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Current Enzyme Inhibition

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ISSN (Print): 1573-4080
ISSN (Online): 1875-6662

Research Article

Anticholinesterase and Antioxidant Activities of Spilanthes filicaulis Whole Plant Extracts for the Management of Alzheimer’s Disease

Author(s): Taiwo O. Elufioye *, Cynthia C. Unachukwu and Adebola O. Oyedeji

Volume 15, Issue 2, 2019

Page: [103 - 113] Pages: 11

DOI: 10.2174/1573408015666190730113405

open access plus

Abstract

Background: Spilanthes filicaulis is a tropical herb implicated as a memory enhancer in ethnomedicine.

Objective: The study investigated acetyl/butyryl cholinesterase inhibitory and antioxidant activities of different extracts of S. filicaulis whole plant and correlated them to its phytochemical constituents.

Methods: The powdered whole plant was successively extracted with n-hexane, ethyl acetate and methanol. Acetyl cholinesterase (AChE) and Butyryl cholinesterase (BuChE) inhibitory activity were evaluated by Ellman colorimetry assay. Antioxidant activity was tested using 1, 1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging, ferric reducing power and nitric oxide scavenging assays. Total phenolic, flavonoid and tannin were estimated using standard methods. Correlation was determined using Quest Graph™ Regression Calculator.

Results: Various extracts exhibited concentration-dependent AChE and BuChE inhibitory activity with ethyl acetate extract being the highest with IC50 of 0.77 μg/mL and 0.92 μg/mL for AChE and BuChE respectively. The ethyl acetate extract also showed the highest reducing power when compared with the other extracts. The methanol extract had slightly higher phenolic and flavonoid content and showed the highest DPPH radical scavenging effect. DPPH scavenging, AChE and BuChE inhibition had high correlation with the total flavonoid content with R2 values of 1.00, 0.800 and 0.992 respectively while nitric oxide scavenging had high correlation with phenolics and tannins with R2 = 0.942 and 0.806 respectively.

Conclusion: These results show that the extracts of the whole plant of S. filicaulis possess significant AChE/BuChE inhibitory and antioxidant properties, mostly due to its flavonoid content, suggesting the possible use of the plant in neurodegenerative diseases such as AD.

Keywords: Alzheimer’s disease, anticholinesterase, antioxidant, Spilanthes filicaulis, total flavonoids, total phenolic.

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[1]
Hyman, B.T.; Phelps, C.H.; Beach, T.G.; Bigio, E.H.; Cairns, N.J.; Carrillo, M.C.; Dickson, D.W.; Duyckaerts, C.; Frosch, M.P.; Masliah, E.; Mirra, S.S. National Institute on Aging-Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer’s disease. Alzheimers Dement., 2012, 8(1), 1-3.
[http://dx.doi.org/10.1016/j.jalz.2011.10.007]
[2]
Medeiros, R.; Baglietto‐Vargas, D.; LaFerla, F.M. The role of tau in Alzheimer’s disease and related disorders. CNS Neurosci. Ther., 2011, 5, 514-524.
[http://dx.doi.org/10.1111/j.1755-5949.2010.00177.x]
[3]
Armstrong, R. What causes Alzheimer’s disease? Folia Neuropathol., 2013, 51(3), 169-188.
[http://dx.doi.org/10.5114/fn.2013.37702]
[4]
Smith, M.A.; Rottkamp, C.A.; Nunomura, A.; Raina, A.K. Perry. G. Oxidative stress in Alzheimer’s disease. Biochimica et Biophysica Acta (BBA)-. Mol. Basis Dis., 2000, 1502(1), 139-144.
[http://dx.doi.org/10.1016/S0925-4439(00)00040-5]
[5]
Spires, T.L.; Orne, J.D.; SantaCruz, K.; Pitstick, R.; Carlson, G.A.; Ashe, K.H.; Hyman, B.T. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am. J. Pathol., 2006, 168(5), 1598-1607.
[http://dx.doi.org/10.2353/ajpath.2006.050840]
[6]
Chen, K.H.; Reese, E.A.; Kim, H.W.; Rapoport, S.I.; Rao, J.S. Disturbed neurotransmitter transporter expression in Alzheimer disease brain. J. Alzheimers Dis., 2011, 26(4), 755.
[http://dx.doi.org/10.3233/JAD-2011-110002]
[7]
Rogers, J. The inflammatory response in Alzheimer’s disease. J. Periodontol., 2008, 79, 1535-1543.
[http://dx.doi.org/10.1902/jop.2008.080171]
[8]
Álvarez‐Arellano, L.; Pedraza‐Escalona, M.; Blanco‐Ayala, T.; Camacho‐Concha, N.; Cortés‐Mendoza, J.; Pérez‐Martínez, L.; Pedraza‐Alva, G. Autophagy impairment by caspase‐1‐dependent inflammation mediates memory loss in response to β‐Amyloid peptide accumulation. J. Neurosci. Res., 2018, 96(2), 234-246.
[http://dx.doi.org/10.1002/jnr.24130]
[9]
Perry, E.K.; Tomilinson, B.E.; Blessed, G.; Bergmann, K.; Gibson, P.H.; Perry, R.H. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Brazilian Med. J., 1978, 6150, 1457-1459.
[http://dx.doi.org/10.1136/bmj.2.6150.1457]
[10]
Kumar, A.; Singh, A. A review on Alzheimer’s disease pathophysiology and its management: an update. Pharmacol. Rep., 2015, 67(2), 195-203.
[http://dx.doi.org/10.1016/j.pharep.2014.09.004]
[11]
Greig, N.H.; Lahiri, D.K.; Sambamurti, K. Butyrylcholinesterase: an important new target in Alzheimer’s disease therapy. Int. Psychogeriatr., 2002, 14(S1), 77-91.
[http://dx.doi.org/10.1017/S1041610203008676]
[12]
Tabet, N. Acetylcholinesterase inhibitors for Alzheimer’s disease: anti-inflammatories in acetylcholine clothing. Age Ageing, 2006, 35(4), 336-338.
[http://dx.doi.org/10.1093/ageing/afl027]
[13]
Balunas, M.J.; Kinghorn, A.D. Drug discovery from medicinal plants. Life Sci., 2005, 78(5), 431-441.
[http://dx.doi.org/10.1016/j.lfs.2005.09.012]
[14]
Orhan, I.; Şener, B.; Choudhary, M.I.; Khalid, A. Acetylcholinesterase and butyrylcholinesterase inhibitory activity of some Turkish medicinal plants. J. Ethnopharmacol., 2004, 91(1), 57-60.
[http://dx.doi.org/10.1016/j.jep.2003.11.016]
[15]
Vinutha, B.; Prashanth, D.; Salma, K.; Sreeja, S.L.; Pratiti, D.; Padmaja, R.; Radhika, S.; Amit, A.; Venkateshwarlu, K.; Deepak, M. Screening of selected Indian medicinal plants for acetylcholinesterase inhibitory activity. J. Ethnopharmacol., 2007, 109(2), 359-363.
[http://dx.doi.org/10.1016/j.jep.2006.06.014]
[16]
Elufioye, T.O.; Obuotor, E.M.; Sennuga, A.T.; Agbedahunsi, J.M.; Adesanya, S.A. Acetylcholinesterase and butyrylcholinesterase inhibitory activity of some selected Nigerian medicinal plants. Rev. Bras. Farmacogn., 2010, 20(4), 472-477.
[http://dx.doi.org/10.1590/S0102-695X2010000400002]
[17]
Tiwari, K.L.; Jadhav, S.K.; Joshi, V. An updated review on medicinal herb genus Spilanthes. J. Chin. Integr. Med., 2011, 9(11), 1170-1178.
[http://dx.doi.org/10.3736/jcim20111103]
[18]
Akoachere, J.F.; Suylika, Y.; Mbah, A.J.; Ayimele, A.G.; Assob, J.C.; Fodouop, S.P.; Kodjio, N.; Gatsing, D. In vitro Antimicrobial Activity of agents from Spilanthes filicaulis and Laportea ovalifolia against some drug resistant bacteria. Br. J. Pharm. Res., 2015, 6(2), 76-87.
[http://dx.doi.org/10.9734/BJPR/2015/15582]
[19]
Simbo, D.J. An ethnobotanical survey of medicinal plants in Babungo, North west Region, Cameroon. J. Ethnobiol. Ethnomed., 2010, 1, 8.
[http://dx.doi.org/10.1186/1746-4269-6-8]
[20]
Ndenecho, E.N. Herbalism and resources for the development of ethnopharmacology in Mount Cameroon region. Afr. J. Pharm. Pharmacol., 2009, 3(3), 78-86.
[21]
Ekor, M.; Ashorobi, R.B.; Ibitoye, S.F.; Kasimi, L.S. Acute toxicity, analgesic potential and preliminary antimocrobial studies of the aqueous plant extract of Spilanthes filicaulis. Nigerian J. Health Biomed. Sci., 2005, 4(1), 30-34.
[http://dx.doi.org/10.4314/njhbs.v4i1.11534]
[22]
Donfack, V.D.; Roque, S.; Trigo, G.; Fokou, P.T.; Tchokouaha, L.Y.; Tsabang, N.; Zollo, P.A.; Correia-Neves, M.; Boyom, F.F. Antimycobacterial activity of selected medicinal plants extracts from Cameroon. Int. J. Biol. Chem. Sci., 2014, 8(1), 273-288.
[http://dx.doi.org/10.4314/ijbcs.v8i1.24]
[23]
Samuel, T.A.; James, B.; Oshodi, T.; Odii, U.; Odukoya, O.A.; Magbagbeola, O.A. Evaluation of retinoblastoma (Rb) and protein-53 (p53) gene expression levels in breast cancer cell lines (MCF-7) induced with some selected cytotoxic plants. Planta Med., 2013, 79(13), PE33.
[http://dx.doi.org/10.1055/s-0033-1352052]
[24]
Singleton, V.L.; Rossi, J.A. Colorimetric of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic., 1965, 16, 144-158.
[25]
Chang, C.; Yang, M.; Wen, H.; Chern, J. Estimation of total flavonoid content in Propolis by two complementary colorimetric methods. Yao Wu Shi Pin Fen Xi, 2002, 10, 178-182.
[26]
Broadhurst, R.B.; Jones, W.T. Analysis of condensed tannins using acidified vanillin. J. Sci. Food Agric., 1978, 29(9), 788-796.
[http://dx.doi.org/10.1002/jsfa.2740290908]
[27]
Sanchez-Moreno, C.; Laurrari, J.A.; Saura-Calixto, F. A procedure to measure the antiradical efficacy of polyphenols. J. Sci. Food Agric., 1998, 76, 270-276.
[http://dx.doi.org/10.1002/(SICI)1097-0010(199802)76:2<270:AID-JSFA945>3.0.CO;2-9]
[28]
Oyaizu, M. Studies on products of browning reactions: antioxidative activities of products of browning reaction prepared from glucosamine. Japanese. J. Nutr., 1986, 44, 307-315.
[http://dx.doi.org/10.5264/eiyogakuzashi.44.307]
[29]
Garrat, D.C. The Quantitative analysis of Drugs. Chapman and Hall Ltd, Japan; , 1964. 3, pp. 456-458.
[http://dx.doi.org/10.1007/978-1-4613-3380-7_1]
[30]
Ellman, G.L.; Courtney, K.D.; Andres, V.; Featherstone, R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol., 1961, 7, 88-95.
[http://dx.doi.org/10.1016/0006-2952(61)90145-9]
[31]
Quest Graph™ Linear, Logarithmic, Semi-Log Regression Calculator. AAT Bioquest, Inc, 2019 May 20; - https://www.aatbio.com/tools/linear-logarithmic-semi-log-regression-online-calculator
[32]
Paulraj, J.; Govindarajan, R.; Palpu, P. The genus Spilanthes Ethnopharmacology, phytochemistry, and pharmacological properties: a review. Adv. Pharmacol. Sci., 2013, 2013, 1-22.
[http://dx.doi.org/10.1155/2013/510298]
[33]
Yanga, J.L.; Wanga, R.; Liua, L.L.; Shiab, Y.P. Phytochemicals and biological activities of Saussurea species. J. Asian Nat. Prod. Res., 2010, 12(2), 62-175.
[34]
Velioglu, Y.S.; Mazza, G.; Gao, L.; Oomah, B.D. Antioxidant activity and total phenolics in selected fruits, vegetables and grain products. J. Agric. Food Chem., 1998, 46, 4113-4117.
[http://dx.doi.org/10.1021/jf9801973]
[35]
Tawaha, K.; Alali, F.Q.; Gharaibeh, M.; Mohammad, M.; El-Elimat, T. Antioxidant activity and total phenolic content of selected Jordanian plant species. Food Chem., 2007, 104(4), 1372-1378.
[http://dx.doi.org/10.1016/j.foodchem.2007.01.064]
[36]
Alothman, M.; Bhat, R.; Karim, A.A. Antioxidant capacity and phenolic content of selected tropical fruits from Malaysia, extracted with different solvents. Food Chem., 2009, 115(3), 785-788.
[http://dx.doi.org/10.1016/j.foodchem.2008.12.005]
[37]
Dharmaratne, M.P.; Manoraj, A.; Thevanesam, V.; Ekanayake, A.; Kumar, N.S.; Liyanapathirana, V.; Abeyratne, E.; Bandara, B.R. Terminalia bellirica fruit extracts: in vitro antibacterial activity against selected multidrug-resistant bacteria, radical scavenging activity and cytotoxicity study on BHK-21 cells. BMC Complement. Altern. Med., 2018, 18(1), 325.
[http://dx.doi.org/10.1186/s12906-018-2382-7]
[38]
Bandonien, D.; Pukalskas, A.; Venskutonis, P.R.; Gruzdien, D. Preliminary screening of antioxidant activity of some plant extracts in rapeseed oil. Food Res. Int., 2000, 33(9), 785-791.
[http://dx.doi.org/10.1016/S0963-9969(00)00084-3]
[39]
Wolfe, K.; Wu, X.; Liu, R.H. Antioxidant activity of apple peels. J. Agric. Food Chem., 2003, 51(3), 609-614.
[http://dx.doi.org/10.1021/jf020782a]
[40]
Wang, T.Y.; Li, Q.; Bi, K.S. Bioactive flavonoids in medicinal plants: Structure, activity and biological fate. Asian J. Pharmaceut. Sci., 2018, 13(1), 12-23.
[http://dx.doi.org/10.1016/j.ajps.2017.08.004]
[41]
Cao, G.; Sofic, E.; Prior, R.L. Antioxidant and pro-oxidant behavior of flavonoids: Structure activity relationships. Free Radic. Biol. Med., 2009, 22, 749-760.
[http://dx.doi.org/10.1016/S0891-5849(96)00351-6]
[42]
Hausteen, B. Flavonoids, a class of natural products of high pharmacological potency. Biochem. Pharmacol., 1983, 32, 1141-1148.
[http://dx.doi.org/10.1016/0006-2952(83)90262-9]
[43]
Rice-Evans, C.A.; Miller, N.J. Structure-antioxidant activity relationship of flavonoids and isoflavonoids. Flavonoids in Health and Disease; Rice-Evans, C.A; Packer, L., Ed.; Marcel Dekker: New York, 1997, pp. 199-220.
[44]
Li, H.; Wang, Z.; Liu, Y. Review in the studies on tannins activity of cancer prevention and anticancer. Zhong Yao Cai, 2003, 26(6), 444-448.
[45]
Tan, H.P.; Wong, D.Z.; Ling, S.K.; Chuah, C.H.; Kadir, H.A. Neuroprotective activity of galloylated cyanogenic glucosides and hydrolysable tannins isolated from leaves of Phyllagathis rotundifolia. Fitoterapia, 2012, 83(1), 223-229.
[http://dx.doi.org/10.1016/j.fitote.2011.10.019]
[46]
Kumari, M.; Jain, S. Screening of potential sources of tannin and its therapeutic application. Int. J. Nutr. Food Sci, 2015. 4(2-1), 26-29.
[http://dx.doi.org/10.11648/j.ijnfs.s.2015040201.15]
[47]
Ashafaq, M.; Tabassum, H.; Parvez, S. Modulation of behavioral deficits and neurodegeneration by tannic acid in experimental stroke challenged Wistar rats. Mol. Neurobiol., 2017, 54(8), 5941-5951.
[http://dx.doi.org/10.1007/s12035-016-0096-8]
[48]
Oktay, M.; Gulcin, I.; Kufrevioglu, O.I. Determination of in vitro antioxidant activity of fennel (Foeniculum vulgare) seed extracts. Lebensum-Wiss. U. Technol, 2003, 36, 263-271.
[49]
Kumar, S.; Gupta, A.; Pandey, A.K. Calotropis procera root extract has the capability to combat free radical mediated damage. ISRN Pharmacol., 2013, 2013(9), 1-8.
[http://dx.doi.org/10.1155/2013/691372]
[50]
Wettasinghe, M.; Shahidi, F. Scavenging of reactive-oxygen species and DPPH free radicals by extracts of borage and evening primrose meals. Food Chem., 2000, 70(1), 17-26.
[http://dx.doi.org/10.1016/S0308-8146(99)00269-1]
[51]
Afanas’ ev, I.B.; Dcrozhko, A.I.; Brodskii, A.V.; Kostyuk, V.A.; Potapovitch, A.I. Chelating and free radical scavenging mechanisms of inhibitory action of rutin and quercetin in lipid peroxidation. Biochem. Pharmacol., 1989, 38(11), 1763-1769.
[http://dx.doi.org/10.1016/0006-2952(89)90410-3]
[52]
Lata, H.; Ahuja, G.K. Role of free radicals in health and disease. Ind. J. Physiol. Allied Sci, 2003, 57, 124-128.
[53]
Ialenti, S.; Moncada, M.; Rosa, D.I. Modulation of adjuvant arthritis by endogenous nitric oxide. Br. J. Pharmacol., 1993, 110, 701-705.
[http://dx.doi.org/10.1111/j.1476-5381.1993.tb13868.x]
[54]
Schneider, M.D.; Lon, S. A critical review of cholinesterase inhibitors as a treatment modality in Alzheimer’s disease. Dialogues Clin. Neurosci., 2000, 2(2), 111-128.
[55]
Ballard, C.G. Advances in the treatment of Alzheimer’s disease: benefits of dual cholinesterase inhibition. Eur. Neurol., 2002, 47(1), 64-70.
[http://dx.doi.org/10.1159/000047952]
[56]
Parsons, C.G.; Danysz, W.; Dekundy, A.; Pulte, I. Memantine and cholinesterase inhibitors: complementary mechanisms in the treatment of Alzheimer’s disease. Neurotox. Res., 2013, 24(3), 358-369.
[http://dx.doi.org/10.1007/s12640-013-9398-z]
[57]
Greig, N.H.; Utsuki, T.; Yu, Q.; Zhu, X.; Holloway, H.W.; Perry, T.; Lee, B.; Ingram, D.K.; Lahiri, D.K. A new therapeutic target in Alzheimer’s disease treatment: attention to butyrylcholinesterase. Curr. Med. Res. Opin., 2001, 17(3), 159-165.
[http://dx.doi.org/10.1185/03007990152673800]
[58]
Mukherjee, P.K.; Kumar, V.; Mal, M.; Houghton, P.J. Acetylcholinesterase inhibitors from plants. Phytomedicine, 2007, 14(4), 289-300.
[http://dx.doi.org/10.1016/j.phymed.2007.02.002]
[59]
Babbar, N.; Oberoi, H.S.; Uppal, D.S.; Patil, R.T. Total phenolic content and antioxidant capacity of extracts obtained from six important fruit residues. Food Res. Int., 2011, 44(1), 391-396.
[http://dx.doi.org/10.1016/j.foodres.2010.10.001]
[60]
Cicerale, S.; Lucas, L.; Keast, R. Biological activities of phenolic compounds present in virgin olive oil. Int. J. Mol. Sci., 2010, 11(2), 458-479.
[http://dx.doi.org/10.3390/ijms11020458]
[61]
Pereira, A.; Ferreira, I.; Marcelino, F.; Valentão, P.; Andrade, P.; Seabra, R.; Estevinho, L.; Bento, A.; Pereira, J. Phenolic compounds and antimicrobial activity of olive (Olea europaea L. Cv. Cobrançosa) leaves. Molecules, 2007, 12(5), 1153-1162.
[http://dx.doi.org/10.3390/12051153]
[62]
Zhang, L.; Ravipati, A.S.; Koyyalamudi, S.R.; Jeong, S.C.; Reddy, N.; Smith, P.T.; Bartlett, J.; Shanmugam, K.; Münch, G.; Wu, M.J. Antioxidant and anti-inflammatory activities of selected medicinal plants containing phenolic and flavonoid compounds. J. Agric. Food Chem., 2011, 59(23), 12361-12367.
[http://dx.doi.org/10.1021/jf203146e]
[63]
Uriarte-Pueyo, I.I.; Calvo, M. Flavonoids as acetylcholinesterase inhibitors. Curr. Med. Chem., 2011, 18(34), 5289-5302.
[http://dx.doi.org/10.2174/092986711798184325]
[64]
Gülçin, İ.; Huyut, Z.; Elmastaş, M.; Aboul-Enein, H.Y. Radical scavenging and antioxidant activity of tannic acid. Arab. J. Chem., 2010, 3(1), 43-53.
[http://dx.doi.org/10.1016/j.arabjc.2009.12.008]
[65]
Sabu, M.C.; Kuttan, R. Anti-diabetic activity of medicinal plants and its relationship with their antioxidant property. J. Ethnopharmacol., 2002, 81(2), 155-160.
[http://dx.doi.org/10.1016/S0378-8741(02)00034-X]
[66]
Auddy, B.; Ferreira, M.; Blasina, F.; Lafon, L.; Arredondo, F.; Dajas, F.; Tripathi, P.C.; Seal, T.; Mukherjee, B. Screening of antioxidant activity of three Indian medicinal plants, traditionally used for the management of neurodegenerative diseases. J. Ethnopharmacol., 2003, 84(2-3), 131-138.
[http://dx.doi.org/10.1016/S0378-8741(02)00322-7]
[67]
Khan, N.; Afaq, F.; Mukhtar, H. Cancer chemoprevention through dietary antioxidants: progress and promise. Antioxid. Redox Signal., 2008, 10(3), 475-510.
[http://dx.doi.org/10.1089/ars.2007.1740]
[68]
Ranilla, L.G.; Kwon, Y.I.; Apostolidis, E.; Shetty, K. Phenolic compounds, antioxidant activity and in vitro inhibitory potential against key enzymes relevant for hyperglycemia and hypertension of commonly used medicinal plants, herbs and spices in Latin America. Bioresour. Technol., 2010, 101(12), 4676-4689.
[http://dx.doi.org/10.1016/j.biortech.2010.01.093]
[69]
Hadi, M.Y.; Hameed, I.H.; Ibraheam, I.A. Mentha pulegium: Medicinal uses, Anti-Hepatic, Antibacterial, Antioxidant effect and Analysis of Bioactive Natural Compounds: A Review. Research Journal of Pharmacy and Technology, 2017, 10(10), 3580-3584.
[http://dx.doi.org/10.5958/0974-360X.2017.00648.5]

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