Behavioral and Biochemical Indices of Neurotoxicity in Jimson weed Administered Rats
Keywords:
Food contaminant, Neurotoxicity, Oxidative stress, alkaloid extract.Abstract
This study examined the effect of alkaloid extracts from leaf and fruit of Jimson weed (Datura stramonium L; a toxic food contaminant of global reputation) on cognitive function, antioxidant status and activities of critical enzymes of monoaminergic and cholinergic systems of neurotransmission in rats. Alkaloid extracts were prepared by solvent extraction method. The gas chromatograph coupled with mass spectroscopic (GC-MS) characterization of the extracts was also carried out. Thereafter, rats were administered 100 and 200 mg/kg body weight (p.o) of extracts for thirty days. Prior to termination of the experiment, the rats were subjected to spontaneous alternation and hole-board behavioral tests. Thereafter, rats were sacrificed and activities of acetylcholinesterase (AChE), monoamine oxidase (MAO) and antioxidant enzymes (superoxide dismutase (SOD), glutathione-S-transferase (GST) and catalase), as well as malondialdehyde (MDA) and total thiol (TSH) contents of their brain homogenates were determined. The results showed that rats administered the extracts exhibited reduced memory index and also exhibited increased level of anxiety-like behavior. Furthermore, rats administered the extracts exhibited significantly reduced levels of brain AChE, MAO, SOD, catalase and GST activities, reduced amount of brain TSH and elevated brain MDA content compared to control. Results from the GC-MS characterization revealed the presence of hyoscyamine (atropine), scopolamine, amphetamine, cathine, phenlyephirine and Tropine trifluoroacetate among others in the extracts. Therefore, the alterations in cholinergic, monoaminergic and antioxidant systems in brain of rats administered fruit and leaf alkaloid extracts of Jimson weed could be one of the major biochemical mechanisms underlying their ability to induce impairment of cognitive functions which could be significantly linked to their constituent alkaloids
References
Abdulkarim A. A., Mokuolu O. A., Adeniyi A. (2005): Drug use among adolescents in Ilorin, Nigeria. Trop. Doctor. 35, 225-228.
Adegoke S.A., Alo L.A. (2013): Datura stramonium poisoning in children. Nigerian J. Clin. Prac. 16, 116-118.
Ademiluyi A.O., Ogunsuyi O.B., Oboh G, Agbebi O.J. (2016a): Jimson weed (Datura stramonium L.) alkaloid extracts modulate cholinesterase and monoamine oxidase activities in vitro: possible modulatory effect on neuronal function. Comp. Clin. Pathol. 25, 733-741.
Ademiluyi A. O., Ogunsuyi O. B., Oboh G. (2016b): Alkaloid extracts from Jimson weed (Datura stramonium L.) modulate purinergic enzymes in rat brain. NeuroToxicol. 56, 107-117.
Ademosun A. O., Oboh G. (2014): Comparison of the inhibition of monoamine oxidase and butyrylcholinesterase activities by infusions from green tea and some citrus peels. Int .J. Alzheimer’s Dis. 2014.;1-5
Akinyemi A. J., Oboh G., Oyeleye S. I., Ogunsuyi O. (2017): Anti-amnestic Effect of Curcumin in Combination with Donepezil, an Anticholinesterase Drug: Involvement of Cholinergic System. Neurotox. Res. 1-10.
Akinyemi A.J., Throme G.R., Morsch V.M., Stefanello N., da Costa P., Cardos A., et al. (2016): Effect of dietary supplementation of ginger and turmeric rhizomes on ectonucleosidase, adenosine deminase and acetylcholineesterase in synaptosomes from the cerebral cortex of hypertensive rats. J. Appl. Biomed. 14, 59-70.
Alia M., Horcajo C., Bravo L., Goya L. (2003): Effect of grape antioxidant dietary fiber on the total antioxidant capacity and the activity of liver antioxidant enzymes in rats. Nutri. Res. 23, 1251- 1267.
Allam F., Dao A. T., Chugh G., Bohat R., Jafri F., Patki G., et al. (2013): Grape powder supplementation prevents oxidative stress–induced anxiety-like behavior, memory impairment, and high blood pressure in rats. The J. Nutri. 143, 835-842.
Al-Shaikh A. M., Sablay Z. M. (2005): Hallucinogenic plant poisoning in children. Saudi Med. J. 26, 118-121.
Altameme H. J., Hameed I. H., Kareem M. A. (2015): Analysis of alkaloid phytochemical compounds in the ethanolic extract of Datura stramonium and evaluation of antimicrobial activity. Afri. J. Biotechnol. 14, 1668-1674.
Anoopkumar-Dukie S., Walker R. B., Daya S. (2001): A sensitive and reliable method for the detection of lipid peroxidation in biological tissues. J. Pharm. Pharmacol. 53, 263-266.
Ben-Shlomo Y., Bhatia K. (2004): Using monoamine oxidase type B inhibitors in Parkinsons disease BMJ 329, 581–582.
Berntssen M. H. G., Aatland A., Richard D. H. (2003): Chronic dietary mercury exposure causes oxidative stress, brain lesions, and altered behaviour in Atlantic salmon (Salmo sala) parr. Aq. Toxicol. 65, 55-72.
Bouziri A., Hamdi A., Borgi A., Hadj S. B., Fitouri Z., Menif K., et al. (2011): Datura stramonium L. poisoning in a geophagous child: a case report. Int. J. Emergency Med. 4, 1.
Butterfield D. A., Lauderback C. M. (2002): Lipid peroxidation and protein oxidation in Alzheimer’s disease brain: potential causes and consequences involving amyloid β-peptide-associated free radical oxidative stress 1, 2. Free Radic. Biol. Med. 32, 1050-1060.
Cañadas F., Cardona D., Dávila E., Sánchez-Santed F. (2005): Long-term neurotoxicity of chlorpyrifos: spatial learning impairment on repeated acquisition in a water maze. Toxicol. Sci. 85, 944-951.
Chang S. S., Wu M. L., Deng J. F., Lee C. C., Chin T. F., Liao S. J. (1999): Poisoning by Datura leaves used as edible wild vegetables. Vet. Human Toxicol. 41, 242-245.
Chen L., Ding Y., Cagniard B., Van Laar A. D., Mortimer A., Chi W., et al. (2006): Unregulated cytosolic dopamine causes neurodegeneration associated with oxidative stress in mice. The J. Neurosci. 28, 425-433.
Dugan G. M., Gumbmann M. R., Friedman M. (1989): Toxicological evaluation of Jimson weed (Datura stramonium) seed. Food Chem. Toxicol. 27, 501-510.
Ekanem P. E., Ekanem R., Gaim K. (2016): Histological patterns of neurodegeneration of frontal cortex neurons in datura stramonium treated wistar rats. J. Behav. Brain Sci. 6, 85.
Ellman G.I. (1959): Tissue sulfhydryl groups. Ach. Biochem. Biophysic. 82, 70-74
Ellman G. L., Courtney K. D., Andres V., Jr Featherstone R. M. (1961): A new and rapid cholimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88-95.
Elkashef A. M., Wyatt R. J. (1999): Tardive dyskinesia: possible involvement of free radical and treatment with vitamin E. Schizophr Bull. 25, 731-740.
Fatoye F. O., Morakinyo O. (2002): Substance use among secondary school students in rural and urban communities in south western Nigeria. East African Med. J. 79, 299-305
Fujisaki K., Tsuruya K., Yamato M., Toyonaga J., Noguchi H., Nakano T., et al. (2014): Cerebral oxidative stress induces spatial working memory dysfunction in uremic mice: neuroprotective effect of tempol. Nephrol. Dial. Transplant. 293, 529-538.
Fulda S., Gorman A. M., Hori O., Samali A. (2010): Cellular stress responses: cell survival and cell death. Int. J. Cell Biol.
Funada M, Aoo N, Wada K. (2014): Rewarding Effects of N-Methyl-1-(4-Methoxyphenyl)-2- Aminopropane (PMMA) in Mice: Roleof Modifications of Dopamine System Mediated through its Monoamine Oxidase Inhibition. J. Addict. Res. Ther. 5, 2
Gashawa A, Getachew T. (2015): The Chemistry of Khat and Adverse Effect of Khat Chewing. ASRJETS. 9, 35-46.
Green A.L., Haughton T. M. (1961): A colorimetric method for the estimation of monoamine oxidase. Biochem. J. 78, 172.
Habig W. H., Pabst M. L., Jakpoly W. B. (1974): Glutathione transferase: a first enzymatic step in mercapturicacid and formation. J. Biol. Chem. 249, 7130-7139.
Harborne J. B. (1998): Phytochemical methods a guide to modern techniques of plant analysis. Springer Science & Business Media.
Hasegawa Y., Inoue T., Kawaminami S., Fujita M. (2016): Effects of scallop shell extract on scopolamine-induced memory impairment and MK801-induced locomotor activity. Asian Pacific J. Trop. Med. 9. 662-669.
Herraiz T., Chaparro C. (2005): Human monoamine oxidase is inhibited by tobacco smoke: β-carboline alkaloids act as potent and reversible inhibitors. Biochem Biophysic Res Commun. 326, 378-386.
Ide T., Tsutsui H., Hayashidani S., Kang D., Suematsu N., Nakamura K. I., et al.(2001): Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circulation Res. 88, 529-535.
Işık M., Beydemir Ş., Yılmaz A., Naldan M. E., Aslan H. E., Gülçin İ. (2017): Oxidative stress and mRNA expression of acetylcholinesterase in the leukocytes of ischemic patients. Biomed. Pharmacothe. 87, 561-567.
Kalgutkar A.S., Dalvie D.K., Castagnol N, Taylor T.J. (2001): Interactions of nitrogen-containing xenobiotics with monoamine oxidase (MAO) isozymes A and B: SAR studies on MAO substrates and inhibitors. Chem. Res. Toxicol. 14, 1139– 1162.
Kellogg D. L., Zhao J. L., Coey U., Green J. V. (2005): Acetylcholine-induced vasodilation is mediated by nitric oxide and prostaglandins in human skin. J. Appl. Physiol. 98, 629-632.
Lee S., Kim J., Seo S. G., Choi B. R., Han J. S., Lee K. W., et al. (2014): Sulforaphane alleviates scopolamine-induced memory impairment in mice. Pharmacol. Res. 85, 23-32.
Liu H., Wu J., Yao J. Y., Wang H., Li S. T. (2017): The Role of Oxidative Stress in Decreased Acetylcholinesterase Activity at the Neuromuscular Junction of the Diaphragm during Sepsis. Oxidative Med. Cellular Longevity.
Lowry O.H., Rosebrough N.J., Farr A.L., et al. (1951): Protein measurement with the Folinphenol reagent. J. Biol. Chem. 193: 265–275.
Mahmood K. A., Abbas D. A. (2015): The protective role of datura stramonium leaves ethanolic extract against acute carbaryl toxicity in rats. Int. J. Biomed. Adv. Res. 6, 400–405.
Masood A., Nadeem A., Mustafa S. J., O'Donnell J. M. (2008): Reversal of oxidative stress-induced anxiety by inhibition of phosphodiesterase-2 in mice. J. Pharmacol. Exp. Therapeutics. 326, 369-379.
McDonald B. E., Costa L. G., Murphy S. D. (1988): Spatial memory impairment and central muscarinic receptor loss following prolonged treatment with organophosphates. Toxicol. let. 40, 47-56.
Namdeo A., Tembhre M., Banerjee S., Gour S., Ahirwar S. (2013): Inhibitory efficacy of Chlorpyriphos and Datura stramonium on Acetylcholinesterase activity, Kinetics and histology of Brain of Catla catla. Asian J. Exp. Sci. 27, 47-56.
Oboh G., Nwanna E. E., Oyeleye S. I., Olasehinde T. A., Ogunsuyi O. B., Boligon A. A. (2016): In vitro neuroprotective potentials of aqueous and methanol extracts from Heinsia crinite leaves. Food Sci. Human Wellness. 5(2), 95-102
Ohkawa H., Ohishi N., Yagi K. (1979): Assay of lipid peroxidation in animal tissue by thiobarbituric acid reaction. Anal Biochem. 95, 351-358.
Oshodi O. Y., Aina O. F., Onajole A. T. (2010): Substance use among secondary school students in an urban setting in Nigeria: prevalence and associated factors. African J. Psychiatry. 13, 52-57.
Pereira C. A. L., Nishioka S. D. A. (1994): Poisoning by the use of Datura leaves in a homemade toothpaste. Clin. Toxicol. 32, 329-331.
Pilz J., Meineke I., Gleiter C.H. (2000): Measurement of free and bound malondialdehyde in plasma by high-performance liquid chromatography as the 2,4-dinitrophenylhydrazine derivative. J. Chromatogr B Biomed. Sci. Appl. 742, 315-25.
Ramirez M., Rivera E., Ereu C. (1999): Fifteen cases of hyoscyamine (atropine) poisoning after honey ingestion. Vet. Human Toxicol. 41, 19-20.
Rodrigues S. R., Caldeira C., Castro B. B., Gonçalves F., Nunes B., Antunes S. C. (2011): Cholinesterase (ChE) inhibition in pumpkinseed (Lepomis gibbosus) as environmental biomarker: ChE characterization and potential neurotoxic effects of xenobiotics. Pesticide Biochem. Physiol. 99, 181-188.
Rossignol D. A., Frye R. E. (2012): A review of research trends in physiological abnormalities in autism spectrum disorders: immune dysregulation, inflammation, oxidative stress, mitochondrial dysfunction and environmental toxicant exposures. Mol. Psychiatry. 17, 389-401.
Santillo M. F., Liu Y., Ferguson M., Vohra S. N., Wiesenfeld P. L. (2014): Inhibition of monoamine oxidase (MAO) by β-carbolines and their interactions in live neuronal (PC12) and liver (HuH-7 and MH1C1) cells. Toxicol. in Vitro. 28, 403-410
Shigenaga M. K., Hagen T. M., Ames B. N. (1994): Oxidative damage and mitochondrial decay in aging. Proceedings of the National Academy of Sci. 91, 10771-10778
Sinha A K. (1972): Colorimetric assay of catalase. Anal Biochem. 47, 389–394.
Slatter D. A., Bolton C. H., Bailey A. J. (2000): The importance of lipid derived malondialdehyde in diabetes mellitus. Diabetologia. 43, 550-557
Soni P., Siddiqui A. A., Dwivedi J., Soni V. (2012): Pharmacological properties of Datura stramonium L. as a potential medicinal tree: An overview. Asian Pac. J. Trop. Biomed. 2, 1002-1008.
Stafford G. I., Pedersen P. D., Jäger A. K., Van Staden J. (2007): Monoamine oxidase inhibition by southern African traditional medicinal plants. South African J. Botany. 73, 384-390.
Tabakman R. R., Lecht S., Lazarovici P. (2003): Neuroprotection by monoamine oxidase B inhibitors: a therapeutic strategy for Parkinsons disease? Bio. Essays 26, 80–90.
Tijsseling D., Camm E. J., Lusby C. M., Kane A. D., Derks J. B., Giussani D. A. (2014): Allopurinol prevents object recognition memory impairment in adult offspring following chronic fetal hypoxia. Perinatal glucocorticoid treatment and perspectives for antioxidant therapy, 145.
Vesna E., Zupan G., Varljen J. (2003): Pentylenetetrazol-induced seizures and kindling:changes in freefatty acids, glutathione reductase, superoxide dismutase activity. Neurochem. Int. 42, 173-178.
Wall P. M., Messier C. (2002): Infra limbic kappa opiod and muscarinic MI receptor interactions in the concurrent modulation of anxiety and memory. Psycopharmacol. 160, 233-244.
Wang X., Wang W., Li L., Perry G., Lee H. G., Zhu X. (2014): Oxidative stress and mitochondrial dysfunction in Alzheimer's disease. Biochimica et Biophysica. Acta. (BBA) 1842, 1240-1247
