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ISSN (Online): 2210-3163

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Research Article

Studies on Secondary Metabolites and In vitro and In silico Anticholinesterases Activities of the Sea Urchin Echinometra mathaei Crude Venoms from the Persian Gulf-Bushehr

Author(s): Hamideh Dehghani, Marzieh Rashedinia, Gholamhossein Mohebbi* and Amir Vazirizadeh

Volume 14, Issue 2, 2024

Published on: 01 August, 2023

Article ID: e220623218175 Pages: 18

DOI: 10.2174/2210315514666230622144244

Price: $65

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Abstract

Background: Echinoderms are a unique source of amazing secondary metabolites with a wide spectrum of biological activities. Several species of sea urchins contain various toxins and biologically active metabolites. One of the most attractive approaches to treat Alzheimer's disease is searching for effective marine natural products with cholinesterase inhibitory activities.

Objective: The current study is designed to investigate the in vitro and in silico acetylcholinesterase and butyrylcholinesterase inhibitory activities of the Persian Gulf echinoderm sea urchin Echinometra mathaei venom and related chemical compounds.

Methods: The experiments for LD50, total protein, protein bands, in vitro cholinesterase inhibitory activities, the identity of secondary metabolites, and the in silico evaluations, respectively, were performed by Spearman-Karber, Lowry, SDS-PAGE, Ellman's spectroscopic, GC-MS, and docking methods.

Results: The LD50 (IV rat) of the spine, gonad, and coelomic fluid from sea urchin samples were 2.231 ± 0.09, 1.03 ± 0.05, and 1.12 ± 0.13 mg/ml, respectively. The SDS-PAGE and total protein studies showed that at least a portion of the venom is protein in nature. GC-MS analysis of the identified samples revealed 12, 23, and 21 compounds with different chemical types, including alkaloids, terpenes, and steroids, respectively. According to the results, all samples act as significant inhibitors of both enzymes. In silico data for the identified compounds also confirmed the experimental results.

Conclusion: The alkaloid compound 6H-Indolo[3,2,1-de] [1,5] naphthyridine-6-one,1,2,3a,4,5- hexahydro-8-hydroxy-3-methyl (C7) had the highest affinity for both enzymes. Further research is needed to determine whether C7 could be a therapeutic candidate for Alzheimer's disease.

Graphical Abstract

[1]
Lhullier, C.; Moritz, M.I.G.; Tabalipa, E.O.; Sardá, F.N.; Schneider, N.F.Z.; Moraes, M.H.; Constantino, L.; Reginatto, F.H.; Steindel, M.; Pinheiro, U.S.; Simões, C.M.O.; Pérez, C.D.; Schenkel, E.P. Biological activities of marine invertebrates extracts from the northeast brazilian coast. Braz. J. Biol., 2020, 80(2), 393-404.
[http://dx.doi.org/10.1590/1519-6984.213678] [PMID: 31389485]
[2]
Mohebbi, G.H.; Nabipour, I.; Vazirizadeh, A. The sea, the future pharmacy. Iran South Med. J., 2014, 17(4), 748-788.
[3]
Kong, D.X.; Jiang, Y.Y.; Zhang, H.Y. Marine natural products as sources of novel scaffolds: A chievement and concern. Drug Discov. Today, 2010, 15(21-22), 884-886.
[http://dx.doi.org/10.1016/j.drudis.2010.09.002] [PMID: 20869461]
[4]
Ebrahimi, H.; Mohebbi, G.H. VazirizadeAh, A.; Nabipour, I.; Nafisi, B.M. Sea cucumbers, the ocean of bioactive compounds. Iran. South. Med. J., 2015, 18(3), 664-679.
[5]
Britannica, the Editors of Encyclopaedia. "Brittle star"; Concise Encyclopedia Chemistry, 2018.
[6]
Miller, J.E.; Pawson, D.L. echinoderm; Encyclopedia Britannica, 2020.
[7]
Kalinin, V.I. Echinoderms metabolites: Structure, functions, and biomedical perspectives. Mar. Drugs, 2021, 19(3), 125.
[http://dx.doi.org/10.3390/md19030125] [PMID: 33652699]
[8]
Nabipour, I. The venomous animals of the Persian Gulf; Bushehr University of Medical Sciences Press: Iran, 2012.
[9]
Mohebbi, G.; Vazirizadeh, A.; Nabipour, I. Sea urchin: Toxinology, bioactive compounds and its treatment management. ISMJ, 2016, 19(4), 704-735.
[http://dx.doi.org/10.18869/acadpub.ismj.19.4.704]
[10]
Kamyab, E.; Kellermann, M.Y.; Kunzmann, A.; Schupp, P.J. Chemical biodiversity and bioactivities of saponins in echinodermata with an emphasis on sea cucumbers (Holothuroidea). In: YOUMARES 9- The Oceans: Our Research, Our Future; Kamyab, E.; Kellermann, M.Y.; Kunzmann, A.; Schupp, P.J.; Jungblut, S.; Liebich, V.; Bode-Dalby, M., Eds.; Springer: Cham, USA, 2020, pp. 121-157.
[11]
Dyshlovoy, S.A.; Pelageev, D.N.; Hauschild, J.; Sabutskii, Y.E.; Khmelevskaya, E.A.; Krisp, C.; Kaune, M.; Venz, S.; Borisova, K.L.; Busenbender, T.; Denisenko, V.A.; Schlüter, H.; Bokemeyer, C.; Graefen, M.; Polonik, S.G.; Anufriev, V.P.; von Amsberg, G. Inspired by sea urchins: Warburg effect mediated selectivity of novel synthetic non-glycoside 1,4-naphthoquinone-6S-glucose conjugates in prostate cancer. Mar. Drugs, 2020, 18(5), 251.
[http://dx.doi.org/10.3390/md18050251] [PMID: 32403427]
[12]
Polonik, S.; Likhatskaya, G.; Sabutski, Y.; Pelageev, D.; Denisenko, V.; Pislyagin, E.; Chingizova, E.; Menchinskaya, E.; Aminin, D. Synthesis, cytotoxic activity evaluation and quantitative structure-activityanalysis of substituted 5,8-dihydroxy-1,4-naphthoquinones and their O- and S-glycoside derivatives tested against neuro-2a cancer cells. Mar. Drugs, 2020, 18(12), 602.
[http://dx.doi.org/10.3390/md18120602] [PMID: 33260299]
[13]
Mishchenko, N.P.; Krylova, N.V.; Iunikhina, O.V.; Vasileva, E.A.; Likhatskaya, G.N.; Pislyagin, E.A.; Tarbeeva, D.V.; Dmitrenok, P.S.; Fedoreyev, S.A. Antiviral potential of sea urchin aminated spinochromes against herpes simplex virus type 1. Mar. Drugs, 2020, 18(11), 550.
[http://dx.doi.org/10.3390/md18110550] [PMID: 33167501]
[14]
Ageenko, N.; Kiselev, K.; Dmitrenok, P.; Odintsova, N. Pigment cell differentiation in sea urchin blastula-derived primary cell cultures. Mar. Drugs, 2014, 12(7), 3874-3891.
[http://dx.doi.org/10.3390/md12073874] [PMID: 24979272]
[15]
Mohebbi, G.; Nabipour, I.; Vazirizadeh, A.; Vatanpour, H.; Farrokhnia, M.; Maryamabadi, A.; Bargahi, A. Acetylcholinesterase inhibitory activity of a neurosteroidal alkaloid from the upside-down jellyfish Cassiopea andromeda venom. Rev. Bras. Farmacogn., 2018, 28(5), 568-574.
[http://dx.doi.org/10.1016/j.bjp.2018.06.002]
[16]
Barmak, A.; Niknam, K.; Mohebbi, G.; Pournabi, H. Antibacterial studies of hydroxyspiro[indoline-3,9-xanthene]trione against spiro[indoline3,9-xanthene]trione and their use as acetyl and butyrylcholinesterase inhibitors. Microb. Pathog., 2019, 130, 95-99.
[http://dx.doi.org/10.1016/j.micpath.2019.03.002] [PMID: 30851360]
[17]
Hussein, W. Sağlık, B.; Levent, S.; Korkut, B.; Ilgın, S.; Özkay, Y.; Kaplancıklı, Z. Synthesis and biological evaluation of new cholinesterase inhibitors for alzheimer’s disease. Molecules, 2018, 23(8), 2033.
[http://dx.doi.org/10.3390/molecules23082033] [PMID: 30110946]
[18]
Langjae, R.; Bussarawit, S.; Yuenyongsawad, S.; Ingkaninan, K.; Plubrukarn, A. Acetylcholinesterase-inhibiting steroidal alkaloid from the sponge Corticium sp. Steroids, 2007, 72(9-10), 682-685.
[http://dx.doi.org/10.1016/j.steroids.2007.05.005] [PMID: 17610922]
[19]
Mohebbi, G.; Nabipour, I.; Mohebbi, G.; Vazirizadeh, A.; Vatanpour, H.; Maryamabadi, A. Studies on the cholinesterases inhibiting compounds from the Cassiopea andromeda venom. Bioinformation, 2020, 16(9), 702-709.
[http://dx.doi.org/10.6026/97320630016702] [PMID: 34621116]
[20]
Spearman-karber, R. Alternative methods of analysis for quantal responses. In: Statistical Method in Biological Assay; Finney, D.J., Ed.; Charles Griffin & Company: London, 1978, p. 645.
[21]
Lowry, O.; Rosebrough, N.; Farr, A.L.; Randall, R. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 1951, 193(1), 265-275.
[http://dx.doi.org/10.1016/S0021-9258(19)52451-6] [PMID: 14907713]
[22]
Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 1970, 227(5259), 680-685.
[http://dx.doi.org/10.1038/227680a0] [PMID: 5432063]
[23]
Brinkman, D.; Burnell, J. Partial purification of cytolytic venom proteins from the box jellyfish, Chironex fleckeri. Toxicon, 2008, 51(5), 853-863.
[http://dx.doi.org/10.1016/j.toxicon.2007.12.017] [PMID: 18243272]
[24]
Worek, F.; Mast, U.; Kiderlen, D.; Diepold, C.; Eyer, P. Improved determination of acetylcholinesterase activity in human whole blood. Clin. Chim. Acta, 1999, 288(1-2), 73-90.
[http://dx.doi.org/10.1016/S0009-8981(99)00144-8] [PMID: 10529460]
[25]
Frisch, M.J.; Trucks, G.W.; Schlegel, H.B. Gaussian 09; Gaussian, Inc.: Wallingford, CT, 2009.
[26]
Maryamabadi, A.; Hasaninejad, A.; Nowrouzi, N.; Mohebbi, G.; Asghari, B. Application of PEG-400 as a green biodegradable polymeric medium for the catalyst-free synthesis of spiro-dihydropyridines and their use as acetyl and butyrylcholinesterase inhibitors. Bioorg. Med. Chem., 2016, 24(6), 1408-1417.
[http://dx.doi.org/10.1016/j.bmc.2016.02.019] [PMID: 26879857]
[27]
Biré, R.; Trotereau, S.; Lemée, R.; Oregioni, D.; Delpont, C.; Krys, S.; Guérin, T. Hunt for palytoxins in a wide variety of marine organisms harvested in 2010 on the french mediterranean coast. Mar. Drugs, 2015, 13(8), 5425-5446.
[http://dx.doi.org/10.3390/md13085425] [PMID: 26308009]
[28]
Kazemi, S.; Heidari, B.; Rassa, M. Antibacterial and hemolytic effects of aqueous and organic extracts from different tissues of sea urchin Echinometra mathaei on pathogenic streptococci. Int. Aquatic Research, 2016, 8(4), 299-308.
[http://dx.doi.org/10.1007/s40071-016-0143-0]
[29]
Soleimani, S.; Moein, S.; Yousefzadi, M.; Amrollahi Bioki, N. Effect of sea urchin echinometra mathaei extraction on the ɑ- amylase enzyme activity. I. J. D. M., 2016, 15(2), 75-83.
[30]
Nhu Hieu, V.M.; Thanh Van, T.T.; Hang, C.T.T.; Mischenko, N.P.; Sergey, A F. Truong, H.B. Polyhydroxy naphthoquinone pigment from vietnam sea urchins as a potential bioactive ingredient in cosmeceuticals. Nat. Prod. Commun., 2020, 15(11), 1934578X2097252.
[http://dx.doi.org/10.1177/1934578X20972525]
[31]
Loomis, T.A.; Hayes, A.W. Numbers in toxicology. In: Loomis’s essentials of toxicology; Loomis, T.A.; Hayes, A.W., Eds.; Elsevier: USA, 1996, pp. 208-245.
[http://dx.doi.org/10.1016/B978-012455625-6/50002-7]
[32]
Kuwabara, S. Purification and properties of peditoxin and the structure of its prosthetic group, pedoxin, from the sea urchin Toxopneustes pileolus (Lamarck). J. Biol. Chem., 1994, 269(43), 26734-26738.
[http://dx.doi.org/10.1016/S0021-9258(18)47080-9] [PMID: 7929407]
[33]
Mebs, D. A toxin from the sea urchin Tripneustes gratilla. Toxicon, 1984, 22(2), 306-307.
[http://dx.doi.org/10.1016/0041-0101(84)90031-X] [PMID: 6729846]
[34]
Alender, C.B.; Feigen, G.A.; Tomita, J.T. Isolation and characterization of sea urchin toxin. Toxicon, 1965, 3(1), 9-17.
[http://dx.doi.org/10.1016/0041-0101(65)90062-0] [PMID: 5885375]
[35]
Nakagawa, H.; Kimura, A. Partial purification and characterization of a toxic substance from pedicellariae of the sea urchin Toxopneustes pileolus. Jpn. J. Pharmacol., 1982, 32(5), 966-968.
[http://dx.doi.org/10.1016/S0021-5198(19)62220-1] [PMID: 7176229]
[36]
Oberdorf, J.A.; Lebeche, D.; Head, J.F.; Kaminer, B. Identification of a calsequestrin-like protein from sea urchin eggs. J. Biol. Chem., 1988, 263(14), 6806-6809.
[http://dx.doi.org/10.1016/S0021-9258(18)68714-9] [PMID: 2834390]
[37]
Gingras, D.; White, D.; Garin, J.; Multigner, L.; Job, D.; Cosson, J.; Huitorel, P.; Zingg, H.; Dumas, F.; Gagnon, C. Purification, cloning, and sequence analysis of a Mr = 30,000 protein from sea urchin axonemes that is important for sperm motility. J. Biol. Chem., 1996, 271(22), 12807-12813.
[http://dx.doi.org/10.1074/jbc.271.22.12807] [PMID: 8662724]
[38]
Cragg, G.M.; Newman, D.J. Natural products: A continuing source of novel drug leads. Biochim. Biophys. Acta, Gen. Subj., 2013, 1830(6), 3670-3695.
[http://dx.doi.org/10.1016/j.bbagen.2013.02.008] [PMID: 23428572]
[39]
Copeland, R.A. Evaluation of enzyme inhibitors in drug discovery. A guide for medicinal chemists and pharmacologists. Methods Biochem. Anal., 2005, 46, 1-265.
[PMID: 16350889]
[40]
Murray, A.; Faraoni, M.; Castro, M.; Alza, N.; Cavallaro, V. Natural AChE inhibitors from plants and their contribution to alzheimer’s disease therapy. Curr. Neuropharmacol., 2013, 11(4), 388-413.
[http://dx.doi.org/10.2174/1570159X11311040004] [PMID: 24381530]
[41]
Mizuno, M.; Ito, Y.; Morgan, B.P. Exploiting the nephrotoxic effects of venom from the sea anemone, Phyllodiscus semoni, to create a hemolytic uremic syndrome model in the rat. Mar. Drugs, 2012, 10(12), 1582-1604.
[http://dx.doi.org/10.3390/md10071582] [PMID: 22851928]
[42]
Blunt, J.W.; Carroll, A.R.; Copp, B.R.; Davis, R.A.; Keyzers, R.A.; Prinsep, M.R. Marine natural products. Nat. Prod. Rep., 2018, 35(1), 8-53.
[http://dx.doi.org/10.1039/C7NP00052A] [PMID: 29335692]
[43]
Stöhr, S.; O’Hara, T.D.; Thuy, B. Global diversity of brittle stars (Echinodermata: Ophiuroidea). PLoS One, 2012, 7(3), e31940.
[http://dx.doi.org/10.1371/journal.pone.0031940] [PMID: 22396744]
[44]
Taylor, P. Radić, Z. The cholinesterases: From genes to proteins. Annu. Rev. Pharmacol. Toxicol., 1994, 34(1), 281-320.
[http://dx.doi.org/10.1146/annurev.pa.34.040194.001433] [PMID: 8042853]
[45]
Li, S.; Li, A.J.; Travers, J.; Xu, T.; Sakamuru, S.; Klumpp-Thomas, C.; Huang, R.; Xia, M. Identification of compounds for butyrylcholinesterase inhibition. SLAS Discov., 2021, 26(10), 1355-1364.
[http://dx.doi.org/10.1177/24725552211030897] [PMID: 34269114]
[46]
Chen, V.P.; Gao, Y.; Geng, L.; Parks, R.J.; Pang, Y.P.; Brimijoin, S. Plasma butyrylcholinesterase regulates ghrelin to control aggression. Proc. Natl. Acad. Sci., 2015, 112(7), 2251-2256.
[http://dx.doi.org/10.1073/pnas.1421536112] [PMID: 25646463]
[47]
Giacobini, E. Cholinergic function and Alzheimer’s disease. Int. J. Geriatr. Psychiatry, 2003, 18(S1), S1-S5.
[http://dx.doi.org/10.1002/gps.935] [PMID: 12973744]
[48]
Mushtaq, G.; Greig, N.; Khan, J.; Kamal, M. Status of acetylcholinesterase and butyrylcholinesterase in Alzheimer’s disease and type 2 diabetes mellitus. CNS Neurol. Disord. Drug Targets, 2014, 13(8), 1432-1439.
[http://dx.doi.org/10.2174/1871527313666141023141545] [PMID: 25345511]
[49]
Mesulam, M.M.; Guillozet, A.; Shaw, P.; Levey, A.; Duysen, E.G.; Lockridge, O. Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience, 2002, 110(4), 627-639.
[http://dx.doi.org/10.1016/S0306-4522(01)00613-3] [PMID: 11934471]
[50]
Greig, N.H.; Utsuki, T.; Ingram, D.K.; Wang, Y.; Pepeu, G.; Scali, C.; Yu, Q.S.; Mamczarz, J.; Holloway, H.W.; Giordano, T.; Chen, D.; Furukawa, K.; Sambamurti, K.; Brossi, A.; Lahiri, D.K. Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer β-amyloid peptide in rodent. Proc. Natl. Acad. Sci., 2005, 102(47), 17213-17218.
[http://dx.doi.org/10.1073/pnas.0508575102] [PMID: 16275899]
[51]
Giacobini, E. Selective inhibitors of butyrylcholinesterase: A valid alternative for therapy of Alzheimer’s disease? Drugs Aging, 2001, 18(12), 891-898.
[http://dx.doi.org/10.2165/00002512-200118120-00001] [PMID: 11888344]
[52]
Kovarik, Z. Radić, Z.; Grgas, B.; Škrinjarić-Špoljar, M.; Reiner, E.; Simeon-Rudolf, V. Amino acid residues involved in the interaction of acetylcholinesterase and butyrylcholinesterase with the carbamates Ro 02-0683 and bambuterol, and with terbutaline. Biochim. Biophys. Acta Protein Struct. Mol. Enzymol., 1999, 1433(1-2), 261-271.
[http://dx.doi.org/10.1016/S0167-4838(99)00124-7] [PMID: 10446376]
[53]
Brus, B.; Košak, U.; Turk, S.; Pišlar, A.; Coquelle, N.; Kos, J.; Stojan, J.; Colletier, J.P.; Gobec, S. Discovery, biological evaluation, and crystal structure of a novel nanomolar selective butyrylcholinesterase inhibitor. J. Med. Chem., 2014, 57(19), 8167-8179.
[http://dx.doi.org/10.1021/jm501195e] [PMID: 25226236]
[54]
Giacobini, E. Cholinesterase inhibitors stabilize Alzheimer disease. Neurochem. Res., 2000, 25(9/10), 1185-1190.
[http://dx.doi.org/10.1023/A:1007679709322] [PMID: 11059792]
[55]
Verpoorte, R. Alkaloids. In: Encyclopedia of Analytical Science; Paul, W.P.; Townshend, A.; Poole, C., Eds.; Elsevier: USA, 2005; pp. 56-61.
[56]
Dey, P.; Kundu, A.; Kumar, A.; Gupta, M.; Lee, B.M.; Bhakta, T.; Dash, S.; Kim, H.S. Analysis of alkaloids (indole alkaloids, isoquinoline alkaloids, tropane alkaloids. In: Recent Advances in Natural Products Analysis; Silva, A.S.; Nabavi, S.F.; Saeedi, M.; Nanavi; S.M. Elzevier: USA, 2020, pp. 505-567.
[57]
Aniszewski, T.; Aniszewski, T. Alkaloids-secrets of life. In: Alkaloid Chemistry, Biological Significance, Applications and Ecological Role, 1 ed; Elsevier: USA, 2007.
[58]
Chini, C.; Bilia, A.; Keita, A.; Morelli, I. Protoalkaloids from Boscia angustifolia. Planta Med., 1992, 58(5), 476.
[http://dx.doi.org/10.1055/s-2006-961522] [PMID: 17226509]
[59]
Jakubke, H.D.; Jeschkeit, H. Frontmatter. In: Concise Encyclopedia Chemistry; Berlin: New York: De Gruyter, 2011, pp. I-IV.
[http://dx.doi.org/10.1515/9783110854039]
[60]
Choudhary, M.I.; Nawaz, S.A. Zaheer-ul-Haq; Azim, M.K.; Ghayur, M.N.; Lodhi, M.A.; Jalil, S.; Khalid, A.; Ahmed, A.; Rode, B.M.; Atta-ur-Rahman; Gilani, A.H.; Ahmad, V.U. Juliflorine: A potent natural peripheral anionic-site-binding inhibitor of acetylcholinesterase with calcium-channel blocking potential, a leading candidate for Alzheimer’s disease therapy. Biochem. Biophys. Res. Commun., 2005, 332(4), 1171-1179.
[http://dx.doi.org/10.1016/j.bbrc.2005.05.068] [PMID: 16021692]
[61]
Al-Salman, H.N.K. Antimicrobial activity of the compound 2-piperidinone, N-[4-Bromo-nbutyl]-extracted from pomegranate peels. Asian J. Pharm., 2019, 13(1), 4653.
[62]
Herman, A.; Herman, A.P. Caffeine’s mechanisms of action and its cosmetic use. Skin Pharmacol. Physiol., 2013, 26(1), 8-14.
[http://dx.doi.org/10.1159/000343174] [PMID: 23075568]
[63]
Bharate, S.B.; Manda, S.; Joshi, P.; Singh, B.; Vishwakarma, R.A. Total synthesis and anti-cholinesterase activity of marine-derived bis-indole alkaloid fascaplysin. MedChemComm, 2012, 3(9), 1098-1103.
[http://dx.doi.org/10.1039/c2md20076g]
[64]
He, D.; Wu, H.; Wei, Y.; Liu, W.; Huang, F.; Shi, H.; Zhang, B.; Wu, X.; Wang, C. Effects of harmine, an acetylcholinesterase inhibitor, on spatial learning and memory of APP/PS1 transgenic mice and scopolamine-induced memory impairment mice. Eur. J. Pharmacol., 2015, 768, 96-107.
[http://dx.doi.org/10.1016/j.ejphar.2015.10.037] [PMID: 26526348]
[65]
Vieira, I.J.C.; Medeiros, W.L.B.; Monnerat, C.S.; Souza, J.J.; Mathias, L.; Braz-Filho, R.; Pinto, A.C.; Sousa, P.M.; Rezende, C.M.; Epifanio, R.D.A. Two fast screening methods (GC-MS and TLC-ChEI assay) for rapid evaluation of potential anticholinesterasic indole alkaloids in complex mixtures. An. Acad. Bras. Cienc., 2008, 80(3), 419-426.
[http://dx.doi.org/10.1590/S0001-37652008000300003] [PMID: 18797794]
[66]
Riedel, E.; Kyriakopoulos, I.; Nündel, M. 9,10-Dihydroergotalkaloids as inhibitors of acetylcholinesterase. Arzneimittelforschung, 1981, 31(9), 1387-1388.
[PMID: 6796095]
[67]
Mohammed, A.E.; Abdul-Hameed, Z.H.; Alotaibi, M.O.; Bawakid, N.O.; Sobahi, T.R.; Abdel-Lateff, A.; Alarif, W.M. Chemical diversity and bioactivities of monoterpene indole alkaloids (MIAs) from six apocynaceae genera. Molecules, 2021, 26(2), 488.
[http://dx.doi.org/10.3390/molecules26020488] [PMID: 33477682]
[68]
Osuntokun, O.T.; Cristina, G.M. Bio isolation, chemical purification, identification, antimicrobial and synergistic efficacy of extracted essential oils from stem bark extract of Spondias mombin(Linn). J. Mol. Biol., 2019, 4(4), 135-143.
[http://dx.doi.org/10.15406/ijmboa.2019.04.00110]
[69]
Wiart, C. Alkaloids. In: Lead Compounds from Medicinal Plants for the Treatment of Cancer, 1 ed.; Elzevier: USA, 2012.
[70]
Mallikharjuna, P.B.; Seetharam, Y.N. In vitro antimicrobial screening of alkaloid fractions from strychnos potatorum. E-J. Chem., 2009, 6(4), 1200-1204.
[http://dx.doi.org/10.1155/2009/535643]
[71]
Shang, X.F.; Morris-Natschke, S.L.; Liu, Y.Q.; Guo, X.; Xu, X.S.; Goto, M.; Li, J.C.; Yang, G.Z.; Lee, K.H. Biologically active quinoline and quinazoline alkaloids part I. Med. Res. Rev., 2018, 38(3), 775-828.
[http://dx.doi.org/10.1002/med.21466] [PMID: 28902434]
[72]
Michael, J.P. Quinoline, quinazoline and acridonealkaloids. Nat. Prod. Rep., 2008, 25(1), 166-187.
[http://dx.doi.org/10.1039/B612168N] [PMID: 18250901]
[73]
Proksch, P.; Ebel, R.; Edrada, R.; Riebe, F.; Liu, H.; Diesel, A.; Bayer, M.; Li, X.; Han, Lin W.; Grebenyuk, V.; Müller, W.E.G.; Draeger, S.; Zuccaro, A.; Schulz, B. Sponge-associated fungi and their bioactive compounds: The Suberites case. botm, 2008, 51(3), 209-218.
[http://dx.doi.org/10.1515/BOT.2008.014]
[74]
Tsuda, M.; Hirano, K.; Kubota, T.; Kobayashi, J. Pyrinodemin A, a cytotoxic pyridine alkaloid with an isoxazolidine moiety from sponge Amphimedon sp. Tetrahedron Lett., 1999, 40(26), 4819-4820.
[http://dx.doi.org/10.1016/S0040-4039(99)00852-7]
[75]
Kobayashi, J.; Kubota, T.; Ishiguro, Y.; Yamamoto, S.; Fromont, J. Platisidines A-C, N-methylpyridinium alkaloids from an okinawan marine sponge of plakortis species. Heterocycles, 2010, 80(2), 1407-1412.
[http://dx.doi.org/10.3987/COM-09-S(S)131]
[76]
National Center for Biotechnology Information. "PubChem Compound Summary for CID 2564. 2021. Available from: https://pubchem.ncbi.nlm.nih.gov/compound/Carbinoxamine (Accessed on: November 13, 2021).
[77]
Santos, T.C.; Gomes, T.M.; Pinto, B.A.S.; Camara, A.L.; Paes, A.M.A. Naturally occurring acetylcholinesterase inhibitors and their potential use for alzheimer’s disease therapy. Front. Pharmacol., 2018, 9, 1192.
[http://dx.doi.org/10.3389/fphar.2018.01192] [PMID: 30405413]
[78]
Konrath, E.L.; Passos, C.S.; Klein-Júnior, L.C.; Henriques, A.T. Alkaloids as a source of potential anticholinesterase inhibitors for the treatment of Alzheimer’s disease. J. Pharm. Pharmacol., 2013, 65(12), 1701-1725.
[http://dx.doi.org/10.1111/jphp.12090] [PMID: 24236981]
[79]
Zaheer-ul-haq, Z.U.; Wellenzohn, B.; Liedl, K.R.; Rode, B.M. Molecular docking studies of natural cholinesterase-inhibiting steroidal alkaloids from Sarcococca saligna. J. Med. Chem., 2003, 46(23), 5087-5090.
[http://dx.doi.org/10.1021/jm0309194] [PMID: 14584959]
[80]
Castro-Silva, E.S.; Bello, M.; Hernández-Rodríguez, M.; Correa-Basurto, J.; Murillo-Álvarez, J.I.; Rosales-Hernández, M.C.; Muñoz-Ochoa, M. In vitro a nd in silico evaluation of fucosterol from Sargassum horridum as potential human acetylcholinesterase inhibitor. J. Biomol. Struct. Dyn., 2019, 37(12), 3259-3268.
[http://dx.doi.org/10.1080/07391102.2018.1505551] [PMID: 30088792]
[81]
Liu, Y.; Yan, H.; Wen, K.; Zhang, J.; Xu, T.; Wang, L.; Zhou, X.; Yang, X. Identification of epidioxysterol from South China Sea urchin Tripneustes gratilla Linnaeus and its cytotoxic activity. J. Food Biochem., 2011, 35(3), 932-938.
[http://dx.doi.org/10.1111/j.1745-4514.2010.00426.x]
[82]
Tajmirriahi, M.; Momayez, F.; Karimi, K. The critical impact of rice straw extractives on biogas and bioethanol production. Bioresour. Technol., 2021, 319, 124167.
[http://dx.doi.org/10.1016/j.biortech.2020.124167] [PMID: 33017776]
[83]
Khalid, A. Zaheer-ul-Haq; Ghayur, M.N.; Feroz, F.; Atta-ur-Rahman; Gilani, A.H.; Choudhary, M.I. Cholinesterase inhibitory and spasmolytic potential of steroidal alkaloids. J. Steroid Biochem. Mol. Biol., 2004, 92(5), 477-484.
[http://dx.doi.org/10.1016/j.jsbmb.2004.08.003] [PMID: 15795993]
[84]
Habtemariam, S. Introduction to plant secondary metabolites—From biosynthesis to chemistry and antidiabetic action. In:Medicinal Foods as Potential Therapies for Type-2 Diabetes and Associated Diseases; Elsevier: USA, 2019, pp. 109-132.
[85]
Machado, L.P.; Carvalho, L.R.; Young, M.C.M.; Cardoso-Lopes, E.M.; Centeno, D.C.; Zambotti-Villela, L.; Colepicolo, P.; Yokoya, N.S. Evaluation of acetylcholinesterase inhibitory activity of Brazilian red macroalgae organic extracts. Rev. Bras. Farmacogn., 2015, 25(6), 657-662.
[http://dx.doi.org/10.1016/j.bjp.2015.09.003]
[86]
Çeli̇k, K.; Toğar, B.; Türkez, H.; Taşpinar, N. In vitro cytotoxic, genotoxic, and oxidative effects of acyclic sesquiterpene farnesene. Turk. J. Biol., 2014, 38(2), 253-259.
[http://dx.doi.org/10.3906/biy-1309-55]
[87]
Ishnava, K.B.; Chauhan, J.B.; Barad, M.B. Anticariogenic and phytochemical evaluation of Eucalyptus globules Labill. Saudi J. Biol. Sci., 2013, 20(1), 69-74.
[http://dx.doi.org/10.1016/j.sjbs.2012.11.003] [PMID: 23961222]
[88]
Arslan, M.E.; Türkez, H. Mardinoğlu, A. In vitro neuroprotective effects of farnesene sesquiterpene on alzheimer’s disease model of differentiated neuroblastoma cell line. Int. J. Neurosci., 2021, 131(8), 745-754.
[http://dx.doi.org/10.1080/00207454.2020.1754211] [PMID: 32308094]
[89]
Castellanos, F.; Amaya-García, F.; Tello, E.; Ramos, F.A.; Umaña, A.; Puyana, M.; Resende, J.A.L.C.; Castellanos, L. Screening of acetylcholinesterase inhibitors in marine organisms from the Caribbean Sea. Nat. Prod. Res., 2019, 33(24), 3533-3540.
[http://dx.doi.org/10.1080/14786419.2018.1481837] [PMID: 29863905]
[90]
Ashraf, A.; Sarfraz, R.A.; Anwar, F.; Ali Shahid, S.; Khalid Alkharf, K. Chemical composition and biological activities of leaves of ziziphus mauritiana L. native to Pakistan. Pak. J. Bot., 2015, 47(1), 367-376.
[91]
Aldred, E.M. Terpenes. In: Pharmacology: A Handbook for Complementary Healthcare Professionals;Pharmacology: A Handbook for Complementary Healthcare Professionals; Elzevier: USA, , 2009; pp. pp. 167-174.
[92]
Abed, S.A.; Sirat, H.M.; Taher, M. Tyrosinase inhibition, anti-acetylcholinesterase, and antimicrobial activities of the phytochemicals from Gynotroches axillaris Blume. Pak. J. Pharm. Sci., 2016, 29(6), 2071-2078.
[PMID: 28375126]
[93]
Lin, J.; Huang, L.; Yu, J.; Xiang, S.; Wang, J.; Zhang, J.; Yan, X.; Cui, W.; He, S.; Wang, Q. Fucoxanthin, a marine carotenoid, reverses scopolamine-induced cognitive impairments in mice and inhibits acetylcholinesterase in vitro. Mar. Drugs, 2016, 14(4), 67.
[http://dx.doi.org/10.3390/md14040067] [PMID: 27023569]
[94]
D’Auria, M.V.; Riccio, R.; Minale, L. Ophioxanthin, a new marine carotonoid sulphate from the Ophiuroid Ophioderma longicaudum. Tetrahedron Lett., 1985, 26, 1871-1872.
[http://dx.doi.org/10.1016/S0040-4039(00)94760-9]

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