Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Sulfur-containing Secondary Metabolites as Neuroprotective Agents

Author(s): Alessandro Venditti* and Armandodoriano Bianco

Volume 27, Issue 26, 2020

Page: [4421 - 4436] Pages: 16

DOI: 10.2174/0929867325666180912105036

Price: $65

Abstract

Sulfur-containing secondary metabolites are a relatively small group of substances of plant origin. The present review is focused on their neuroprotective properties. The results obtained in a series of in vitro and in vivo studies are reported. Among glucosinolates, the wide class of compounds in the sulfur-containing metabolites, glucoraphanin, sulforaphane and isothiocyanates proved to be the more studied in this context and showed interesting properties as modulators of several systems involved in the pathogenesis of neurologic diseases such as oxidative stress, inflammation and apoptosis. Allium sativum L. (garlic) is widely known for its sulfur-containing components endowed with health-promoting activities and its medicinal properties are known from ancient times. In recent studies, garlic components proved active in neuroprotection due to the direct and indirect antioxidant properties, modulation of apoptosis mediators and inhibiting the formation of amyloid protein. Dihydroasparagusic acid, the first dimercaptanic compound isolated from a natural source, effectively inhibited inflammatory and oxidative processes that are important factors for the etiopathogenesis of neurodegenerative diseases, not only for its antioxidant and radical scavenging properties but also because it may down-regulate the expression of several microglial-derived inflammatory mediators. Serofendic acid represents a rare case of sulfur-containing animal-derived secondary metabolite isolated from fetal calf serum extract. It proved effective in the suppression of ROS generation and in the expression of several inflammatory and apoptosis mediators and showed a cytotrophic property in astrocytes, promoting the stellation process. Lastly, the properties of hydrogen sulfide were also reported since in recent times it has been recognized as a signaling molecule and as a mediator in regulating neuron death or survival. It may be produced endogenously from cysteine but may also be released by sulfur-containing secondary metabolites, mainly from those present in garlic.

Keywords: Sulfur-containing secondary metabolites, glucosinolates, dihydroasparagusic acid, serofendic acid, garlic, hydrogen sulfide, neuroprotection.

« Previous
[1]
Fahey, J.W.; Zalcmann, A.T.; Talalay, P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 2001, 56(1), 5-51.
[http://dx.doi.org/10.1016/S0031-9422(00)00316-2] [PMID: 11198818]
[2]
Cartea, M.E.; Velasco, P. Glucosinolates in Brassica foods: Bioavailability in food and significance for human health. Phytochem. Rev., 2008, 7(2), 213-229.
[http://dx.doi.org/10.1007/s11101-007-9072-2]
[3]
Heaney, R.K.; Fenwick, G.R. Natural toxins and protective factors in brassica species, including rapeseed. Nat. Toxins, 1995, 3(4), 233-237.
[http://dx.doi.org/10.1002/nt.2620030412] [PMID: 7582622]
[4]
McMillan, M.; Spinks, E.A.; Fenwick, G.R. Preliminary observations on the effect of dietary brussels sprouts on thyroid function. Hum. Toxicol., 1986, 5(1), 15-19.
[http://dx.doi.org/10.1177/096032718600500104] [PMID: 2419242]
[5]
Shapiro, T.A.; Fahey, J.W.; Dinkova-Kostova, A.T.; Holtzclaw, W.D.; Stephenson, K.K.; Wade, K.L.; Ye, L.; Talalay, P. Safety, tolerance, and metabolism of broccoli sprout glucosinolates and isothiocyanates: a clinical phase I study. Nutr. Cancer, 2006, 55(1), 53-62.
[http://dx.doi.org/10.1207/s15327914nc5501_7] [PMID: 16965241]
[6]
Jeffery, E.H.; Araya, M. Physiological effects of broccoli consumption. Phytochem. Rev., 2009, 8(1), 283-298.
[http://dx.doi.org/10.1007/s11101-008-9106-4]
[7]
Johnson, I.T. Glucosinolates in the human diet. Bioavailability and implications for health. Phytochem. Rev., 2002, 1(2), 183-188.
[http://dx.doi.org/10.1023/A:1022507300374]
[8]
Traka, M.; Mithen, R. Glucosinolates, isothiocyanates and human health. Phytochem. Rev., 2009, 8(1), 269-282.
[http://dx.doi.org/10.1007/s11101-008-9103-7]
[9]
López Salon, M.; Morelli, L.; Castaño, E.M.; Soto, E.F.; Pasquini, J.M. Defective ubiquitination of cerebral proteins in Alzheimer’s disease. J. Neurosci. Res., 2000, 62(2), 302-310.
[http://dx.doi.org/10.1002/1097-4547(20001015)62:2<302::AID-JNR15>3.0.CO;2-L] [PMID: 11020223]
[10]
Hoozemans, J.J.M.; Veerhuis, R.; Van Haastert, E.S.; Rozemuller, J.M.; Baas, F.; Eikelenboom, P.; Scheper, W. The unfolded protein response is activated in Alzheimer’s disease. Acta Neuropathol., 2005, 110(2), 165-172.
[http://dx.doi.org/10.1007/s00401-005-1038-0] [PMID: 15973543]
[11]
Behl, C. Alzheimer’s disease and oxidative stress: implications for novel therapeutic approaches. Prog. Neurobiol., 1999, 57(3), 301-323.
[http://dx.doi.org/10.1016/S0301-0082(98)00055-0] [PMID: 10096843]
[12]
Salminen, A.; Ojala, J.; Kauppinen, A.; Kaarniranta, K.; Suuronen, T. Inflammation in Alzheimer’s disease: amyloid-beta oligomers trigger innate immunity defence via pattern recognition receptors. Prog. Neurobiol., 2009, 87(3), 181-194.
[http://dx.doi.org/10.1016/j.pneurobio.2009.01.001] [PMID: 19388207]
[13]
Shamim, A.; Mahmood, T.; Ahsan, F.; Kumar, A.; Bagga, P. Lipids: An insight into the neurodegenerative disorders. Clin Nutr Exp, 2018, 20, 1-19.
[http://dx.doi.org/10.1016/j.yclnex.2018.05.001]
[14]
Gosselet, F.; Candela, P.; Cecchelli, R.; Fenart, L. [Role of the blood-brain barrier in Alzheimer’s disease]. Med. Sci. (Paris), 2011, 27(11), 987-992.
[http://dx.doi.org/10.1051/medsci/20112711015] [PMID: 22130026]
[15]
Erickson, M.A.; Banks, W.A. Blood-brain barrier dysfunction as a cause and consequence of Alzheimer’s disease. J. Cereb. Blood Flow Metab., 2013, 33(10), 1500-1513.
[http://dx.doi.org/10.1038/jcbfm.2013.135] [PMID: 23921899]
[16]
Millucci, L.; Ghezzi, L.; Bernardini, G.; Santucci, A. Conformations and biological activities of amyloid beta peptide 25-35. Curr. Protein Pept. Sci., 2010, 11(1), 54-67.
[http://dx.doi.org/10.2174/138920310790274626] [PMID: 20201807]
[17]
Cárdenas-Aguayo, M.D.C.; Silva-Lucero, M.D.C.; Cortes-Ortiz, M.; Jiménez-Ramos, B.; Gómez-Virgilio, L.; Ramírez-Rodríguez, G. Meraz-Ríos, M.A.). Physiological role of amyloid beta in neural cells: the cellular trophic activity.Neurochemistry; InTech, 2014.
[http://dx.doi.org/10.5772/57398]
[18]
Takeshita, Y.; Kanda, T. The Blood-Brain Barrier (BBB) and in vitro BBB Models. Brain nerve, 2015, 67(8), 1035-1042.
[http://dx.doi.org/10.11477/mf.1416200250] [PMID: 21705306]
[19]
Sherman, M.Y.; Goldberg, A.L. Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron, 2001, 29(1), 15-32.
[http://dx.doi.org/10.1016/S0896-6273(01)00177-5] [PMID: 11182078]
[20]
Park, H-M.; Kim, J-A.; Kwak, M-K. Protection against amyloid beta cytotoxicity by sulforaphane: role of the proteasome. Arch. Pharm. Res., 2009, 32(1), 109-115.
[http://dx.doi.org/10.1007/s12272-009-1124-2] [PMID: 19183883]
[21]
Gan, N.; Wu, Y.C.; Brunet, M.; Garrido, C.; Chung, F.L.; Dai, C.; Mi, L. Sulforaphane activates heat shock response and enhances proteasome activity through up-regulation of Hsp27. J. Biol. Chem., 2010, 285(46), 35528-35536.
[http://dx.doi.org/10.1074/jbc.M110.152686] [PMID: 20833711]
[22]
Kim, H.V.; Kim, H.Y.; Ehrlich, H.Y.; Choi, S.Y.; Kim, D.J.; Kim, Y. Amelioration of Alzheimer’s disease by neuroprotective effect of sulforaphane in animal model. Amyloid, 2013, 20(1), 7-12.
[http://dx.doi.org/10.3109/13506129.2012.751367] [PMID: 23253046]
[23]
Kim, J.K.; Shin, E-C.; Kim, C.R.; Park, G.G.; Choi, S.J.; Park, C-S.; Shin, D.H. Effects of brussels sprouts and their phytochemical components on oxidative stress-induced neuronal damages in PC12 cells and ICR mice. J. Med. Food, 2013, 16(11), 1057-1061.
[http://dx.doi.org/10.1089/jmf.2012.0280] [PMID: 24175656]
[24]
Ganguly, R.; Ray, K.; Guha, D. Effect of Moringa oleifera in experimental model of Alzheimer’s disease: role of antioxidants. Ann. Neurosci., 2005, 12, 36-39.
[http://dx.doi.org/10.5214/ans.0972.7531.2005.120301]
[25]
Ganguly, R.; Guha, D. Alteration of brain monoamines & EEG wave pattern in rat model of Alzheimer’s disease & protection by Moringa oleifera. Indian J. Med. Res., 2008, 128(6), 744-751.
[PMID: 19246799]
[26]
Yang, T.; Liu, Y.Q.; Wang, C.H.; Wang, Z.T. Advances on investigation of chemical constituents, pharmacological activities and clinical applications of Capparis spinosa China J. Chin. Materia Medica, 2008, 33, 2453-2458.
[27]
Spillantini, M.G.; Schmidt, M.L.; Lee, V.M.; Trojanowski, J.Q.; Jakes, R.; Goedert, M. α-synuclein in Lewy bodies. Nature, 1997, 388(6645), 839-840.
[http://dx.doi.org/10.1038/42166] [PMID: 9278044]
[28]
Polymeropoulos, M.H.; Lavedan, C.; Leroy, E.; Ide, S.E.; Dehejia, A.; Dutra, A.; Pike, B.; Root, H.; Rubenstein, J.; Boyer, R.; Stenroos, E.S.; Chandrasekharappa, S.; Athanassiadou, A.; Papapetropoulos, T.; Johnson, W.G.; Lazzarini, A.M.; Duvoisin, R.C.; Di Iorio, G.; Golbe, L.I.; Nussbaum, R.L. Mutation in the α-synuclein gene identified in families with Parkinson’s disease. Science,, 1997, 276(5321), 2045-2047.
[http://dx.doi.org/10.1126/science.276.5321.2045]
[29]
Krüger, R.; Kuhn, W.; Müller, T.; Woitalla, D.; Graeber, M.; Kösel, S.; Przuntek, H.; Epplen, J.T.; Schöls, L.; Riess, O. Ala30Pro mutation in the gene encoding α-synuclein in Parkinson’s disease. Nat. Genet., 1998, 18(2), 106-108.
[http://dx.doi.org/10.1038/ng0298-106] [PMID: 9462735]
[30]
Zarranz, J.J.; Alegre, J.; Gómez-Esteban, J.C.; Lezcano, E.; Ros, R.; Ampuero, I.; Vidal, L.; Hoenicka, J.; Rodriguez, O.; Atarés, B.; Llorens, V.; Gomez Tortosa, E.; del Ser, T.; Muñoz, D.G.; de Yebenes, J.G. The new mutation, E46K, of α-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol., 2004, 55(2), 164-173.
[http://dx.doi.org/10.1002/ana.10795] [PMID: 14755719]
[31]
Cuervo, A.M.; Stefanis, L.; Fredenburg, R.; Lansbury, P.T.; Sulzer, D. Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy. Science, 2004, 305(5688), 1292-1295.
[http://dx.doi.org/10.1126/science.1101738] [PMID: 15333840]
[32]
Dawson, T.M.; Dawson, V.L. Molecular pathways of neurodegeneration in Parkinson’s disease. Science, 2003, 302(5646), 819-822.
[http://dx.doi.org/10.1126/science.1087753] [PMID: 14593166]
[33]
Dinkova-Kostova, A.T.; Kostov, R.V. Glucosinolates and isothiocyanates in health and disease. Trends Mol. Med., 2012, 18(6), 337-347.
[http://dx.doi.org/10.1016/j.molmed.2012.04.003] [PMID: 22578879]
[34]
Tarozzi, A.; Angeloni, C.; Malaguti, M.; Morroni, F.; Hrelia, S.; Hrelia, P. Sulforaphane as a potential protective phytochemical against neurodegenerative diseases. Oxid. Med. Cell. Longev., 2013, 2013, 415078
[http://dx.doi.org/10.1155/2013/415078] [PMID: 23983898]
[35]
Jazwa, A.; Rojo, A.I.; Innamorato, N.G.; Hesse, M.; Fernández-Ruiz, J.; Cuadrado, A. Pharmacological targeting of the transcription factor Nrf2 at the basal ganglia provides disease modifying therapy for experimental parkinsonism. Antioxid. Redox Signal., 2011, 14(12), 2347-2360.
[http://dx.doi.org/10.1089/ars.2010.3731] [PMID: 21254817]
[36]
Deng, C.; Tao, R.; Yu, S.Z.; Jin, H. Inhibition of 6-hydroxydopamine-induced endoplasmic reticulum stress by sulforaphane through the activation of Nrf2 nuclear translocation. Mol. Med. Rep., 2012, 6(1), 215-219.
[http://dx.doi.org/10.3892/mmr.2012.894] [PMID: 22552270]
[37]
Deng, C.; Tao, R.; Yu, S.Z.; Jin, H. Sulforaphane protects against 6-hydroxydopamine-induced cytotoxicity by increasing expression of heme oxygenase-1 in a PI3K/Akt-dependent manner. Mol. Med. Rep., 2012, 5(3), 847-851.
[http://dx.doi.org/10.3892/mmr.2011.731] [PMID: 22200816]
[38]
Tarozzi, A.; Morroni, F.; Merlicco, A.; Hrelia, S.; Angeloni, C.; Cantelli-Forti, G.; Hrelia, P. Sulforaphane as an inducer of glutathione prevents oxidative stress-induced cell death in a dopaminergic-like neuroblastoma cell line. J. Neurochem., 2009, 111(5), 1161-1171.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06394.x] [PMID: 19780897]
[39]
Morroni, F.; Tarozzi, A.; Sita, G.; Bolondi, C.; Zolezzi Moraga, J.M.; Cantelli-Forti, G.; Hrelia, P. Neuroprotective effect of sulforaphane in 6-hydroxydopamine-lesioned mouse model of Parkinson’s disease. Neurotoxicology, 2013, 36, 63-71.
[http://dx.doi.org/10.1016/j.neuro.2013.03.004] [PMID: 23518299]
[40]
Ross, C.A.; Tabrizi, S.J. Huntington’s disease: from molecular pathogenesis to clinical treatment. Lancet Neurol., 2011, 10(1), 83-98.
[http://dx.doi.org/10.1016/S1474-4422(10)70245-3] [PMID: 21163446]
[41]
Kwak, M-K.; Cho, J-M.; Huang, B.; Shin, S.; Kensler, T.W. Role of increased expression of the proteasome in the protective effects of sulforaphane against hydrogen peroxide-mediated cytotoxicity in murine neuroblastoma cells. Free Radic. Biol. Med., 2007, 43(5), 809-817.
[http://dx.doi.org/10.1016/j.freeradbiomed.2007.05.029] [PMID: 17664144]
[42]
Liu, Y.; Hettinger, C.L.; Zhang, D.; Rezvani, K.; Wang, X.; Wang, H. Sulforaphane enhances proteasomal and autophagic activities in mice and is a potential therapeutic reagent for Huntington’s disease. J. Neurochem., 2014, 129(3), 539-547.
[http://dx.doi.org/10.1111/jnc.12647] [PMID: 24383989]
[43]
Noseworthy, J.H.; Lucchinetti, C.; Rodriguez, M.; Weinshenker, B.G. Multiple sclerosis. N. Engl. J. Med., 2000, 343(13), 938-952.
[http://dx.doi.org/10.1056/NEJM200009283431307] [PMID: 11006371]
[44]
Lassmann, H. Multiple sclerosis pathology: evolution of pathogenetic concepts. Brain Pathol., 2005, 15(3), 217-222.
[http://dx.doi.org/10.1111/j.1750-3639.2005.tb00523.x] [PMID: 16196388]
[45]
Brownell, B.; Hughes, J.T. The distribution of plaques in the cerebrum in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry, 1962, 25, 315-320.
[http://dx.doi.org/10.1136/jnnp.25.4.315] [PMID: 14016083]
[46]
Bø, L.; Vedeler, C.A.; Nyland, H.; Trapp, B.D.; Mørk, S.J. Intracortical multiple sclerosis lesions are not associated with increased lymphocyte infiltration. Mult. Scler., 2003, 9(4), 323-331.
[http://dx.doi.org/10.1191/1352458503ms917oa] [PMID: 12926836]
[47]
Kutzelnigg, A.; Lucchinetti, C.F.; Stadelmann, C.; Brück, W.; Rauschka, H.; Bergmann, M.; Schmidbauer, M.; Parisi, J.E.; Lassmann, H. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain, 2005, 128(Pt 11), 2705-2712.
[http://dx.doi.org/10.1093/brain/awh641] [PMID: 16230320]
[48]
Giacoppo, S.; Galuppo, M.; Iori, R.; De Nicola, G.R.; Cassata, G.; Bramanti, P.; Mazzon, E. Protective role of (RS )-glucoraphanin bioactivated with myrosinase in an experimental model of multiple sclerosis. CNS Neurosci. Ther., 2013, 19(8), 577-584.
[http://dx.doi.org/10.1111/cns.12106] [PMID: 23638842]
[49]
Giacoppo, S.; Galuppo, M.; Iori, R.; De Nicola, G.R.; Bramanti, P.; Mazzon, E. The protective effects of bioactive (RS)-glucoraphanin on the permeability of the mice blood-brain barrier following experimental autoimmune encephalomyelitis. Eur. Rev. Med. Pharmacol. Sci., 2014, 18(2), 194-204.
[PMID: 24488908]
[50]
Gaetz, M. The neurophysiology of brain injury. Clin. Neurophysiol,, 2004, 115(1), 4-18.
[http://dx.doi.org/10.1016/S1388-2457(03)00258-X]
[51]
Bramlett, H.M.; Dietrich, W.D. Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Prog. Brain Res., 2007, 161, 125-141.
[http://dx.doi.org/10.1016/S0079-6123(06)61009-1] [PMID: 17618974]
[52]
Maas, A.I.; Stocchetti, N.; Bullock, R. Moderate and severe traumatic brain injury in adults. The Lancet Neurology, 2008, 7(8), 728-741.
[http://dx.doi.org/10.1016/S1474-4422(08)70164-9]
[53]
Masel, B.E.; DeWitt, D.S. Traumatic brain injury: a disease process, not an event. Journal of Neurotrauma, 2010, 27(8), 1529-1540.
[http://dx.doi.org/10.1089/neu.2010.1358]
[54]
Woodcock, T.; Morganti-Kossmann, M.C. The role of markers of inflammation in traumatic brain injury. Front. Neurol., 2013, 4, 18.
[http://dx.doi.org/10.3389/fneur.2013.00018] [PMID: 23459929]
[55]
Galuppo, M.; Giacoppo, S.; De Nicola, G.R.; Iori, R.; Mazzon, E.; Bramanti, P. RS-Glucoraphanin bioactivated with myrosinase treatment counteracts proinflammatory cascade and apoptosis associated to spinal cord injury in an experimental mouse model. J. Neurol. Sci., 2013, 334(1-2), 88-96.
[http://dx.doi.org/10.1016/j.jns.2013.07.2514] [PMID: 23992921]
[56]
Mao, L.; Wang, H.; Wang, X.; Liao, H.; Zhao, X. Transcription factor Nrf2 protects the spinal cord from inflammation produced by spinal cord injury. J. Surg. Res., 2011, 170(1), e105-e115.
[http://dx.doi.org/10.1016/j.jss.2011.05.049] [PMID: 21764072]
[57]
Wang, X.; de Rivero Vaccari, J.P.; Wang, H.; Diaz, P.; German, R.; Marcillo, A.E.; Keane, R.W. Activation of the nuclear factor E2-related factor 2/antioxidant response element pathway is neuroprotective after spinal cord injury. J. Neurotrauma, 2012, 29(5), 936-945.
[http://dx.doi.org/10.1089/neu.2011.1922] [PMID: 21806470]
[58]
Zhao, X.; Sun, G.; Zhang, J.; Strong, R.; Dash, P.K.; Kan, Y.W.; Grotta, J.C.; Aronowski, J. Transcription factor Nrf2 protects the brain from damage produced by intracerebral hemorrhage. Stroke, 2007, 38(12), 3280-3286.
[http://dx.doi.org/10.1161/STROKEAHA.107.486506] [PMID: 17962605]
[59]
Zhao, X.; Song, S.; Sun, G.; Strong, R.; Zhang, J.; Grotta, J.C.; Aronowski, J. Neuroprotective role of haptoglobin after intracerebral hemorrhage. J. Neurosci., 2009, 29(50), 15819-15827.
[http://dx.doi.org/10.1523/JNEUROSCI.3776-09.2009] [PMID: 20016097]
[60]
Chen, G.; Fang, Q.; Zhang, J.; Zhou, D.; Wang, Z. Role of the Nrf2-ARE pathway in early brain injury after experimental subarachnoid hemorrhage. J. Neurosci. Res., 2011, 89(4), 515-523.
[http://dx.doi.org/10.1002/jnr.22577] [PMID: 21259333]
[61]
Kim, D.; You, B.; Jo, E.K.; Han, S.K.; Simon, M.I.; Lee, S.J. NADPH oxidase 2-derived reactive oxygen species in spinal cord microglia contribute to peripheral nerve injury-induced neuropathic pain. Proc. Natl. Acad. Sci. USA, 2010, 107(33), 14851-14856.
[62]
Innamorato, N.G.; Rojo, A.I.; García-Yagüe, A.J.; Yamamoto, M.; de Ceballos, M.L.; Cuadrado, A. The transcription factor Nrf2 is a therapeutic target against brain inflammation. J. Immunol., 2008, 181(1), 680-689.
[http://dx.doi.org/10.4049/jimmunol.181.1.680] [PMID: 18566435]
[63]
Noyan-Ashraf, M.H.; Sadeghinejad, Z.; Juurlink, B.H. Dietary approach to decrease aging-related CNS inflammation. Nutr. Neurosci., 2005, 8(2), 101-110.
[http://dx.doi.org/10.1080/10284150500069470] [PMID: 16053242]
[64]
Giacoppo, S.; Galuppo, M.; Iori, R.; De Nicola, G.R.; Bramanti, P.; Mazzon, E. (RS)-glucoraphanin purified from Tuscan black kale and bioactivated with myrosinase enzyme protects against cerebral ischemia/reperfusion injury in rats. Fitoterapia, 2014, 99, 166-177.
[http://dx.doi.org/10.1016/j.fitote.2014.09.016] [PMID: 25281776]
[65]
Soane, L.; Li Dai, W.; Fiskum, G.; Bambrick, L.L. Sulforaphane protects immature hippocampal neurons against death caused by exposure to hemin or to oxygen and glucose deprivation. J. Neurosci. Res., 2010, 88(6), 1355-1363.
[PMID: 19998483]
[66]
Danilov, C.A.; Chandrasekaran, K.; Racz, J.; Soane, L.; Zielke, C.; Fiskum, G. Sulforaphane protects astrocytes against oxidative stress and delayed death caused by oxygen and glucose deprivation. Glia, 2009, 57(6), 645-656.
[http://dx.doi.org/10.1002/glia.20793] [PMID: 18942756]
[67]
Ping, Z.; Liu, W.; Kang, Z.; Cai, J.; Wang, Q.; Cheng, N.; Wang, S.; Wang, S.; Zhang, J.H.; Sun, X. Sulforaphane protects brains against hypoxic-ischemic injury through induction of Nrf2-dependent phase 2 enzyme. Brain Res., 2010, 1343(1343), 178-185.
[http://dx.doi.org/10.1016/j.brainres.2010.04.036] [PMID: 20417626]
[68]
Li, L.; Rose, P.; Moore, P.K. Hydrogen sulfide and cell signaling. Annu. Rev. Pharmacol. Toxicol., 2011, 51, 169-187.
[http://dx.doi.org/10.1146/annurev-pharmtox-010510-100505] [PMID: 21210746]
[69]
Goodwin, L.R.; Francom, D.; Dieken, F.P.; Taylor, J.D.; Warenycia, M.W.; Reiffenstein, R.J.; Dowling, G. Determination of sulfide in brain tissue by gas dialysis/ion chromatography: postmortem studies and two case reports. J. Anal. Toxicol., 1989, 13(2), 105-109.
[http://dx.doi.org/10.1093/jat/13.2.105] [PMID: 2733387]
[70]
Savage, J.C.; Gould, D.H. Determination of sulfide in brain tissue and rumen fluid by ion-interaction reversed-phase high-performance liquid chromatography. J. Chromatogr. A, 1990, 526(2), 540-545.
[http://dx.doi.org/10.1016/S0378-4347(00)82537-2] [PMID: 2361993]
[71]
Warenycia, M.W.; Goodwin, L.R.; Benishin, C.G.; Reiffenstein, R.J.; Francom, D.M.; Taylor, J.D.; Dieken, F.P. Acute hydrogen sulfide poisoning. Demonstration of selective uptake of sulfide by the brainstem by measurement of brain sulfide levels. Biochem. Pharmacol., 1989, 38(6), 973-981.
[http://dx.doi.org/10.1016/0006-2952(89)90288-8] [PMID: 2930598]
[72]
Abe, K.; Kimura, H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci., 1996, 16(3), 1066-1071.
[http://dx.doi.org/10.1523/JNEUROSCI.16-03-01066.1996] [PMID: 8558235]
[73]
Hosoki, R.; Matsuki, N.; Kimura, H. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem. Biophys. Res. Commun., 1997, 237(3), 527-531.
[http://dx.doi.org/10.1006/bbrc.1997.6878] [PMID: 9299397]
[74]
Shibuya, N.; Tanaka, M.; Yoshida, M.; Ogasawara, Y.; Togawa, T.; Ishii, K.; Kimura, H. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid. Redox Signal., 2009, 11(4), 703-714.
[http://dx.doi.org/10.1089/ars.2008.2253] [PMID: 18855522]
[75]
Benavides, G.A.; Squadrito, G.L.; Mills, R.W.; Patel, H.D.; Isbell, T.S.; Patel, R.P.; Darley-Usmar, V.M.; Doeller, J.E.; Kraus, D.W. Hydrogen sulfide mediates the vasoactivity of garlic. Proc. Natl. Acad. Sci. USA, 2007, 104(46), 17977-17982.
[http://dx.doi.org/10.1073/pnas.0705710104] [PMID: 17951430]
[76]
Nagai, Y.; Tsugane, M.; Oka, J.; Kimura, H. Hydrogen sulfide induces calcium waves in astrocytes. FASEB J., 2004, 18(3), 557-559.
[http://dx.doi.org/10.1096/fj.03-1052fje] [PMID: 14734631]
[77]
Kimura, Y.; Kimura, H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J., 2004, 18(10), 1165-1167.
[http://dx.doi.org/10.1096/fj.04-1815fje] [PMID: 15155563]
[78]
Kimura, Y.; Goto, Y.; Kimura, H. Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid. Redox Signal., 2010, 12(1), 1-13.
[http://dx.doi.org/10.1089/ars.2008.2282] [PMID: 19852698]
[79]
Kimura, Y.; Dargusch, R.; Schubert, D.; Kimura, H. Hydrogen sulfide protects HT22 neuronal cells from oxidative stress. Antioxid. Redox Signal., 2006, 8(3-4), 661-670.
[http://dx.doi.org/10.1089/ars.2006.8.661] [PMID: 16677109]
[80]
Eto, K.; Asada, T.; Arima, K.; Makifuchi, T.; Kimura, H. Brain hydrogen sulfide is severely decreased in Alzheimer’s disease. Biochem. Biophys. Res. Commun., 2002, 293(5), 1485-1488.
[http://dx.doi.org/10.1016/S0006-291X(02)00422-9] [PMID: 12054683]
[81]
Conway, K.A.; Harper, J.D.; Lansbury, P.T., Jr Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson’s disease are typical amyloid. Biochemistry, 2000, 39(10), 2552-2563.
[http://dx.doi.org/10.1021/bi991447r] [PMID: 10704204]
[82]
Kantcheva, R.B.; Mason, R.; Giorgini, F. Aggregation-prone proteins modulate huntingtin inclusion body formation in yeast. PLoS Curr. Huntington’s Dis, 2014, 6, 1-11.
[http://dx.doi.org/10.1371/currents.hd.501008f3051342c9a5 c0cd0f3a5bf3a4] [PMID: 24804153]
[83]
Serpell, L.C. Alzheimer’s amyloid fibrils: structure and assembly. Biochim. Biophys. Acta, 2000, 1502(1), 16-30.
[http://dx.doi.org/10.1016/S0925-4439(00)00029-6] [PMID: 10899428]
[84]
Rosario-Alomar, M.F.; Quiñones-Ruiz, T.; Kurouski, D.; Sereda, V.; Ferreira, E.B.; Jesús-Kim, L.D.; Hernández-Rivera, S.; Zagorevski, D.V.; López-Garriga, J.; Lednev, I.K. Hydrogen sulfide inhibits amyloid formation. J. Phys. Chem. B, 2015, 119(4), 1265-1274.
[http://dx.doi.org/10.1021/jp508471v] [PMID: 25545790]
[85]
Jansen, E.F. The isolation and identification of 2,2′- dithiolisobutyric acid from asparagus. J. Biol. Chem., 1948, 176(2), 657-664.
[PMID: 18889921]
[86]
Ferris, A.F. The action of mineral acid on diethyl bis(hydroxymethyl)malonate. J. Org. Chem., 1955, 20, 780-787.
[http://dx.doi.org/10.1021/jo01124a011]
[87]
Schotte, L.; Ström, H. The preparation of 1,2-ditholane-4-carboxylic acid. Acta Chem. Scand., 1956, 10, 687-688.
[http://dx.doi.org/10.3891/acta.chem.scand.10-0687]
[88]
Yanagawa, H.; Kato, T.; Sagami, H.; Kitahara, Y. Convenient procedure for the synthesis of asparagusic acid. Synthesis, 1973, 10, 607-608.
[http://dx.doi.org/10.1055/s-1973-22265]
[89]
Singh, R.; Whitesides, G.M. Comparison of rate constant for thiolate-disulfide interchange in water and in polar aprotic solvents using dynamic 1H NMR line shape analysis. J. Am. Chem. Soc., 1990, 112, 1190-1197.
[http://dx.doi.org/10.1021/ja00159a046]
[90]
Venditti, A.; Mandrone, M.; Serrilli, A.M.; Bianco, A.; Iannello, C.; Poli, F.; Antognoni, F. Dihydroasparagusic acid: antioxidant and tyrosinase inhibitory activities and improved synthesis. J. Agric. Food Chem., 2013, 61(28), 6848-6855.
[http://dx.doi.org/10.1021/jf401120h] [PMID: 23790134]
[91]
Yanagawa, Y.; Kato, T.; Kitahara, Y. Asparagusic acid, dihidroasparagusic acid and S-acetyldihydroasparagusic acid, a new plant growth inhibitor in etiolated young asparagus shoots. Tetrahedron Lett., 1972, 25, 2549-2552.
[http://dx.doi.org/10.1016/S0040-4039(01)84871-1]
[92]
Takasugi, M.; Yachida, Y.; Anetai, M.; Masamune, T.; Kegasawa, K. Identification of asparagusic acid as a nematicide occurring naturally in the roots of asparagus. Chem. Lett., 1975, 4, 43-44.
[http://dx.doi.org/10.1246/cl.1975.43]
[93]
Yanagawa, H.; Kato, T.; Kitahara, Y.; Yakahashi, N. Stimulation of growth and pyruvate oxidation in Streptococcus faecalis by asparagusic acid and its derivatives. Plant Cell Physiol., 1973, 14, 791-795.
[http://dx.doi.org/10.1093/oxfordjournals.pcp.a074915]
[94]
Yanagawa, H.; Kato, T.; Kitahara, Y. Stimulation of pyruvate oxidation in asparagus mitochondria by asparagusic acid. Plant Cell Physiol., 1973, 14, 1213-1216.
[http://dx.doi.org/10.1093/oxfordjournals.pcp.a074964]
[95]
Bianco, A.; Bottari, E.; Festa, M.R.; Gentile, L.; Serrilli, A.M.; Venditti, A. Properties of DHAA and its use as an antidote against mercury(II) poisoning. Monatsh. Chem., 2013, 144, 1767-1773.
[http://dx.doi.org/10.1007/s00706-013-1095-3]
[96]
Salemme, A.; Togna, A.R.; Mastrofrancesco, A.; Cammisotto, V.; Ottaviani, M.; Bianco, A.; Venditti, A. Anti-inflammatory effects and antioxidant activity of dihydroasparagusic acid in lipopolysaccharide-activated microglial cells. Brain Res. Bull., 2016, 120, 151-158.
[http://dx.doi.org/10.1016/j.brainresbull.2015.11.014] [PMID: 26592472]
[97]
Kume, T.; Kohchiyama, H.; Nishikawa, H.; Maeda, T.; Kaneko, S.; Akaike, A.; Noda, N.; Fujita, T. Ether extract of fetal calf serum protects cultured rat cortical neurons against glutamate cytotoxicity. Jpn. J. Pharmacol., 1997, 73(4), 371-374.
[http://dx.doi.org/10.1254/jjp.73.371] [PMID: 9165377]
[98]
Kume, T.; Asai, N.; Nishikawa, H.; Mano, N.; Terauchi, T.; Taguchi, R.; Shirakawa, H.; Osakada, F.; Mori, H.; Asakawa, N.; Yonaga, M.; Nishizawa, Y.; Sugimoto, H.; Shimohama, S.; Katsuki, H.; Kaneko, S.; Akaike, A. Isolation of a diterpenoid substance with potent neuroprotective activity from fetal calf serum. Proc. Natl. Acad. Sci. USA, 2002, 99(5), 3288-3293.
[http://dx.doi.org/10.1073/pnas.052693999] [PMID: 11867740]
[99]
Osakada, F.; Kawato, Y.; Kume, T.; Katsuki, H.; Sugimoto, H.; Akaike, A. Serofendic acid, a sulfur-containing diterpenoid derived from fetal calf serum, attenuates reactive oxygen species-induced oxidative stress in cultured striatal neurons. J. Pharmacol. Exp. Ther., 2004, 311(1), 51-59.
[http://dx.doi.org/10.1124/jpet.104.070334] [PMID: 15159446]
[100]
Doi, Y.; Liang, J.; Kuno, R.; Zang, G.; Kawanokuchi, J.; Yawata, I.; Takeuchi, H.; Mizuno, T.; Suzumura, A. The direct and indirect effects of serofendic acid on neuroprotection. Ann. N. Y. Acad. Sci., 2006, 1086, 91-103.
[http://dx.doi.org/10.1196/annals.1377.009] [PMID: 17185508]
[101]
Terauchi, T.; Asai, N.; Doko, T.; Taguchi, R.; Takenaka, O.; Sakurai, H.; Yonaga, M.; Kimura, T.; Kajiwara, A.; Niidome, T.; Kume, T.; Akaike, A.; Sugimoto, H. Synthesis and pharmacological profile of serofendic acids A and B. Bioorg. Med. Chem., 2007, 15(22), 7098-7107.
[http://dx.doi.org/10.1016/j.bmc.2007.07.037] [PMID: 17804246]
[102]
Terauchi, T.; Doko, T.; Yonaga, M.; Kajiwara, A.; Niidome, T.; Taguchi, R.; Kume, T.; Akaike, A.; Sugimoto, H. Synthesis and neuroprotective effects of serofendic acid analogues. Bioorg. Med. Chem. Lett., 2006, 16(19), 5080-5083.
[http://dx.doi.org/10.1016/j.bmcl.2006.07.038] [PMID: 16904319]
[103]
Inden, M.; Kitamura, Y.; Kondo, J.; Hayashi, K.; Yanagida, T.; Takata, K.; Tsuchiya, D.; Yanagisawa, D.; Nishimura, K.; Taniguchi, T.; Shimohama, S.; Sugimoto, H.; Akaike, A. Serofendic acid prevents 6-hydroxydopamine-induced nigral neurodegeneration and drug-induced rotational asymmetry in hemi-parkinsonian rats. J. Neurochem., 2005, 95(4), 950-961.
[http://dx.doi.org/10.1111/j.1471-4159.2005.03413.x] [PMID: 16135081]
[104]
Ioroi, T.; Taguchi, K.; Izumi, Y.; Takada-Takatori, Y.; Akaike, A.; Kume, T. Protective effect of serofendic acid, administered intravenously, on cerebral ischemiareperfusion injury in rats. Brain Res., 2013, 1532, 99-105.
[http://dx.doi.org/10.1016/j.brainres.2013.08.013] [PMID: 23954678]
[105]
Kume, T.; Ito, R.; Taguchi, R.; Izumi, Y.; Katsuki, H.; Niidome, T.; Takada-Takatori, Y.; Sugimoto, H.; Akaike, A. Serofendic acid promotes stellation induced by cAMP and cGMP analogs in cultured cortical astrocytes. J. Pharmacol. Sci., 2009, 109(1), 110-118.
[http://dx.doi.org/10.1254/jphs.08254FP] [PMID: 19122367]
[106]
Srivastava, K.C. Evidence for the mechanism by which garlic inhibits platelet aggregation. Prostaglandins Leukot. Med., 1986, 22(3), 313-321.
[http://dx.doi.org/10.1016/0262-1746(86)90142-3] [PMID: 3088604]
[107]
Silagy, C.A.; Neil, H.A. A meta-analysis of the effect of garlic on blood pressure. J. Hypertens., 1994, 12(4), 463-468.
[http://dx.doi.org/10.1097/00004872-199404000-00017] [PMID: 8064171]
[108]
Anwar, M.M.; Meki, A.R. Oxidative stress in streptozotocin-induced diabetic rats: effects of garlic oil and melatonin. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 2003, 135(4), 539-547.
[http://dx.doi.org/10.1016/S1095-6433(03)00114-4] [PMID: 12890544]
[109]
Augusti, K.T.; Sheela, C.G. Antiperoxide effect of S-allyl cysteine sulfoxide, an insulin secretagogue, in diabetic rats. Experientia, 1996, 52(2), 115-120.
[http://dx.doi.org/10.1007/BF01923354] [PMID: 8608811]
[110]
Rahman, K. Effects of garlic on platelet biochemistry and physiology. Mol. Nutr. Food Res., 2007, 51(11), 1335-1344.
[http://dx.doi.org/10.1002/mnfr.200700058] [PMID: 17966136]
[111]
Ried, K.; Frank, O.R.; Stocks, N.P. Aged garlic extract lowers blood pressure in patients with treated but uncontrolled hypertension: a randomised controlled trial. Maturitas, 2010, 67(2), 144-150.
[http://dx.doi.org/10.1016/j.maturitas.2010.06.001] [PMID: 20594781]
[112]
Zeng, T.; Guo, F.F.; Zhang, C.L.; Song, F.Y.; Zhao, X.L.; Xie, K.Q. A meta-analysis of randomized, double-blind, placebo-controlled trials for the effects of garlic on serum lipid profiles. J. Sci. Food Agric., 2012, 92(9), 1892-1902.
[http://dx.doi.org/10.1002/jsfa.5557] [PMID: 22234974]
[113]
Kumar, R.; Chhatwal, S.; Arora, S.; Sharma, S.; Singh, J.; Singh, N.; Bhandari, V.; Khurana, A. Antihyperglycemic, antihyperlipidemic, anti-inflammatory and adenosine deaminase- lowering effects of garlic in patients with type 2 diabetes mellitus with obesity. Diabetes Metab. Syndr. Obes., 2013, 6, 49-56.
[http://dx.doi.org/10.2147/DMSO.S38888] [PMID: 23378779]
[114]
Moyers, S. Garlic in Health, History, and World Cuisine; Suncoast Press: St. Petersburg, FL, 1996.
[115]
Rivlin, R.S. Historical perspective on the use of garlic. J. Nutr., 2001, 131(3s), 951S-954S.
[http://dx.doi.org/10.1093/jn/131.3.951S] [PMID: 11238795]
[116]
Petrovska, B.B.; Cekovska, S. Extracts from the history and medical properties of garlic. Pharmacogn. Rev., 2010, 4(7), 106-110.
[http://dx.doi.org/10.4103/0973-7847.65321] [PMID: 22228949]
[117]
Gupta, V.B.; Rao, K.S. Anti-amyloidogenic activity of S-allyl-L-cysteine and its activity to destabilize Alzheimer’s beta-amyloid fibrils in vitro. Neurosci. Lett., 2007, 429(2-3), 75-80.
[http://dx.doi.org/10.1016/j.neulet.2007.09.042] [PMID: 18023978]
[118]
Tsai, S.J.; Chiu, C.P.; Yang, H.T.; Yin, M.C. s-Allyl cysteine, s-ethyl cysteine, and s-propyl cysteine alleviate β-amyloid, glycative, and oxidative injury in brain of mice treated by D-galactose. J. Agric. Food Chem., 2011, 59(11), 6319-6326.
[http://dx.doi.org/10.1021/jf201160a] [PMID: 21548553]
[119]
Maldonado, P.D.; Barrera, D.; Rivero, I.; Mata, R.; Medina-Campos, O.N.; Hernández-Pando, R.; Pedraza-Chaverrí, J. Antioxidant S-allylcysteine prevents gentamicin-induced oxidative stress and renal damage. Free Radic. Biol. Med., 2003, 35(3), 317-324.
[http://dx.doi.org/10.1016/S0891-5849(03)00312-5] [PMID: 12885594]
[120]
Javed, H.; Khan, M.M.; Khan, A.; Vaibhav, K.; Ahmad, A.; Khuwaja, G.; Ahmed, M.E.; Raza, S.S.; Ashafaq, M.; Tabassum, R.; Siddiqui, M.S.; El-Agnaf, O.M.; Safhi, M.M.; Islam, F. S-allyl cysteine attenuates oxidative stress associated cognitive impairment and neurodegeneration in mouse model of streptozotocin-induced experimental dementia of Alzheimer’s type. Brain Res., 2011, 1389, 133-142.
[http://dx.doi.org/10.1016/j.brainres.2011.02.072] [PMID: 21376020]
[121]
Peng, Q.; Buz’Zard, A.R.; Lau, B.H. Neuroprotective effect of garlic compounds in amyloid-beta peptide-induced apoptosis in vitro. Med. Sci. Monit., 2002, 8(8), BR328-BR337.
[PMID: 12165737]
[122]
Ito, Y.; Ito, M.; Takagi, N.; Saito, H.; Ishige, K. Neurotoxicity induced by amyloid beta-peptide and ibotenic acid in organotypic hippocampal cultures: protection by S-allyl-L-cysteine, a garlic compound. Brain Res., 2003, 985(1), 98-107.
[http://dx.doi.org/10.1016/S0006-8993(03)03173-1] [PMID: 12957372]
[123]
Kosuge, Y.; Koen, Y.; Ishige, K.; Minami, K.; Urasawa, H.; Saito, H.; Ito, Y. S-allyl-L-cysteine selectively protects cultured rat hippocampal neurons from amyloid beta-protein- and tunicamycin-induced neuronal death. Neuroscience, 2003, 122(4), 885-895.
[http://dx.doi.org/10.1016/j.neuroscience.2003.08.026] [PMID: 14643758]
[124]
Imai, T.; Kosuge, Y.; Ishige, K.; Ito, Y. Amyloid beta-protein potentiates tunicamycin-induced neuronal death in organotypic hippocampal slice cultures. Neuroscience, 2007, 147(3), 639-651.
[http://dx.doi.org/10.1016/j.neuroscience.2007.04.057] [PMID: 17560726]
[125]
Ishige, K.; Takagi, N.; Imai, T.; Rausch, W.D.; Kosuge, Y.; Kihara, T.; Kusama-Eguchi, K.; Ikeda, H.; Cools, A.R.; Waddington, J.L.; Koshikawa, N.; Ito, Y. Role of caspase-12 in amyloid beta-peptide-induced toxicity in organotypic hippocampal slices cultured for long periods. J. Pharmacol. Sci., 2007, 104(1), 46-55.
[http://dx.doi.org/10.1254/jphs.FP0061533] [PMID: 17452809]
[126]
Ito, Y.; Kosuge, Y.; Sakikubo, T.; Horie, K.; Ishikawa, N.; Obokata, N.; Yokoyama, E.; Yamashina, K.; Yamamoto, M.; Saito, H.; Arakawa, M.; Ishige, K. Protective effect of S-allylL-cysteine, a garlic compound, on amyloid betaprotein-induced cell death in nerve growth factor-differentiated PC12 cells. Neurosci. Res., 2003, 46(1), 119-125.
[http://dx.doi.org/10.1016/S0168-0102(03)00037-3] [PMID: 12725918]
[127]
Jackson, R.; McNeil, B.; Taylor, C.; Holl, G.; Ruff, D.; Gwebu, E.T. Effect of aged garlic extract on caspase-3 activity, in vitro. Nutr. Neurosci., 2002, 5(4), 287-290.
[http://dx.doi.org/10.1080/10284150290032012] [PMID: 12168692]
[128]
Dragunow, M.; Faull, R.L.M.; Lawlor, P.; Beilharz, E.J.; Singleton, K.; Walker, E.B.; Mee, E. In situ evidence for DNA fragmentation in Huntington’s disease striatum and Alzheimer’s disease temporal lobes. Neuroreport, 1995, 6(7), 1053-1057.
[http://dx.doi.org/10.1097/00001756-199505090-00026] [PMID: 7632894]
[129]
Lassmann, H.; Bancher, C.; Breitschopf, H.; Wegiel, J.; Bobinski, M.; Jellinger, K.; Wisniewski, H.M. Cell death in Alzheimer’s disease evaluated by DNA fragmentation in situ. Acta Neuropathol., 1995, 89(1), 35-41.
[http://dx.doi.org/10.1007/BF00294257] [PMID: 7709729]
[130]
Lucassen, P.J.; Chung, W.C.J.; Kamphorst, W.; Swaab, D.F. DNA damage distribution in the human brain as shown by in situ end labeling; area-specific differences in aging and Alzheimer disease in the absence of apoptotic morphology. J. Neuropathol. Exp. Neurol., 1997, 56(8), 887-900.
[http://dx.doi.org/10.1097/00005072-199708000-00007] [PMID: 9258259]
[131]
Migheli, A.; Cavalla, P.; Marino, S.; Schiffer, D. A study of apoptosis in normal and pathologic nervous tissue after in situ end-labeling of DNA strand breaks. J. Neuropathol. Exp. Neurol., 1994, 53(6), 606-616.
[http://dx.doi.org/10.1097/00005072-199411000-00008] [PMID: 7525880]
[132]
Portera-Cailliau, C.; Hedreen, J.C.; Price, D.L.; Koliatsos, V.E. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci., 1995, 15(5 Pt 2), 3775-3787.
[http://dx.doi.org/10.1523/JNEUROSCI.15-05-03775.1995] [PMID: 7751945]
[133]
Smale, G.; Nichols, N.R.; Brady, D.R.; Finch, C.E.; Horton, W.E., Jr Evidence for apoptotic cell death in Alzheimer’s disease. Exp. Neurol., 1995, 133(2), 225-230.
[http://dx.doi.org/10.1006/exnr.1995.1025] [PMID: 7544290]
[134]
Su, J.H.; Anderson, A.J.; Cummings, B.J.; Cotman, C.W. Immunohistochemical evidence for apoptosis in Alzheimer’s disease. Neuroreport, 1994, 5(18), 2529-2533.
[http://dx.doi.org/10.1097/00001756-199412000-00031] [PMID: 7696596]
[135]
Tompkins, M.M.; Basgall, E.J.; Zamrini, E.; Hill, W.D. Apoptotic-like changes in Lewy-body-associated disorders and normal aging in substantia nigral neurons. Am. J. Pathol., 1997, 150(1), 119-131.
[PMID: 9006329]
[136]
Troncoso, J.C.; Sukhov, R.R.; Kawas, C.H.; Koliatsos, V.E. In situ labeling of dying cortical neurons in normal aging and in Alzheimer’s disease: correlations with senile plaques and disease progression. J. Neuropathol. Exp. Neurol., 1996, 55(11), 1134-1142.
[http://dx.doi.org/10.1097/00005072-199611000-00004] [PMID: 8939196]
[137]
Stadelmann, C.; Brück, W.; Bancher, C.; Jellinger, K.; Lassmann, H. Alzheimer disease: DNA fragmentation indicates increased neuronal vulnerability, but not apoptosis. J. Neuropathol. Exp. Neurol., 1998, 57(5), 456-464.
[http://dx.doi.org/10.1097/00005072-199805000-00009] [PMID: 9596416]
[138]
Chauhan, N.B. Effect of aged garlic extract on APP processing and tau phosphorylation in Alzheimer’s transgenic model Tg2576. J. Ethnopharmacol., 2006, 108(3), 385-394.
[http://dx.doi.org/10.1016/j.jep.2006.05.030] [PMID: 16842945]
[139]
Moriguchi, T.; Matsuura, H.; Kodera, Y.; Itakura, Y.; Katsuki, H.; Saito, H.; Nishiyama, N. Neurotrophic activity of organosulfur compounds having a thioallyl group on cultured rat hippocampal neurons. Neurochem. Res., 1997, 22(12), 1449-1452.
[http://dx.doi.org/10.1023/A:1021946210399] [PMID: 9357009]
[140]
Cray, C. Acute phase proteins in animals. Prog. Mol. Biol. Transl. Sci., 2012, 105, 113-150.
[http://dx.doi.org/10.1016/B978-0-12-394596-9.00005-6] [PMID: 22137431]
[141]
Moriguchi, T.; Nishiyama, N.; Saito, H.; Katsuki, H. Trophic Effects of Aged Garlic Extract (AGE) and its Fractions on Primary Cultured Hippocampal Neurons from Fetal Rat Brain. Phytother. Res., 1996, 10, 468-472.
[http://dx.doi.org/10.1002/(SICI)1099- 1573(199609)10:6<468::AID-PTR877>3.0.CO;2-I]
[142]
Aguilera, P.; Chánez-Cárdenas, M.E.; Ortiz-Plata, A.; León-Aparicio, D.; Barrera, D.; Espinoza-Rojo, M.; Villeda-Hernández, J.; Sánchez-García, A.; Maldonado, P.D. Aged garlic extract delays the appearance of infarct area in a cerebral ischemia model, an effect likely conditioned by the cellular antioxidant systems. Phytomedicine, 2010, 17(3-4), 241-247.
[http://dx.doi.org/10.1016/j.phymed.2009.06.004] [PMID: 19577455]
[143]
Colín-González, A.L.; Ortiz-Plata, A.; Villeda-Hernández, J.; Barrera, D.; Molina-Jijón, E.; Pedraza-Chaverrí, J.; Maldonado, P.D. Aged garlic extract attenuates cerebral damage and cyclooxygenase-2 induction after ischemia and reperfusion in rats. Plant Foods Hum. Nutr., 2011, 66(4), 348-354.
[http://dx.doi.org/10.1007/s11130-011-0251-3] [PMID: 21850441]
[144]
Zimniak, P. Relationship of electrophilic stress to aging. Free Radic. Biol. Med., 2011, 51(6), 1087-1105.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.05.039] [PMID: 21708248]
[145]
Di Bona, D.; Scapagnini, G.; Candore, G.; Castiglia, L.; Colonna-Romano, G.; Duro, G.; Nuzzo, D.; Iemolo, F.; Lio, D.; Pellicanò, M.; Scafidi, V.; Caruso, C.; Vasto, S. Immune-inflammatory responses and oxidative stress in Alzheimer’s disease: therapeutic implications. Curr. Pharm. Des., 2010, 16(6), 684-691.
[http://dx.doi.org/10.2174/138161210790883769] [PMID: 20388078]
[146]
Corona, A.W.; Fenn, A.M.; Godbout, J.P. Cognitive and behavioral consequences of impaired immunoregulation in aging. J. Neuroimmune Pharmacol., 2012, 7(1), 7-23.
[http://dx.doi.org/10.1007/s11481-011-9313-4] [PMID: 21932047]
[147]
Lee, D.Y.; Li, H.; Lim, H.J.; Lee, H.J.; Jeon, R.; Ryu, J.H. Anti-inflammatory activity of sulfur-containing compounds from garlic. J. Med. Food, 2012, 15(11), 992-999.
[http://dx.doi.org/10.1089/jmf.2012.2275] [PMID: 23057778]
[148]
Suh, J.H.; Shenvi, S.V.; Dixon, B.M.; Liu, H.; Jaiswal, A.K.; Liu, R.M.; Hagen, T.M. Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proc. Natl. Acad. Sci. USA, 2004, 101(10), 3381-3386.
[http://dx.doi.org/10.1073/pnas.0400282101] [PMID: 14985508]
[149]
Duan, W.; Zhang, R.; Guo, Y.; Jiang, Y.; Huang, Y.; Jiang, H.; Li, C. Nrf2 activity is lost in the spinal cord and its astrocytes of aged mice. In Vitro Cell. Dev. Biol. Anim., 2009, 45(7), 388-397.
[http://dx.doi.org/10.1007/s11626-009-9194-5] [PMID: 19452231]
[150]
Cheng, X.; Siow, R.C.; Mann, G.E. Impaired redox signaling and antioxidant gene expression in endothelial cells in diabetes: a role for mitochondria and the nuclear factor-E2-related factor 2-Kelch-like ECH-associated protein 1 defense pathway. Antioxid. Redox Signal., 2011, 14(3), 469-487.
[http://dx.doi.org/10.1089/ars.2010.3283] [PMID: 20524845]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy