Berberine: A potential multipotent natural product to combat Alzheimer's disease

Molecules

Volumn 16, Issue 8, 2011, Pages 6732-6740

  Ji, Hong Fang ^a   Shen, Liang ^a  

^a SHANDONG UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Alzheimer's disease; Berberine; Multipotent agent

Indexed keywords

ACETYLCHOLINESTERASE; ALKALOID; AMINE OXIDASE (FLAVIN CONTAINING); AMYLOID PRECURSOR PROTEIN; ANTIOXIDANT; APP PROTEIN, HUMAN; BERBERINE; CHOLESTEROL; CHOLINESTERASE; CHOLINESTERASE INHIBITOR; HYPOCHOLESTEROLEMIC AGENT; MONOAMINE OXIDASE INHIBITOR;

AGED; ALZHEIMER DISEASE; ARACEAE; CHEMISTRY; DRUG ANTAGONISM; HUMAN; METABOLISM; METHODOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; PHYTOTHERAPY; REVIEW;

ACETYLCHOLINESTERASE; AGED; ALKALOIDS; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANTICHOLESTEREMIC AGENTS; ANTIOXIDANTS; ARACEAE; BERBERINE; BUTYRYLCHOLINESTERASE; CHOLESTEROL; CHOLINESTERASE INHIBITORS; HUMANS; MONOAMINE OXIDASE; MONOAMINE OXIDASE INHIBITORS; PHYTOTHERAPY;

EID: 80052252471     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules16086732     Document Type: Review

References (68)

1. Cummings, J.L. Alzheimer's disease. N. Engl. J. Med. 2004, 351, 56-67.
2. Ballard, C.; Gauthier, S.; Corbett, A.; Brayne, C.; Aarsland, D.; Jones, E. Alzheimer's disease. Lancet 2011, 377, 1019-1031.
3. Blennow, K.; de Leon, MJ.; Zetterberg, H. Alzheimer's disease. Lancet 2006, 368, 387-403. (Pubitemid 44108123)
4. Plassman, B.L.; Langa, K.M.; Fisher, G.G.; Heeringa, S.G.; Weir, D.R.; Ofstedal, M.B.; Burke, J.R.; Hurd, M.D.; Potter, G.G.; Rodgers, W.L.; et al. Prevalence of dementia in the United States: The aging, demographics, and memory study. Neuroepidemiology 2007, 29, 125-132. (Pubitemid 350191430)
5. Barnham, KJ.; Masters, C.L.; Bush, A.I. Neurodegenerative diseases and oxidative stress. Nat Rev. Drug. Discov. 2004, 3, 205-214.
6. Muñoz-Torrero, D. Acetylcholinesterase inhibitors as disease-modifying therapies for Alzheimer's disease. Curr. Med. Chem. 2008, 15, 2433-2455.
7. Brown, D.R.; Kozlowski, H. Biological inorganic and bioinorganic chemistry of neurodegeneration based on prion and Alzheimer diseases. Dalton Trans. 2004, 1907-1917.
8. Hardy, J.; Allsop, D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 1991, 12, 383-388.
9. Hashimoto, M.; Rockenstein, E.; Crews, L.; Masliah, E. Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromolecular Med. 2003, 4, 21-36.
10. Benson, A. Alzheimer's disease: A tangled issue. Drug Discov. Today 2005, 10, 749-751. (Pubitemid 40744917)
11. Imanshahidi, M.; Hosseinzadeh, H. Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine. Phytother. Res. 2008, 22, 999-1012.
12. Kuo, C.L.; Chi, C.W.; Liu, T.Y. The anti-inflammatory potential of berberine in vitro and in vivo. Cancer Lett. 2004, 203, 127-137.
13. Kettmann, V.; Kosfálová, D.; Jantová, S.; Cernáková, M.; Drímal, J. In vitro cytotoxicity of berberine against HeLa and L1210 cancer cell lines. Pharmazie 2004, 59, 548-551. (Pubitemid 38962828)
14. Stermitz, F.R.; Lorenz, P.; Tawara, J.N.; Zenewicz, L.A.; Lewis, K. Synergy in a medicinal plant: Antimicrobial action of berberine potentiated by 5-methoxyhydrocarpin, a multidrug pump inhibitor. Proc. Natl. Acad. Sci. USA 2000, 97, 1433-1437. (Pubitemid 30118458)
15. Racková, L.; Májeková, M.; Kost'álová, D.; Stefek, M. Antiradical and antioxidant activities of alkaloids isolated from Mahonia aquifoliu. Structural aspects. Bioorg. Med. Chem. 2003, 12, 4709-4715. (Pubitemid 39044358)
16. Iwasa, K.; Kamigauchi, M.; Ueki, M.; Taniguchi, M. Antibacterial activity and structure-activity relationships of berberine analogs. Eur. J. Med. Chem. 1996, 31, 469-478. (Pubitemid 26188038)
17. Jung, H.A.; Min, B.S.; Yokozawa, T.; Lee, J.H.; Kim, Y.S.; Choi, J.S. Anti-Alzheimer and antioxidant activities of Coptidis Rhizoma alkaloids. Biol. Pharm. Bull. 2009, 32, 1433-1438.
18. Zhu, F.; Qian, C. 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 Neurosci. 2006, 7, 78.
19. Jomova, K.; Vondrakova, D.; Lawson, M.; Valko, M. Metals, oxidative stress and neurodegenerative disorders. Mol. Cell Biochem. 2010, 345, 91-104.
20. Markesbery, W.R. Oxidative stress hypothesis in Alzheimer's disease. Free Radic. Biol. Med. 1997, 23, 134-147. (Pubitemid 27217017)
21. Agostinho, P.; Cunha, R.A.; Oliveira, C. Neuroinflammation, oxidative stress and the pathogenesis of Alzheimer's disease. Curr. Pharm. Des. 2010, 16, 2766-2778.
22. Butterfield, D.A.; Reed, T.; Newman, S.F.; Sultana, R. Roles of amyloid beta-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment. Free Radic. Biol. Med. 2007, 43, 658-677. (Pubitemid 47102132)
23. Racková, L.; Májeková, M.; Kost'álová, D.; Stefek, M. Antiradical and antioxidant activities of alkaloids isolated from Mahonia aquifolium. Structural aspects. Bioorg. Med. Chem. 2004, 12, 4709-4715. (Pubitemid 39044358)
24. Yokozawa, T.; Satoh, A.; Cho, EJ.; Kashiwada, Y.; Ikeshiro, Y. Protective role of Coptidis Rhizoma alkaloids against peroxynitrite-induced damage to renal tubular epithelial cells. J. Pharm. Pharmacol. 2005, 57, 367-374. (Pubitemid 40314436)
25. Yokozawa, T.; Ishida, A.; Kashiwada, Y.; Cho, EJ.; Kim, H.Y.; Ikeshiro, Y. Coptidis Rhizoma: Protective effects against peroxynitrite-induced oxidative damage and elucidation of its active components. J. Pharm. Pharmacol. 2004, 56, 547-556. (Pubitemid 38455621)
26. Sarna, L.K.; Wu, N.; Hwang, S.Y.; Siow, Y.L.; Karmin, O. Berberine inhibits NADPH oxidase mediated superoxide anion production in macrophages. Can. J. Physiol. Pharmacol. 2010, 88, 369-378.
27. Hsieh, Y.S.; Kuo, W.H.; Lin, T.W.; Chang, H.R.; Lin, T.H.; Chen, P.N.; Chu, S.C. Protective effects of berberine against low-density lipoprotein (LDL) oxidation and oxidized LDL-induced cytotoxicity on endothelial cells. J. Agric. Food Chem. 2007, 55, 10437-10445.
28. Shirwaikar, A.; Shirwaikar, A.; Rajendran, K.; Punitha, I.S. In vitro antioxidant studies on the benzyl tetra isoquinoline alkaloid berberine. Biol. Pharm. Bull. 2006, 29, 1906-1910. (Pubitemid 44338416)
29. Scarpini, E.; Scheltens, P.; Feldman, H. Treatment of Alzheimer's disease: Current status and new perspectives. Lancet Neurol. 2003, 2, 539-547. (Pubitemid 36994993)
30. Greig, N.H.; Utsuki, T.; Yu, Q.; Zhu, X.; Holloway, H.W.; Perry, T.; Lee, B.; Ingram, D.K.; Lahiri, D.K. A new therapeutic target in Alzheimer's disease treatment: Attention to butyrylcholinesterase. Curr. Med. Res. Opin. 2001, 17, 159-165. (Pubitemid 34003119)
31. Barber, K.; Mesulam, M.M.; Kraft, G.A.; Klein, W.L. Butyrylcholinesterase alters the aggregation state ofß-amyloid. Proc. Soc. Neurosci. 1996, 72, 1172.
32. Lehmann, D.; Johnston, C.; Smith, A.D. Synergy between the genes for butyrylcholinesterase K variant apolipoprotein E4 in late-onset confirmed Alzheimer's disease. Hum. Mol. Genet. 1997, 6, 933-935.
33. Hung, T.M.; Na, M.; Dat, N.T.; Ngoc, T.M.; Youn, U.; Kim, HJ.; Min, B.S.; Lee, J.; Bae, K. Cholinesterase inhibitory and anti-amnesic activity of alkaloids from Corydalis turtschaninovii. J. Ethnopharmacol. 2008, 119, 74-80.
34. Ingkaninan, K.; Phengpa, P.; Yuenyongsawad, S.; Khorana, N. Acetylcholinesterase inhibitors from Stephania venosa tuber. J. Pharm. Pharmacol. 2006, 58, 695-700.
35. Huang, L.; Shi, A.; He, F.; Li, X. Synthesis, biological evaluation, and molecular modeling of berberine derivatives as potent acetylcholinesterase inhibitors. Bioorg. Med. Chem. 2010, 18, 1244-1251.
36. Kim, D.K.; Lee, K.T.; Baek, N.I.; Kim, S.H.; Park, H.W.; Lim, J.P.; Shin, T.Y.; Eom, D.O.; Yang, J.H.; Eun, J.S. Acetylcholinesterase inhibitors from the aerial parts of Corydalis speciosa. Arch. Pharm. Res. 2004, 27, 1127-1131.
37. Huang, L.; Luo, Z.; He, F.; Shi, A.; Qin, F.; Li, X. Berberine derivatives, with substituted amino groups linked at the 9-position, as inhibitors of acetylcholinesterase/butyrylcholinesterase. Bioorg. Med. Chem. Lett. 2010, 20, 6649-6652.
38. Xiang, J.; Yu, C.; Yang, F. Conformation-activity studies on the interaction of berberine with acetylcholinesterase: Physical chemistry approach. Prog. Nat Sci. 2009, 19, 1721-1725.
39. Riederer, P.; Lachenmayer, L.; Laux, G. Clinical applications of MAO-inhibitors. Curr. Med. Chem. 2004, 11, 2033-2043. (Pubitemid 38967728)
40. Riederer, P.; Danielczyk, W.; Grünblatt, E. Monoamine oxidase-B inhibition in Alzheimer's disease. Neurotoxicology 2004, 25, 271-277. (Pubitemid 38044188)
41. Kong, L.D.; Cheng, C.H.; Tan, R.X. Monoamine oxidase inhibitors from rhizoma of Coptis chinensis. Planta Med. 2001, 67, 74-76. (Pubitemid 32199950)
42. Lee, S.S.; Kai, M.; Lee, M.K. Effects of natural isoquinoline alkaloids on monoamine oxidase activity in mouse brain: Inhibition by berberine and palmatine. Med. Sci. Res. 1999, 27, 749-751. (Pubitemid 29535079)
43. Kulkarni, S.K.; Dhir, A. On the mechanism of antidepressant-like action of berberine chloride. Eur. J. Pharmacol. 2008, 589,163-172.
44. Castillo, J.; Hung, J.; Rodriguez, M.; Bastidas, E.; Laboren, I.; Jaimes, A. LED fluorescence spectroscopy for direct determination of monoamine oxidase B inactivation. Anal. Biochem. 2005, 343, 293-298. (Pubitemid 41074043)
45. Asai, M.; Iwata, N.; Yoshikawa, A.; Aizaki, Y.; Ishiura, S.; Saido, T.C.; Maruyama, K. Berberine alters the processing of Alzheimer's amyloid precursor protein to decrease Abeta secretion. Biochem. Biophys. Res. Commun. 2007, 352, 498-502. (Pubitemid 44838513)
46. Wolozin, B.; Kellman, W.; Ruosseau, P.; Celesi,a G.G.; Siegel, G. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3- methyglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 2000, 57, 1439-1443.
47. Simons, M.; Keller, P.; Dichgans, J.; Schulz, J.B. Cholesterol and Alzheimer's disease: Is there a link? Neurology 2001, 57, 1089-1093. (Pubitemid 32880208)
48. Puglielli, L.; Tanzi, R.E.; Kovacs, D.M. Alzheimer's disease: The cholesterol connection. Nat Neurosci. 2003, 6, 345-351. (Pubitemid 36373979)
49. Wolozin, B. Cholesterol and the biology of Alzheimer's disease. Neuron 2004, 41, 7-10. (Pubitemid 38068431)
50. Kong, W.; Wei, J.; Abidi, P.; Lin, M.; Inaba, S.; Li, C.; Wang, Y.; Wang, Z.; Si, S.; Pan, H.; et al. Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med. 2004, 10, 1344-1351. (Pubitemid 40022716)
51. Akter, K.; Lanza, E.A.; Martin, S.A.; Myronyuk, N.; Rua, M.; Raffa, R.B. Diabetes mellitus and Alzheimer's disease: Shared pathology and treatment? Br. J. Clin. Pharmacol. 2011, 71, 365-376.
52. McClean, P.L.; Parthsarathy, V.; Faivre, E.; Hölscher, C. The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease. J. Neurosci. 2011, 31, 6587-6594.
53. Zhang, Y.; Li, X.; Zou, D.; Liu, W.; Yang, J.; Zhu, N.; Huo, L.; Wang, M.; Hong, J.; Wu, P.; et al. Treatment of type 2 diabetes and dyslipidemia with the natural plant alkaloid berberine. J. Clin. Endocrinol. Metab. 2008, 93, 2559-2565. (Pubitemid 352008520)
54. Yin, J.; Xing, H.; Ye, J. Efficacy of berberine in patients with type 2 diabetes mellitus. Metabolism 2008, 57, 712-717. (Pubitemid 351608234)
55. Bhutada, P.; Mundhada, Y.; Bansod, K.; Tawari, S.; Patil, S.; Dixit, P.; Umathe, S.; Mundhada, D. Protection of cholinergic and antioxidant system contributes to the effect of berberine ameliorating memory dysfunction in rat model of streptozotocin-induced diabetes. Behav. Brain Res. 2011, 220, 30-41.
56. Chen, J.X.; Yan, S.S. Role of mitochondrial amyloid-beta in Alzheimer's disease. J. Alzheimer's Dis. 2010, 20, S569-S578.
57. Hölscher, C. The role of GLP-1 in neuronal activity and neurodegeneration. Vitam. Horm. 2010, 84, 331-354.
58. Perry, T.; Greig, N.H. The glucagon-like peptides: A new genre in therapeutic targets for intervention in Alzheimer's disease. J. Alzheimer's Dis. 2002, 4, 487-496. (Pubitemid 36142838)
59. Lu, S.S.; Yu, Y.L.; Zhu, HJ.; Liu, X.D.; Liu, L.; Liu, Y.W.; Wang, P.; Xie, L.; Wang, GJ. Berberine promotes glucagon-like peptide-1 (7-36) amide secretion in streptozotocin-induced diabetic rats. J. Endocrinol. 2009, 200, 159-165.
60. Yu, Y.; Liu, L.; Wang, X.; Liu, X.; Liu, X.; Xie, L.; Wang, G. Modulation of glucagon-like peptide-1 release by berberine: In vivo and in vitro studies. Biochem. Pharmacol. 2010, 79, 1000-1006.
61. Pereira, C.V.; Machado, N.G.; Oliveira, PJ. Mechanisms of berberine (natural yellow 18)-induced mitochondrial dysfunction: Interaction with the adenine nucleotide translocator. Toxicol. Sci. 2008, 105, 408-417.
62. Pereira, G.C.; Branco, A.F.; Matos, J.A.; Pereira, S.L.; Parke, D.; Perkins, E.L.; Serafim, T.L.; Sardão V.A.; Santos, M.S.; Moreno, AJ.; et al. Mitochondrially targeted effects of berberine [Natural Yellow 18, 5,6-dihydro-9,10-dimethoxybenzo(g)-1,3-benzodioxolo(5,6-a) quinolizinium] on K1735-M2 mouse melanoma cells: Comparison with direct effects on isolated mitochondrial fractions. J. Pharmacol. Exp. Ther. 2007, 323, 636-649. (Pubitemid 350005145)
63. Rabbani, G.H.; Butler, T.; Knight, J.; Sanyal, S.C.; Alam, K. Randomized controlled trial of berberine sulfate therapy for diarrhea due to enterotoxigenic Escherichia coli and Vibrio cholerae. J. Infect. Dis. 1987, 155, 979-984. (Pubitemid 17062836)
64. Birdsall, T.C.; Kelly, G.S. Berberine: Therapeutic potential of an alkaloid found in several medicinal plants. Altern. Med. Rev. 1997, 2, 94-103. (Pubitemid 127735667)
65. Diogo, C.V.; Machado, N.G.; Barbosa, I.A.; Serafim, T.L.; Burgeiro, A.; Oliveira, PJ. Berberine as a promising safe anti-cancer agent - is there a role for mitochondria? Curr. Drug Targets 2011, 12, 850-859.
66. Imanshahidi, M.; Hosseinzadeh, H. Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine. Phytother. Res. 2008, 22, 999-1012.
67. Ye, M.; Fu, S.; Pi, R.; He, F. Neuropharmacological and pharmacokinetic properties of berberine: A review of recent research. J. Pharm. Pharmacol. 2009, 61, 831-837.
68. Wang, X.; Wang, R.; Xing, D.; Su, H.; Ma, C.; Ding, Y.; Du, L. Kinetic difference of berberine between hippocampus and plasma in rat after intravenous administration of Coptidis rhizoma extract. Life Sci. 2005, 77, 3058-3067. (Pubitemid 41423743)