Hippocampal synaptic plasticity restoration and anti-apoptotic effect underlie berberine improvement of learning and memory in streptozotocin-diabetic rats

European Journal of Pharmacology

Volumn 698, Issue 1-3, 2013, Pages 259-266

  Kalalian Moghaddam, Hamid ^a   Baluchnejadmojarad, Tourandokht ^a   Roghani, Mehrdad ^b   Goshadrou, Fatemeh ^c   Ronaghi, Abdolaziz ^c  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b SHAHED UNIVERSITY   (Iran)

^c SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Apoptosis; Berberine; Diabetes mellitus; Learning and memory; Streptozotocin; Synaptic plasticity

Indexed keywords

BERBERINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; LEARNING DISORDER; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; NERVE CELL PLASTICITY; NEUROPROTECTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPIKE; STREPTOZOCIN DIABETES;

ADMINISTRATION, ORAL; ANIMALS; APOPTOSIS; AVOIDANCE LEARNING; BERBERINE; CA1 REGION, HIPPOCAMPAL; DENTATE GYRUS; DIABETES MELLITUS, EXPERIMENTAL; ELECTROPHYSIOLOGICAL PHENOMENA; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMORY; NEURONAL PLASTICITY; NEURONS; RATS; RATS, WISTAR; SPATIAL BEHAVIOR; SYNAPSES;

EID: 84871921455     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2012.10.020     Document Type: Article

References (63)

1. K. Abe, T. Fujimoto, T. Akaishi, and M. Misawa Basolateral amygdala D1- and D2-dopaminergic system promotes the formation of long-term potentiation in the dentate gyrus of anesthetized rats Prog. Neuropsychopharmacol. Biol. Psychiatry 33 2009 552 556
2. A. Artola Diabetes-, stress- and ageing-related changes in synaptic plasticity in hippocampus and neocortex - the same metaplastic process? Eur. J. Pharmacol. 585 2008 153 162
3. M. Bagheri, M.T. Joghataei, S. Mohseni, and M. Roghani Genistein ameliorates learning and memory deficits in amyloid beta(1-40) rat model of Alzheimer's disease Neurobiol. Learn. Mem. 95 2011 270 276
4. T. Baluchnejadmojarad, and M. Roghani Effect of naringenin on intracerebroventricular streptozotocin-induced cognitive deficits in rat: a behavioral analysis Pharmacology 78 2006 193 197 (Pubitemid 44948058)
5. T. Baluchnejadmojarad, and M. Roghani Chronic epigallocatechin-3-gallate ameliorates learning and memory deficits in diabetic rats via modulation of nitric oxide and oxidative stress Behav. Brain Res. 224 2011 305 310
6. P. Bhutada, Y. Mundhada, K. Bansod, S. Tawari, S. Patil, P. Dixit, S. Umathe, and D. Mundhada 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. 220 2011 30 41
7. G.J. Biessels, A. Kamal, G.M. Ramakers, I.J. Urban, B.M. Spruijt, D.W. Erkelens, and W.H. Gispen Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats Diabetes 45 1996 1259 1266 (Pubitemid 26296329)
8. G.J. Biessels, A. Kamal, I.J. Urban, B.M. Spruijt, D.W. Erkelens, and W.H. Gispen Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: effects of insulin treatment Brain Res. 800 1998 125 135 (Pubitemid 28361929)
9. G.J. Biessels, A. Kerssen, E.H. de Haan, and L.J. Kappelle Cognitive dysfunction and diabetes: implications for primary care Primary Care Diabetes 1 2007 187 193
10. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 1993 31 39 (Pubitemid 23020772)
11. C.L. Bon, and J. Garthwaite On the role of nitric oxide in hippocampal long-term potentiation J. Neurosci. 23 2003 1941 1948 (Pubitemid 36314749)
12. A.M. Brands, G.J. Biessels, E.H. de Haan, L.J. Kappelle, and R.P. Kessels The effects of type 1 diabetes on cognitive performance: a meta-analysis Diabetes Care 28 2005 726 735 (Pubitemid 40315341)
13. Z. Cai, Y. Zhao, S. Yao, and B. Bin Zhao Increases in beta-amyloid protein in the hippocampus caused by diabetic metabolic disorder are blocked by minocycline through inhibition of NF-kappaB pathway activation Pharmacol. Rep. 63 2011 381 391
14. P.M. Canas, L.O. Porciuncula, G.M. Cunha, C.G. Silva, N.J. Machado, J.M. Oliveira, C.R. Oliveira, and R.A. Cunha Adenosine A2A receptor blockade prevents synaptotoxicity and memory dysfunction caused by beta-amyloid peptides via p38 mitogen-activated protein kinase pathway J. Neurosci. 29 2009 14741 14751
15. C.H. Chae, S.L. Jung, S.H. An, B.Y. Park, S.W. Wang, I.H. Cho, J.Y. Cho, and H.T. Kim Treadmill exercise improves cognitive function and facilitates nerve growth factor signaling by activating mitogen-activated protein kinase/extracellular signal-regulated kinase1/2 in the streptozotocin-induced diabetic rat hippocampus Neuroscience 164 2009 1665 1673
16. D.M. Chetkovich, E. Klann, and J.D. Sweatt Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus Neuroreport 4 1993 919 922 (Pubitemid 23202249)
17. S.Z. Choi, and M.W. Son Novel botanical drug for the treatment of diabetic neuropathy Arch. Pharm. Res. 34 2011 865 867
18. A. Cok, C. Plaisier, M.J. Salie, D.S. Oram, J. Chenge, and L.L. Louters Berberine acutely activates the glucose transport activity of GLUT1 Biochimie 93 2011 1187 1192
19. D. Comin, L. Gazarini, J.N. Zanoni, H. Milani, and R.M. de Oliveira Vitamin E improves learning performance and changes the expression of nitric oxide-producing neurons in the brains of diabetic rats Behav. Brain Res. 210 2010 38 45
20. S.F. Cooke, and T.V.P. Bliss Plasticity in the human central nervous system Brain 129 2006 1659 1673 (Pubitemid 43999401)
21. J.M. Duarte, P.M. Agostinho, R.A. Carvalho, and R.A. Cunha Caffeine consumption prevents diabetes-induced memory impairment and synaptotoxicity in the hippocampus of NONcZNO10/LTJ mice PLoS One 7 2012 e21899
22. S.S. Durairajan, L.F. Liu, J.H. Lu, L.L. Chen, Q. Yuan, S.K. Chung, L. Huang, X.S. Li, J.D. Huang, and M. Li Berberine ameliorates beta-amyloid pathology, gliosis, and cognitive impairment in an Alzheimer's disease transgenic mouse model Neurobiol. Aging 33 2012 2903 2919
23. B.M. Frier Cognitive functioning in type 1 diabetes: the Diabetes Control and Complications Trial (DCCT) revisited Diabetologia 54 2011 233 236
24. K. Fukui, N.O. Omoi, T. Hayasaka, T. Shinnkai, S. Suzuki, K. Abe, and S. Urano Cognitive impairment of rats caused by oxidative stress and aging, and its prevention by vitamin E Ann. N. Y. Acad. Sci. 959 2002 275 284 (Pubitemid 34457568)
25. Y. Gu, Y. Zhang, X. Shi, X. Li, J. Hong, J. Chen, W. Gu, X. Lu, G. Xu, and G. Ning Effect of traditional Chinese medicine berberine on type 2 diabetes based on comprehensive metabonomics Talanta 81 2010 766 772
26. C. Holscher Different strains of rats show different sensitivity to block of long-term potentiation by nitric oxide synthase inhibitors Eur. J. Pharmacol. 457 2002 99 106 (Pubitemid 35452544)
27. J.S. Hong, Y.K. Chu, H. Lee, B.H. Ahn, J.H. Park, M.J. Kim, S. Lee, H.S. Ryoo, J.H. Jang, S.R. Lee, and J.W. Park Effects of berberine on hippocampal neuronal damage and matrix metalloproteinase-9 activity following transient global cerebral ischemia J. Neurosci. Res. 90 2012 489 497
28. J. Hu, Y. Chai, Y. Wang, M.M. Kheir, H. Li, Z. Yuan, H. Wan, D. Xing, F. Lei, and L. Du PI3K p55gamma promoter activity enhancement is involved in the anti-apoptotic effect of berberine against cerebral ischemia-reperfusion Eur. J. Pharmacol. 674 2012 132 142
29. L. Huang, A.D. Shi, F. He, and X.S. Li Synthesis, biological evaluation, and molecular modeling of berberine derivatives as potent acetylcholinesterase inhibitors Bioorg. Med. Chem. 18 2010 1244 1251
30. M. Imanshahidi, and H. Hosseinzadeh Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine Phytother. Res. 22 2008 999 1012
31. T. Iwai, M. Suzuki, K. Kobayashi, K. Mori, Y. Mogi, and J. Oka The influences of juvenile diabetes on memory and hippocampal plasticity in rats: improving effects of glucagon-like peptide-1 Neurosci. Res. 64 2009 67 74
32. J.O. Kang, S.K. Kim, S.E. Hong, T.H. Lee, and C.J. Kim Low dose radiation overcomes diabetes-induced suppression of hippocampal neuronal cell proliferation in rats J. Korean Med. Sci. 21 2006 500 505
33. V. Khan, A.K. Najmi, M. Akhtar, M. Aqil, M. Mujeeb, and K.K. Pillai A pharmacological appraisal of medicinal plants with antidiabetic potential J. Pharm. Bioallied Sci. 4 2012 27 42
34. W.J. Kong, H. Zhang, D.Q. Song, R. Xue, W. Zhao, J. Wei, Y.M. Wang, N. Shan, Z.X. Zhou, P. Yang, X.F. You, Z.R. Li, S.Y. Si, L.X. Zhao, H.N. Pan, and J.D. Jiang Berberine reduces insulin resistance through protein kinase C-dependent up-regulation of insulin receptor expression Metab. Clin. Exp. 58 2009 109 119
35. V. Kucukatay, A. Agar, S. Gumuslu, and P. Yargicoglu Effect of sulfur dioxide on active and passive avoidance in experimental diabetes mellitus: relation to oxidant stress and antioxidant enzymes Int. J. Neurosci. 117 2007 1091 1107 (Pubitemid 47026890)
36. S.K. Kulkarni, and A. Dhir Possible involvement of l-arginine-nitric oxide (NO)-cyclic guanosine monophosphate (cGMP) signaling pathway in the antidepressant activity of berberine chloride Eur. J. Pharmacol. 569 2007 77 83 (Pubitemid 47175875)
37. S.K. Kulkarni, and A. Dhir On the mechanism of antidepressant-like action of berberine chloride Eur. J. Pharmacol. 589 2008 163 172
38. S.K. Kulkarni, and A. Dhir On the mechanism of antidepressant-like action of berberine chloride Eur. J. Pharmacol. 589 2008 163 172
39. S.K. Kulkarni, and A. Dhir Berberine: a plant alkaloid with therapeutic potential for central nervous system disorders Phytother. Res. 24 2010 317 324
40. Z.G. Li, W. Zhang, G. Grunberger, and A.A. Sima Hippocampal neuronal apoptosis in type 1 diabetes Brain Res. 946 2002 221 231 (Pubitemid 34876334)
41. E. Mossello, E. Ballini, M. Boncinelli, M. Monami, G. Lonetto, A.M. Mello, F. Tarantini, S. Baldasseroni, E. Mannucci, and N. Marchionni Glucagon-like peptide-1, diabetes, and cognitive decline: possible pathophysiological links and therapeutic opportunities Exp. Diabetes Res. 2011 2011 281674
42. D. Muller, I. Nikonenko, P. Jourdain, and S. Alberi LTP, memory and structural plasticity Curr. Mol. Med. 2 2002 605 611 (Pubitemid 35256292)
43. E.A. Northam, D. Rankins, A. Lin, R.M. Wellard, G.S. Pell, S.J. Finch, G.A. Werther, and F.J. Cameron Central nervous system function in youth with type 1 diabetes 12 years after disease onset Diabetes Care 32 2009 445 450
44. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 2nd ed. 1986 Academic Press San Diego
45. W.H. Peng, M.T. Hsieh, and C.R. Wu Effect of long-term administration of berberine on scopolamine-induced amnesia in rats Jpn. J. Pharmacol. 74 1997 261 266
46. D.W. Porter, B.D. Kerr, P.R. Flatt, C. Holscher, and V.A. Gault Four weeks administration of Liraglutide improves memory and learning as well as glycaemic control in mice with high fat dietary-induced obesity and insulin resistance Diabetes Obes. Metab. 12 2010 891 899
47. H. Rasoolijazi, M.T. Joghataie, M. Roghani, and M. Nobakht The beneficial effect of (-)-epigallocatechin-3-gallate in an experimental model of Alzheimer's disease in rat: a behavioral analysis Iran Biomed. J. 11 2007 237 243 (Pubitemid 350021925)
48. P. Reisi, S. Babri, H. Alaei, M.R. Sharifi, G. Mohaddes, and R. Lashgari Effects of treadmill running on short-term pre-synaptic plasticity at dentate gyrus of streptozotocin-induced diabetic rats Brain Res. 1211 2008 30 36
49. P. Reisi, S. Babri, H. Alaei, M.R. Sharifi, G. Mohaddes, S.M. Noorbakhsh, and R. Lashgari Treadmill running improves long-term potentiation (LTP) defects in streptozotocin-induced diabetes at dentate gyrus in rats Pathophysiology 17 2010 33 38
50. J.W. Russell, and E.L. Feldman Insulin-like growth factor-I prevents apoptosis in sympathetic neurons exposed to high glucose Horm. Metab. Res. 31 1999 90 96 (Pubitemid 29169481)
51. A. Sherin, J. Anu, K.T. Peeyush, S. Smijin, M. Anitha, B.T. Roshni, and C.S. Paulose Cholinergic and GABAergic receptor functional deficit in the hippocampus of insulin-induced hypoglycemic and streptozotocin-induced diabetic rats Neuroscience 202 2012 69 76
52. A.M. Stranahan, K. Lee, P.J. Pistell, C.M. Nelson, N. Readal, M.G. Miller, E.L. Spangler, D.K. Ingram, and M.P. Mattson Accelerated cognitive aging in diabetic rats is prevented by lowering corticosterone levels Neurobiol. Learn. Mem. 90 2008 479 483
53. F. Wang, G. Zhao, L. Cheng, H.Y. Zhou, L.Y. Fu, and W.X. Yao Effects of berberine on potassium currents in acutely isolated CA1 pyramidal neurons of rat hippocampus Brain Res. 999 2004 91 97 (Pubitemid 38121454)
54. X. Wang, W. Zheng, J.W. Xie, T. Wang, S.L. Wang, W.P. Teng, and Z.Y. Wang Insulin deficiency exacerbates cerebral amyloidosis and behavioral deficits in an Alzheimer transgenic mouse model Mol. Neurodegener. 5 2010 46
55. L. Ye, F. Wang, and R.H. Yang Diabetes impairs learning performance and affects the mitochondrial function of hippocampal pyramidal neurons Brain Res. 1411 2011 57 64
56. Y. Yu, L. Liu, X. Wang, X. Liu, L. Xie, and G. Wang Modulation of glucagon-like peptide-1 release by berberine: in vivo and in vitro studies Biochem. Pharmacol. 79 2010 1000 1006
57. A.V. Zarch, H.P. Toroudi, M. Soleimani, A. Bakhtiarian, M. Katebi, and B. Djahanguiri Neuroprotective effects of diazoxide and its antagonism by glibenclamide in pyramidal neurons of rat hippocampus subjected to ischemia-reperfusion-induced injury Int. J. Neurosci. 119 2009 1346 1361
58. Y.F. Zhang, X.Y. Li, D.J. Zou, W. Liu, J.L. Yang, N. Zhu, L. Huo, M.A. Wang, J. Hong, P.H. Wu, G.G. Ren, and G. Ning Treatment of type 2 diabetes and dyslipidemia with the natural plant alkaloid berberine J. Clin. Endocrinol. Metab. 93 2008 2559 2565 (Pubitemid 352008520)
59. H.L. Zhao, Y. Sui, C.F. Qiao, K.Y. Yip, R.K. Leung, S.K. Tsui, H.M. Lee, H.K. Wong, X. Zhu, J.J. Siu, L. He, J. Guan, L.Z. Liu, H.X. Xu, P.C. Tong, and J.C. Chan Sustained antidiabetic effects of a berberine-containing Chinese herbal medicine through regulation of hepatic gene expression Diabetes 61 2012 933 943
60. 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 82 2011 184 189
61. J.Y. Zhou, S.W. Zhou, J.L. Tang, K.B. Zhang, L.X. Guang, Y.P. Huang, Y. Xu, Y. Ying, L. Zhang, and D.D. Li Protective effect of berberine on beta cells in streptozotocin- and high-carbohydrate/high-fat diet-induced diabetic rats Eur. J. Pharmacol. 606 2009 262 268
62. F.Q. Zhu, and C.Y. Qian Berberine chloride can ameliorate the spatial memory impairment and increase the expression of interleukin-1 beta and inducible nitric oxide synthase in the rat model of Alzheimer's disease BMC Neurosci. 7 2006 78
63. Zhu, X., Guo, X., Mao, G., Gao, Z., Wang, H., He, Q., Li, D. Hepatoprotection of berberine against hydrogen peroxide-induced apoptosis by upregulation of sirtuin 1. Phytother. Res., http://dx.doi.org/10.1002/ptr.4728, in press.