Garcinia binucao crude ethanolic leaf extract prevents alcohol-induced neurotoxic effects on learning, short-term memory, and motor functions in Drosophila melanogaster

Ourlad Alzeus G. Tantengco; Joanne Jennifer E. Tan; Nicholas Robert C. Tan; Maria Concepcion C. Sison; Paul Mark B. Medina

doi:10.7324/JAPS.2018.81014

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Abstract

Excessive alcohol consumption is associated with cognitive and behavioral impairments. Drosophila melanogaster is a commonly used model for learning, memory, and motor function studies. We looked at Garcinia binucao to determine the ability of its crude ethanolic leaf extract to reduce deficits in learning, short-term memory, and motor functions due to alcohol exposure. Chronic alcohol exposure significantly decreased motor function by 22% (p < 0.05), learning function by 37% (p < 0.05), and short-term memory by 33% (p > 0.05). However, in flies fed with G. binucao extract (GBE) chronically exposed to alcohol effects of certain compounds, no significant reductions in motor, learning and in short-term memory functions were observed; instead, these functions increased (p < 0.05) in a dose-dependent manner, suggesting that the extract is not only neuroprotective but is also potentially nootropic. GBE had low antioxidant activity despite the presence of triterpenes, flavonoids, and quinones, although these may have contributed minimally to the neuroprotective ability of GBE. The neuroprotective ability of GBE may then be explained by other mechanisms not dependent on the direct radical or oxidant scavenging properties of the phytochemicals in GBE, as in the modulation of signaling cascades which prevent neuronal apoptosis.

Keyword: Garcinia binucao Drosophila melanogaster alcohol-induced neurotoxicity learning short-term memory motor function.

Citation:

Tantengco OAG, Tan JJE, Tan NRC, Sison MCC, Medina PMB. Garcinia binucao crude ethanolic leaf extract prevents alcoholinduced neurotoxic effects on learning, short-term memory, and motor functions in Drosophila melanogaster. J App Pharm Sci, 2018; 8(10): 106-112.

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Catalán A, Hutter S, Parsch J. Population and sex differences in Drosophila melanogaster brain gene expression. BMC Genomics, 2012; 13:654. https://doi.org/10.1186/1471-2164-13-654
Chua-Barcelo RT. Ethno-botanical survey of edible wild fruits in Benguet, Cordillera administrative region, the Philippines. Asian Pac J Trop Biomed, 2014; 4:S525-38. https://doi.org/10.12980/APJTB.4.201414B36
Devineni AV, Heberlein U. The Evolution of Drosophila melanogaster as a Model for Alcohol Research. Annu Rev Neurosci, 2013; 36:21–128. https://doi.org/10.1146/annurev-neuro-062012-170256
Dong Y, Guha S, Sun X, Cao M, Wang X, Zou S. Nutraceutical Interventions for Promoting Healthy Aging in Invertebrate Models. Oxid Med Cell Longev, 2012; 718491. https://doi.org/10.1155/2012/718491
French RL, Heberlein U. Glycogen synthase kinase-3/Shaggy mediates ethanol-induced excitotoxic cell death of Drosophila olfactory neurons. Proc Natl Acad Sci USA, 2009; 106(49):20924–20929 https://doi.org/10.1073/pnas.0910813106
Gutierrez-Orozco, Failla ML. Biological Activities and Bioavailability of Mangosteen Xanthones: A Critical Review of the Current Evidence. Nutrients, 2013; 5(8):3163–3183. https://doi.org/10.3390/nu5083163
Harper C, Matsumoto I. Ethanol and brain damage. Curr Opin Pharmacol, 2005; 5(1):73–78. https://doi.org/10.1016/j.coph.2004.06.011
Hemshekhar M, Sunitha K, Sebastin Santhosh M, Devaraja S, Kemparaju K, Vishwanath BS, Niranjana SR, Girish KS. An overview on genus garcinia: phytochemical and therapeutical aspects. Phytochem Rev, 2011; 10:325–351. https://doi.org/10.1007/s11101-011-9207-3
Maples T, Rothenfluh A. A simple way to measure ethanol sensitivity in flies. J Vis Exp, 2011; 48:e2541. https://doi.org/10.3791/2541
Nehlig A. The neuroprotective effects of cocoa flavanol and its influence on cognitive performance. Br J Clin Pharmacol, 2013; 75(3):716- 27 https://doi.org/10.1111/j.1365-2125.2012.04378.x
Obolskiy D, Pischel I, Siriwatanametanon N, Heinrich M. Garcinia mangostana L.: A Phytochemical and Pharmacological Review. Phytother. Res., 2009; 23:1047–1065. https://doi.org/10.1002/ptr.2730
Oscar-Berman M, Marinkovi K. Alcohol: Effects on Neurobehavioral Functions and the Brain Marlene, Neuropsychol Rev, 2014; 17:239–257. https://doi.org/10.1007/s11065-007-9038-6
Pedraza-Chaverrí J, Reyes-Fermín LM, Nolasco-Amaya EG, Orozco-Ibarra M, Medina-Campos ON, González-Cuahutencos O, Rivero- Cruz I, Mata R. ROS scavenging capacity and neuroprotective effect of a-mangostin against 3-nitropropionic acid in cerebellar granule neurons, Exp Toxicol Pathol, 2009: 61:491–501. https://doi.org/10.1016/j.etp.2008.11.002
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Wong R, Piper MDW, Wertheim B, Partridge L. Quantification of Food Intake in Drosophila. PLoS One, 2009; 4(6):e6063. https://doi.org/10.1371/journal.pone.0006063
World Health Organization, Global Status Report on Alcohol and Health 2014, WHO Press, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland, 2014.

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Tantengco O A G [PubMed] [Google Scholar ]

Tan J J E [PubMed] [Google Scholar ]

Tan N R C [PubMed] [Google Scholar ]

Sison M C C [PubMed] [Google Scholar ]

Medina P M B [PubMed] [Google Scholar ]

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Berger KH, Kong EC, Dubnau J, Tully T, Moore MS. Ethanol Sensitivity and Tolerance in Long-Term Memory Mutants of Drosophila melanogaster. Alcohol Clin Exp Res, 2011; 32(5):895–908. https://doi.org/10.1111/j.1530-0277.2008.00659.x

Catalán A, Hutter S, Parsch J. Population and sex differences in Drosophila melanogaster brain gene expression. BMC Genomics, 2012; 13:654. https://doi.org/10.1186/1471-2164-13-654

Chua-Barcelo RT. Ethno-botanical survey of edible wild fruits in Benguet, Cordillera administrative region, the Philippines. Asian Pac J Trop Biomed, 2014; 4:S525-38. https://doi.org/10.12980/APJTB.4.201414B36

Devineni AV, Heberlein U. The Evolution of Drosophila melanogaster as a Model for Alcohol Research. Annu Rev Neurosci, 2013; 36:21–128. https://doi.org/10.1146/annurev-neuro-062012-170256

Dong Y, Guha S, Sun X, Cao M, Wang X, Zou S. Nutraceutical Interventions for Promoting Healthy Aging in Invertebrate Models. Oxid Med Cell Longev, 2012; 718491. https://doi.org/10.1155/2012/718491

French RL, Heberlein U. Glycogen synthase kinase-3/Shaggy mediates ethanol-induced excitotoxic cell death of Drosophila olfactory neurons. Proc Natl Acad Sci USA, 2009; 106(49):20924–20929 https://doi.org/10.1073/pnas.0910813106

Gutierrez-Orozco, Failla ML. Biological Activities and Bioavailability of Mangosteen Xanthones: A Critical Review of the Current Evidence. Nutrients, 2013; 5(8):3163–3183. https://doi.org/10.3390/nu5083163

Harper C, Matsumoto I. Ethanol and brain damage. Curr Opin Pharmacol, 2005; 5(1):73–78. https://doi.org/10.1016/j.coph.2004.06.011

Hemshekhar M, Sunitha K, Sebastin Santhosh M, Devaraja S, Kemparaju K, Vishwanath BS, Niranjana SR, Girish KS. An overview on genus garcinia: phytochemical and therapeutical aspects. Phytochem Rev, 2011; 10:325–351. https://doi.org/10.1007/s11101-011-9207-3

Maples T, Rothenfluh A. A simple way to measure ethanol sensitivity in flies. J Vis Exp, 2011; 48:e2541. https://doi.org/10.3791/2541

Nehlig A. The neuroprotective effects of cocoa flavanol and its influence on cognitive performance. Br J Clin Pharmacol, 2013; 75(3):716- 27 https://doi.org/10.1111/j.1365-2125.2012.04378.x

Obolskiy D, Pischel I, Siriwatanametanon N, Heinrich M. Garcinia mangostana L.: A Phytochemical and Pharmacological Review. Phytother. Res., 2009; 23:1047–1065. https://doi.org/10.1002/ptr.2730

Oscar-Berman M, Marinkovi K. Alcohol: Effects on Neurobehavioral Functions and the Brain Marlene, Neuropsychol Rev, 2014; 17:239–257. https://doi.org/10.1007/s11065-007-9038-6

Pedraza-Chaverrí J, Reyes-Fermín LM, Nolasco-Amaya EG, Orozco-Ibarra M, Medina-Campos ON, González-Cuahutencos O, Rivero- Cruz I, Mata R. ROS scavenging capacity and neuroprotective effect of a-mangostin against 3-nitropropionic acid in cerebellar granule neurons, Exp Toxicol Pathol, 2009: 61:491–501. https://doi.org/10.1016/j.etp.2008.11.002

Prieto P, Pineda M, Aguilar M. Spectrophotometric Quantitation of Antioxidant Capacity through the Formation of a Phosphomolybdenum Complex: Specific Application to the Determination of Vitamin E. Anal Biochem, 1999; 269:337–341. https://doi.org/10.1006/abio.1999.4019

Quevedo ES, Pham LJ, Merca FE, Laurena AC. Physicochemical Properties, Lipid and Fatty Acid Profile of "Batuan" [Garcinia binucao (Blco.) Choisy] Seed Oil. Ann Trop Res, 2015; 37(2):11-22.

Ragasa C, Torres O, Marasigan E, Shen C. Sterols and triglyceride from the fruit of Garcinia binucao. Der Pharma Chemica, 2014, 6(6):229-232.

Robinson BG, Khurana S, Pohl JB, Li W, Ghezzi A, Cady AM, Najjar K, Hatch MM, Shah RR, Bhat A, Hariri O, Haroun KB, Young MC, Fife, Hooten J, Tran T, Goan D, Desai F, Husain F, Godinez RM, Sun JC, Corpuz J, Moran J, Zhong AC, Chen WY, Atkinson NS. A Low Concentration of Ethanol Impairs Learning but Not Motor and Sensory Behavior in Drosophila Larvae. PLoS ONE, 2012; 7(5):e37394. https://doi.org/10.1371/journal.pone.0037394

Rukachaisirikul V1, Adair A, Dampawan P, Taylor WC, Turner PC. Lanostanes and friedolanostanes from the pericarp of Garcinia hombroniana. Phytochemistry, 2000; 55(2):183-8. https://doi.org/10.1016/S0031-9422(00)00191-6

Schroeter H, Spencer JP, Rice-Evans C, Williams RJ. Flavonoids protect neurons from oxidized low-density-lipoprotein-induced apoptosis involving c-Jun N-terminal kinase (JNK), c-Jun and caspase-3. Biochem J, 2001; 30:1211–1219

Tangpong J, Miriyala S, Noel T, Sinthupibulyakot C, Jungsuwadee P, Clair DKS. Doxorubicin-induced Central Nervous System Toxicity and Protection by Xanthone Derivative of Garcinia mangostana. Neuroscience, 2012; 175:292–299. https://doi.org/10.1016/j.neuroscience.2010.11.007

Testa ND, Ghosh SM, Shingleton AW. Sex-Specific Weight Loss Mediates Sexual Size Dimorphism in Drosophila melanogaster. PLoS One, 2013; 8(3):e58936. https://doi.org/10.1371/journal.pone.0058936

Vauzour D, Vafeiadou K, Rice-Evans C, Williams RJ, Spencer JP. Activation of pro-survival Akt and ERK1/2 signalling pathways underlie the anti-apoptotic effects of flavanones in cortical neurons. J Neurochem, 2007; 103(4):1355-67. https://doi.org/10.1111/j.1471-4159.2007.04841.x

Velasco AJD, Medina PMB. Crude Anthocyanin Extract (CAE) from Ballatinao Black Rice Does Not Alter Longevity and Increases Stress Susceptibility of Drosophila melanogaster. Int J Curr Res Biosci Plant Biol, 2014; 1(4):35–42.

Vinluan M. Adolescent and Youth Health Program (AYHP), Dep. Heal. (2003). [ONLINE] Available at http://www.doh.gov.ph/adolescent-and-youth-health-program [Accessed 26 December 2017]. 2003.

Wong R, Piper MDW, Wertheim B, Partridge L. Quantification of Food Intake in Drosophila. PLoS One, 2009; 4(6):e6063. https://doi.org/10.1371/journal.pone.0006063

World Health Organization, Global Status Report on Alcohol and Health 2014, WHO Press, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland, 2014.