Rutin as Neuroprotective Agent: From Bench to Bedside

Author(s): Barbara Budzynska, Caterina Faggio, Marta Kruk-Slomka, Dunja Samec, Seyed Fazel Nabavi, Antoni Sureda, Kasi Pandima Devi, Seyed Mohammad Nabavi*

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 27 , 2019

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Abstract:

Flavonoids are major dietary constituents of plant-based food found ubiquitously in plant kingdom where they are usually present in substantial amounts. Rutin is a flavonol-type polyphenol which consists of the flavonol quercetin and the disaccharide rutinose. Rutin has been reported to exert diverse biological effects such as antitumor and antimicrobial mainly associated to its antioxidant and anti-inflammatory activities. Mental, neurological, and behavioural disorders are an important and growing cause of morbidity. Most of these disorders combine a high prevalence, early onset, progressive clinical course, and impairment of critical brain functions making them a major contributor to the global disease burden. In the present work, the biological in vitro and in vivo effects and the potential therapeutic applications of rutin in neurodegenerative processes are reviewed, as well as their bioavailability and pharmacokinetics, which are essential for a better understanding of its biological effectiveness. Moreover, the present review also provides an overview of the molecular mechanisms through which rutin is proposed to exert its neuroprotective effects.

Keywords: Alzheimer's disease, antioxidant, flavonoid, neurodegenerative diseases, polyphenols, rutin.

[1]
Ahmed, T.; Gilani, A.U.; Abdollahi, M.; Daglia, M.; Nabavi, S.F.; Nabavi, S.M. Berberine and neurodegeneration: A review of literature. Pharmacol. Rep., 2015, 67(5), 970-979.
[http://dx.doi.org/10.1016/j.pharep.2015.03.002] [PMID: 26398393]
[2]
Orhan, I.E.; Daglia, M.; Nabavi, S.F.; Loizzo, M.R.; Sobarzo-Sánchez, E.; Nabavi, S.M. Flavonoids and dementia: an update. Curr. Med. Chem., 2015, 22(8), 1004-1015.
[http://dx.doi.org/10.2174/0929867322666141212122352] [PMID: 25515512]
[3]
Sánchez-Barceló, E.J.; Rueda, N.; Mediavilla, M.D.; Martínez-Cué, C.; Reiter, R.J. Clinical uses of melatonin in neurological diseases and mental and behavioural disorders. Curr. Med. Chem., 2017, 24(35), 3851-3878.
[http://dx.doi.org/10.2174/0929867324666170718105557] [PMID: 28721826]
[4]
Wolmarans, W.; Stein, D.J.; Harvey, B.H. A psycho-behavioral perspective on modelling obsessive-compulsive disorder (OCD) in animals: The role of context. Curr. Med. Chem., 2017, 25(41), 5662-5689.
[http://dx.doi.org/10.2174/0929867324666170523125256] [PMID: 28545371]
[5]
Barreto, G.E.; Avila-Rodriguez, M.; Foitzick, M.; Aliev, G.; Echeverria, V. Advances in medicinal plants with effects on anxiety behavior associated to mental and health conditions. Curr. Med. Chem., 2017, 24(4), 411-423.
[http://dx.doi.org/10.2174/0929867323666161101140908] [PMID: 27804869]
[6]
Hussain, Z.; Thu, H.E.; Shuid, A.N. New insight in improving therapeutic efficacy of antipsychotic agents: An overview of improved in vitro and in vivo performance, efficacy upgradation and future prospects Curr. Drug. Targets, 2016.https://www.ncbi.nlm.nih.gov/pubmed/27894237
[7]
Reitz, C.; Mayeux, R. Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem. Pharmacol., 2014, 88(4), 640-651.
[http://dx.doi.org/10.1016/j.bcp.2013.12.024] [PMID: 24398425]
[8]
Murray, C.J.; Vos, T.; Lozano, R.; Naghavi, M.; Flaxman, A.D.; Michaud, C.; Ezzati, M.; Shibuya, K.; Salomon, J.A.; Abdalla, S.; Aboyans, V.; Abraham, J.; Ackerman, I.; Aggarwal, R.; Ahn, S.Y.; Ali, M.K.; Alvarado, M.; Anderson, H.R.; Anderson, L.M.; Andrews, K.G.; Atkinson, C.; Baddour, L.M.; Bahalim, A.N.; Barker-Collo, S.; Barrero, L.H.; Bartels, D.H.; Basáñez, M.G.; Baxter, A.; Bell, M.L.; Benjamin, E.J.; Bennett, D.; Bernabé, E.; Bhalla, K.; Bhandari, B.; Bikbov, B.; Bin Abdulhak, A.; Birbeck, G.; Black, J.A.; Blencowe, H.; Blore, J.D.; Blyth, F.; Bolliger, I.; Bonaventure, A.; Boufous, S.; Bourne, R.; Boussinesq, M.; Braithwaite, T.; Brayne, C.; Bridgett, L.; Brooker, S.; Brooks, P.; Brugha, T.S.; Bryan-Hancock, C.; Bucello, C.; Buchbinder, R.; Buckle, G.; Budke, C.M.; Burch, M.; Burney, P.; Burstein, R.; Calabria, B.; Campbell, B.; Canter, C.E.; Carabin, H.; Carapetis, J.; Carmona, L.; Cella, C.; Charlson, F.; Chen, H.; Cheng, A.T.; Chou, D.; Chugh, S.S.; Coffeng, L.E.; Colan, S.D.; Colquhoun, S.; Colson, K.E.; Condon, J.; Connor, M.D.; Cooper, L.T.; Corriere, M.; Cortinovis, M.; de Vaccaro, K.C.; Couser, W.; Cowie, B.C.; Criqui, M.H.; Cross, M.; Dabhadkar, K.C.; Dahiya, M.; Dahodwala, N.; Damsere-Derry, J.; Danaei, G.; Davis, A.; De Leo, D.; Degenhardt, L.; Dellavalle, R.; Delossantos, A.; Denenberg, J.; Derrett, S.; Des Jarlais, D.C.; Dharmaratne, S.D.; Dherani, M.; Diaz-Torne, C.; Dolk, H.; Dorsey, E.R.; Driscoll, T.; Duber, H.; Ebel, B.; Edmond, K.; Elbaz, A.; Ali, S.E.; Erskine, H.; Erwin, P.J.; Espindola, P.; Ewoigbokhan, S.E.; Farzadfar, F.; Feigin, V.; Felson, D.T.; Ferrari, A.; Ferri, C.P.; Fèvre, E.M.; Finucane, M.M.; Flaxman, S.; Flood, L.; Foreman, K.; Forouzanfar, M.H.; Fowkes, F.G.; Fransen, M.; Freeman, M.K.; Gabbe, B.J.; Gabriel, S.E.; Gakidou, E.; Ganatra, H.A.; Garcia, B.; Gaspari, F.; Gillum, R.F.; Gmel, G.; Gonzalez-Medina, D.; Gosselin, R.; Grainger, R.; Grant, B.; Groeger, J.; Guillemin, F.; Gunnell, D.; Gupta, R.; Haagsma, J.; Hagan, H.; Halasa, Y.A.; Hall, W.; Haring, D.; Haro, J.M.; Harrison, J.E.; Havmoeller, R.; Hay, R.J.; Higashi, H.; Hill, C.; Hoen, B.; Hoffman, H.; Hotez, P.J.; Hoy, D.; Huang, J.J.; Ibeanusi, S.E.; Jacobsen, K.H.; James, S.L.; Jarvis, D.; Jasrasaria, R.; Jayaraman, S.; Johns, N.; Jonas, J.B.; Karthikeyan, G.; Kassebaum, N.; Kawakami, N.; Keren, A.; Khoo, J.P.; King, C.H.; Knowlton, L.M.; Kobusingye, O.; Koranteng, A.; Krishnamurthi, R.; Laden, F.; Lalloo, R.; Laslett, L.L.; Lathlean, T.; Leasher, J.L.; Lee, Y.Y.; Leigh, J.; Levinson, D.; Lim, S.S.; Limb, E.; Lin, J.K.; Lipnick, M.; Lipshultz, S.E.; Liu, W.; Loane, M.; Ohno, S.L.; Lyons, R.; Mabweijano, J.; MacIntyre, M.F.; Malekzadeh, R.; Mallinger, L.; Manivannan, S.; Marcenes, W.; March, L.; Margolis, D.J.; Marks, G.B.; Marks, R.; Matsumori, A.; Matzopoulos, R.; Mayosi, B.M.; McAnulty, J.H.; McDermott, M.M.; McGill, N.; McGrath, J.; Medina-Mora, M.E.; Meltzer, M.; Mensah, G.A.; Merriman, T.R.; Meyer, A.C.; Miglioli, V.; Miller, M.; Miller, T.R.; Mitchell, P.B.; Mock, C.; Mocumbi, A.O.; Moffitt, T.E.; Mokdad, A.A.; Monasta, L.; Montico, M.; Moradi-Lakeh, M.; Moran, A.; Morawska, L.; Mori, R.; Murdoch, M.E.; Mwaniki, M.K.; Naidoo, K.; Nair, M.N.; Naldi, L.; Narayan, K.M.; Nelson, P.K.; Nelson, R.G.; Nevitt, M.C.; Newton, C.R.; Nolte, S.; Norman, P.; Norman, R.; O’Donnell, M.; O’Hanlon, S.; Olives, C.; Omer, S.B.; Ortblad, K.; Osborne, R.; Ozgediz, D.; Page, A.; Pahari, B.; Pandian, J.D.; Rivero, A.P.; Patten, S.B.; Pearce, N.; Padilla, R.P.; Perez-Ruiz, F.; Perico, N.; Pesudovs, K.; Phillips, D.; Phillips, M.R.; Pierce, K.; Pion, S.; Polanczyk, G.V.; Polinder, S.; Pope, C.A., III; Popova, S.; Porrini, E.; Pourmalek, F.; Prince, M.; Pullan, R.L.; Ramaiah, K.D.; Ranganathan, D.; Razavi, H.; Regan, M.; Rehm, J.T.; Rein, D.B.; Remuzzi, G.; Richardson, K.; Rivara, F.P.; Roberts, T.; Robinson, C.; De Leòn, F.R.; Ronfani, L.; Room, R.; Rosenfeld, L.C.; Rushton, L.; Sacco, R.L.; Saha, S.; Sampson, U.; Sanchez-Riera, L.; Sanman, E.; Schwebel, D.C.; Scott, J.G.; Segui-Gomez, M.; Shahraz, S.; Shepard, D.S.; Shin, H.; Shivakoti, R.; Singh, D.; Singh, G.M.; Singh, J.A.; Singleton, J.; Sleet, D.A.; Sliwa, K.; Smith, E.; Smith, J.L.; Stapelberg, N.J.; Steer, A.; Steiner, T.; Stolk, W.A.; Stovner, L.J.; Sudfeld, C.; Syed, S.; Tamburlini, G.; Tavakkoli, M.; Taylor, H.R.; Taylor, J.A.; Taylor, W.J.; Thomas, B.; Thomson, W.M.; Thurston, G.D.; Tleyjeh, I.M.; Tonelli, M.; Towbin, J.A.; Truelsen, T.; Tsilimbaris, M.K.; Ubeda, C.; Undurraga, E.A.; van der Werf, M.J.; van Os, J.; Vavilala, M.S.; Venketasubramanian, N.; Wang, M.; Wang, W.; Watt, K.; Weatherall, D.J.; Weinstock, M.A.; Weintraub, R.; Weisskopf, M.G.; Weissman, M.M.; White, R.A.; Whiteford, H.; Wiebe, N.; Wiersma, S.T.; Wilkinson, J.D.; Williams, H.C.; Williams, S.R.; Witt, E.; Wolfe, F.; Woolf, A.D.; Wulf, S.; Yeh, P.H.; Zaidi, A.K.; Zheng, Z.J.; Zonies, D.; Lopez, A.D.; AlMazroa, M.A.; Memish, Z.A. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet, 2012, 380(9859), 2197-2223.
[http://dx.doi.org/10.1016/S0140-6736(12)61689-4] [PMID: 23245608]
[9]
Prince, M.; Bryce, R.; Albanese, E.; Wimo, A.; Ribeiro, W.; Ferri, C.P. The global prevalence of dementia: a systematic review and metaanalysis. Alzheimers Dement., 2013, 9(1), 63-75.
[http://dx.doi.org/10.1016/j.jalz.2012.11.007]
[10]
Savitt, J.M.; Dawson, V.L.; Dawson, T.M. Diagnosis and treatment of parkinson disease: molecules to medicine. J. Clin. Invest., 2006, 116(7), 1744-1754.
[http://dx.doi.org/10.1172/JCI29178] [PMID: 16823471]
[11]
[12]
Pringsheim, T.; Jette, N.; Frolkis, A.; Steeves, T.D. The prevalence of parkinson’s disease: a systematic review and meta-analysis. Mov. Disord., 2014, 29(13), 1583-1590.
[http://dx.doi.org/10.1002/mds.25945] [PMID: 24976103]
[13]
Lu, M-F.; Xiao, Z-T.; Zhang, H-Y. Where do health benefits of flavonoids come from? Insights from flavonoid targets and their evolutionary history. Biochem. Biophys. Res. Commun., 2013, 434(4), 701-704.
[http://dx.doi.org/10.1016/j.bbrc.2013.04.035] [PMID: 23624504]
[14]
Pathak, L.; Agrawal, Y.; Dhir, A. Natural polyphenols in the management of major depression. Expert Opin. Investig. Drugs, 2013, 22(7), 863-880.
[http://dx.doi.org/10.1517/13543784.2013.794783] [PMID: 23642183]
[15]
Sharma, S.; Ali, A.; Ali, J.; Sahni, J.K.; Baboota, S. Rutin: therapeutic potential and recent advances in drug delivery. Expert Opin. Investig. Drugs, 2013, 22(8), 1063-1079.
[http://dx.doi.org/10.1517/13543784.2013.805744] [PMID: 23795677]
[16]
Nijveldt, R.J.; van Nood, E.; van Hoorn, D.E.; Boelens, P.G.; van Norren, K.; van Leeuwen, P.A. Flavonoids: a review of probable mechanisms of action and potential applications. Am. J. Clin. Nutr., 2001, 74(4), 418-425.
[http://dx.doi.org/10.1093/ajcn/74.4.418] [PMID: 11566638]
[17]
Dajas, F.; Juan Andres, A-C.; Florencia, A.; Carolina, E.; Felicia, R-M. Neuroprotective actions of flavones and flavonols: mechanisms and relationship to flavonoid structural features. Cent. Nerv. Syst. Agents Med. Chem., 2013, 13(1), 30-35.
[18]
Couch, J.F.; Naghski, J.; Krewson, C.F. Buckwheat as a source of rutin. Science, 1946, 103(2668), 197.
[http://dx.doi.org/10.1126/science.103.2668.197]
[19]
Habtemariam, S. Rutin as a natural therapy for alzheimer’s disease: insights into its mechanisms of action. Curr. Med. Chem., 2016, 23(9), 860-873.
[http://dx.doi.org/10.2174/0929867323666160217124333] [PMID: 26898570]
[20]
Suzuki, T.; Morishita, T.; Kim, S-J.; Park, S-U.; Woo, S-h.; Noda, T.; Takigawa, S. Physiological Roles of Rutin in the Buckwheat Plant. Jpn. Agric. Res. Q., 2015, 49(1), 37-43.
[http://dx.doi.org/10.6090/jarq.49.37]
[21]
Suzuki, T.; Honda, Y.; Mukasa, Y. Effects of UV-B radiation, cold and desiccation stress on rutin concentration and rutin glucosidase activity in tartary buckwheat (Fagopyrum tataricum) leaves. Plant Sci., 2005, 168(5), 1303-1307.
[http://dx.doi.org/10.1016/j.plantsci.2005.01.007]
[22]
Chua, L.S. A review on plant-based rutin extraction methods and its pharmacological activities. J. Ethnopharmacol., 2013, 150(3), 805-817.
[http://dx.doi.org/10.1016/j.jep.2013.10.036] [PMID: 24184193]
[23]
Wang, J.; Zhao, L-L.; Sun, G-X.; Liang, Y.; Wu, F-A.; Chen, Z.; Cui, S. A comparison of acidic and enzymatic hydrolysis of rutin. Afr. J. Biotechnol., 2011, 10(8), 1460-1466.
[24]
You, H.J.; Ahn, H.J.; Ji, G.E. Transformation of rutin to antiproliferative quercetin-3-glucoside by Aspergillus niger. J. Agric. Food Chem., 2010, 58(20), 10886-10892.
[http://dx.doi.org/10.1021/jf102871g] [PMID: 20886886]
[25]
Lukšič, L.; Bonafaccia, G.; Timoracka, M.; Vollmannova, A.; Trček, J.; Nyambe, T.K.; Melini, V.; Acquistucci, R.; Germ, M.; Kreft, I. Rutin and quercetin transformation during preparation of buckwheat sourdough bread. J. Cereal Sci., 2016, 69, 71-76.
[http://dx.doi.org/10.1016/j.jcs.2016.02.011]
[26]
Amaretti, A.; Raimondi, S.; Leonardi, A.; Quartieri, A.; Rossi, M. Hydrolysis of the rutinose-conjugates flavonoids rutin and hesperidin by the gut microbiota and bifido bacteria. Nutrients, 2015, 7(4), 2788-2800.
[http://dx.doi.org/10.3390/nu7042788] [PMID: 25875120]
[27]
Sofic, E.; Copra-Janicijevic, A.; Salihovic, M.; Tahirovic, I.; Kroyer, G. Screening of medicinal plant extracts for quercetin-3-rutinoside (rutin) in Bosnia and Herzegovina. in medicinal plants. Int. J. Phytomed. Relat. Indust., 2010, 2, 97.
[http://dx.doi.org/10.5958/j.0975-4261.2.2.015]
[28]
Fabjan, N.; Rode, J.; Košir, I.J.; Wang, Z.; Zhang, Z.; Kreft, I. Tartary buckwheat (Fagopyrum tataricum Gaertn.) as a source of dietary rutin and quercitrin. J. Agric. Food Chem., 2003, 51(22), 6452-6455.
[http://dx.doi.org/10.1021/jf034543e] [PMID: 14558761]
[29]
Jiang, P.; Burczynski, F.; Campbell, C.; Pierce, G.; Austria, J.; Briggs, C. Rutin and flavonoid contents in three buckwheat species Fagopyrum esculentum, F. tataricum, and F. homotropicum and their protective effects against lipid peroxidation. Food Res. Int., 2007, 40(3), 356-364.
[http://dx.doi.org/10.1016/j.foodres.2006.10.009]
[30]
Kreft, I.; Fabjan, N.; Yasumoto, K. Rutin content in buckwheat (Fagopyrum esculentum Moench) food materials and products. Food Chem., 2006, 98(3), 508-512.
[http://dx.doi.org/10.1016/j.foodchem.2005.05.081]
[31]
Atanassova, M.; Bagdassarian, V. Rutin content in plant products. J. Univ. Chem. Technol. Metall., 2009, 44(2), 201-203.
[32]
Vollmannova, A.; Margitanova, E.; Toth, T.; Timoracka, M.; Urminska, D.; Bojnanska, T.; Cicova, I. Cultivar influence on total polyphenol and rutin contents and total antioxidant capacity in buckwheat, amaranth, and quinoa seeds. Czech J. Food Sci., 2013, 31(6), 589-595.
[http://dx.doi.org/10.17221/452/2012-CJFS]
[33]
Manach, C.; Williamson, G.; Morand, C.; Scalbert, A.; Rémésy, C. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr., 2005, 81(1)(Suppl.), 230S-242S.
[http://dx.doi.org/10.1093/ajcn/81.1.230S] [PMID: 15640486]
[34]
Hollman, P.C. Absorption, bioavailability, and metabolism of flavonoids. Pharm. Biol, 2004, 42(sup1). , 74-83.
[35]
de Oliveira, M.R.; Nabavi, S.M.; Braidy, N.; Setzer, W.N.; Ahmed, T.; Nabavi, S.F. Quercetin and the mitochondria: A mechanistic view. Biotechnol. Adv., 2016, 34(5), 532-549.
[http://dx.doi.org/10.1016/j.biotechadv.2015.12.014] [PMID: 26740171]
[36]
Graefe, E.U.; Wittig, J.; Mueller, S.; Riethling, A.K.; Uehleke, B.; Drewelow, B.; Pforte, H.; Jacobasch, G.; Derendorf, H.; Veit, M. Pharmacokinetics and bioavailability of quercetin glycosides in humans. J. Clin. Pharmacol., 2001, 41(5), 492-499.
[http://dx.doi.org/10.1177/00912700122010366] [PMID: 11361045]
[37]
Gonzales, G.B.; Van Camp, J.; Smagghe, G.; Raes, K.; Mackie, A. Flavonoid–gastrointestinal mucus interaction and its potential role in regulating flavonoid bioavailability and mucosal biophysical properties. Food Res. Int., 2016, 88, 342-347.
[http://dx.doi.org/10.1016/j.foodres.2015.12.023]
[38]
Mascaraque, C.; López-Posadas, R.; Monte, M.J.; Romero-Calvo, I.; Daddaoua, A.; González, M.; Martínez-Plata, E.; Suárez, M.D.; González, R.; Marín, J.J.G. The small intestinal mucosa acts as a rutin reservoir to extend flavonoid anti-inflammatory activity in experimental ileitis and colitis. J. Funct. Foods, 2015, 13, 117-125.
[http://dx.doi.org/10.1016/j.jff.2014.12.041]
[39]
Andlauer, W.; Stumpf, C.; Fürst, P. Intestinal absorption of rutin in free and conjugated forms. Biochem. Pharmacol., 2001, 62(3), 369-374.
[http://dx.doi.org/10.1016/S0006-2952(01)00638-4] [PMID: 11434911]
[40]
Carbonaro, M.; Grant, G. Absorption of quercetin and rutin in rat small intestine. Ann. Nutr. Metab., 2005, 49(3), 178-182.
[http://dx.doi.org/10.1159/000086882] [PMID: 16006787]
[41]
Miyake, K.; Arima, H.; Hirayama, F.; Yamamoto, M.; Horikawa, T.; Sumiyoshi, H.; Noda, S.; Uekama, K. Improvement of solubility and oral bioavailability of rutin by complexation with 2-hydroxypropyl-β-cyclodextrin. Pharm. Dev. Technol., 2000, 5(3), 399-407.
[http://dx.doi.org/10.1081/PDT-100100556] [PMID: 10934740]
[42]
Mauludin, R.; Müller, R.H.; Keck, C.M. Development of an oral rutin nanocrystal formulation. Int. J. Pharm., 2009, 370(1-2), 202-209.
[http://dx.doi.org/10.1016/j.ijpharm.2008.11.029] [PMID: 19114097]
[43]
Hollman, P.C.; de Vries, J.H.; van Leeuwen, S.D.; Mengelers, M.J.; Katan, M.B. Absorption of dietary quercetin glycosides and quercetin in healthy ileostomy volunteers. Am. J. Clin. Nutr., 1995, 62(6), 1276-1282.
[http://dx.doi.org/10.1093/ajcn/62.6.1276] [PMID: 7491892]
[44]
Zhang, M-Q.; Wilkinson, B. Drug discovery beyond the ‘rule-of-five’. Curr. Opin. Biotechnol., 2007, 18(6), 478-488.
[http://dx.doi.org/10.1016/j.copbio.2007.10.005] [PMID: 18035532]
[45]
Masoodi, T.A.; Alhamdanz, A.H. Inhibitory effect of flavonoids on mutant H-Rasp protein. Bioinformation, 2010, 5(1), 11-15.
[http://dx.doi.org/10.6026/97320630005011] [PMID: 21346872]
[46]
Tamura, M.; Nakagawa, H.; Tsushida, T.; Hirayama, K.; Itoh, K. Effect of pectin enhancement on plasma quercetin and fecal flora in rutin-supplemented mice. J. Food Sci., 2007, 72(9), S648-S651.
[http://dx.doi.org/10.1111/j.1750-3841.2007.00557.x] [PMID: 18034749]
[47]
Tenore, G.C.; Campiglia, P.; Ritieni, A.; Novellino, E. In vitro bioaccessibility, bioavailability and plasma protein interaction of polyphenols from Annurca apple (M. pumila Miller cv Annurca). Food Chem., 2013, 141(4), 3519-3524.
[http://dx.doi.org/10.1016/j.foodchem.2013.06.051] [PMID: 23993515]
[48]
Ou-Yang, Z.; Cao, X.; Wei, Y.; Zhang, W-W-Q.; Zhao, M.; Duan, J-a. Pharmacokinetic study of rutin and quercetin in rats after oral administration of total flavones of mulberry leaf extract. Rev. Bras. Farmacogn., 2013, 23(5), 776-782.
[http://dx.doi.org/10.1590/S0102-695X2013000500009]
[49]
Reinboth, M.; Wolffram, S.; Abraham, G.; Ungemach, F.R.; Cermak, R. Oral bioavailability of quercetin from different quercetin glycosides in dogs. Br. J. Nutr., 2010, 104(2), 198-203.
[http://dx.doi.org/10.1017/S000711451000053X] [PMID: 20230651]
[50]
Gohlke, A.; Ingelmann, C.J.; Nürnberg, G.; Starke, A.; Wolffram, S.; Metges, C.C. Bioavailability of quercetin from its aglycone and its glucorhamnoside rutin in lactating dairy cows after intraduodenal administration. J. Dairy Sci., 2013, 96(4), 2303-2313.
[http://dx.doi.org/10.3168/jds.2012-6234] [PMID: 23403185]
[51]
Maciej, J.; Schäff, C.T.; Kanitz, E.; Tuchscherer, A.; Bruckmaier, R.M.; Wolffram, S.; Hammon, H.M. Bioavailability of the flavonol quercetin in neonatal calves after oral administration of quercetin aglycone or rutin. J. Dairy Sci., 2015, 98(6), 3906-3917.
[http://dx.doi.org/10.3168/jds.2015-9361] [PMID: 25795488]
[52]
Kandale, V.V.; Mujawar, S.N.; Welasly, P.J.; Nimbalkar, J.M. Development of integrated database of Neurodegenerative Diseases (IDND) Rev. Res, 2013, 2(9)
[53]
Streissguth, A.P.; O’Malley, K. Neuropsychiatric implications and long-term consequences of fetal alcohol spectrum disorders. Semin. Clin. Neuropsychiatry, 2000, 5, 177-190.
[PMID: 11291013]
[54]
Song, K.; Na, J.Y.; Kim, S.; Kwon, J. Rutin upregulates neurotrophic factors resulting in attenuation of ethanol-induced oxidative stress in HT22 hippocampal neuronal cells. J. Sci. Food Agric., 2015, 95(10), 2117-2123.
[http://dx.doi.org/10.1002/jsfa.6927] [PMID: 25251136]
[55]
Song, K.; Kim, S.; Na, J-Y.; Park, J-H.; Kim, J-K.; Kim, J-H.; Kwon, J. Rutin attenuates ethanol-induced neurotoxicity in hippocampal neuronal cells by increasing aldehyde dehydrogenase 2. Food Chem. Toxicol., 2014, 72, 228-233.
[http://dx.doi.org/10.1016/j.fct.2014.07.028] [PMID: 25084483]
[56]
Pourentezari, M.; Talebi, A.; Abbasi, A.; Khalili, M.A.; Mangoli, E.; Anvari, M.; Anvari, M. Effects of acrylamide on sperm parameters, chromatin quality, and the level of blood testosterone in mice. Iran. J. Reprod. Med., 2014, 12(5), 335-342.
[PMID: 25031578]
[57]
Motamedshariaty, V.S.; Amel Farzad, S.; Nassiri-Asl, M.; Hosseinzadeh, H. Effects of rutin on acrylamide-induced neurotoxicity. Daru, 2014, 22(1), 27.
[http://dx.doi.org/10.1186/2008-2231-22-27] [PMID: 24524427]
[58]
Machawal, L.; Kumar, A. Possible involvement of nitric oxide mechanism in the neuroprotective effect of rutin against immobilization stress induced anxiety like behaviour, oxidative damage in mice. Pharmacol. Rep., 2014, 66(1), 15-21.
[http://dx.doi.org/10.1016/j.pharep.2013.08.001] [PMID: 24905301]
[59]
Reijmer, Y.D.; van den Berg, E.; Ruis, C.; Kappelle, L.J.; Biessels, G.J. Cognitive dysfunction in patients with type 2 diabetes. Diabetes Metab. Res. Rev., 2010, 26(7), 507-519.
[http://dx.doi.org/10.1002/dmrr.1112] [PMID: 20799243]
[60]
Ola, M.S.; Ahmed, M.M.; Ahmad, R.; Abuohashish, H.M.; Al-Rejaie, S.S.; Alhomida, A.S. Neuroprotective effects of rutin in streptozotocin-induced diabetic rat retina. J. Mol. Neurosci., 2015, 56(2), 440-448.
[http://dx.doi.org/10.1007/s12031-015-0561-2] [PMID: 25929832]
[61]
Suganya, S.N.; Sumathi, T. Effect of rutin against a mitochondrial toxin, 3-nitropropionicacid induced biochemical, behavioral and histological alterations-a pilot study on Huntington’s disease model in rats. Metab. Brain Dis., 2017, 32(2), 471-481.
[http://dx.doi.org/10.1007/s11011-016-9929-4] [PMID: 27928694]
[62]
Trachootham, D.; Lu, W.; Ogasawara, M.A.; Nilsa, R.D.; Huang, P. Redox regulation of cell survival. Antioxid. Redox Signal., 2008, 10(8), 1343-1374.
[http://dx.doi.org/10.1089/ars.2007.1957] [PMID: 18522489]
[63]
Dröge, W.; Schipper, H.M. Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell, 2007, 6(3), 361-370.
[http://dx.doi.org/10.1111/j.1474-9726.2007.00294.x] [PMID: 17517043]
[64]
Lee, J.; Giordano, S.; Zhang, J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem. J., 2012, 441(2), 523-540.
[http://dx.doi.org/10.1042/BJ20111451] [PMID: 22187934]
[65]
Rebrin, I.; Kamzalov, S.; Sohal, R.S. Effects of age and caloric restriction on glutathione redox state in mice. Free Radic. Biol. Med., 2003, 35(6), 626-635.
[http://dx.doi.org/10.1016/S0891-5849(03)00388-5] [PMID: 12957655]
[66]
Al-Rejaie, S.S.; Aleisa, A.M.; Sayed-Ahmed, M.M. AL-Shabanah, O.A.; Abuohashish, H.M.; Ahmed, M.M.; Al-Hosaini, K.A.; Hafez, M.M., Protective effect of rutin on the antioxidant genes expression in hypercholestrolemic male Westar rat. BMC Complement. Altern. Med., 2013, 13(1), 1.
[http://dx.doi.org/10.1186/1472-6882-13-136]
[67]
Dirnagl, U.; Iadecola, C.; Moskowitz, M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci., 1999, 22(9), 391-397.
[http://dx.doi.org/10.1016/S0166-2236(99)01401-0] [PMID: 10441299]
[68]
Chan, P.H. Reactive oxygen radicals in signaling and damage in the ischemic brain. J. Cereb. Blood Flow Metab., 2001, 21(1), 2-14.
[http://dx.doi.org/10.1097/00004647-200101000-00002] [PMID: 11149664]
[69]
Graham, S.H.; Chen, J. Programmed cell death in cerebral ischemia. J. Cereb. Blood Flow Metab., 2001, 21(2), 99-109.
[http://dx.doi.org/10.1097/00004647-200102000-00001] [PMID: 11176275]
[70]
Jang, J-W.; Lee, J-K.; Hur, H.; Kim, T-W.; Joo, S-P.; Piao, M-S. Rutin improves functional outcome via reducing the elevated matrix metalloproteinase-9 level in a photothrombotic focal ischemic model of rats. J. Neurol. Sci., 2014, 339(1-2), 75-80.
[http://dx.doi.org/10.1016/j.jns.2014.01.024] [PMID: 24507948]
[71]
Annapurna, A.; Ansari, M.A.; Manjunath, P.M. Partial role of multiple pathways in infarct size limiting effect of quercetin and rutin against cerebral ischemia-reperfusion injury in rats. Eur. Rev. Med. Pharmacol. Sci., 2013, 17(4), 491-500.
[PMID: 23467948]
[72]
Rodrigues, A.M.G. Marcilio, Fdos.S.; Frazão Muzitano, M.; Giraldi-Guimarães, A. Therapeutic potential of treatment with the flavonoid rutin after cortical focal ischemia in rats. Brain Res., 2013, 1503, 53-61.
[http://dx.doi.org/10.1016/j.brainres.2013.01.039] [PMID: 23370003]
[73]
Pu, F.; Mishima, K.; Irie, K.; Motohashi, K.; Tanaka, Y.; Orito, K.; Egawa, T.; Kitamura, Y.; Egashira, N.; Iwasaki, K.; Fujiwara, M. Neuroprotective effects of quercetin and rutin on spatial memory impairment in an 8-arm radial maze task and neuronal death induced by repeated cerebral ischemia in rats. J. Pharmacol. Sci., 2007, 104(4), 329-334.
[http://dx.doi.org/10.1254/jphs.FP0070247] [PMID: 17666865]
[74]
Ahmad, N.; Ahmad, R.; Naqvi, A.A.; Alam, M.A.; Ashafaq, M.; Samim, M.; Iqbal, Z.; Ahmad, F.J. Rutin-encapsulated chitosan nanoparticles targeted to the brain in the treatment of Cerebral Ischemia. Int. J. Biol. Macromol., 2016, 91, 640-655.
[http://dx.doi.org/10.1016/j.ijbiomac.2016.06.001] [PMID: 27264648]
[75]
Nassiri-Asl, M.; Zamansoltani, F.; Javadi, A.; Ganjvar, M. The effects of rutin on a passive avoidance test in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2010, 34(1), 204-207.
[http://dx.doi.org/10.1016/j.pnpbp.2009.11.006] [PMID: 19914327]
[76]
Kumar, A.; Rinwa, P.; Dhar, H. Possible nitric oxide modulation in the protective effects of rutin against experimental head trauma-induced cognitive deficits: behavioral, biochemical, and molecular correlates. J. Surg. Res., 2014, 188(1), 268-279.
[http://dx.doi.org/10.1016/j.jss.2013.12.028] [PMID: 24484907]
[77]
Pyrzanowska, J.; Piechal, A.; Blecharz-Klin, K.; Joniec-Maciejak, I.; Zobel, A.; Widy-Tyszkiewicz, E. Influence of long-term administration of rutin on spatial memory as well as the concentration of brain neurotransmitters in aged rats. Pharmacol. Rep., 2012, 64(4), 808-816.
[http://dx.doi.org/10.1016/S1734-1140(12)70876-9] [PMID: 23087133]
[78]
Zhang, L.; Zhao, Q.; Chen, C-H.; Qin, Q-Z.; Zhou, Z.; Yu, Z-P. Synaptophysin and the dopaminergic system in hippocampus are involved in the protective effect of rutin against trimethyltin-induced learning and memory impairment. Nutr. Neurosci., 2014, 17(5), 222-229.
[http://dx.doi.org/10.1179/1476830513Y.0000000085] [PMID: 24001577]
[79]
Koda, T.; Kuroda, Y.; Imai, H. Protective effect of rutin against spatial memory impairment induced by trimethyltin in rats. Nutr. Res., 2008, 28(9), 629-634.
[http://dx.doi.org/10.1016/j.nutres.2008.06.004] [PMID: 19083469]
[80]
Ramalingayya, G.V.; Nampoothiri, M.; Nayak, P.G.; Kishore, A.; Shenoy, R.R.; Mallikarjuna Rao, C.; Nandakumar, K. Naringin and rutin alleviates episodic memory deficits in two differentially challenged object recognition tasks. Pharmacogn. Mag., 2016, 12(Suppl. 1), S63-S70.
[http://dx.doi.org/10.4103/0973-1296.176104] [PMID: 27041861]
[81]
Richetti, S.K.; Blank, M.; Capiotti, K.M.; Piato, A.L.; Bogo, M.R.; Vianna, M.R.; Bonan, C.D. Quercetin and rutin prevent scopolamine-induced memory impairment in zebrafish. Behav. Brain Res., 2011, 217(1), 10-15.
[http://dx.doi.org/10.1016/j.bbr.2010.09.027] [PMID: 20888863]
[82]
Tongjaroenbuangam, W.; Ruksee, N.; Chantiratikul, P.; Pakdeenarong, N.; Kongbuntad, W.; Govitrapong, P. Neuroprotective effects of quercetin, rutin and okra (Abelmoschus esculentus Linn) in dexamethasone-treated mice. Neurochem. Int., 2011, 59(5), 677-685.
[http://dx.doi.org/10.1016/j.neuint.2011.06.014] [PMID: 21740943]
[83]
Motamedi, G.K.; Meador, K.J. Antiepileptic drugs and memory. Epilepsy Behav., 2004, 5(4), 435-439.
[http://dx.doi.org/10.1016/j.yebeh.2004.03.006] [PMID: 15256178]
[84]
Dubey, S.; Ganeshpurkar, A.; Bansal, D.; Dubey, N. Protective effect of rutin on cognitive impairment caused by phenytoin. Indian J. Pharmacol., 2015, 47(6), 627-631.
[http://dx.doi.org/10.4103/0253-7613.169581] [PMID: 26729954]
[85]
Man, Y-G.; Zhou, R-G.; Zhao, B. Efficacy of rutin in inhibiting neuronal apoptosis and cognitive disturbances in sevoflurane or propofol exposed neonatal mice. Int. J. Clin. Exp. Med., 2015, 8(8), 14397-14409.
[PMID: 26550427]
[86]
Marsh, N.V.; Ludbrook, M.R.; Gaffaney, L.C. Cognitive functioning following traumatic brain injury: A five-year follow-up. NeuroRehabilitation, 2016, 38(1), 71-78.
[http://dx.doi.org/10.3233/NRE-151297] [PMID: 26889800]
[87]
Ramalingayya, G.V.; Cheruku, S.P.; Nayak, P.G.; Kishore, A.; Shenoy, R.; Rao, C.M.; Krishnadas, N. Rutin protects against neuronal damage in vitro and ameliorates doxorubicin-induced memory deficits in vivo in Wistar rats. Drug Des. Devel. Ther., 2017, 11, 1011-1026.
[http://dx.doi.org/10.2147/DDDT.S103511] [PMID: 28408800]
[88]
Babri, S.; Mohaddes, G.; Feizi, I.; Mohammadnia, A.; Niapour, A.; Alihemmati, A.; Amani, M. Effect of troxerutin on synaptic plasticity of hippocampal dentate gyrus neurons in a β-amyloid model of Alzheimer׳s disease: an electrophysiological study. Eur. J. Pharmacol., 2014, 732, 19-25.
[http://dx.doi.org/10.1016/j.ejphar.2014.03.018] [PMID: 24681055]
[89]
Choi, J.Y.; Lee, J.M.; Lee, D.G.; Cho, S.; Yoon, Y-H.; Cho, E.J.; Lee, S. The n-butanol fraction and rutin from tartary buckwheat improve cognition and memory in an in vivo model of amyloid-β-induced Alzheimer’s disease. J. Med. Food, 2015, 18(6), 631-641.
[http://dx.doi.org/10.1089/jmf.2014.3292] [PMID: 25785882]
[90]
Xie, Z.; Tanzi, R.E. Alzheimer’s disease and post-operative cognitive dysfunction. Exp. Gerontol., 2006, 41(4), 346-359.
[http://dx.doi.org/10.1016/j.exger.2006.01.014] [PMID: 16564662]
[91]
Li, R-S.; Wang, X-B.; Hu, X-J.; Kong, L-Y. Design, synthesis and evaluation of flavonoid derivatives as potential multifunctional acetylcholinesterase inhibitors against Alzheimer’s disease. Bioorg. Med. Chem. Lett., 2013, 23(9), 2636-2641.
[http://dx.doi.org/10.1016/j.bmcl.2013.02.095] [PMID: 23511019]
[92]
Braidy, N.; Jugder, B-E.; Poljak, A.; Jayasena, T.; Mansour, H.; Nabavi, S.M.; Sachdev, P.; Grant, R. Resveratrol as a potential therapeutic candidate for the treatment and management of alzheimer’s disease. Curr. Top. Med. Chem., 2016, 16(17), 1951-1960.
[http://dx.doi.org/10.2174/1568026616666160204121431] [PMID: 26845555]
[93]
Kumar, A.; Dogra, S.; Prakash, A. Protective effect of naringin, a citrus flavonoid, against colchicine-induced cognitive dysfunction and oxidative damage in rats. J. Med. Food, 2010, 13(4), 976-984.
[http://dx.doi.org/10.1089/jmf.2009.1251] [PMID: 20673063]
[94]
Spencer, J.P. The interactions of flavonoids within neuronal signalling pathways. Genes Nutr., 2007, 2(3), 257-273.
[http://dx.doi.org/10.1007/s12263-007-0056-z] [PMID: 18850181]
[95]
Wang, S.W.; Wang, Y-J.; Su, Y.J.; Zhou, W.W.; Yang, S.G.; Zhang, R.; Zhao, M.; Li, Y.N.; Zhang, Z.P.; Zhan, D.W.; Liu, R.T. Rutin inhibits β-amyloid aggregation and cytotoxicity, attenuates oxidative stress, and decreases the production of nitric oxide and proinflammatory cytokines. Neurotoxicology, 2012, 33(3), 482-490.
[http://dx.doi.org/10.1016/j.neuro.2012.03.003] [PMID: 22445961]
[96]
Javed, H.; Khan, M.M.; Ahmad, A.; Vaibhav, K.; Ahmad, M.E.; Khan, A.; Ashafaq, M.; Islam, F.; Siddiqui, M.S.; Safhi, M.M.; Islam, F. Rutin prevents cognitive impairments by ameliorating oxidative stress and neuroinflammation in rat model of sporadic dementia of Alzheimer type. Neuroscience, 2012, 210, 340-352.
[http://dx.doi.org/10.1016/j.neuroscience.2012.02.046] [PMID: 22441036]
[97]
Moghbelinejad, S.; Nassiri-Asl, M.; Farivar, T.N.; Abbasi, E.; Sheikhi, M.; Taghiloo, M.; Farsad, F.; Samimi, A.; Hajiali, F. Rutin activates the MAPK pathway and BDNF gene expression on beta-amyloid induced neurotoxicity in rats. Toxicol. Lett., 2014, 224(1), 108-113.
[http://dx.doi.org/10.1016/j.toxlet.2013.10.010] [PMID: 24148604]
[98]
Xu, P.X.; Wang, S.W.; Yu, X.L.; Su, Y.J.; Wang, T.; Zhou, W.W.; Zhang, H.; Wang, Y.J.; Liu, R.T. Rutin improves spatial memory in Alzheimer’s disease transgenic mice by reducing Aβ oligomer level and attenuating oxidative stress and neuroinflammation. Behav. Brain Res., 2014, 264, 173-180.
[http://dx.doi.org/10.1016/j.bbr.2014.02.002] [PMID: 24512768]
[99]
Yu, X-L.; Li, Y-N.; Zhang, H.; Su, Y-J.; Zhou, W-W.; Zhang, Z-P.; Wang, S-W.; Xu, P-X.; Wang, Y-J.; Liu, R-T. Rutin inhibits amylin-induced neurocytotoxicity and oxidative stress. Food Funct., 2015, 6(10), 3296-3306.
[http://dx.doi.org/10.1039/C5FO00500K] [PMID: 26242245]
[100]
Khan, M.M.; Raza, S.S.; Javed, H.; Ahmad, A.; Khan, A.; Islam, F.; Safhi, M.M.; Islam, F. Rutin protects dopaminergic neurons from oxidative stress in an animal model of Parkinson’s disease. Neurotox. Res., 2012, 22(1), 1-15.
[http://dx.doi.org/10.1007/s12640-011-9295-2] [PMID: 22194158]
[101]
Park, S-E.; Sapkota, K.; Choi, J-H.; Kim, M-K.; Kim, Y.H.; Kim, K.M.; Kim, K.J.; Oh, H-N.; Kim, S-J.; Kim, S. Rutin from Dendropanax morbifera Leveille protects human dopaminergic cells against rotenone induced cell injury through inhibiting JNK and p38 MAPK signaling. Neurochem. Res., 2014, 39(4), 707-718.
[http://dx.doi.org/10.1007/s11064-014-1259-5] [PMID: 24549762]
[102]
Magalingam, K.B.; Radhakrishnan, A.; Ramdas, P.; Haleagrahara, N. Quercetin glycosides induced neuroprotection by changes in the gene expression in a cellular model of Parkinson’s disease. J. Mol. Neurosci., 2015, 55(3), 609-617.
[http://dx.doi.org/10.1007/s12031-014-0400-x] [PMID: 25129099]
[103]
Magalingam, K.B.; Radhakrishnan, A.; Haleagrahara, N. Protective effects of quercetin glycosides, rutin, and isoquercetrin against 6-hydroxydopamine (6-OHDA)-induced neurotoxicity in rat pheochromocytoma (PC-12) cells. Int. J. Immunopathol. Pharmacol., 2016, 29(1), 30-39.
[http://dx.doi.org/10.1177/0394632015613039] [PMID: 26542606]


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