Effects of melatonin on aluminium-induced neurobehavioral and neurochemical changes in aging rats

Food and Chemical Toxicology

Volumn 70, Issue , 2014, Pages 84-93

  Allagui, M S ^a,b   Feriani, A ^a   Saoudi, M ^a   Badraoui, R ^c   Bouoni, Z ^a   Nciri, R ^a   Murat, J C ^b   Elfeki, A ^a  

^a University of Sfax   (Tunisia)

^b Laboratory Biologie Cellulaire et pollution   (France)

^c UNIVERSITY OF SFAX   (Tunisia)

Author keywords

AChE activity; Aging; Aluminium toxicity; Brain; Melatonin; Oxidative stress

Indexed keywords

ACETYLCHOLINESTERASE; ALUMINUM CHLORIDE; CHLORAMPHENICOL ACETYLTRANSFERASE; GLUTATHIONE PEROXIDASE; MELATONIN; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; ALUMINUM; CATALASE;

AGING; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ELEVATED PLUS MAZE TEST; ENZYME ACTIVITY; HIPPOCAMPUS; HISTOLOGY; LIPID PEROXIDATION; MALE; MORTALITY; MOUSE; NEUROPROTECTION; NONHUMAN; OPEN FIELD TEST; OXIDATIVE STRESS; RADIAL ARM MAZE TEST; TASK PERFORMANCE; WEIGHT REDUCTION; ANIMAL; BODY WEIGHT; BRAIN; CHEMICALLY INDUCED; DEGENERATIVE DISEASE; DRUG EFFECTS; METABOLISM; PATHOLOGY; RAT; TOXICITY; WISTAR RAT;

ACETYLCHOLINESTERASE; AGING; ALUMINUM; ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN; CATALASE; GLUTATHIONE PEROXIDASE; LIPID PEROXIDATION; MALE; MELATONIN; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS; RATS; RATS, WISTAR; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84901428865     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2014.03.043     Document Type: Article

References (98)

1. Aebi H. Catalase in vitro. Methods Enzymol. 1984, 105:121-126.
2. Arbos K.A., Carlo L.M., Borges L., Santos C.A., Weffort-Santos A.M. Human erythrocytes as a system for evaluating the antioxidant capacity of vegetable extracts. Nut. Res. 2008, 28:457-463.
3. Asha Devi S., Manjula K.R., Subramanyam M.V.V. Protective role of vitamins E and C against oxidative stress caused by intermittent cold exposure in aging rat's frontoparietal cortex. Neurosci. Lett. 2012, 529:155-160.
4. Assaf N., Shalby A.B., Khalil W.K.B., Ahmed H.H. Biochemical and genetic alterations of oxidant/antioxidant status of the brain in rats treated with dexamethasone: protective roles of melatonin and acetyl-L-carnitine. J. Physiol. Biochem. 2012, 68:77-90.
5. Benot S., Goberna R., Garcia-Marino S., Osuna C., Reiter R.J., Guerrero M. Physiological levels of melatonin contribute to the antioxidant capacity of human serum. J. Pineal Res. 1999, 27:59-64.
6. Betancourt A.M., Carr R.L. The effect of chlorpyrifos and chlorpyrifos-oxon on brain cholinesterase, muscarinic receptor binding, and eurotrophin levels in rats following early postnatal exposure. Toxicol. Sci. 2004, 77:63-71.
7. Bharathi Shamasundar N.M., Sathyanarayana Rao T.S., Dhanunjaya Naidu M., Ravid R., Rao K.S. A new insight on Al-maltolate-treated aged rabbit as Alzheimer's animal model. Brain Res. Rev. 2006, 52(2):275-292.
8. Brzezinski A. Melatonin in humans. N. Engl. J. Med. 1997, 336:186-195.
9. Bubenik G.A., Konturek S.J. Melatonin and aging: prospect for human treatment. J. Physiol. Pharmacol. 2011, 62(1):13-19.
10. Buege J.A., Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 1984, 105:302-310.
11. Carrillo-Vico A., Guerrero J.M., Lardone P.J., Reiter R.J. A review of the multiple actions of melatonin on the immune system. Endocrine 2005, 27(2):189-200.
12. Ceyran H., Narin F., Narin N., Akgun H., Ceyran A.B., Ozturk F., Akcali Y. The effect of high dose melatonin on cardiac ischemia-reperfusion Injury. Yonsei Med. J. 2008, 49(5):735-741.
13. Chen T.J., Hung H.S., Wang D.C., Chen S.S. The protective effect of Rho-associated kinase inhibitor on aluminum-induced neurotoxicity in rat cortical neurons. Toxicol. Sci. 2010, 116(1):264-272. 10.1093/toxsci/kfq114.
14. Colomina M.T., Roig J.L., Sanchez D.L., Domingo J.L. Influence of age on aluminium induced neurobehavioural effects of changes in rat brain. Neurotoxicology 2002, 23:775-781.
15. Ciobica A., Hritcu L., Padurariu M., Dobrin R., Bild V. Effects of serotonin depletion on behavior and neuronal oxidative stress status in rat: relevance for anxiety and affective disorders. Adv. Med. Sci. 2010, 55:289-296.
16. Deloncle R., Huguet F., Fernandez B., Quellard N., Babin P., Guillard O. Ultrastructural study of rat hippocampus after chronic administration of aluminum L-glutamate: an acceleration of the aging process. Exp. Gerontol. 2001, 36:231-244.
17. Deng W.G., Tang S.T., Tseng H.P., Wu K.K. Melatonin suppresses macrophage cyclooxygenase 2 and inducible nitric oxide synthase expression by inhibiting p52 acetylation and binding. Blood 2006, 108(2):518-524.
18. Dickstein D.L., Kabaso D., Rocher A.B., Luebke J.I., Wearne S.L., Hof P.R. Changes in the structural complexity of the aged brain. Aging Cell 2007, 6:275-284.
19. Dilek M., Naziroǧlu M., Baha Oral H., Suat Ovey I., Küçükayaz M., Mungan M.T., Kara H.Y., Sütçü R. Melatonin modulates hippocampus NMDA receptors, blood and brain oxidative stress levels in ovariectomized rats. J. Membr. Biol. 2010, 233(1-3):135-142.
20. Ellman G.L., Courtney K.D, Andres V., Feather-Stone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 1961, 7:88-95.
21. Escames G., León J., Macías M., Khaldy H., Acuña-Castroviejo D. Melatonin counteracts lipopolysaccharide-induced expression and activity of mitochondrial nitric oxide synthase in rats. FASEB J. 2003, 17(8):932-934.
22. Esparza J.L., Gómez M., Nogués M.R., Paternain J.L., Mallol J., Domingo J.L. Melatonin reduces oxidative stress and increases gene expression in the cerebral cortex and cerebellum of aluminum-exposed rats. J. Pineal Res. 2005, 39:129-136.
23. Exley C. The pro-oxidant activity of aluminum. Free Radic. Biol. Med. 2004, 36(3):380-387.
24. Flohe L., Gunzler W.A. Assays of glutathione peroxidase. Methods Enzymol. 1984, 105:114-121.
25. Galano A., Tan D.X., Reiter R.J. On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK. JPineal Res. 2013, 54(3):245-257.
26. García T., Ribes D., Colomina M.T., Cabré M., Domingo J.L., Gómez M. Evaluation of the protective role of melatonin on the behavioral effects of aluminum in a mouse model of Alzheimer's disease. Toxicology 2009, 265(1-2):49-55.
27. García J.J., López-Pingarrón L., Almeida-Souza P., Tres A., Escudero P., García-Gil F.A., Tan D.X., Reiter R.J., Ramírez J.M., Bernal-Pérez M. Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: a review. J. Pineal Res. 2014, 225-237. 10.1111/jpi. 1 2 128.
28. Garcia-Macia M., Vega-Naredo I., De Gonzalo-Calvo D., Rodríguez-González S.M., Camello P.J., Camello-Almaraz C., Martín-Cano F.E., Rodríguez-Colunga M.J., Pozo M.J., Coto-Montes A.M. Melatonin induces neural SOD2 expression independent of the NF-kappaB pathway and improves the mitochondrial population and function in old mice. J. Pineal Res. 2011, 50:54-63.
29. Gómez M., Esparza J.L., Nogués M.R., Giralt M., Cabré M., Domingo J.L. Pro-oxidant activity of aluminum in the rat hippocampus: gene expression of antioxidant enzymes after melatonin administration. Free Radic. Biol. Med. 2005, 38:104-111.
30. Hardeland R. Melatonin and the theories of aging: a critical appraisal of melatonin's role in antiaging mechanisms. J. Pineal Res. 2013, 55(4):325-356.
31. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11:298-300.
32. Hawkins C.L., Davies M.J. Generation and propagation of radical reactions on proteins. Biochem. Biophys. Acta 2001, 1504:196-219.
33. Herholz K., Weisenbach S., Kalbe E., Diederich N.J., Heiss W.D. Cerebral acetylcholine esterase activity in mild cognitive impairment. NeuroReport 2005, 16:1431-1434.
34. Herholz K., Weisenbach S., Zundorf G., Lenz O., Schroder H., Bauer B., Kalbe E., Heiss W.D. In vivo study of acetylcholine esterase in basal forebrain, amygdala, and cortex in mild to moderate Alzheimer disease. Neuroimage 2004, 21:136-143.
35. Jyoti A., Sethi P., Sharma D. Bacopa monniera prevents from aluminium neurotoxicity in the cerebral cortex of rat brain. J. Ethnopharmacol. 2007, 111:56-62.
36. Kaur R., Chopra K., Singh D. Role of alpha2 receptors in quercetin- induced behavioral despair in mice. J. Med. Food 2007, 10:165-168.
37. Kawahara M., Kato-Negishi M. Link between aluminum and the pathogenesis of Alzheimer's disease: the integration of the aluminum and amyloid cascade hypotheses. Int. J. Alzheimers Dis. 2011, doi:10.4061/2011/276393.
38. Kilic E., Kilic U., Bacigaluppi M., Guo Z., Abdallah N.B., Wolfer D.P., Reiter R.J., Hermann D.M., Bassetti C.L. Delayed melatonin administration promotes neuronal survival neurogenesis and motor recovery and attenuates hyperactivity and anxiety after mild focal cerebral ischemia in mice. J. Pineal Res. 2008, 45:142-148.
39. Koizumi M.H., fujii S., Ono A., Hirose A., Imai T., Ogawa K., Ema M., Nishikawa A. Two generation reproductive toxicity study of aluminium sulfate in rats. Reprod. Toxicol. 2010, 31:219-230.
40. Kumar A., Prakash A., Dogra S. Neuroprotective effect of carvedilol against aluminium induced toxicity: possible behavioral and biochemical alterations in rats. Pharmacol. Rep. 2011, 63(4):915-923.
41. Kumar V., Bal A., Gill K.D. Susceptibility of mitochondrial superoxide dismutase to aluminium induced oxidative damage. Toxicology 2009, 255(3):117-123.
42. Kumar V., Gill K.D. Aluminium neurotoxicity: neurobehavioural and oxidative aspects. Arch. Toxicol. 2009, 83:965-978.
43. Kvetnoy I.M. Extrapineal melatonin: location and role within diffuse neuroendocrine system. Histochem. J. 1999, 31:1-12.
44. Li Q., Zhao H., Zhao M., Zhang Z., Li Y. Chronic green tea catechins administration prevents oxidative stress-related brain aging in C57BL/6J mice. Brain Res. 2010, 1353:28-35.
45. Linardaki Z.I., Orkoula M.G., Kokkosis A.G., Lamari F.N., Margarity M. Investigation of the neuroprotective action of saffron (Crocus sativus L.) in aluminum-exposed adult mice through behavioral and neuro-biochemical assessment. Food Chem. Toxicol. 2013, 52:163-170.
46. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
47. Lukyanenko L.M., Skarabahatava A.S., Slobozhanina E.I., Kovaliova S.A., Falcioni M.L. In vitro effect of AlCl3 on human erythrocytes: changes in membrane morphology and functionality. J Trace Elem Med Bio 2013, 27:160-167.
48. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007, 87:873-904.
49. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 5(430):631-639.
50. Miu A.C., Benga O. Aluminium and Alzheimer's disease: a new look. J. Alzheimers Dis. 2006, 10:179-201.
51. Miu A.C., Andreescu C.E., Vasiu R., Olteanu A.I. A behavioral and histological study of the effects of long-term exposure of adult rats to aluminum. Int J Neurosci 2003, 113:1197-1211.
52. Pandi-Perumal S.R., Srinivasan V., Maestroni G.J., Cardinali D.P., Poeggeler B., Hardeland R. Melatonin: nature's most versatile biological signal?. FEBS J. 2006, 273(13):2813-2838.
53. Pandi-Perumal S.R., BaHammam A.S., Brown G.M., Spence D.W., Bharti V.K., Kaur C., Hardeland R., Cardinali D.P. Melatonin antioxidative defense: therapeutical implications for aging and neurodegenerative processes. Neurotox. Res. 2013, 23(3):267-300.
54. Platt B., Fiddler G., Riedel G., Henderson Z. Aluminium toxicity in the rat brain: histochemical and immunocytochemical evidence. Brain Res. Bull. 2001, 55:257-267.
55. Poeggeler B. Melatonin, aging, and age-related diseases: perspectives for prevention, intervention, and therapy. Endocrine 2005, 27:201-212.
56. Power A.E., Vazdarjanova A., McGaugh J.L. Muscarinic cholinergic influences in memory consolidation. Neurobiol. Learn Mem. 2003, 80(3):178-193.
57. Prakash D., Gopinath K., Sudhandiran G. Fistein enhances behavioral performances and attenuates reactive gliosis and inflammation during aluminum chloride-induced neurotoxicity. Neuromol. Med. 2013, 15(1):192-208.
58. Reiter R.J. The melatonin rhythm: both a clock and a calendar. Experientia 1993, 49:654-664.
59. Reiter R.J., Manchester L.C., Tan D.X. Neurotoxins: free radical mechanisms and melatonin protection. Curr. Neuropharmacol. 2010, 8(3):194-210.
60. Richter S.H., Zeuch B., Lankisch K., Gass P., Durstewitz D., Vollmayr B. Where have I been? Where should I go? spatial working memory on a radial arm maze in a rat model of depression. PLoS One 2013, 8(4):e62458.
61. Roig J.L., Fuentes S., Teresa Colomina M., Vicens P., Domingo J.L. Aluminum, restraint stress and aging: behavioral effects in rats after 1 and 2 years of aluminum exposure. Toxicology 2006, 218:112-124.
62. Romero A., Ramos E., Los Ríos C., Egea J., Del Pino J., Reiter R.J. A review of metal-catalyzed molecular damage: protection by melatonin. J. Pineal Res. 2014, 10.1111/jpi.12132.
63. Rondeau V., Jacqmin-Gadda H., Commenges D., Helmer C., Dartigues J.F. Aluminum and silica in drinking water and the risk of Alzheimer's disease or cognitive decline: findings from 15-year follow-up of the PAQUID cohort. Am. J. Epidemiol. 2009, 169:489-496.
64. Rosales-Corral S.A., Acuña-Castroviejo D., Coto-Montes A., Boga J.A., Manchester L.C., Fuentes-Broto L., Korkmaz A., Ma S., Tan D.X., Reiter R.J. Alzheimer's disease: pathological mechanisms and the beneficial role of melatonin. J. Pineal Res. 2012, 52(2):167-202.
65. Sanchez -Hidalgo M., Alarcon de la Lastra C., Carrascosa-Salmoral M.P., Naranjo M.C., Gomez-Corvera A., Caballero B., Guerrero J.M. Age-related changes in melatonin synthessis in rats tissues. Exp. Gerontol. 2009, 44:328-334.
66. Sandhu S.K., Kaur G. Alterations in oxidative stress scavenger system in aging rat brain and lymphocytes. Biogerontology 2002, 3(3):161-173.
67. Sandstrom N.J., Hart S.R. Isolation stress during the third postnatal week alters radial arm maze performance and corticosterone levels in adulthood. Behav. Brain Res. 2005, 156:289-296.
68. Senthil Kumaran V., Arulmathi K., Srividhya R., Kalaiselvi P. Repletion of antioxidant status by EGCG and retardation of oxidative damage induced macromolecular anomalies in aged rats. Exp. Gerontol. 2008, 43:176-183.
69. Serrano F., Klann E. Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Res. Rev. 2004, 3(4):431-443.
70. Sethi P., Jyoti A., Singh R., Hussain E., Sharma D. Aluminium-induced electrophysiological, biochemical and cognitive modifications in the hippocampus of aging rats. Neurotoxicology 2008, 29(6):1069-1079.
71. Sharma D.R., Wani W.Y., Sunkaria A., Kandimalla R.J., Verma D., Cameotra S.S., Gill K.D. Quercetin protects against chronic aluminum-induced oxidative stress and ensuing biochemical, cholinergic, and neurobehavioral impairments in rats. Neurotox. Res. 2013, 23(4):336-357.
72. Sohal R.S., Mockett R.J., Orr W.C. Current issues concerning the role of oxidative stress in aging: a perspective. Results Probl. Cell Differ. 2000, 29:45-66.
73. Solfrizzi V., Colacicco A.M., D'Introno A., Capurso C., Parigi A.D., Capurso S.A., Torres F., Capurso A., Panza F. Macronutrients, aluminium from drinking water and foods, and other metals in cognitive decline and dementia. J. Alzheimers Dis. 2006, 10(2-3):303-330.
74. Sonmez M.F., Narin F., Akkus D., Türkmen A.B. Melatonin and vitamin C ameliorate alcohol-induced oxidative stress and eNOS expression in rat kidney. Ren. Fail. 2012, 34:480-486.
75. Sood P.K., Nahar U., Nehru B. Curcumin attenuates aluminum-induced oxidative stress and mitochondrial dysfunction in rat brain. Neurotox. Res. 2011, 20:351-361.
76. Srinivasan V. Melatonin oxidative stress and neurodegenerative diseases. Indian J. Exp. Biol. 2002, 40(6):668.
77. Srinivasan V., Pandi-Perumal S.R., Cardinali D.P., Poeggeler B., Hardeland R. Melatonin in Alzheimer's disease and other neurodegenerative disorders. Behav. Brain Funct. 2006, 2:15.
78. Srividhya R., Gayathri R., Kalaiselvi P. Impact of epigallo catechin-3-gallate on acetylcholine-acetylcholine esterase cycle in aged rat brain. Neurochem. Int. 2012, 60:517-522.
79. Srividhya R., Jyothilakshmi V., Arulmathi K., Senthilkumaran V., Kalaiselvi P. Attenuation of senescence-induced oxidative exacerbations in aged rat brain by (-)-epigallocatechin-3-gallate. Int. J. Dev. Neurosci. 2008, 26:217-223.
80. Struys-Ponsar C., Kerkhofs A., Gauthier A., Soffie M., Van den Bosch de Aguilar P. Effect of aluminum induced exposure on behavioural parameters in the rat. Pharmacol. Biochem. Behav. 1997, 56:643-648.
81. Sudnikovich E.J., Maksimchik Y.Z., Zabrodskaya S.V., Kubyshin V.L., Lapshina E.A., Bryszewska M., Reiter R.J., Zavodnik I.B. Melatonin attenuates metabolic disorders due to streptozotocin-induced diabetes in rats. Eur. J. Pharmacol. 2007, 569(3):180-187.
82. Sun Y., Oberley L.W., Li Y. A simple method for clinical assay of superoxide dismutase. Clin. Chem. 1988, 34:497-500.
83. Tan D.X., Manchester L.C., Liu X., Rosales-Corral S.A., Acuna-Castroviejo D., Reiter R.J. Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin's primary function and evolution in eukaryotes. J. Pineal Res. 2013, 54(2):127-138.
84. Tan D.X., Manchester L.C., Terron M.P., Flores L.J., Reiter R.J. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species?. J. Pineal Res. 2007, 42:28-42.
85. Tripathi S., Mahdi A.A., Nawab A., Chander R., Hasan M., Siddiqui M.S., Mahdi F., Mitra K., Bajpai V.K. Influence of age on aluminum induced lipid peroxidation and neurolipofuscin in frontal cortex of rat brain: a behavioral, biochemical and ultrastructural study. Brain Res. 2009, 1253:107-116.
86. Tunez I., Munoz M.C., Medina F.J., Salcedo M., Feijóo M., Montilla P. Comparison of melatonin, vitamin E and L-carnitine in the treatment of neuro- and hepatotoxicity induced by thioacetamide. Cell Biochem. Funct. 2007, 25:119-127.
87. Turchi J., Saunders R.C., Mishkin M. Effects of cholinergic deafferentation of the rhinal cortex on visual recognition memory in monkeys. Proc. Natl. Acad. Sci. USA 2005, 102:2158-2161.
88. Vanguilder H.D., Freeman W.M. The hippocampal neuroproteome with aging and cognitive decline: past progress and future directions. Front Aging Neurosci. 2011, 23(3):8.
89. Vishwas D.K., Mukherjee A., Haldar C., Dash D., Nayak M.K. Improvement of oxidative stress and immunity by melatonin: an age dependent study in golden hamster. Exp. Gerontol. 2013, 48(2):168-182.
90. Walsh R.N., Cummins R.A. The Open-Field Test: a critical review. Psychol. Bull. 1976, 83:482-504.
91. Wang H., Li L., Zhao M., Chen Y.H., Zhang Z.H., Zhang C., Ji Y.L., Meng X.H., Xu D.X. Melatonin alleviates lipopolysaccharide-induced placental cellular stress response in mice. J. Pineal Res. 2011, 50(4):418-426.
92. Weinberger N.M. Food for Thought: Honeybee Foraging, Memory, and Acetylcholine. Sci. STKE 2006 2006, (336):pe23.
93. Xu N., Majidi V., Markesbery W.R., Ehmann W.D. Brain aluminum in Alzheimer's disease using an improved GFAAS method. Neurotoxicology 1992, 13:735-743.
94. Yao Y., Han D.D., Zhang T., Yang Z. Quercetin improves cognitive deficits in rats with chronic cerebral ischemia and inhibits voltage-dependent sodium channels in hippocampal CA1 pyramidal neurons. Phytother. Res. 2010, 24:136-140.
95. Yokel R.A. The toxicology of aluminum in the brain: a review. Neurotoxicology 2000, 21:813-828.
96. Yu B.P. Aging and oxidative stress: modulation by dietary restriction. Free Radic. Biol. Med. 1996, 21(5):651-668.
97. Zatta P., Ibn-Lkhayat-Idrissi M., Zambenedetti P., Kilyen M., Kiss T. In vivo and in vitro effects of aluminum on the activity of mouse brain acetylcholinesterase. Brain Res. Bull. 2002, 59(1):41-45.
98. Zhu Y., Li X., Chen C., Wang F., Li J., Hu C., Li Y., Miao L. Effects of aluminium trichloride on the trace elements and cytokines in the spleen of rats. Food Chem. Toxicol. 2012, 50:2911-2915.