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Cytotechnology

, Volume 63, Issue 2, pp 191–200 | Cite as

3,4,5-tri-O-caffeoylquinic acid inhibits amyloid β-mediated cellular toxicity on SH-SY5Y cells through the upregulation of PGAM1 and G3PDH

  • Yusaku Miyamae
  • Junkyu Han
  • Kazunori Sasaki
  • Mika Terakawa
  • Hiroko IsodaEmail author
  • Hideyuki ShigemoriEmail author
JAACT Special Issue

Abstract

Caffeoylquinic acid (CQA) is one of the phenylpropanoids found in a variety of natural resources and foods, such as sweet potatoes, propolis, and coffee. Previously, we reported that 3,5-di-O-caffeoylquinic acid (3,5-di-CQA) has a neuroprotective effect against amyloid-β (Aβ)-induced cell death through the overexpression of glycolytic enzyme. Additionally, 3,5-di-CQA administration induced the improvement of spatial learning and memory on senescence accelerated-prone mice (SAMP8). The aim of this study was to investigate whether 3,4,5-tri-O-caffeoylquinic acid (3,4,5-tri-CQA), isolated from propolis, shows a neuroprotective effect against Aβ-induced cell death on human neuroblastoma SH-SY5Y cells. To clarify the possible mechanism, we performed proteomics and real-time RT–PCR as well as a measurement of the intracellular adenosine triphosphate (ATP) level. These results showed that 3,4,5-tri-CQA attenuated the cytotoxicity and prevented Aβ-mediated apoptosis. Glycolytic enzymes, phosphoglycerate mutase 1 (PGAM1) and glyceraldehyde-3-phosphate dehydrogenase (G3PDH) were overexpressed in co-treated cells with both 3,4,5-tri-CQA and Aβ. The mRNA expression of PGAM1, G3PDH, and phosphoglycerate kinase 1 (PGK1), and intracellular ATP level were also increased in 3,4,5-tri-CQA treated cells. Taken together the findings in our study suggests that 3,4,5-tri-CQA shows a neuroprotective effect against Aβ-induced cell death through the upregulation of glycolytic enzyme mRNA as well as ATP production activation.

Keywords

3,4,5-tri-O-caffeoylquinic acid SH-SY5Y cells G3PDH PGAM1 Glycolytic enzyme ATP 

References

  1. Atamna H, Frey WHII (2007) Mechanisms of mitochondrial dysfunction and energy deficiency in Alzheimer’s disease. Mitochondrion 7:297–310CrossRefGoogle Scholar
  2. Boyd-Kimball D, Sultana R, Poon HF, Lynn BC, Casamenti F, Pepeu G, Klein JB, Butterfield DA (2005) Proteomic identification of proteins specifically oxidized by intracerebral injection of amyloid β-peptide (1–42) into rat brain: implications for Alzheimer’s disease. Neuroscience 132:313–324CrossRefGoogle Scholar
  3. Butterfield DA, Boyd-Kimball D (2005) The critical role of methionine 35 in Alzheimer’s amyloid beta-peptide (1–42)-induced oxidative stress and neurotoxicity. Biochim Biophys Acta 1703:149–156Google Scholar
  4. Canback B, Andersson SGE, Kurland CG (2002) The global phylogency of glycolytic enzymes. Proc Natl Acad Sci USA 99:6097–6102CrossRefGoogle Scholar
  5. Cardoso SM, Santos S, Swerdlow RH, Oliveira CR (2001) Functional mitochondria are required for amyloid beta-mediated neurotoxicity. FASEB J 15:1439–1441Google Scholar
  6. Castegna A, Thongboonkerd V, Klein JB, Lynn B, Markesbery WR, Butterfield DA (2003) Proteomic identification of nitrated proteins in Alzheimer’s disease brain. J Neurochem 85:1394–1401CrossRefGoogle Scholar
  7. Clifford MN, Wu W, Kirkpatrick J, Kuhnert N (2007) Profiling the chlorogenic acids and other caffeic acid derivatives of herbal chrysanthemum by LC-MS. J Agric Food Chem 55:929–936CrossRefGoogle Scholar
  8. Farah A, Paulis TD, Trugo LC, Martin PR (2005) Effect of roasting on the formation of chlorogenic acid lactone in coffee. J Agric Food Chem 53:1505–11513CrossRefGoogle Scholar
  9. Ferrer I (2009) Altered mitochondria, energy metabolism, voltage-dependent anion channel, and lipid rafts converge to exhaust neurons in Alzheimer’s disease. J Bioenerg Biomembr 41:425–431CrossRefGoogle Scholar
  10. Han J, Miyamae Y, Shigemori H, Isoda H (2010) Neuroprotective effect of 3, 5-di-O-caffeoylquinic acid on SH-SY5Y cells and SAMP8 mice through the up-regulation of PGK1. Neuroscience 169:1039–1045CrossRefGoogle Scholar
  11. Isoda H, Talorete TPN, Han J, Nakamura K (2006) Expresion of galectin-3, glutathione S-transferase A2 and peroxiredoxin-1 by nonyphenol-incubated Caco-2 cells and reduction in transepithelial electrical resistance by nonyphenol. Toxicol In Vitro 20:63–70CrossRefGoogle Scholar
  12. Kim JW, Dang CV (2005) Multifaceted roles of glycolytic enzymes. Trends Biochem Sci 30:142–150CrossRefGoogle Scholar
  13. Kimura Y, Okuda H, Okuda H, Hatano T, Agata I, Arichi S (1985) Inhibitory effects of caffeoylquinic acids on histamine release from rat peritoneal mast cells. Chem Pharm Bull 33:690–696Google Scholar
  14. Kondoh H, Lleonart ME, Gil J, Wang J, Degan P, Peters G, Martinez D, Carnero A, Beach D (2005) Glycolytic enzymes can modulate cellular life span. Cancer Res 65:177–185Google Scholar
  15. Korolainen MA, Goldsteins G, Nyman TA, Alafuzoff I, Pirttila T (2005) Proteomic analysis of glial fibrillary acidic protein in Alzheimer’s disease and aging brain. Neurobiol Dis 20:858–870CrossRefGoogle Scholar
  16. Korolainen MA, Goldsteins G, Nyman TA, Alafuzoff I, Koistinaho J, Pirttilä T (2006) Oxidative modification of proteins in the frontal cortex of Alzheimer’s disease brain. Neurobiol Aging 27:42–53CrossRefGoogle Scholar
  17. Kurata R, Adachi M, Yamakawa O, Yoshimoto M (2007) Growth suppression of human cancer cells by polyphenolics from sweetpotato (Ipomoea batatas L.) leaves. J Agric Food Chem 55:185–190CrossRefGoogle Scholar
  18. Liu X, Shibata T, Hisaka S, Osawa T (2009) Astaxanthin inhibits reactive oxygen species-mediated cellular toxicity in dopaminergic SH-SY5Y cells via mitochondria-targeted protective mechanism. Brain Res 1254:18–27CrossRefGoogle Scholar
  19. Matharu B, Gibson G, Parsons R, Huckerby TN, Moore SA, Cooper LJ, Millichamp R, Allsop D, Austen B (2009) Galantamine inhibits β-amyloid aggregation and cytotoxicity. J Neurol Sci 280:49–58CrossRefGoogle Scholar
  20. Matsui T, Ebuchi S, Fujise T, Abesundara KJ, Doi S, Yamada H, Matsumoto K (2004) Strong anti hyperglycemic effects of water-soluble fraction of Brazilian propolis and its bioactive constituent, 3, 4, 5-tri-O-caffeoylquinic acid. Biol Pharm Bull 27:1797–1803CrossRefGoogle Scholar
  21. Mazzolaa JL, Sirover MA (2003) Subcellular alternation of glyceraldehyde-3-phosphate dehydrogenase in Alzheimer’s disease fibroblasts. J Neurosci Res 71:279–285CrossRefGoogle Scholar
  22. Merfort I (1992) Caffeoylquinic acids from flowers of Arnica Montana and Arnica chamissonis. Phytochemistry 31:2111–2113CrossRefGoogle Scholar
  23. Miranda S, Opazo C, Larrondo LF, Munoz FJ, Ruiz F, Leighton F, Inestrosa NC (2000) The role of oxidative stress in the toxicity induced by amyloid β-peptide in Alzheimer’s disease. Prog Neurobiol 62:633–648CrossRefGoogle Scholar
  24. Mishima S, Inoh Y, Narita Y, Ohta S, Sakamoto T, Araki Y, Suzuki K, Akao Y, Nozawa Y (2005) Identification of caffeoylquinic acid derivatives from Brazilian propolis as constituents involved in induction of granulocytic differentiation of HL-60 cells. Bioorg Med Chem 13:5814–5818CrossRefGoogle Scholar
  25. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity. Anal Biochem 65:55–63Google Scholar
  26. Qi XL, Xiu J, Shan KR, Xiao Y, Gu R, Liu RY, Guan ZZ (2005) Oxidative stress induced by beta-amyloid peptide1–42 is involved in the altered composition of cellular membrane lipids and the decreased expression of nicotinic receptors in human SH-SY5Y neuroblastoma cells. Neurochem Int 46:613–621CrossRefGoogle Scholar
  27. Ramassamy C, Averill D, Beffert U, Bastianetto S, Theroux L, Lussier-Cacan S, Chon JS, Christen Y, Davignon J, Quirion R, Poirier J (1999) Oxidative damage and protection by antioxidants in the frontal cortex of Alzheimer’s disease is related to the apolipoprotein E genotype. Free Radic Biol Med 27:544–553CrossRefGoogle Scholar
  28. Reed T, Perluigi M, Sultana R, Pierce WN, Klein JB, Turner DM, Coccia R, Markesbery WR, Butterfield DA (2008) Redox proteomic identification of 4-Hydroxy-2-nonenal-modified brain proteins in amnestic mild cognitive impairment: insight into the role lipid peroxidation in the progression and pathogenesis of Alzheimer’s disease. Neurobiol Dis 30:107–120CrossRefGoogle Scholar
  29. Shi C, Zhao L, Zhu B, Li Q, Yew DT, Yao Z, Xu J (2009) Protective effects of Ginkgo biloba extract (EGb761) and its constituents quercetin and ginkgolide B against β-amyloid peptide-induced toxicity in SH-SY5Y cells. Chem Biol Interact 181:115–123CrossRefGoogle Scholar
  30. Sirover MA (1999) New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochem Biophys Acta 1432:159–184CrossRefGoogle Scholar
  31. Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, Merchantt M, Markesbery WR, Butterfield DA (2006) Redox proteomics identification of oxidized proteins in Alzheimer’s disease hippocampus and cerebellum: an approach to understand pathological and biochemical alternations in AD. Neurobiol Aging 27:1564–1576CrossRefGoogle Scholar
  32. Wang H, Xu Y, Yan J, Zhao X, Sun X, Zhang Y, Guo J, Zhu C (2009) Acteoside protects human neuroblastoma SH-SY5Y cells against β-amyloid-induced cell injury. Brain Res 1283:139–147CrossRefGoogle Scholar
  33. Yang JL, Weissman L, Bohr VA, Mattson MP (2008) Mitochondrial DNA damage and repair in neurodegenerative disorders. DNA Repair 7:1110–1120CrossRefGoogle Scholar
  34. Yoshimoto M, Yahara S, Okuno S, Islam MS, Ishiguro K, Yamakawa O (2002) Antimutagenicity of mono, di, and tri caffeoylquinic acid derivatives isolated from sweetpotato (Ipomoea batatas L.) leaf. Biosci Biotechnol Biochem 66:2336–2441CrossRefGoogle Scholar
  35. Zheng L, Roeder RG, Luo YS (2003) Phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114:255–266CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Yusaku Miyamae
    • 1
  • Junkyu Han
    • 1
    • 2
  • Kazunori Sasaki
    • 1
  • Mika Terakawa
    • 3
  • Hiroko Isoda
    • 1
    • 2
    Email author
  • Hideyuki Shigemori
    • 1
    Email author
  1. 1.Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukuba, IbarakiJapan
  2. 2.Alliance for Research on North Africa (ARENA), University of TsukubaTsukuba, IbarakiJapan
  3. 3.Kato Brothers Honey Co., Ltd.Yokohama, KanagawaJapan

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