Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2019, Article ID 7593608, 11 pages
https://doi.org/10.1155/2019/7593608
Research Article

Berberine Alleviates Amyloid β-Induced Mitochondrial Dysfunction and Synaptic Loss

Chunhui Zhao,1,2,3 Ping Su,1,2,3 Cui Lv,1,2,4 Limin Guo,1,2,5 Guoqiong Cao,1,2,5 Chunxia Qin,1,2,5 and Wensheng Zhang1,2,5,6

1Beijing Area Major Laboratory of Protection and Utilization of Traditional Chinese Medicine, Beijing Normal University, Beijing 100088, China
2Engineering Research Center of Natural Medicine, Ministry of Education, Beijing Normal University, Beijing 100088, China
3Institute of Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China
4Laboratory of Immunology for Environment and Health, Shandong Analysis and Test Center, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250014, China
5Faculty of Geographical Science, Beijing Normal University, Beijing 100875, China
6National & Local United Engineering Research Center for Sanqi Resources Protection and Utilization Technology, Kunming 650000, China

Correspondence should be addressed to Wensheng Zhang; nc.ude.unb@swz

Received 26 November 2018; Accepted 12 March 2019; Published 2 May 2019

Academic Editor: Ana Lloret

Copyright © 2019 Chunhui Zhao 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. S. Hauptmann, I. Scherping, S. Dröse et al., “Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice,” Neurobiology of Aging, vol. 30, no. 10, pp. 1574–1586, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Pozueta, R. Lefort, and M. L. Shelanski, “Synaptic changes in Alzheimer’s disease and its models,” Neuroscience, vol. 251, no. 5, pp. 51–65, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. P. H. Reddy, R. Tripathi, Q. Troung et al., “Abnormal mitochondrial dynamics and synaptic degeneration as early events in Alzheimer’s disease: implications to mitochondria-targeted antioxidant therapeutics,” Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, vol. 1822, no. 5, pp. 639–649, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. T. J. Ryan and S. G. Grant, “The origin and evolution of synapses,” Nature Reviews Neuroscience, vol. 10, no. 10, pp. 701–712, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. R. J. Evans, V. Derkach, and A. Surprenant, “ATP mediates fast synaptic transmission in mammalian neurons,” Nature, vol. 357, no. 6378, pp. 503–505, 1992. View at Publisher · View at Google Scholar · View at Scopus
  6. 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 of the United States of America, vol. 107, no. 43, pp. 18670–18675, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. Z. Li, K. I. Okamoto, Y. Hayashi, and M. Sheng, “The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses,” Cell, vol. 119, no. 6, pp. 873–887, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. D. T. Chang, A. S. Honick, and I. J. Reynolds, “Mitochondrial trafficking to synapses in cultured primary cortical neurons,” The Journal of Neuroscience, vol. 26, no. 26, pp. 7035–7045, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. Q. Cai and P. Tammineni, “Alterations in mitochondrial quality control in Alzheimer’s disease,” Frontiers in Cellular Neuroscience, vol. 10, no. 1, p. 24, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. P. H. Reddy, “Amyloid beta, mitochondrial structural and functional dynamics in Alzheimer’s disease,” Experimental Neurology, vol. 218, no. 2, pp. 286–292, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. P. H. Reddy and M. F. Beal, “Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer’s disease,” Trends in Molecular Medicine, vol. 14, no. 2, pp. 45–53, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Takuma, F. Fang, W. Zhang et al., “RAGE-mediated signaling contributes to intraneuronal transport of amyloid-β and neuronal dysfunction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 47, pp. 20021–20026, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. C. A. Hansson Petersen, N. Alikhani, H. Behbahani et al., “The amyloid β-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 35, article 13145, 13150 pages, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Hedskog, C. M. Pinho, R. Filadi et al., “Modulation of the endoplasmic reticulum–mitochondria interface in Alzheimer’s disease and related models,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 19, pp. 7916–7921, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. J. X. Chen and S. S. Yan, “Role of mitochondrial amyloid-β in Alzheimer's disease,” Journal of Alzheimers Disease, vol. 20, no. s2, pp. S569–S578, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. F. Akhter, D. Chen, S. F. Yan, and S. S. Yan, “Chapter Eleven - Mitochondrial perturbation in Alzheimer’s disease and diabetes,” Progress in Molecular Biology and Translational Science, vol. 146, pp. 341–361, 2017. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Takuma, J. Yao, J. Huang et al., “ABAD enhances Abeta-induced cell stress via mitochondrial dysfunction,” Faseb Journal, vol. 19, no. 6, pp. 597-598, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. J. W. Lustbader, M. Cirilli, C. Lin et al., “ABAD directly links a to mitochondrial toxicity in Alzheimer’s disease,” Science, vol. 304, no. 5669, pp. 448–452, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Du, L. Guo, F. Fang et al., “Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer’s disease,” Nature Medicine, vol. 14, no. 10, pp. 1097–1105, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Du, L. Guo, W. Zhang, M. Rydzewska, and S. Yan, “Cyclophilin D deficiency improves mitochondrial function and learning/memory in aging Alzheimer disease mouse model,” Neurobiology of Aging, vol. 32, no. 3, pp. 398–406, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Rui, P. Tiwari, Z. Xie, and J. Q. Zheng, “Acute impairment of mitochondrial trafficking by β-amyloid peptides in hippocampal neurons,” The Journal of Neuroscience, vol. 26, no. 41, pp. 10480–10487, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Huang, S. Chen, Y. Liang, and Y. Guo, “The role of berberine in the multi-target treatment of senile dementia,” Current Topics in Medicinal Chemistry, vol. 16, no. 8, pp. 867–873, 2016. View at Google Scholar
  23. T. Ahmed, A. U. H. Gilani, M. Abdollahi, M. Daglia, S. F. Nabavi, and S. M. Nabavi, “Berberine and neurodegeneration: a review of literature,” Pharmacological Reports, vol. 67, no. 5, pp. 970–979, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. S. S. Durairajan, L. F. Liu, J. H. Lu et al., “Berberine ameliorates β-amyloid pathology, gliosis, and cognitive impairment in an Alzheimer’s disease transgenic mouse model,” Neurobiology of Aging, vol. 33, no. 12, pp. 2903–2919, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Zhu and C. Qian, “Berberine chloride can ameliorate the spatial memory impairment and increase the expression of interleukin-1beta and inducible nitric oxide synthase in the rat model of Alzheimer’s disease,” BMC Neuroscience, vol. 7, no. 1, p. 78, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. X. Wang, R. Wang, D. Xing et al., “Kinetic difference of berberine between hippocampus and plasma in rat after intravenous administration of Coptidis rhizoma extract,” Life Sciences, vol. 77, no. 24, pp. 3058–3067, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Chen, M. Tan, M. Jing et al., “Berberine protects homocysteic acid-induced HT-22 cell death: involvement of Akt pathway,” Metabolic Brain Disease, vol. 30, no. 1, pp. 137–142, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. X. Liu, J. Zhou, M. D. Abid et al., “Correction: berberine attenuates axonal transport impairment and axonopathy induced by calyculin a in N2a cells,” PLoS One, vol. 11, no. 3, article e0152609, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. F. Negahdar, M. Mehdizadeh, M. T. Joghataei, M. Roghani, F. Mehraeen, and E. Poorghayoomi, “Berberine chloride pretreatment exhibits neuroprotective effect against 6-hydroxydopamine-induced neuronal insult in rat,” Iranian Journal of Pharmaceutical Research, vol. 14, no. 4, pp. 1145–1152, 2015. View at Google Scholar
  30. A. Kumar, Ekavali, J. Mishra, K. Chopra, and D. K. Dhull, “Possible role of P-glycoprotein in the neuroprotective mechanism of berberine in intracerebroventricular streptozotocin-induced cognitive dysfunction,” Psychopharmacology, vol. 233, no. 1, pp. 137–152, 2016. View at Publisher · View at Google Scholar · View at Scopus
  31. A. E. Abdel Moneim, “The neuroprotective effect of berberine in mercury-induced neurotoxicity in rats,” Metabolic Brain Disease, vol. 30, no. 4, pp. 935–942, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Liang, M. Huang, X. Jiang, Q. Liu, X. Chang, and Y. Guo, “The neuroprotective effects of berberine against amyloid β-protein-induced apoptosis in primary cultured hippocampal neurons via mitochondria-related caspase pathway,” Neuroscience Letters, vol. 655, pp. 46–53, 2017. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Lv, L. Wang, X. Liu et al., “Geniposide attenuates oligomeric Aβ1-42-induced inflammatory response by targeting RAGE-dependent signaling in BV2 cells,” Current Alzheimer Research, vol. 11, no. 5, pp. 430–440, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Zhang, C. Zhao, C. Lv et al., “Geniposide alleviates amyloid-induced synaptic injury by protecting axonal mitochondrial trafficking,” Frontiers in Cellular Neuroscience, vol. 10, p. 309, 2017. View at Publisher · View at Google Scholar · View at Scopus
  35. V. Todorova and A. Blokland, “Mitochondria and synaptic plasticity in the mature and aging nervous system,” Current Neuropharmacology, vol. 15, no. 1, pp. 166–173, 2017. View at Google Scholar
  36. S. M. Cardoso, S. Santos, R. H. Swerdlow, and C. R. Oliveira, “Functional mitochondria are required for amyloid beta-mediated neurotoxicity,” Faseb Journal Official Publication of the Federation of American Societies for Experimental Biology, vol. 15, no. 8, pp. 1439–1441, 2001. View at Publisher · View at Google Scholar
  37. M. Manczak, T. S. Anekonda, E. Henson, B. S. Park, J. Quinn, and P. H. Reddy, “Mitochondria are a direct site of Aβ accumulation in Alzheimer’s disease neurons: implications for free radical generation and oxidative damage in disease progression,” Human Molecular Genetics, vol. 15, no. 9, pp. 1437–1449, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. L. D. Zorova, V. A. Popkov, E. Y. Plotnikov et al., “Mitochondrial membrane potential,” Analytical Biochemistry, vol. 552, pp. 50–59, 2017. View at Publisher · View at Google Scholar · View at Scopus
  39. V. P. Skulachev, “Mitochondrial filaments and clusters as intracellular power-transmitting cables,” Trends in Biochemical Sciences, vol. 26, no. 1, pp. 23–29, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. G. A. Banker and W. M. Cowan, “Further observations on hippocampal neurons in dispersed cell culture,” Journal of Comparative Neurology, vol. 187, no. 3, pp. 469–493, 1979. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. L. Siow, L. Sarna, and O. Karmin, “Redox regulation in health and disease — therapeutic potential of berberine,” Food Research International, vol. 44, no. 8, pp. 2409–2417, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. J.-M. Hwang, C.-J. Wang, F.-P. Chou et al., “Inhibitory effect of berberine on tert-butyl hydroperoxide-induced oxidative damage in rat liver,” Archives of Toxicology, vol. 76, no. 11, pp. 664–670, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Y. Zhou and S. W. Zhou, “Protective effect of berberine on antioxidant enzymes and positive transcription elongation factor b expression in diabetic rat liver,” Fitoterapia, vol. 82, no. 2, pp. 184–189, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Kumar, K. Ekavali, M. Chopra, R. P. Mukherjee, and D. K. Dhull, “Current knowledge and pharmacological profile of berberine: an update,” European Journal of Pharmacology, vol. 761, pp. 288–297, 2015. View at Publisher · View at Google Scholar · View at Scopus