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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 7023091, 8 pages
https://doi.org/10.1155/2017/7023091
Research Article

Centella asiatica Attenuates Mitochondrial Dysfunction and Oxidative Stress in Aβ-Exposed Hippocampal Neurons

1Department of Neurology, Oregon Health and Science University, Portland, OR 97239, USA
2Department of Cell, Developmental and Cancer Biology, Oregon Health and Science University, Portland, OR 97239, USA
3Department of Neurology and Parkinson’s Disease Research Education and Clinical Care Center (PADRECC), Portland Veterans Affairs Medical Center, Portland, OR 97239, USA

Correspondence should be addressed to Nora E. Gray; ude.usho@nyarg

Received 18 April 2017; Revised 16 June 2017; Accepted 27 June 2017; Published 13 August 2017

Academic Editor: Swaran J. S. Flora

Copyright © 2017 Nora E. Gray 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. Alzheimer’s Association, “2016 Alzheimer’s disease facts and figures,” Alzheimer’s & Dementia, vol. 12, pp. 459–509, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. S. J. Baloyannis, “Dendritic pathology in Alzheimer’s disease,” Journal of the Neurological Sciences, vol. 283, pp. 153–157, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. I. A. Mavroudis, D. F. Fotiou, M. G. Manani et al., “Dendritic pathology and spinal loss in the visual cortex in Alzheimer’s disease: a Golgi study in pathology,” The International Journal of Neuroscience, vol. 121, pp. 347–354, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Leuner, W. E. Müller, and A. S. Reichert, “From mitochondrial dysfunction to amyloid beta formation: novel insights into the pathogenesis of Alzheimer’s disease,” Molecular Neurobiology, vol. 46, pp. 186–193, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Yao, R. W. Irwin, L. Zhao, J. Nilsen, R. T. Hamilton, and R. D. Brinton, “Mitochondrial bioenergetic deficit precedes Alzheimer’s pathology in female mouse model of Alzheimer’s disease,” Proceedings of the National Academy of Sciences, vol. 106, pp. 14670–14675, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Manczak, B. S. Park, Y. Jung, and P. H. Reddy, “Differential expression of oxidative phosphorylation genes in patients with Alzheimer’s disease: implications for early mitochondrial dysfunction and oxidative damage,” Neuromolecular Medicine, vol. 5, pp. 147–162, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. S. J. Baloyannis, “Mitochondrial alterations in Alzheimer’s disease,” Journal of Alzheimer's Disease, vol. 9, pp. 119–126, 2006. View at Publisher · View at Google Scholar
  8. A. M. Brown, R. K. Sheu, R. Mohs, V. Haroutunian, and J. P. Blass, “Correlation of the clinical severity of Alzheimer’s disease with an aberration in mitochondrial DNA (mtDNA),” Journal of Molecular Neuroscience, vol. 16, pp. 41–48, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Serrano and E. Klann, “Reactive oxygen species and synaptic plasticity in the aging hippocampus,” Ageing Research Reviews, vol. 3, pp. 431–443, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. M. A. Lovell and W. R. Markesbery, “Oxidative damage in mild cognitive impairment and early Alzheimer’s disease,” Journal of Neuroscience Research, vol. 85, pp. 3036–3040, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Cuadrado-Tejedor, J. F. Cabodevilla, M. Zamarbide, T. Gómez-Isla, R. Franco, and A. Perez-Mediavilla, “Age-related mitochondrial alterations without neuronal loss in the hippocampus of a transgenic model of Alzheimer’s disease,” Current Alzheimer Research, vol. 10, pp. 390–405, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Du, L. Guo, S. Yan, A. A. Sosunov, G. M. McKhann, and S. S. Yan, “Early deficits in synaptic mitochondria in an Alzheimer’s disease mouse model,” Proceedings of the National Academy of Sciences, vol. 107, pp. 18670–18675, 2010. View at Google Scholar
  13. V. Rhein, G. Baysang, S. Rao et al., “Amyloid-beta leads to impaired cellular respiration, energy production and mitochondrial electron chain complex activities in human neuroblastoma cells,” Cellular and Molecular Neurobiology, vol. 29, pp. 1063–1071, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. G. K. M. Shinomol and M. M. Bharath, “Exploring the role of “Brahmi” (Bocopa monnieri and Centella asiatica) in brain function and therapy,” Recent Patents on Endocrine, Metabolic & Immune Drug Discovery, vol. 5, pp. 33–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Tabassum, K. Vaibhav, P. Shrivastava et al., “Centella asiatica Attenuates the neurobehavioral, neurochemical and histological changes in transient focal middle cerebral artery occlusion rats,” Neurological Sciences, vol. 34, pp. 925–933, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Soumyanath, Y. P. Zhong, S. A. Gold et al., “Centella asiatica Accelerates nerve regeneration upon oral administration and contains multiple active fractions increasing neurite elongation in vitro,” Journal of Pharmacy & Pharmacology, vol. 57, pp. 1221–1229, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Gupta and S. J. Flora, “Effect of Centella asiatica on arsenic induced oxidative stress and mental distribution in rats,” Journal of Applied Toxicology, vol. 26, article 21322, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Soumyanath, Y. Zhang, E. Henson et al., “Centella asiatica Extract improves behavioral deficits in a mouse model of Alzheimer’s disease: investigation of a possible mechanism of action,” International Journal of Alzheimer's Disease, vol. 2012, Article ID 381974, 9 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. N. E. Gray, C. J. Harris, J. F. Quinn, and A. Soumyanath, “Centella asiatica Modulates antioxidant and mitochondrial pathways and improves cognitive function in mice,” Journal of Ethnopharmacology, vol. 180, pp. 78–86, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. N. E. Gray, J. Morré, J. Kelley et al., “Caffeoylquinic acids in Centella asiatica protect against amyloid-β toxicity,” Journal of Alzheimer's Disease, vol. 40, pp. 359–373, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. N. E. Gray, H. Sampath, J. A. Zweig, J. F. Quinn, and A. Soumyanath, “Centella asiatica Attenuates amyloid-β-induced oxidative stress and mitochondrial dysfunction,” Journal of Alzheimer's Disease, vol. 45, pp. 933–946, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Schneider, S. Giordano, B. R. Zelicksonm et al., “Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress,” Free Radical Biology and Medicine, vol. 51, pp. 2007–2017, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Wagner, Plant Drug Analysis. A Thin-Layer Chromatographic Atlas, Springer-Verlag, Berlin, 1996.
  24. N. E. Gray, J. A. Zweig, C. Murchison et al., “Centella asiatica attenuates Aβ-induced neurodegenerative spine loss and dendritic simplification,” Neuroscience Letters, vol. 646, pp. 24–29, 2017. View at Publisher · View at Google Scholar
  25. K. Hsiao, P. Chapman, S. Nilsen et al., “Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice,” Science, vol. 274, pp. 99–102, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. D. King, G. W. Arendash, F. Crawford, T. Sterk, J. Menendez, and M. J. Mullan, “Progressive and gender-dependent cognitive impairment in the APP(SW) transgenic mouse model for Alzheimer’s disease,” Behavioural Brain Research, vol. 103, pp. 145–162, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. M. J. Calkins, M. Manczak, P. Mao, U. Shirendeb, and P. H. Reddy, “Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer’s disease,” Human Molecular Genetics, vol. 20, pp. 4515–4529, 2011. View at Google Scholar
  28. H. Y. Wu, E. Hudry, T. Hashimoto et al., “Amyloid beta induces the morphological neurodegenerative triad of spine loss, dendritic simplification, and neuritic dystrophies through calcineurin activation,” The Journal of Neuroscience, vol. 30, pp. 2636–2649, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Kaech and G. Banker, “Culturing hippocampal neurons,” Nature Protocols, vol. 1, pp. 2406–2415, 2006. View at Google Scholar
  30. M. Wu, A. Neilson, A. L. Swift et al., “Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells,” American Journal of Physiology. Cell Physiology, vol. 292, pp. C125–C136, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. M. H. Veerendra Kumar and Y. K. Gupta, “Effect of Centella asiatica on cognition and oxidative stress in an intracerebroventricular streptozotocin model of Alzheimer’s disease in rats,” Clinical and Experimental Pharmacology & Physiology, vol. 30, pp. 336–342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. K. Gupta, M. H. Veerendra Kumar, and A. K. Srivastava, “Effect of Centella asiatica on pentylenetetrazole-induced kindling, cognition and oxidative stress in rats,” Pharmacology, Biochemistry, and Behavior, vol. 74, pp. 579–585, 2003. View at Google Scholar
  33. M. H. V. Kumar and Y. K. Gupta, “Effect of different extracts of Centella asiatica on cognition and markers of oxidative stress in rats,” Journal of Ethnopharmacology, vol. 79, pp. 253–260, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. G. K. Shinomol and Muralidhara, “Effect of Centella asiatica leaf powder on oxidative markers in brain regions of prepubertal mice in vivo and its in vitro efficacy to ameliorate 3-NPA-induced oxidative stress in mitochondria,” Phytomedicine, vol. 15, pp. 971–984, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. C. L. Chen, W. H. Tsai, C. J. Chen, and T. M. Pan, “Centella asiatica Extract protects against amyloid β 1-40-induced neurotoxicity in neuronal cells by activating the antioxidative defence system,” Journal of Traditional and Complementary Medicine, vol. 6, pp. 362–369, 2015. View at Google Scholar
  36. M. Dhanasekaran, L. A. Holcomb, A. R. Hitt et al., “Centella asiatica Extract selectively decreases amyloid beta levels in hippocampus of Alzheimer’s disease animal model,” Phytotherapy Research, vol. 23, pp. 14–19, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Ferreiro, R. Resende, R. Costa, C. R. Oliveira, and C. M. F. Pereira, “An endoplasmic-reticulum-specific apoptotic pathway is involved in prion and amyloid-beta peptides neurotoxicity,” Neurobiology of Disease, vol. 23, pp. 669–678, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Ferreiro, C. R. Oliveira, and C. M. F. Pereira, “Involvement of endoplasmic reticulum Ca2+ release through ryanodine and inositol 1,4,5-triphosphate receptors in the neurotoxic effects induced by the amyloid-β peptide,” Journal of Neuroscience Research, vol. 76, pp. 872–880, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Haleagrahara and K. Ponnusamy, “Neuroprotective effect of Centella asiatica extract (CAE) on experimentally induced parkinsonism in aged Sprague Dawley rats,” The Journal of Toxicological Sciences, vol. 35, pp. 41–47, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. M. F. Xu, Y. Y. Xiong, J. K. Liu, J. J. Qian, L. Zhu, and J. Gao, “Asiatic acid, a pentacyclic triterpene in Centella asiatica, attenuates glutamate-induced cognitive deficits in mice and apoptosis in SH-SY5Y cells,” Acta Pharmacologica Sinica, vol. 33, pp. 578–587, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Trushina, E. Nemutlu, S. Zhang et al., “Defects in mitochondrial dynamics and metabolomic signatures of evolving energetic stress in mouse models of familial Alzheimer’s disease,” PloS One, vol. 7, article e32737, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. R. H. Olsen, L. A. Johnson, D. G. Zuloaga, C. L. Limoli, and J. Raber, “Enhanced hippocampus-dependent memory and reduced anxiety in mice over-expressing human catalase in mitochondria,” Journal of Neurochemistry, vol. 25, pp. 303–313, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Chen, R. Na, and Q. Ran, “Enhanced defense against mitochondrial hydrogen peroxide attenuates age-associated cognition decline,” Neurobiology of Aging, vol. 35, no. 11, pp. 2552–2561, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. P. Mao, M. Manczak, M. J. Calkins et al., “Mitochondria-targeted catalase reduces abnormal APP processing, amyloid β production and BACE1 in a mouse model of Alzheimer’s disease: implications for neuroprotection and lifespan extension,” Human Molecular Genetics, vol. 21, pp. 2973–2990, 2012. View at Publisher · View at Google Scholar · View at Scopus