Possible role of P-glycoprotein in the neuroprotective mechanism of berberine in intracerebroventricular streptozotocin-induced cognitive dysfunction

Psychopharmacology

Volumn 233, Issue 1, 2016, Pages 137-152

  Kumar, Anil ^a   Ekavali, ^a   Mishra, Jitendriya ^a   Chopra, Kanwaljit ^a   Dhull, Dinesh K ^a  

^a PANJAB UNIVERSITY   (India)

Author keywords

Alzheimer; Berberine; Cognition; Neuroinflammation; Neuroprotection; Oxidative stress; P glycoprotein; Streptozotocin; Verapamil

Indexed keywords

BERBERINE; MEMANTINE; MULTIDRUG RESISTANCE PROTEIN; STREPTOZOCIN; VERAPAMIL; NEUROPROTECTIVE AGENT;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BEHAVIOR CHANGE; CALCIUM HOMEOSTASIS; COGNITIVE DEFECT; CONTROLLED STUDY; DEMENTIA; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG DOSE COMPARISON; DRUG POTENTIATION; HISTOPATHOLOGY; MALE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; COGNITION DISORDERS; DRUG EFFECTS; MAZE TEST; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ANIMALS; BERBERINE; COGNITION DISORDERS; MALE; MAZE LEARNING; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; P-GLYCOPROTEIN; RATS; RATS, WISTAR; STREPTOZOCIN; VERAPAMIL;

EID: 84952893165     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-015-4095-7     Document Type: Article

References (91)

1. Agrawal R, Tyagi E, Shukla R, Nath C (2009) A study of brain insulin receptors, AChE activity and oxidative stress in rat model of ICV STZ induced dementia. Neuropharmacology 56:779-787
2. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J et al (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421
3. Berman SB, Hastings TG (1999) Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: implications for Parkinson's disease. J Neurochem 73(3):1127-1137
4. Bhutada P, Mundhada Y, Bansod K, Tawari S, Patil S et al (2011) 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 220:30-41
5. Birdsall TC, Kelly GS (1997) Berberine therapeutic potential of an alkaloid found in several medicinal plants. Altern Med Rev 2:94-103
6. Bojarski L, Herms J, Kuznicki J (2008) Calcium dysregulation in Alzheimer's disease. Neurochem Int 52:621-633
7. Buchhave P, Zetterberg H, Blennow K, Minthon L, Janciauskiene S, Hansson O (2010) Soluble TNF receptors are associated with Abeta metabolism and conversion to dementia in subjects with mild cognitive impairment. Neurobiol Aging 31:1877-1884
8. Butterfield DA (2014) The 2013 discovery award from the society for free radical biology and medicine: selected discoveries from the Butterfield Laboratory of Oxidative Stress and its sequelae in brain in cognitive disorders exemplified by Alzheimer disease and chemotherapy induced cognitive impairment. Free Radic Biol Med 74:157-174
9. Butterfield DA, Howard B, Yatin S, Koppal T, Drake J et al (1999) Elevated oxidative stress in models of normal brain aging and Alzheimer's disease. Life Sci 65:1883-1892
10. Choi JS, Li X (2005) The effect of verapamil on the pharmacokinetics of paclitaxel in rats. Eur J Pharm Sci 24:95-100
11. Correia SC, Santos RX, Carvalho C, Cardoso S, Candeias E et al (2012) Insulin signaling, glucose metabolism and mitochondria: major players in Alzheimer's disease and diabetes interrelation. Brain Res 1441:64-78
12. Eckert A, Schmitt K, Gotz J (2011) Mitochondrial dysfunction - the beginning of the end in Alzheimer's disease? Separate and synergistic modes of tau and amyloid-beta toxicity. Alzheimers Res Ther 3:15
13. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70-77
14. Ellman GL, Courtney KD, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88-95
15. Essali A, Deirawan H, Soares-Weiser K, Adams CE (2011) Calcium channel blockers for neuroleptic-induced tardive dyskinesia. Cochrane Database of Systemic Reviews 11: CDO, 00206.
16. Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751-766
17. Grammas P (2011) Neurovascular dysfunction, inflammation and endothelial activation: implications for the pathogenesis of Alzheimer's disease. J Neuroinflammation 8:26
18. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131-138
19. Griffin WS, Sheng JG, Roberts GW, Mrak RE (1995) Interleukin-1 expression in different plaque types in Alzheimer's disease: significance in plaque evolution. J Neuropathol Exp Neurol 54:276-281
20. Grünblatt E, Salkovic-Petrisic M, Osmanovic J, Riederer P, Hoyer S (2007) Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J Neurochem 101:757-770
21. Harris ME, Carney JM, Cole PS, Hensley K, Howard BJ et al (1995) [beta]-Amyloid peptide-derived, oxygen-dependent free radicals inhibit glutamate uptake in cultured astrocytes: implications for Alzheimer's disease. Neuroreport 6:1875-1879
22. He P, Zhong Z, Lindholm K, Berning L, Lee W et al (2007) Deletion of tumor necrosis factor death receptor inhibits amyloid beta generation and prevents learning and memory deficits in Alzheimer's mice. J Cell Biol 178:829-841
23. Hoyer S, Lannert H (2008) Long-term effects of corticosterone on behavior, oxidative and energy metabolism of parietotemporal cerebral cortex and hippocampus of rats: comparison to intracerebroventricular streptozotocin. J Neural Transm 115:1241-1249
24. Hsu YY, Tseng YT, Lo YC (2013) Berberine, a natural antidiabetes drug, attenuates glucose neurotoxicity and promotes Nrf2-related neurite outgrowth. Toxicol Appl Pharmacol 272:787-796
25. Javed H, Khan M, Ahmad A, Vaibhav K, Ahmad M et al (2012) Rutin prevents cognitive impairments by ameliorating oxidative stress and neuroinflammation in rat model of sporadic dementia of Alzheimer type. Neuroscience 210:340-352
26. Ji HF, Shen L (2011) Berberine: a potential multipotent natural product to combat Alzheimer's disease. Molecules 16:6732-6740
27. Kajiyama K, Pauly DF, Hughes H, Yoon SB, Entman ML, McMillin-Wood JB (1987) Protection by verapamil of mitochondrial glutathione equilibrium and phospholipid changes during reperfusion of ischemic canine myocardium. Circ Res 61:301-310
28. Kalonia H, Kumar P, Kumar A (2011) Attenuation of proinflammatory cytokines and apoptotic process by verapamil and diltiazem against quinolinic acid induced Huntington like alterations in rats. Brain Res 1372:115-126
29. King T (1967) Preparation of succinate dehydrogenase and reconstitution of succinate oxidase. In: Estabrook R, Pullman M (eds) Methods in enzymology. Academic, New York, pp 322-331
30. King T, Howard R (1967) Preparations and properties of soluble NADH dehydrogenases from cardiac muscle. In: Estabrook R, Pullman M (eds) Methods in enzymology. Academic, New York, pp 275-294
31. Kono Y (1978) Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186:189-195
32. Kovalskii I, Krasnyuk I, Krasnyuk I Jr, Nikulina O, Belyatskaya A et al (2014) Mechanisms of rutin pharmacological action (review). Pharm Chem J 48:73-76
33. Kuhlmann O, Carlile D, Noe J, Bentley D (2014) Interaction potential of Carmegliptin with P-glycoprotein (Pgp) transporter in healthy volunteers. J Drug Assessment 3:28-37
34. Kulkarni S, Dhir A (2010) Berberine: a plant alkaloid with therapeutic potential for central nervous system disorders. Phytother Res 24:317-324
35. Kumar A, Dogra S (2008) Neuropathology and therapeutic management of Alzheimer's disease - an update. Drugs Future 33:433-446
36. Kumar A, Prakash A, Pahwa D, Mishra J (2012) Montelukast potentiates the protective effect of rofecoxib against kainic acid-induced cognitive dysfunction in rats. Pharmacol Biochem Behavior 103:43-52
37. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787-795
38. Liu Y, Lo YC, Qian L, Crews FT, Wilson B et al (2011) Verapamil protects dopaminergic neuron damage through a novel anti-inflammatory mechanism by inhibition of microglial activation. Neuropharmacology 60:373-380
39. Luck H (1965) Catalase. In: Hans UB (ed) Methods of enzymatic analysis. Academic, New York, pp 885-894
40. Lupo E, Locher R, Weisser B, Vetter W (1994) In vitro antioxidant activity of calcium antagonists against LDL oxidation compared with α-tocopherol. Biochem Biophys Res Commun 203:1803-1808
41. Maeng HJ, Yoo HJ, Kim IW, Song IS, Chung SJ, Shim CK (2002) P-glycoprotein-mediated transport of berberine across Caco-2 cell monolayers. J Pharm Sci 91:2614-2621
42. Mak I, Weglicki W (1990) Comparative antioxidant activities of propranolol, nifedipine, verapamil, and diltiazem against sarcolemmal membrane lipid peroxidation. Circ Res 66:1449-1452
43. Marier JF, Deschênes JL, Hage A, Seliniotakis E, Gritsas A et al (2005) Enhancing the uptake of dextromethorphan in the CNS of rats by concomitant administration of the P-gp inhibitor verapamil. Life Sci 77:2911-2926
44. 2+ homeostasis and cell death. J Neurosci 15:6239-6249
45. Mason RP, Mak IT, Trumbore MW, Mason PE (1999) Antioxidant properties of calcium antagonists related to membrane biophysical interactions. Am J Cardiol 84:16-22
46. Mehla J, Pahuja M, Gupta P, Dethe S, Agarwal A, Gupta YK (2013) Clitoria ternatea ameliorated the intracerebroventricularly injected streptozotocin induced cognitive impairment in rats: behavioral and biochemical evidence. Psychopharmacology (Berl) 230:589-605
47. Misra S, Tiwari V, Kuhad A, Chopra K (2011) Modulation of nitrergic pathway by sesamol prevents cognitive deficits and associated biochemical alterations in intracerebroventricular streptozotocin administered rats. Eur J Pharmacol 659:177-186
48. Morales I, Guzmán-Martínez L, Cerda-Troncoso C, Farías GA, Maccioni RB (2014) Neuroinflammation in the pathogenesis of Alzheimer's disease. A rational framework for the search of novel therapeutic approaches. Front Cell Neurosci 8:1-9
49. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60
50. Nicita F, Spalice A, Papetti L, Nikanorova M, Iannetti P, Parisi P (2014) Efficacy of verapamil as an adjunctive treatment in children with drug-resistant epilepsy: a pilot study. Seizure 23:36-40
51. Nimmrich V, Eckert A (2013) Calcium channel blockers and dementia. Br J Pharmacol 169:1203-1210
52. Pagani L, Eckert A (2011) Amyloid-Beta interaction with mitochondria. Int J Alzheimers Dis 2011:1-12
53. Paola D, Domenicotti C, Nitti M, Vitali A, Borghi R et al (2000) Oxidative stress induces increase in intracellular amyloid β-protein production and selective activation of βI and βII PKCs in NT2 cells. Biochem Biophys Res Commun 268:642-646
54. Pauli-Magnus C, von Richter O, Burk O, Ziegler A, Mettang T et al (2000) Characterization of the major metabolites of verapamil as substrates and inhibitors of P-glycoprotein. J Pharmacol Exp Ther 293:376-382
55. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic, San Diego
56. Peng WH, Lo KL, Lee YH, Hung TH, Lin YC (2007) Berberine produces antidepressant-like effects in the forced swim test and in the tail suspension test in mice. Life Sci 81:933-938
57. Peng WH, Wu CR, Chen CS, Chen CF, Leu ZC, Hsieh MT (2004) Anxiolytic effect of berberine on exploratory activity of the mouse in two experimental anxiety models: interaction with drugs acting at 5-HT receptors. Life Sci 75:2451-2462
58. Pirker S, Baumgartner C (2011) Termination of refractory focal status epilepticus by the P-glycoprotein inhibitor verapamil. Eur J Neurol 18:e151-e51
59. Plaschke K, Hoyer S (1993) Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int J Dev Neurosci 11:477-483
60. Popović M, Caballero-Bleda M, Popović N, Puelles L, van Groen T, Witter MP (2006) Verapamil prevents, in a dose-dependent way, the loss of ChAT-immunoreactive neurons in the cerebral cortex following lesions of the rat nucleus basalis magnocellularis. Exp Brain Res 170:368-3675
61. Rai S, Kamat PK, Nath C, Shukla R (2014) Glial activation and post-synaptic neurotoxicity: the key events in streptozotocin (ICV) induced memory impairment in rats. Pharmacol Biochem Behavior 117:104-117
62. Salkovic-Petrisic M, Hoyer S (2007) Central insulin resistance as a trigger for sporadic Alzheimer-like pathology: an experimental approach. J Neural Trans 72:217-233
63. Salkovic-Petrisic M, Osmanovic-Barilar J, Knezovic A, Hoyer S, Mosetter K, Reutter W (2014) Long-term oral galactose treatment prevents cognitive deficits in male Wistar rats treated intracerebroventricularly with streptozotocin. Neuropharmacology 77:68-80
64. Salkovic-Petrisic M, Tribl F, Schmidt M, Hoyer S, Riederer P (2006) Alzheimer-like changes in protein kinase B and glycogen synthase kinase-3 in rat frontal cortex and hippocampus after damage to the insulin signalling pathway. J Neurochem 96:1005-1015
65. Salmon SE, Dalton WS, Grogan TM, Plezia P, Lehnert M et al (1991) Multidrug-resistant myeloma: laboratory and clinical effects of verapamil as a chemosensitizer. Blood 78:44-50
66. Shoham S, Bejar C, Kovalev E, Schorer-Apelbaum D, Weinstock M (2007) Ladostigil prevents gliosis, oxidative-nitrative stress and memory deficits induced by intracerebroventricular injection of streptozotocin in rats. Neuropharmacology 52:836-843
67. Shoham S, Bejar C, Kovalev E, Weinstock M (2003) Intracerebroventricular injection of streptozotocin causes neurotoxicity to myelin that contributes to spatial memory deficits in rats. Exp Neurol 184:1043-1052
68. Shonesy BC, Thiruchelvam K, Parameshwaran K, Rahman EA, Karuppagounder SS et al (2012) Central insulin resistance and synaptic dysfunction in intracerebroventricular-streptozotocin injected rodents. Neurobiol Aging 33(2):430, e5-18
69. Singh DP, Chopra K (2013) Verapamil augments the neuroprotectant action of berberine in rat model of transient global cerebral ischemia. Eur J Pharmacol 720:98-106
70. Sonkusare S, Srinivasan K, Kaul C, Ramarao P (2005) Effect of donepezil and lercanidipine on memory impairment induced by intracerebroventricular streptozotocin in rats. Life Sci 77:1-14
71. Sottocasa GL, Kuylenstierna B, Ernster L, Bergstrand A (1967) An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J Cell Biol 32:415-438
72. Tan ZS, Beiser AS, Vasan RS, Roubenoff R, Dinarello CA (2007) Inflammatory markers and the risk of Alzheimer disease: the Framingham Study. Neurology 68:1902-1908
73. Tarkowski E, Andreasen N, Tarkowski A, Blennow K (2003) Intrathecal inflammation precedes development of Alzheimer's disease. J Neurol Neurosurg Psychiatry 74:1200-1205
74. Tarrago T, Kichik N, Seguí J, Giralt E (2007) The natural product berberine is a human prolyl oligopeptidase inhibitor. ChemMedChem 2:354-359
75. Thies W, Bleiler L (2013) 2013 Alzheimer's disease facts and figures. Alzheimers Dement 9:208-245
76. Tiwari V, Kuhad A, Bishnoi M, Chopra K (2009) Chronic treatment with tocotrienol, an isoform of vitamin E, prevents intracerebroventricular streptozotocin-induced cognitive impairment and oxidative-nitrosative stress in rats. Pharmacol Biochem Behavior 93:183-189
77. Tobinick EL, Gross H (2008) Rapid cognitive improvement in Alzheimer's disease following perispinal etanercept administration. J Neuroinflammation 5:2
78. Toescu EC, Verkhratsky A (2007) The importance of being subtle: small changes in calcium homeostasis control cognitive decline in normal aging. Aging Cell 6:267-273
79. Tuzcu M, Baydas G (2006) Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats. Eur J Pharmacol 537:106-110
80. Vuddanda PR, Chakraborty S, Singh S (2010) Berberine: a potential phytochemical with multispectrum therapeutic activities. Expert Opin Investig Drugs 19:1297-1307
81. Weinstock M, Shoham S (2004) Rat models of dementia based on reductions in regional glucose metabolism, cerebral blood flow and cytochrome oxidase activity. J Neural Trans 111:347-366
82. Widener LL, Mela-Riker LM (1983) Verapamil pretreatment preserves mitochondrial function and tissue magnesium in the ischemic kidney. Circ Shock 13:27-37
83. Wills E (1966) Mechanisms of lipid peroxide formation in animal tissues. Biochem J 99:667-676
84. Wisner KL, Peindl KS, Perel JM, Hanusa BH, Piontek CM, Baab S (2002) Verapamil treatment for women with bipolar disorder. Biol Psychiatry 51:745-752
85. Witte ME, Geurts JJ, De Vries HE, van der Valk P, van Horssen J (2010) Mitochondrial dysfunction: a potential link between neuroinflammation and neurodegeneration? Mitochondrion 10:411-418
86. Xiang J, Yu C, Yang F, Yang L, Ding H (2009) Conformation-activity studies on the interaction of berberine with acetylcholinesterase: physical chemistry approach. Prog Nat Sci 19:1721-1725
87. Yamamoto M, Kiyota T, Horiba M, Buescher JL, Walsh SM et al (2007) Interferon-gamma and tumor necrosis factor-alpha regulate amyloid-beta plaque deposition and beta-secretase expression in Swedish mutant APP transgenic mice. Am J Pathol 170:680-692
88. Yasojima K, Schwab C, McGeer EG, McGeer PL (1999) Up-regulated production and activation of the complement system in Alzheimer's disease brain. Am J Pathol 154:927-936
89. Zhang Y, Cui YL, Gao LN, Jiang HL (2013) Effects of beta-cyclodextrin on the intestinal absorption of berberine hydrochloride, a P-glycoprotein substrate. Int J Bio Macromol 59:363-71
90. Zhu F, Qian C (2006) 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 7:78
91. Zhu X, Raina AK, Lee H-g, Casadesus G, Smith MA, Perry G (2004) Oxidative stress signalling in Alzheimer's disease. Brain Res 1000:32-39