Expression pattern of NMDA receptors reveals antiepileptic potential of apigenin 8-C-glucoside and chlorogenic acid in pilocarpine induced epileptic mice

Biomedicine and Pharmacotherapy

Volumn 82, Issue , 2016, Pages 54-64

  Aseervatham, G Smilin Bell ^a   Suryakala, U ^a   Doulethunisha, ^b   Sundaram, S ^a   Bose, P Chandra ^c   Sivasudha, T ^a  

^a BHARATHIDASAN UNIVERSITY   (India)

^b MAHATMA GANDHI MEDICAL COLLEGE AND RESEARCH INSTITUTE   (India)

^c ANNA UNIVERSITY   (India)

Author keywords

Acetylcholinesterase; Antioxidant; Apigenin 8 C glucoside; Chlorogenic acid; Epilepsy; NMDAR

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINESTERASE; AMINE OXIDASE (FLAVIN CONTAINING); CHLOROGENIC ACID; DIAZEPAM; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 5; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PILOCARPINE; VITEXIN; ANTICONVULSIVE AGENT; ANTIOXIDANT; APIGENIN; GLUTATHIONE; NEUROPROTECTIVE AGENT; NITRIC OXIDE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ANTIOXIDANT ASSAY; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; HISTOPATHOLOGY; MALE; MOUSE; NEUROCHEMISTRY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEIZURE; ANIMAL; ANIMAL BEHAVIOR; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; EPILEPSY; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; METABOLISM; PATHOLOGY;

ANIMALS; ANTICONVULSANTS; ANTIOXIDANTS; APIGENIN; BEHAVIOR, ANIMAL; CHLOROGENIC ACID; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GLUTAMIC ACID; GLUTATHIONE; HIPPOCAMPUS; MALE; MICE; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; PILOCARPINE; RECEPTORS, N-METHYL-D-ASPARTATE; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84971222308     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2016.04.066     Document Type: Article

References (77)

1. Papandreou D., Pavlou E., Kalimeri E., Mavromichalis I. The ketogenic diet in children with epilepsy. Br. J. Nutr. 2006, 95:5-13.
2. Swamy A.V., Patel N.L., Gadad P.C., Koti B.C., Patel U.M., Thippeswamy A., Manjula D.V. Neuroprotective activity of Pongamia pinnata in monosodium glutamate induced neurotoxicity in rats. Indian J. Pharm. Sci. 2013, 75:657-663.
3. Gupta Y.K., Gupta M., Kohli K. Neuroprotective role of melatonin in oxidative stress vulnerable brain. Indian J. Physiol. Pharmacol. 2003, 47:373-386.
4. De Sarro G., Gitto R., Russo E., Ibbadu G.F., Barreca M.L., De Luca L., Chimirri A. AMPA receptor antagonists as potential anticonvulsant drugs. Curr. Top. Med. Chem. 2005, 5:31-42.
5. Lang U.E., Puls I., Muller D.J., Strutz-Seebohm N., Gallinat J. Molecular mechanisms of schizophrenia. Cell. Physiol. Biochem. 2007, 20:687-702.
6. Mellor I.R. The AMPA receptor as a therapeutic target: current perspectives and emerging possibilities. Future Med. Chem. 2010, 2:877-891.
7. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 2010, 62:405-416.
8. Takano T., Lin J.H., Arcuino G., Gao Q., Yang J., Nedergaard M. Glutamate release promotes growth of malignant gliomas. Nat. Med. 2001, 7:1010-1015.
9. 2+ influx through acquired and native N-methyl-d-aspartate-receptor channels. J. Pharmacol. Sci. 2010, 112:273-281.
10. Mahendran S., Thippeswamyb B., Veerapurb V., Badami S. Anticonvulsant activity of embelin isolated from Embelia ribes. Phytomedicine 2011, 18:186-188.
11. Devasagayam T.P.A., Sainis K.B. Immune system and antioxidants, especially those derived from Indian medicinal plants. Indian J. Exp. Biol. 2002, 40:639-655.
12. Park E.J., Pezzuto J.M. Botanicals in cancer chemoprevention. Cancer Metastasis Rev. 2002, 31:231-255.
13. Govindarajan R., Vijayakumar M., Pushpangadan P. Antioxidant approach to disease management and the role of Rasayana herbs of Ayurveda. J. Ethnopharmacol. 2005, 99:165-178.
14. Liang N., Kitts D.D. Role of chlorogenic acids in controlling oxidative and inflammatory stress conditions. Nutrients 2016, 8:16.
15. Kelly E.H., Anthony R.T., Dennis J.B. Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J. Nutr. Biochem. 2002, 13:572-584.
16. Pandey A.K., Mishra A.K., Mishra A. Antifungal and antioxidative potential of oil and extracts derived from leaves of Indian spice plant Cinnamomum tamala. Cell. Mol. Biol. 2012, 58:142-147.
17. Pietta P.G. Flavonoids and antioxidants. J. Nat. Prod. 2000, 63:1035-1042.
18. Belay A., Gholap A.V. Characterization and determination of chlorogenic acids (CGA) in coffee beans by UV-vis spectroscopy. Afr. J. Pure Appl. Chem. 2009, 3:234-240.
19. Jiang Y., Satoh K., Watanabe S. Inhibition of chlorogenic acid-induced cytotoxicity by CoC12. Anticancer Res. 2001, 21:3349-3353.
20. Ma B., Liang S. Progress report on extraction and separation of chlorogenic acid from eucomiaulmoides. Shanxi For. Sci. Technol. 2003, 4:74-79.
21. Tan Z., Zhang Y., Deng J., Zeng G., Zhang Y. Purified vitexin compound 1 suppresses tumor growth and induces cell apoptosis in a mouse model of human choriocarcinoma. Int. J. Gynecol. Cancer. 2012, 22:360-366.
22. Yang S.H., Liao P.H., Pan Y.F., Chen S.L., Chou S.S., Chou M.Y. The novel p53-dependent metastatic and apoptotic pathway induced by vitexin in human oral cancer OC2 cells. Phytother. Res. 2013, 27:1154-1161.
23. Salahdeen H.M., Yemitan O.K. Neuropharmacological effects of aqueous leaf extract of Bryophyllum pinnatum in mice. Afr. J. Biol. Med. Res. 2006, 9:101-107.
24. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurements with the folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
25. Pachauri S.D., Tota S., Khandelwal K., Verma P.R., Nath C., Hanif K., Shukla R., Saxena J.K., Dwivedi A.K. Protective effect of fruits of Morinda citrifolia L. on scopolamine induced memory impairment in mice: a behavioral, biochemical and cerebral blood flow study. J. Ethanopharmacol. 2012, 139:34-41.
26. Nagatsu T., Udenfriend S. Photometric assay of dopamine-β-hydroxylase activity in human blood. Clin. Chem. 1972, 18:980-983.
27. Tabor H., Mehler A.H., Stadtman E.R. The enzymatic acetylation of amines. J. Biol. Chem. 1953, 204:127-138.
28. Verma A.K., Kumar A., Kayastha A.M. GABA and glutamate in immobilized stressed rats brain under influence of some plant extracts. Int. J. Res. Pharm. Biomed. Sci. 2011, 2:1090-1094.
29. Ramanathan M., Babu C.S., Justin A., Shanthakumari S. Elucidation of neuroprotective role of endogenous GABA and energy metabolites in middle cerebral artery occluded model in rats. Indian J. Exp. Biol. 2012, 391-397.
30. Kakkar P., Dos B., Viswnathan P.N. A modified spectrophotometric assay of superoxide dismutase. Indian J. Biochem. 1984, 21:130-132.
31. Sinha K.A. Colorimetric assay of catalase. Anal. Biochem. 1972, 47:389-394.
32. Oliveira A.A., Almeida J.P.C., Freitas R.M., Nascimento V.S., Aguiar L.M.V., Junior H.V.N., Fonseca F.N., Viana G.S.B., Sousa F.C.F., Fonteles M.M.F. Effects of levetiracetam in lipid peroxidation level, nitrite-nitrate formation and antioxidant enzymatic activity in mice brain after pilocarpine-induced seizures. Cell. Mol. Neurobiol. 2007, 27:395-406.
33. Huong N.T.T., Malsumato K., Kasai R., Yamasaki K., Watanabe H. In vitro antioxidant activity of Vietnamese ginseng saponin and its components. Biol. Pharm. Bull. 1998, 21:978-981.
34. Green L.C., Tannenbaum S.R., Goldman P. Nitrate synthesis in the germ free and conventional rat. Science 1981, 212:56-58.
35. Radenovic L., Selakovic V. Differential effects of NMDA and AMPA/kainate receptor antagonists on nitric oxide production in rat brain following intra hippocampal injection. Brain Res. Bull. 2005, 67:133-141.
36. Youdim K.A., Shukitt-Hale B., Joseph J.A. Flavonoids and the brain: interactions at the blood-brain barrier and their physiological effects on the central nervous system. Free Radic. Biol. Med. 2004, 37:1683-1693.
37. Heitman E., Ingram D.K. Cognitive and neurological health effects of chlorogenic acid. Nutr. Neurosci. 2014.
38. Almeida I.F., Fernandes E., Lima J.L., Valentao P., Andrade P.B., Seabra R.M., Costa P.C., Bahia M.F. Oxygen and nitrogen reactive species are effectively scavenged by Eucalyptus globulus leaf water extract. J. Med. Food 2009, 12:175-183.
39. Bernatoniene J., Masteikova R., Majiene D., Savickas A., Kevelaitis E., Bernatoniene R., Dvorackova K., Civinskiene G., Lekas R., Vitkevicius K., Peciura R. Free radical-scavenging activities of Crataegus monogyna extracts. Medicina (Kaunas) 2008, 44:706-712.
40. Maas F., Petereit A. Caffeic acid derivatives from Eupatorium perfoliatum L. Molecules 2009, 14:36-45.
41. McIntyre C.S., Harris A., Saleem L.P., Beaulieu C.A., Ta P.S. Seasonal phytochemical variation of anti-glycation principles in lowbush blueberry (Vaccinium angustifolium). Planta Med. 2009, 75:286-292.
42. Barros D.O., Xavier S.M., Barbosa C.O., Silva R.F., Maia F.D., Oliveira A.A., Freitas R.M. Effects of the vitamin E in catalase activities in hippocampus after status epilepticus induced by pilocarpine in Wistar rats. Neurosci. Lett. 2007, 416:227-230.
43. Xavier S.M.L., Barbosa C.O., Barros D.O., Silva R.F., Oliveira A.A., Freitas R.M. Vitamin C antioxidant in hippocampus of adult Wistar rats after seizures and status epilepticus induced by pilocarpine. Neurosci. Lett. 2007, 420:76-79.
44. Santos L.F., Freitas R.L., Xavier S.M., Saldanha G.B., Freitas R.M. Neuroprotective actions of vitamin C related to decreased lipid peroxidation and increased catalase activity in adult rats after pilocarpine-induced seizure. Pharmacol. Biochem. Behav. 2008, 89:1-5.
45. Youdim K.A., Dobbie M.S., Kuhnle G., Proteggente A.R., Abbott N.J., Rice-Evans C. Interaction between flavonoids and the blood-brain barrier: in vitro studies. J. Neurochem. 2003, 85:180-192.
46. Youdim K.A., Qaiser M.Z., Begley D.J., Rice-Evans C.A., Abbott N.J. Flavonoid permeability across an in situ model of the blood-brain barrier. Free Radic. Biol. Med. 2004, 36:592-604.
47. Chu Y.F., Brown P.H., Lyle B.J., Chen Y., Black R.M., Williams C.E., Lin Y.C., Hsu C.W., Cheng H. Roasted coffees high in lipophilic antioxidants and chlorogenic acid lactones are more neuroprotective than green coffees. J. Agric. Food Chem. 2009, 57:9801-9808.
48. Schmatz R., Mazzanti C.M., Spanevello R., Stefanello N., Gutierres J., Correa M., da Rosa M.M., Rubin M.A., Chitolina Schetinger M.R., Morsch V.M. Resveratrol prevents memory deficits and the increase in acetylcholinesterase activity in streptozotocin-induced diabetic rats. Eur. J. Pharmacol. 2009, 610:42-48.
49. Bernhardi R.V., Alarcon R.D., Mezzano D., Fuentes P., Inestrosa N.C. Blood cells cholinesterase activity in early Alzeimer's disease and vascular dementia. Dement. Geriatr. Cogn. Disord. 2005, 19:204-212.
50. Musial A., Bajda M., Malawska B. Recent development in cholinesterase inhibitors for Alzheimer's disease treatment. Curr. Med. Chem. 2007, 14:2654-2679.
51. Francis P.T., Perry E.K. Cholinergic and other neurotransmitter mechanism in Parkinson's disease, Parkinson's disease dementia and dementia with lewy bodies. Mov. Disord. 2008, 22:351-357.
52. Diniz T.C., Silva J.C., de Lima-Saraiva S.R.G., de Almeida Ribeiro F.P.R., Pacheco A.G.M., de Freitas R.M., Quintans-Júnior L.J., de Souza Siqueira Quintans J., Mendes R.L., da Silva Almeida J.R.G. The role of flavonoids on oxidative stress in epilepsy. Oxid. Med. Cell. Longev. 2015, 171756.
53. Costa D.A., Lopes de Oliveira G.A., Lima T.C., dos Santos P.S., de Sousa D.P., de Freitas R.M. Anticonvulsant and antioxidant effects of cyano-carvone and its action on acetylcholinesterase activity in mice hippocampus. Cell. Mol. Neurobiol. 2012, 32:633-640.
54. Cohen G., Farooqui R., Kesler N. Parkinson disease: a new link between monoamine oxidase and mitochondrial electron flow. Proc. Natl. Acad. Sci. 1997, 94:4890-4894.
55. Szot P., Weinshenker D., White S.S., Robbins C.A., Rust N.C., Schwartzkroin P.A., Palmiter R.D. Norepinephrine-deficient mice have increased susceptibility to seizure-inducing stimuli. J. Neurosci. 1999, 19:10985-10992.
56. Karamanakos P.N., Pappas P., Stephanou P., Marselos M. Differentiation of disulfiram effects on central catecholamines and hepatic ethanol metabolism. Pharmacol. Toxicol. 2001, 88:106-110.
57. Bourdelat-Parks B.N., Anderson G.M., Donaldson Z.R., Weiss J.M., Bonsall R.W., Emery M.S., Liles L.C., Weinshenker D. Effects of dopamine beta-hydroxylase genotype and disulfiram inhibition on catecholamine homeostasis in mice. Psychopharmacology (Berl.) 2005, 183:72-80.
58. Haile C.N., During M.J., Jatlow P.I., Kosten T.R., Kosten T.A. Disulfiram facilitates the development and expression of locomotor sensitization to cocaine in rats. Biol. Psychiatry 2003, 54:915-921.
59. Ramanathan M., Babu C.S., Justin A., Shanthakumari S. Elucidation of neuroprotective role of endogenous GABA and energy metabolites in middle cerebral artery occluded model in rats. Indian J. Exp. Biol. 2012, 50:391-397.
60. Babu C.S., Kesavanarayanan K.S., Kalaivani P., Ranju V., Ramanathan M. A simple densitometric method for the quantification of inhibitory neurotransmitter gamma-aminobutyric acid (GABA) in rat brain tissue. Chromatogr. Res. Int. 2011, 10.4061/2011/732409.
61. Agrawal A.D. Pharmacological activities of flavonoids: a review. Int. J. Pharm. Sci. Nanotechnol. 2011, 4:1394-1397.
62. Ziyaurrahman A.R., Patel J. Anticonvulsant effect of Phylanthus amarus by modulation of endogenous biomarkers. J. Nat. Prod. Plant Resour. 2012, 2:401-418.
63. Avallone R., Zanoli P., Puia G., Kleinschnitz M., Schreier P., Baraldi M. Pharmacological profile of apigenin, a flavonoid isolated from Matricaria chamomilla. Biochem. Pharmacol. 2000, 59:1387-1394.
64. Dekermendjian K., Kahnberg P., Witt M.R., Sterner O., Nielsen M., Liljefors T. Structure-activity relationships and molecular modeling analysis of flavonoids binding to the benzodiazepine site of the rat brain GABAA receptor complex. J. Med. Chem. 1999, 42:4343-4350.
65. Campbell E.L., Chebib M., Johnston G.A.R. The dietary flavonoids apigenin and (-)-epigallocatechin gallate enhance the positive modulation by diazepam of the activation by GABA of recombinant GABAA receptors. Biochem. Pharmacol. 2004, 68:1631-1638.
66. Fernández S.P., Wasowski C., Loscalzo L.M., Granger R.E., Johnston G.A.R., Paladini A.C., Marder M. Central nervous system depressant action of flavonoid glycosides. Eur. J. Pharmacol. 2006, 539:168-176.
67. Chang S.J., Yu B.C. Mitochondrial matters of the brain: mitochondrial dysfunction and oxidative status in epilepsy. J. Bioenerg. Biomembr. 2010, 42:457-459.
68. Liang L.P., Patel M. Seizure-induced changes in mitochondrial redox status. Free Radic. Biol. Med. 2006, 40:316-322.
69. Chuang Y.C. Mitochondrial dysfunction and oxidative stress in seizure-induced neuronal cell death. Acta Neurol. Taiwan 2010, 19:3-15.
70. Cock H.R. The role of mitochondria and oxidative stress in neuronal damage after brief and prolonged seizures. Prog. Brain Res. 2002, 135:187-196.
71. Valko M., Rhodes C.J., Moncol J., Izakovic M., Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006, 160:1-40.
72. Lau A., Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 2010, 460:525-542.
73. Wang Y., Qin Z.H. Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis 2010, 15:1382-1402.
74. Barbon A., Barlati S. Glutamate receptor RNA editing in health and disease. Biochemistry (Moscow) 2011, 76:882-889.
75. Dong X.X., Wang Y., Qin Z.H. Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol. Sin. 2009, 30:379-387.
76. Storto M., Ngomba R.T., Battaglia G., Freitas I., Griffini P., ichelmi P., Nicoletti F., Vairetti M. Selective blockade of mGlu5 metabotropic glutamate receptors is protective against acetaminophen hepatotoxicity in mice. J. Hepatol. 2003, 38:179-187.
77. Jesse C.R., Wilhelm E.A., Bortolatto C.F., Savegnago L., Nogueira C.W. Selective blockade of mGlu5 metabotropic glutamate receptors is hepatoprotective against fulminant hepatic failure induced by lipopolysaccharide and d-galactosamine in mice. J. Appl. Toxicol. 2009, 29:323-329.