted proteins,” Molecular and Cellular Biology, vol. 13, no. 5, pp. 3050–3057, 1993. View at Google Scholar · View at Scopus
  23. M. Chomova, Z. Tatarkova, D. Dobrota, and P. Racay, “Ischemia-induced inhibition of mitochondrial complex I in rat brain: effect of permeabilization method and electron acceptor,” Neurochemical Research, vol. 37, no. 5, pp. 965–976, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Cortés-Rojo, E. Calderón-Cortés, M. Clemente-Guerrero et al., “Elucidation of the effects of lipoperoxidation on the mitochondrial electron transport chain using yeast mitochondria with manipulated fatty acid content,” Journal of Bioenergetics and Biomembranes, vol. 41, no. 1, pp. 15–28, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. T. P. M. Akerboom and H. Sies, “Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples,” Methods in Enzymology, vol. 77, pp. 373–382, 1981. View at Publisher · View at Google Scholar · View at Scopus
  26. O. Ortiz-Avila, M. A. Gallegos-Corona, L. A. Sánchez-Briones et al., “Protective effects of dietary avocado oil on impaired electron transport chain function and exacerbated oxidative stress in liver mitochondria from diabetic rats,” Journal of Bioenergetics and Biomembranes. In press.
  27. G. J. Biessels and W. H. Gispen, “The impact of diabetes on cognition: what can be learned from rodent models?” Neurobiology of Aging, vol. 26, supplement 1, pp. 36–41, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. W. H. Gispen and G. J. Biessels, “Cognition and synaptic plasticity in diabetes mellitus,” Trends in Neurosciences, vol. 23, no. 11, pp. 542–549, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Messier, “Impact of impaired glucose tolerance and type 2 diabetes on cognitive aging,” Neurobiology of Aging, vol. 26, supplement 1, pp. S26–S30, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. G. J. Biessels, A. C. Kappelle, B. Bravenboer, D. W. Erkelens, and W. H. Gispen, “Cerebral function in diabetes mellitus,” Diabetologia, vol. 37, no. 7, pp. 643–650, 1994. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Ott, R. P. Stolk, F. van Harskamp, H. A. P. Pols, A. Hofman, and M. M. B. Breteler, “Diabetes mellitus and the risk of dementia: the rotterdam study,” Neurology, vol. 53, no. 9, pp. 1937–1942, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Detka, A. Kurek, A. Basta-Kaim, M. Kubera, W. Lasoñz, and B. Budziszewska, “Neuroendocrine link between stress, depression and diabetes,” Pharmacological Reports, vol. 65, no. 6, pp. 1591–1600, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Verkhratsky and P. Fernyhough, “Mitochondrial malfunction and Ca2+ dyshomeostasis drive neuronal pathology in diabetes,” Cell Calcium, vol. 44, no. 1, pp. 112–122, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Thapa, C. E. Nichols, S. E. Lewis et al., “Transgenic overexpression of mitofilin attenuates diabetes mellitus-associated cardiac and mitochondria dysfunction,” Journal of Molecular and Cellular Cardiology, vol. 79, pp. 212–223, 2015. View at Publisher · View at Google Scholar
  35. J. Hao, W. Shen, L. Sun et al., “Mitochondrial dysfunction in the liver of type 2 diabetic Goto-Kakizaki rats: improvement by a combination of nutrients,” British Journal of Nutrition, vol. 106, no. 5, pp. 648–655, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. S. S. Katyare and J. G. Satav, “Effect of streptozotocin-induced diabetes on oxidative energy metabolism in rat kidney mitochondria. A comparative study of early and late effects,” Diabetes, Obesity & Metabolism, vol. 7, no. 5, pp. 555–562, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. M. D. C. Ortiz, S. Lores-Arnaiz, M. F. Albertoni Borghese et al., “Mitochondrial dysfunction in brain cortex mitochondria of STZ-diabetic rats: effect of L-arginine,” Neurochemical Research, vol. 38, no. 12, pp. 2570–2580, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Cardoso, R. X. Santos, S. C. Correia et al., “Insulin-induced recurrent hypoglycemia exacerbates diabetic brain mitochondrial dysfunction and oxidative imbalance,” Neurobiology of Disease, vol. 49, no. 1, pp. 1–12, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. M. E. Patti, A. J. Butte, S. Crunkhorn et al., “Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 14, pp. 8466–8471, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. S. K. Roy Chowdhury, E. Zherebitskaya, D. R. Smith et al., “Mitochondrial respiratory chain dysfunction in dorsal root ganglia of streptozotocin-induced diabetic rats and its correction by insulin treatment,” Diabetes, vol. 59, no. 4, pp. 1082–1091, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Noriega-Cisneros, C. Cortés-Rojo, S. Manzo-Avalos et al., “Mitochondrial response to oxidative and nitrosative stress in early stages of diabetes,” Mitochondrion, vol. 13, no. 6, pp. 835–840, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. Q.-Y. Lu, J. R. Arteaga, Q. Zhang, S. Huerta, V. L. W. Go, and D. Heber, “Inhibition of prostate cancer cell growth by an avocado extract: role of lipid-soluble bioactive substances,” The Journal of Nutritional Biochemistry, vol. 16, no. 1, pp. 23–30, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. S. M. D'Ambrosio, C. Han, L. Pan, A. D. Kinghorn, and H. Ding, “Aliphatic acetogenin constituents of avocado fruits inhibit human oral cancer cell proliferation by targeting the EGFR/RAS/RAF/MEK/ERK1/2 pathway,” Biochemical and Biophysical Research Communications, vol. 409, no. 3, pp. 465–469, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Munusamy, H. Saba, T. Mitchell, J. K. Megyesi, R. W. Brock, and L. A. MacMillan-Crow, “Alteration of renal respiratory complex-III during experimental type-1 diabetes,” BMC Endocrine Disorders, vol. 9, article 2, 9 pages, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. S. Katyare and S. P. Patel, “Insulin status differentially affects energy transduction in cerebral mitochondria from male and female rats,” Brain Research Bulletin, vol. 69, no. 4, pp. 458–464, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. J. St-Pierre, J. A. Buckingham, S. J. Roebuck, and M. D. Brand, “Topology of superoxide production from different sites in the mitochondrial electron transport chain,” The Journal of Biological Chemistry, vol. 277, no. 47, pp. 44784–44790, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Dröse and U. Brandt, “Molecular mechanisms of superoxide production by the mitochondrial respiratory chain,” Advances in Experimental Medicine and Biology, vol. 748, pp. 145–169, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. M. D. Brand and D. G. Nicholls, “Assessing mitochondrial dysfunction in cells,” Biochemical Journal, vol. 435, no. 2, pp. 297–312, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Aminzadeh, A. R. Dehpour, M. Safa, S. Mirzamohammadi, and A. M. Sharifi, “Investigating the protective effect of lithium against high glucose-induced neurotoxicity in PC12 cells: involvements of ROS, JNK and P38 MAPKs, and apoptotic mitochondria pathway,” Cellular and Molecular Neurobiology, vol. 34, no. 8, pp. 1143–1150, 2014. View at Publisher · View at Google Scholar
  50. R. T. Holman, “Autoxidation of fats and related substances,” Progress in the Chemistry of Fats and Other Lipids, vol. 2, pp. 51–98, 1954. View at Publisher · View at Google Scholar · View at Scopus
  51. M. P. Murphy, “Development of lipophilic cations as therapies for disorders due to mitochondrial dysfunction,” Expert Opinion on Biological Therapy, vol. 1, no. 5, pp. 753–764, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. I. Batinic-Haberle, Z. Rajic, A. Tovmasyan et al., “Diverse functions of cationic Mn(III) N-substituted pyridylporphyrins, recognized as SOD mimics,” Free Radical Biology and Medicine, vol. 51, no. 5, pp. 1035–1053, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. M. S. Santos, D. L. Santos, C. M. Palmeira, R. Seiça, A. J. Moreno, and C. R. Oliveira, “Brain and liver mitochondria isolated from diabetic Goto-Kakizaki rats show different susceptibility to induced oxidative stress,” Diabetes/Metabolism Research and Reviews, vol. 17, no. 3, pp. 223–230, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. S. S. Kamboj, K. Chopra, and R. Sandhir, “Neuroprotective effect of N-acetylcysteine in the development of diabetic encephalopathy in streptozotocin-induced diabetes,” Metabolic Brain Disease, vol. 23, no. 4, pp. 427–443, 2008. View at Publisher · View at Google Scholar · View at Scopus