Chemical basis for the disparate neuroprotective effects of the anthocyanins, callistephin and kuromanin, against nitrosative stress

Free Radical Biology and Medicine

Volumn 103, Issue , 2017, Pages 23-34

  Winter, Aimee N ^a   Ross, Erika K ^a   Khatter, Sonia ^a   Miller, Keith ^a   Linseman, Daniel A ^a,b  

^a UNIVERSITY OF DENVER   (United States)

^b UNIVERSITY OF DENVER   (United States)

Author keywords

Anthocyanins; Excitotoxicity; Neurodegeneration; Neuroprotection; Nitric Oxide; Nitrosative stress

Indexed keywords

ANTHOCYANIN; ANTIOXIDANT; CALLISTEPHIN; CATECHOL; COPPER ZINC SUPEROXIDE DISMUTASE; CYANIDIN 3 GLUCOSIDE; HYDROXYL GROUP; NITRIC OXIDE; SUPEROXIDE; UNCLASSIFIED DRUG; CYANIDIN 3-O-GLUCOPYRANOSIDE; GLUCOSIDE; GLUTAMIC ACID; NEUROPROTECTIVE AGENT; PELARGONIDIN-3-GLUCOSIDE; PLANT EXTRACT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CEREBELLUM; CONTROLLED STUDY; DEGENERATIVE DISEASE; EXCITOTOXICITY; NERVE CELL; NEUROPROTECTION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; VARIANCE; ANIMAL; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; FRAGARIA; METABOLISM; PHYSIOLOGY; PRECLINICAL STUDY; RUBUS; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; ANTHOCYANINS; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; FRAGARIA; GLUCOSIDES; GLUTAMIC ACID; NEURONS; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; NITROSATIVE STRESS; PLANT EXTRACTS; RATS, SPRAGUE-DAWLEY; RUBUS; SIGNAL TRANSDUCTION; SUPEROXIDES;

EID: 85005980955     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.12.012     Document Type: Article

References (58)

1. [1] Calabrese, V., Bates, T.E., Stella, A.M., NO synthase and NO-dependent signal pathways in brain aging and neurodegenerative disorders: the role of oxidant/antioxidant balance. Neurochem. Res. 25 (2000), 1315–1341.
2. [2] Gu, Z., Nakamura, T., Lipton, S.A., Redox reactions induced by nitrosative stress mediate protein misfolding and mitochondrial dysfunction in neurodegenerative diseases. Mol. Neurobiol. 41 (2010), 55–72.
3. [3] Lin, M.T., Beal, M.F., Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006), 787–795.
4. [4] Radi, E., Formichi, P., Battisti, C., Federico, A., Apoptosis and oxidative stress in neurodegenerative diseases. J. Alzheimers Dis. 42:Suppl 3 (2014), S125–S152.
5. [5] Hamalainen, M., Nieminen, R., Vuorela, P., Heinonen, M., Moilanen, E., Anti-inflammatory effects of flavonoids: genistein, kaempferol, quercetin, and daidzein inhibit STAT-1 and NF-kappaB activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-kappaB activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediat. Inflamm., 2007, 2007, 45673.
6. [6] Hirano, R., Sasamoto, W., Matsumoto, A., Itakura, H., Igarashi, O., Kondo, K., Antioxidant ability of various flavonoids against DPPH radicals and LDL oxidation. J. Nutr. Sci. Vitam. 47 (2001), 357–362.
7. [7] Ishikawa, Y., Kitamura, M., Anti-apoptotic effect of quercetin: intervention in the JNK- and ERK-mediated apoptotic pathways. Kidney Int. 58 (2000), 1078–1087.
8. [8] Kumazawa, Y., Kawaguchi, K., Takimoto, H., Immunomodulating effects of flavonoids on acute and chronic inflammatory responses caused by tumor necrosis factor alpha. Curr. Pharm. Des. 12 (2006), 4271–4279.
9. [9] Kwon, Y.S., Kim, S.S., Sohn, S.J., Kong, P.J., Cheong, I.Y., Kim, C.M., et al. Modulation of suppressive activity of lipopolysaccharide-induced nitric oxide production by glycosidation of flavonoids. Arch. Pharm. Res. 27 (2004), 751–756.
10. [10] Schroeter, H., Spencer, J.P., Rice-Evans, C., Williams, R.J., Flavonoids protect neurons from oxidized low-density-lipoprotein-induced apoptosis involving c-Jun N-terminal kinase (JNK), c-Jun and caspase-3. Biochem. J. 358 (2001), 547–557.
11. [11] Vauzour, D., Vafeiadou, K., Rice-Evans, C., Williams, R.J., Spencer, J.P., Activation of pro-survival Akt and ERK1/2 signalling pathways underlie the anti-apoptotic effects of flavanones in cortical neurons. J. Neurochem. 103 (2007), 1355–1367.
12. [12] Vauzour, D., Vafeiadou, K., Rodriguez-Mateos, A., Rendeiro, C., Spencer, J.P., The neuroprotective potential of flavonoids: a multiplicity of effects. Genes Nutr. 3 (2008), 115–126.
13. [13] Ross, E., Kelsey, N.A., Linseman, D.A., Anthocyanins: janus nutraceuticals displaying chemotherapeutic and neuroprotective properties. Noworyta, K., Diederich, M., (eds.) Natural Compounds as Inducers of Cell Death, 2012, Springer, 491–513.
14. [14] Wallace, T.C., Anthocyanins in cardiovascular disease. Adv. Nutr. 2 (2011), 1–7.
15. [15] Wang, L.S., Stoner, G.D., Anthocyanins and their role in cancer prevention. Cancer Lett. 269 (2008), 281–290.
16. [16] Ross, E.K., Winter, A.N., Linseman, D.A., Effects of anthocyanins on neuronal and cognitive brain function. Wallace, T.C., Giusti, M.M., (eds.) Anthocyanins in Health and Disease, 2013, CRC Press, 279–308.
17. [17] Carey, A.N., Fisher, D.R., Rimando, A.M., Gomes, S.M., Bielinski, D.F., Shukitt-Hale, B., Stilbenes and anthocyanins reduce stress signaling in BV-2 mouse microglia. J. Agric Food Chem. 61 (2013), 5979–5986.
18. [18] Jeong, J.W., Lee, W.S., Shin, S.C., Kim, G.Y., Choi, B.T., Choi, Y.H., Anthocyanins downregulate lipopolysaccharide-induced inflammatory responses in BV2 microglial cells by suppressing the NF-kappaB and Akt/MAPKs signaling pathways. Int. J. Mol. Sci. 14 (2013), 1502–1515.
19. [19] Poulose, S.M., Fisher, D.R., Larson, J., Bielinski, D.F., Rimando, A.M., Carey, A.N., et al. Anthocyanin-rich acai (Euterpe oleracea Mart.) fruit pulp fractions attenuate inflammatory stress signaling in mouse brain BV-2 microglial cells. J. Agric. Food Chem. 60 (2012), 1084–1093.
20. [20] Kelsey, N., Hulick, W., Winter, A., Ross, E., Linseman, D., Neuroprotective effects of anthocyanins on apoptosis induced by mitochondrial oxidative stress. Nutr. Neurosci. 14 (2011), 249–259.
21. [21] Kim, H.S., Sul, D., Lim, J.Y., Lee, D., Joo, S.S., Hwang, K.W., et al. Delphinidin ameliorates beta-amyloid-induced neurotoxicity by inhibiting calcium influx and tau hyperphosphorylation. Biosci. Biotechnol. Biochem. 73 (2009), 1685–1689.
22. [22] Shih, P.H., Wu, C.H., Yeh, C.T., Yen, G.C., Protective effects of anthocyanins against amyloid beta-peptide-induced damage in neuro-2A cells. J. Agric. Food Chem. 59 (2011), 1683–1689.
23. [23] Tarozzi, A., Merlicco, A., Morroni, F., Franco, F., Cantelli-Forti, G., Teti, G., et al. Cyanidin 3-O-glucopyranoside protects and rescues SH-SY5Y cells against amyloid-beta peptide-induced toxicity. Neuroreport 19 (2008), 1483–1486.
24. [24] Tarozzi, A., Morroni, F., Hrelia, S., Angeloni, C., Marchesi, A., Cantelli-Forti, G., et al. Neuroprotective effects of anthocyanins and their in vivo metabolites in SH-SY5Y cells. Neurosci. Lett. 424 (2007), 36–40.
25. [25] Tarozzi, A., Morroni, F., Merlicco, A., Bolondi, C., Teti, G., Falconi, M., et al. Neuroprotective effects of cyanidin 3-O-glucopyranoside on amyloid beta (25-35) oligomer-induced toxicity. Neurosci. Lett. 473 (2010), 72–76.
26. [26] Qin, L., Zhang, J., Qin, M., Protective effect of cyanidin 3-O-glucoside on beta-amyloid peptide-induced cognitive impairment in rats. Neurosci. Lett. 534 (2013), 285–288.
27. [27] Roghani, M., Niknam, A., Jalali-Nadoushan, M.R., Kiasalari, Z., Khalili, M., Baluchnejadmojarad, T., Oral pelargonidin exerts dose-dependent neuroprotection in 6-hydroxydopamine rat model of hemi-parkinsonism. Brain Res. Bull. 82 (2010), 279–283.
28. [28] Brown, J.E., Kelly, M.F., Inhibition of lipid peroxidation by anthocyanins, anthocyanidins and their phenolic degradation products. Eur. J. Lipid Sci. Technol. 106 (2007), 66–71.
29. [29] Yi, W., Akoh, C.C., Fischer, J., Krewer, G., Absorption of anthocyanins from blueberry extracts by caco-2 human intestinal cell monolayers. J. Agric. Food Chem. 54 (2006), 5651–5658.
30. [30] Rodriguez-Saona, L.E., Wrolstad, R.E., Extraction, Isolation, and Purification of Anthocyanins. Current Protocols in Food Analytical Chemistry. 2001, John Wiley & Sons, Inc (F1.-F.11).
31. [31] Linseman, D.A., Laessig, T., Meintzer, M.K., McClure, M., Barth, H., Aktories, K., et al. An essential role for Rac/Cdc42 GTPases in cerebellar granule neuron survival. J. Biol. Chem. 276 (2001), 39123–39131.
32. [32] Luetjens, C.M., Bui, N.T., Sengpiel, B., Munstermann, G., Poppe, M., Krohn, A.J., et al. Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J. Neurosci. 20 (2000), 5715–5723.
33. [33] Helton, T.D., Otsuka, T., Lee, M.C., Mu, Y., Ehlers, M.D., Pruning and loss of excitatory synapses by the parkin ubiquitin ligase. Proc. Natl. Acad. Sci. USA 105 (2008), 19492–19497.
34. [34] Miguel-Hidalgo, J.J., Alvarez, X.A., Cacabelos, R., Quack, G., Neuroprotection by memantine against neurodegeneration induced by beta-amyloid(1-40). Brain Res. 958 (2002), 210–221.
35. [35] Sun, H., Kawahara, Y., Ito, K., Kanazawa, I., Kwak, S., Slow and selective death of spinal motor neurons in vivo by intrathecal infusion of kainic acid: implications for AMPA receptor-mediated excitotoxicity in ALS. J. Neurochem. 98 (2006), 782–791.
36. [36] Di Filippo, M., Chiasserini, D., Tozzi, A., Picconi, B., Calabresi, P., Mitochondria and the link between neuroinflammation and neurodegeneration. J. Alzheimers Dis. 20:Suppl. 2 (2010), S369–S379.
37. [37] Chichirau, A., Flueraru, M., Chepelev, L.L., Wright, J.S., Willmore, W.G., Durst, T., et al. Mechanism of cytotoxicity of catechols and a naphthalenediol in PC12-AC cells: the connection between extracellular autoxidation and molecular electronic structure. Free Radic. Biol. Med. 38 (2005), 344–355.
38. [38] Baiamonte, I., Raffo, A., Nardo, N., Poaoletti, F., Bonoli, M., Baruzzi, G., et al. Anthocyanin content of strawberries (Fragaria ananassa) grown in either organic or integrated production systems. Acta Hortic. 873 (2010), 303–308.
39. [39] Elisia, I., Gu, J., Popovich, D.G., Kitts, D.D., Antioxidant assessment of an anthocyanin-enriched blackberry extract. Food Chem. 101 (2007), 1052–1058.
40. [40] Prochazkova, D., Bousova, I., Wilhelmova, N., Antioxidant and prooxidant properties of flavonoids. Fitoterapia 82 (2011), 513–523.
41. [41] Yen, G.C., Duh, P.D., Tsai, H.L., Huang, S.L., Pro-oxidative properties of flavonoids in human lymphocytes. Biosci. Biotechnol. Biochem. 67 (2003), 1215–1222.
42. [42] Fu, Y., Buryanovskyy, L., Zhang, Z., Quinone reductase 2 is a catechol quinone reductase. J. Biol. Chem. 283 (2008), 23829–23835.
43. [43] Boots, A.W., Li, H., Schins, R.P., Duffin, R., Heemskerk, J.W., Bast, A., et al. The quercetin paradox. Toxicol. Appl. Pharmacol. 222 (2007), 89–96.
44. [44] Feng, R., Ni, H.M., Wang, S.Y., Tourkova, I.L., Shurin, M.R., Harada, H., et al. Cyanidin-3-rutinoside, a natural polyphenol antioxidant, selectively kills leukemic cells by induction of oxidative stress. J. Biol. Chem. 282 (2007), 13468–13476.
45. [45] Lee, K.W., Hur, H.J., Lee, H.J., Lee, C.Y., Antiproliferative effects of dietary phenolic substances and hydrogen peroxide. J. Agric. Food Chem. 53 (2005), 1990–1995.
46. [46] Weisburg, J.H., Weissman, D.B., Sedaghat, T., Babich, H., In vitro cytotoxicity of epigallocatechin gallate and tea extracts to cancerous and normal cells from the human oral cavity. Basic Clin. Pharmacol. Toxicol. 95 (2004), 191–200.
47. [47] Carlsen, H., Myhrstad, M.C., Thoresen, M., Moskaug, J.O., Blomhoff, R., Berry intake increases the activity of the gamma-glutamylcysteine synthetase promoter in transgenic reporter mice. J. Nutr. 133 (2003), 2137–2140.
48. [48] Hassimotto, N.M., Lajolo, F.M., Antioxidant status in rats after long-term intake of anthocyanins and ellagitannins from blackberries. J. Sci. Food Agric. 91 (2011), 523–531.
49. [49] Raoul, C., Buhler, E., Sadeghi, C., Jacquier, A., Aebischer, P., Pettmann, B., et al. Chronic activation in presymptomatic amyotrophic lateral sclerosis (ALS) mice of a feedback loop involving Fas, Daxx, and FasL. Proc. Natl. Acad. Sci. USA 103 (2006), 6007–6012.
50. [50] Uehara, T., Nakamura, T., Yao, D., Shi, Z.Q., Gu, Z., Ma, Y., et al. S-Nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441 (2006), 513–517.
51. [51] Heijnen, C.G., Haenen, G.R., van Acker, F.A., van der Vijgh, W.J., Bast, A., Flavonoids as peroxynitrite scavengers: the role of the hydroxyl groups. Toxicol. In Vitro 15 (2001), 3–6.
52. [52] Delgado-Esteban, M., Martin-Zanca, D., Andres-Martin, L., Almeida, A., Bolanos, J.P., Inhibition of PTEN by peroxynitrite activates the phosphoinositide-3-kinase/Akt neuroprotective signaling pathway. J. Neurochem. 102 (2007), 194–205.
53. [53] Garcia-Nogales, P., Almeida, A., Bolanos, J.P., Peroxynitrite protects neurons against nitric oxide-mediated apoptosis. A key role for glucose-6-phosphate dehydrogenase activity in neuroprotection. J. Biol. Chem. 278 (2003), 864–874.
54. [54] Li, X., Improved pyrogallol autoxidation method: a reliable and cheap superoxide-scavenging assay suitable for all antioxidants. J. Agric. Food Chem. 60 (2012), 6418–6424.
55. [55] Faria, A., Meireles, M., Fernandes, I., Santos-Buelga, C., Gonzalez-Manzano, S., Duenas, M., et al. Flavonoid metabolites transport across a human BBB model. Food Chem. 149 (2014), 190–196.
56. [56] Youdim, K.A., Dobbie, M.S., Kuhnle, G., Proteggente, A.R., Abbott, N.J., Rice-Evans, C., Interaction between flavonoids and the blood-brain barrier: in vitro studies. J. Neurochem. 85 (2003), 180–192.
57. [57] Azzini, E., Vitaglione, P., Intorre, F., Napolitano, A., Durazzo, A., Foddai, M.S., et al. Bioavailability of strawberry antioxidants in human subjects. Br. J. Nutr. 104 (2010), 1165–1173.
58. [58] Tsuda, T., Horio, F., Osawa, T., Absorption and metabolism of cyanidin 3-O-beta-D-glucoside in rats. FEBS Lett. 449 (1999), 179–182.