Role of curcumin in the prevention of cholinergic mediated cortical dysfunctions in streptozotocin-induced diabetic rats

Molecular and Cellular Endocrinology

Volumn 331, Issue 1, 2011, Pages 1-10

  Peeyush Kumar, T ^a   Antony, Sherin ^a   Soman, Smijin ^a   Kuruvilla, Korah P ^a   George, Naijil ^a   Paulose, C S ^a  

^a Department of Physics   (India)

Author keywords

Curcumin; Diabetes; Insulin and cerebral cortex; Muscarinic

Indexed keywords

ACETYLCHOLINESTERASE; BUNGAROTOXIN RECEPTOR; CHOLINE ACETYLTRANSFERASE; CURCUMIN; GLUCOSE; GLUCOSE TRANSPORTER 3; INSULIN; INSULIN RECEPTOR; MUSCARINIC M1 RECEPTOR; MUSCARINIC M3 RECEPTOR; STREPTOZOCIN; SUPEROXIDE DISMUTASE;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BRAIN CORTEX; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEUROPATHY; DISEASE ASSOCIATION; GENE EXPRESSION REGULATION; GENE LOCATION; GLUCOSE TRANSPORT; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; MALE; MAZE TEST; MORNING DOSAGE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REVIEW; STREPTOZOCIN DIABETES;

ACETYLCHOLINESTERASE; ANIMALS; ANTIBODIES; ATROPINE; CEREBRAL CORTEX; CHOLINE O-ACETYLTRANSFERASE; CURCUMIN; DIABETES MELLITUS, EXPERIMENTAL; DIPHENYLACETIC ACIDS; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORTER TYPE 3; MALE; MAZE LEARNING; PIPERIDINES; PIRENZEPINE; RATS; RATS, WISTAR; RECEPTOR, INSULIN; RECEPTOR, MUSCARINIC M1; RECEPTOR, MUSCARINIC M3; RECEPTORS, CHOLINERGIC; RECEPTORS, NICOTINIC; SUPEROXIDE DISMUTASE;

EID: 78149403787     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.07.004     Document Type: Review

References (90)

1. Ahmad M., Saleem S., Ahmad A.S., Yousuf S., Ansari M.A., Khan M.B., Ishrat T., Chaturvedi R.K., Agrawal A.K., Islam F. Ginkgo biloba affords dose-dependent protection against 6-hydroxydopamine-induced parkinsonism in rats: neurobehavioural, neurochemical and immunohistochemical evidences. J. Neurochem. 2005, 93:94-104.
2. Akwa Y., Ladurelle N., Covey D.F., Baulieu E.E. The synthetic enantiomer of pregnenolone sulfate is very active on memory in rats and mice, even more so than its physiological neurosteroid counterpart: distinct mechanisms. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:14033-14037.
3. Aragno M., Parola S., Tamagno E., Brignardello E., Manti R., Danni O., Boccuzzi G. Oxidative derangement in rat synaptosomes induced by hyperglycemia: restorative effect of dehydroepiandrosterone treatment. Biochem. Pharmacol. 2000, 60:389-395.
4. Arison R.N., Ciaccio E.I., Glitzer M.S., Cassaro A.V., Pruss M. Light and electron microscopy of lesions in rats rendered diabetic with streptozotocin. Diabetes 1967, 16:51-56.
5. Armitage A.K., Hall G.H. Sellers CM effects of nicotine on electrocortical activity and acetylcholine release from the cat cerebral cortex. Br. J. Pharmacol. 1969, 35:152-160.
6. Artola A., Kamal A., Ramakers G.M., Biessels G.J., Gispen W.H. Diabetes mellitus concomitantly facilitates the induction of long-term depression and inhibits that of long-term potentiation in hippocampus. Eur. J. Neurosci. 2005, 22:169-178.
7. Bala K., Tripathy B.C., Sharma D. Neuroprotective and antiageing effects of curcumin in aged rat brain regions. Biogerontology 2006, 7:81-89.
8. Balabanova S., Richter H.P., Antoniadis G., Homoki J., Kremmer N., Hanle J., Teller W.M. 25-Hydroxyvitamin D, 24,25-dihydroxyvitamin D and 1,25-dihydroxyvitamin D in human cerebrospinal fluid. Klin. Wochenschr. 1984, 62:1086-1090.
9. Banks W.A., Jaspan J.B., Huang W., Kastin A.J. Transport of insulin across the blood-brain barrier: saturability at euglycemic doses of insulin. Peptides 1997, 18:1423-1429.
10. Banks W.A., Jaspan J.B., Kastin A.J. Selective, physiological transport of insulin across the blood-brain barrier: novel demonstration by species-specific radioimmunoassay. Peptides 1997, 28:1257-1262.
11. Banks W.A., Kastin A.J. Differential permeability of the blood-brain barrier to two pancreatic peptides: insulin and amylin. Peptides 1998, 19:883-889.
12. Bartus R.T. On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp. Neurol. 2000, 163:495-529.
13. Bartus R.T., Dean R.L., Pontecorvo M.J., Flicker C. The cholinergic hypothesis: a historical overview, current perspective, and future directions. Ann. N.Y. Acad. Sci. 1985, 444:332-358.
14. Baynes J.W., Thrope S.R. Role of oxidative stress in diabetic complications. Diabetes 1999, 48:1-9.
15. Bhardwaj S.K., Sandhu S.K., Sharma P., Kaur G. Impact of diabetes on CNS. Role of signal transduction cascade. Brain Res. Bull. 1999, 49:155-162.
16. Biessels G., Gispen W.H. The calcium hypothesis of brain aging and neurodegenerative disorders: significance in diabetic neuropathy. Life. Sci. 1996, 59(5-6):379-387.
17. Biessels G.J., Staekenborg S., Brunner E., Brayne C., Scheltens P. Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol. 2006, 5:64-74.
18. Bitner R.S., Bunnelle W.H., Anderson D.J., Briggs C.A., Buccafusco J., Curzon P., Decker M.W., Frost J.M., Gronlien J.H., Gubbins E., Li J., Malysz J., Markosyan S., Marsh K., Meyer M.D., Nikkel A.L., Radek R.J., Robb H.M., Timmermann D., Sullivan J.P., Gopalakrishnan M. Broad-spectrum efficacy across cognitive domains by alpha7 nicotinic acetylcholine receptor agonism correlates with activation of ERK1/2 and CREB phosphorylation pathways. J. Neurosci. 2007, 27:10578-10587.
19. Blanchard J.G., Duncan P.M. Effect of combinations of insulin, glucose and scopolamine on radial arm maze performance. Pharmacol. Biochem. Behav. 1997, 58:209-214.
20. Boess F.G., De Vry J., Erb C., Flessner T., Hendrix M., Luithle J., Methfessel C. Brain insulin receptors and spatial memory. J. Biol. Chem. 2006, 274:34893-34902.
21. Bonnefont-Rousselot D. Glucose and reactive oxygen species. Curr. Opin. Clin. Nutr. Metab. Care 2002, 5:561-568.
22. Brands A.M., Henselmans J.M., de Haan E.H., Biessels G.J. Diabetic encephalopathy: an underexposed complication of diabetes mellitus. Ned. Tijdschr. Geneeskd. 2003, 147:11-14.
23. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
24. Chen S., Kobayashi M., Honda Y., Kakuta S., Sato F., Kishi K. Preferential neuron loss in the rat piriform cortex following pilocarpine-induced status epilepticus. Epilepsy Res. 2007, 74:1-18.
25. Cole G.M., Bruce T., Sally A.F. Neuroprotective effects of curcumin. Adv. Exp. Med. Biol. 2007, 595:197-212.
26. Commandeur J.N.M., Vermeulen N.P.E. Cytotoxicity and cytoprotective activities of natural compounds the case of curcumin. Xenobiotica 1996, 26(7):667-680.
27. Court J.A., Lloyd S., Johnson M., Griffiths M., Birdsall N.J., Piggott M.A., Oakley A.E., Ince P.G., Perry E.K., Perry R.H. Nicotinic and muscarinic cholinergic receptor binding in the human hippocampal formation during development and aging. Brain. Res. Dev. Brain. Res. 1997, 101(1-2):93-105.
28. Court J.A., Perry E.K., Spurden D., Griffiths M., Kerwin J.M., Morris C.M., et al. The role of the cholinergic system in the development of the human cerebellum. Brain Res. Dev. Brain Res. 1995, 90:159-167.
29. Daneman Denis Diabetes-related mortality. Diabetes Care 2001, 24:5.
30. Das A., Shanker G., Nath C., Pal R., Singh S., Singh H.K. A comparative study rodents of standardized extracts of Bacopa monniera and ginkgo biloba anticholinesterase and cognitive enhancing activities. Pharmacol. Biochem. Behav. 2002, 73:893-900.
31. Devivo D.C., Trifiletti R.R., Jacobson R.I., Rosen G.M., Behmand R.A., Harik S.I. Defective glucose transport across the blood-brain barrier as a cause of persistent hypoglycorrhachia, seizures, and developmental delay. N. Engl. J. Med. 1991, 325:703-709.
32. Friedman H.R., Goldman-Rakic P.S. Coactivation of prefrontal cortex and inferior parietal cortex in working memory tasks revealed by 2DG functional mapping in the rhesus monkey. J. Neurosci. 1994, 14:2775-2788.
33. Frolich L., Blum-degen D., Bernstein H.G., Engelsberger S., Humrich J., Laufer S., Muschner D., Thalheimer A., Turk A., Hoyer S., Zochling R., Boissl K.W., Jellinger K., Piederer P. Brain insulin and insulin receptors in aging and sporadic Alzheimer's disease. J. Neural Transm. 1998, 105:423-438.
34. Garris Age diabetes associated alterations in regional brain norepinephrine concentrations and adrenergic populations in C57BL/KsL mice. Dev. Brain Res. 1990, 51:161-166.
35. Ghareeb D.A., Hussen H.M. Vanadium improves brain acetylcholinesterase activity on early stage alloxan-diabetic rats. Neurosci. Lett. 2008, 436:44-47.
36. 3H]dopa in various regions of brain. J. Neurochem. 1966, 13:655-669.
37. Gold S.M., Dziobek I., Sweat V., Tirsi A., Rogers K., Bruehl H., Tsui W., Richardson S., Javier E., Convit A. Hippocampal damage and memory impairments as possible early brain complications of type 2 diabetes. Diabetologia 2007, 50(4):711-719.
38. Gruefter R., Novotny E.J., Boulware S.D., Rothman D.L., Mason G.G., Shulman G.I., Shulman R.G., Tamborlane W.V. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:1109-1112.
39. Hasanein P., Shahidi S. Effects of combined treatment with vitamins C and E on passive avoidance learning and memory in diabetic rats. Neurobiol. Learn Mem. 2010, 93:472-478.
40. Hashimoto K., Ishima T., Fujita Y., Matsuo M., Kobashi T., Takahagi M., Tsukada H., Iyo M. Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of the novel selective alpha7 nicotinic receptor agonist SSR180711. Biol. Psychiatry 2008, 63:92-97.
41. Hellstrom-Lindahl E., Mousavi M., Zhang X., Ravid R., Nordberg A. Regional distribution of nicotinic receptor subunit mRNAs in human brain: comparison between Alzheimer and normal brain. Brain Res. Mol. Brain Res. 1999, 66:94-103.
42. Hohenegger M., Rudas B. Kidney functions in experimental diabetic ketosis. Diabetologia 1971, 17:334-338.
43. Hosey M.M. Diversity of structure, signaling and regulation within the family of muscarinic cholinergic receptors. FASEB J. 1992, 6:845-852.
44. Hoyer S. Memory function and brain glucose. Metab. Pharmacopsychiat. 2003, 36(Suppl. 1):S62-S67.
45. Ishrat T., Khan M.B., Hoda M.N., Yousuf S., Ahmad M., Ansari M.A., Ahmad A.S., Islam F. Coenzyme Q10 modulates cognitive impairment against intracerebroventricular injection of streptozotocin in rats. Behav. Brain Res. 2006, 171:9-16.
46. Jackson-Guilford J., Leander J.D., Nisenbaum L.K. The effect of streptozotocin-induced diabetes on cell proliferation in the rat dentate gyrus. Neurosci. Lett. 2000, 293:91-94.
47. Junod A., Lambert A.E., Staufferacher W., Renold A.E. Diabetogenic action of streptozotocin relationship of dose to metabolic response. J. Clin. Invest. 1969, 48:2129-2139.
48. Krebs D.L., Parent M.B. The enhancing effects of hippocampal infusions of glucose are not restricted to spatial working memory. Neurobiol. Learn Mem. 2005, 83:168-172.
49. Kuhad A., Chopra K. Curcumin attenuates diabetic encephalopathy in rats: behavioral and biochemical evidences. Eur. J. Pharmacol. 2007, 576:34-42.
50. Levey A.I. Immunological localization of M1-M5 muscarinic acetylcholine receptors in peripheral tissues and brain. J. Life Sci. 1993, 52:441-448.
51. Low P.A., Nickander K.K., Tritschler H.J. The role of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes 1997, 46:38.
52. Lowry O.H., Roserbrough N.J., Farr A.L., Randall R.J. Protein measurement with Folin Phenol reagent. J. Biol. Chem. 1951, 193:265-275.
53. Ma J., Yu L.J., Ma R.D., Zhang Y.P., Fang J.Z., Zhang X.Y., Yu T.X. Repair of glutamate-induced excitotoxic neuronal damage mediated by intracerebroventricular transplantation of neural stem cells in adult mice. Neurosci. Bull. 2007, 23(4):209-214.
54. Maher F., Vannucci S.J., Simpson I.A. Glucose transporter isoforms in brain: absence of GLUT3 from the blood-brain barrier. J. Cereb. Blood Flow Metab. 1993, 13:342-345.
55. McCormick D.A. Cholinergic and noradrenergic modulation of thalamocortical processing. Trends Neurosci. 1989, 12:215-221.
56. McNamara D., Larson D.M., Rapoport S.I., Soncrant T.T. Preferential metabolic activation of subcortical brain areas by acute administration of nicotine to rats. J. Cereb. Blood Flow Metab. 1990, 10:48-56.
57. McNay E.C., Fries T.M., Gold P.E. Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proc. Natl. Acad. Sci. 2000, 97:2881-2885.
58. Meghana K., Sanjeev G., Ramesh B. Curcumin prevents streptozotocin-induced islet damage by scavenging free radicals: a prophylactic and protective role. Eur. J. Pharmacol. 2007, 577(1-3):183-191.
59. Messier C., Destrade C. Insulin attenuates scopolamine-induced memory deficits. Psychobiology 1994, 22:16-21.
60. Mijnhout G.S., Scheltens P., Diamant M., Biessels G.J., Wessels A.M., Simsek S., Snoek F.J., Heine R.J. Diabetic encephalopathy: a concept in need of a definition. Diabetologia 2006, 49:1447-1448.
61. Miller J.S.M., Angeles F.M., Reuter B.K., Bobrowski P., Sandoval M. Dietary antioxidants protect gut epithelial cells from oxidant-induced apoptosis. BMC Complement. Altern. Med. 2001, 1:11.
62. Mokni M., Elkahoui S., Limam F., Amri M., Aouani E. Effect of resveratrol on antioxidant enzyme activities in the brain of healthy rat. Neurochem. Res. 2007, 32:981-987.
63. Nakayama H., Shioda S., Okuda H., Nakashima T., Nakai Y. Immunocytochemical localization of nicotinic acetylcholine receptor in rat cerebral cortex. Mol. Brain. Res. 1995, 32:321-328.
64. Nitta A., Murai R., Suzuki N., Ito H., Nomoto H., Katoh G., Furukawa Y., Furukawa S. Diabetic neuropathies in brain are induced by deficiency of BDNF. Neurotoxicol. Teratol. 2002, 24:695-701.
65. Olton D., Markowska A., Voytko M.L., Givens B., Gorman L., Wenk G. Basal forebrain cholinergic system: a functional analysis. Adv. Exp. Med. Biol. 1991, 295:353-372.
66. Osawa T., Kato Y. Protective role of antioxidative food factors in oxidative stress caused by hyperglycemia. Ann. N.Y. Acad. Sci. 2005, 1043:440-451.
67. Picciotto M.R., Caldarone B.J., King S.L., Zachariou V. Nicotinic receptors in the brain. Links between molecular biology and behavior. Neuropsychopharmacology 2000, 22:451-465.
68. Pramming S., Thorsteinsson B., Theilgaard A., Pinner B.M., Binder C. Cognitive function during hypoglycaemia in type I diabetes mellitus. Br. Med. J. 1986, 292:647-650.
69. Priyadarsini K., Maity D., Naik G., Kumar M., Unnikrishnan M., Satav J., Mohan H. Role of phenolic O_H and methylene hydrogen on the free radical reactions and antioxidant activity of curcumin. Free Radic. Biol. Med. 2003, 35:475-484.
70. Qiu W.Q., Price L.L., Hibberd P., Buell J., Collins L., Leins D., Mwamburi D.M., Rosenberg I., Smaldone L., Scott T.M., Siegel R.D., Summergrad P., Sun X., Wagner C., Wang L., Yee J., Tucker K.L., Folstein M. Executive dysfunction in homebound older people with diabetes mellitus. J. Am. Geriatr. Soc. 2006, 54:496-501.
71. Quincozes-Santos, Andreazzaa A.C., Nardin A.P., Funchala C., Gonçalves C.A., Gottfried C. Resveratrol attenuates oxidative-induced DNA damage in C6 Glioma cells A. Neurotoxicology 2007, 28:886-891.
72. Sato A., Sato Y., Uchida S. Activation of the intracerebral cholinergic nerve fibers originating in the basal forebrain. Neurosci. Lett. 2004, 361:90-93.
73. Scatchard G. The attraction of proteins for small molecules and ions. Ann. N.Y. Acad. Sci. 1949, 51:660-672.
74. Schroder H., Zilles K., Maelicke A., Hajo S.F. Immunohisto and cytochemical localization of cortical nicotinic cholinoceptors in rat and man. Brain. Res. 1989, 502:287-295.
75. Schwartz M.W., Sipols A.J., Kahn S.E., Lattemann D.P., Taborsky G.J., Bergman R.N., Woods S.C., Porte D. Kinetics and specificity of insulin uptake from plasma into cerebrospinal fluid. Am. J. Physiol. 1990, 259:E378-E383.
76. Seo K.-II, Choi M.-S., Jung Un J., Kim H-J., Yeo J., Jeon Seon-Min., Lee M.-K. Effect of curcumin supplementation on blood glucose, plasma insulin, and glucose homeostasis related enzyme activities in diabetic db/db mice. Mol. Nutr. Food Res. 2008, 52(9):995-1004.
77. Sharma S., Kulkarni S.K., Chopra K. Curcumin, the active principle of turmeric (Curcuma longa), ameliorates diabetic nephropathy in rats. Clin. Exp. Pharmacol. Physiol. 2006, 33:940-945.
78. Shishodia S., Sethi G., Aggarwal B.B. Curcumin: getting back to the roots. Ann. N.Y. Acad. Sci. Nov. 2005, 1056:206-217.
79. Soreq H., Seidman S. Acetylcholinesterase-new roles for and old actor. Nat. Rev. Neurosci. 2001, 2:294-302.
80. Surh Y.J., Chun K.S., Cha H.H., Han S.S., Keum Y.S., Park K.K., Lee S.S. Molecular mechanisms underlying chemopreventive activities of anti-inflammatory phytochemicals, down-regulation of COX-2 and iNOS through suppression of NF kappa B activation. Mutat. Res. 2001, 480:243-268.
81. Tõugu V., Kesvatera T. Role of ionic interactions in cholinesterase catalysis. Biochim. Biophys. Acta 1996, 1298:12-30.
82. Uchida S., Kagitani F., Nakayama H., Sato A. Effect of stimulation of nicotinic cholinergic receptors on cortical cerebral blood flow and changes in the effect during aging in anesthetized rats. Neurosci. Lett. 1997, 228:203-206.
83. Van der Zee E.A., Streefland C., Strosberg A.D., Schro der H., Luiten P.G.M. Visualization of cholinoceptive neurons in the rat neocortex: colocalization of muscarinic and nicotinic acetylcholine receptors. Mol. Brain Res. 1992, 14:326-336.
84. Voytko M.L., Olton D.S., Richardson R.T., Gorman L.K., Tobin J.R., Price D.L. Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J. Neurosci. 1994, 14:167-186.
85. Wevers A., Monteggia L., Nowacki S., Bloch W., Schu U., Lindstrom J., Pereira E.F.R., Eisenberg H., Giacobini E., de Vos R.A.I., Jansen Steur E.N.H., Maelicke A., Albuquerque E.X., Schro der H. Expression of nicotinic acetylcholine receptor subunits in the cerebral cortex in Alzheimer's disease-histotopographical correlation with amyloid plaques and hyperphosphorylated tau-protein. Eur. J. Neurosci. 1999, 11:2551-2565.
86. Willis L.M., Shukitt-Hale B., Joseph J.A. Modulation of cognition and behavior in aged animals: role for antioxidant- and essential fatty acid-rich plant foods. Am. J. Clin. Nutr. 2009, 89:1602S-1606S.
87. Woo E., Schmitter-Edgecombe M., Fancher J.B. Memory prediction accuracy in younger and older adults: a cross-sectional and longitudinal analysis. Neuropsychol. Dev. Cogn. B. Aging. Neuropsychol. Cogn. 2008, 15(1):68-94.
88. 3H] QNB in rat brain. Proc. Natl. Acad. Sci. U.S.A. 1981, 71:1725-1729.
89. Zhao W.-Q., Alkon D.L. Role of insulin and insulin receptor in learning and memory. Mol. Cell. Endocrinol. 2001, 177:125-134.
90. Zhao W., Chen H., Xu H., Moore E., Meiri N., Quon M.J., Alkon D.L. Brain insulin receptors and spatial memory. Correlated changes in gene expression, tyrosine phosphorylation, and signaling molecules in the hippocampus of water maze trained rats. J. Biol. Chem. 1999, 274(49):34893-34902.