Phenolic acids from malt are efficient acetylcholinesterase and butyrylcholinesterase inhibitors

Journal of the Institute of Brewing

Volumn 118, Issue 1, 2012, Pages 40-48

  Szwajgier, Dominik ^a   Borowiec, Kamila ^a  

^a University of Natural Sciences   (Poland)

Author keywords

Acetylcholinesterase; Alzheimer's disease; Butyrylcholinesterase; Malt; Mash; Phenolic acids

Indexed keywords

ENZYMES; NEURODEGENERATIVE DISEASES; PHENOLS; SPECTROPHOTOMETRY;

ACETYLCHOLINESTERASE; ALZHEIMER'S DISEASE; BUTYRYLCHOLINESTERASE; MALT; MASH; PHENOLIC ACIDS;

BENZOIC ACID;

EID: 84868611196     PISSN: 00469750     EISSN: 20500416     Source Type: Journal    
DOI: 10.1002/jib.5     Document Type: Article

References (85)

1. Whitehouse, P.J., Price, D.L., Clark, A.W., Coyle, J.T., and DeLong, M.R. (1981) Alzheimer's disease: evidence for selective loss of cholinergic neurons in the nucleus basalis, Ann. Neurol. 10, 115-126.
2. Rao, A.A., Sridhar, G.R., and Das, U.N. (2007) Elevated butyrylcholinesterase and acetylcholinesterase may predict the development of type 2 diabetesmelitus and Alzheimer's disease, Med. Hypotheses 69, 1272-1276.
3. Selkoe, D.J. (1996) Amyloid b-protein and the genetics of Alzheimer's disease, J. Biol. Chem. 271, 18295-18298.
4. Alvarez, A., Opazo, C., Alarcon, R., Garrdio, J., and Inestrosa, N. (1997) Acetylcholinesterase promotes the aggregation of amyloid b-protein fragments by forming a complex with the growing fibrils, J. Mol. Biol. 272, 348-361.
5. Giacobini, E. (2004) Cholinesterase inhibitors: new roles and therapeutic alternatives, Pharmacol. Res. 50, 433-440.
6. Karczmar, A.Q. (1998) Anticholinesterases: dramatic aspect of their use and misuse, Neurochem. Int. 32, 401-411.
7. Ferreira, A., Proença, C., Serralheiro, M.L.M., and Araújo, M.E.M. (2006) The in vitro screening for acetylcholinesterase inhibition and antioxidant activity ofmedicinal plants fromPortugal, J. Epidemiol. 108, 31-37.
8. Suh, S.-J., Koo, B.-S., Jin, U.-H., Hwang, M.-J., Lee, I.-S., and Kim, C.-H. (2006) Pharmacological characterization of orally active cholinesterase inhibitory activity of Prunus persica L. Batsch in rats, J. Mol. Neurosci. 29, 101-108.
9. Gupta, A., and Gupta, R. (1997) A survey of plants for presence of cholinesterase activity, Phytochemistry 46, 827-831.
10. Ingkaninan, K., Temkitthawon, P., Chuenchom, K., Yuyaem, T., and Thongnoi, W. (2003) Screening for acetylcholinesterase inhibitory activity in plants used in Thai traditional rejuvenating and neurotonic remedies, J. Ethnopharmacol. 89, 261-264.
11. Orhan, I., Şener, B., Choudhary,M.I., and Khalid, A. (2004) Acetylcholinesterase and butyrylcholinesterase inhibitory activity of some Turkish medicinal plants, J. Ethnopharmacol. 91, 57-60.
12. Adsersen, A., Gauguin, B., Gudiksen, L., and Jäger, A.K. (2006) Screening of plants used in Danish folk medicine to treat memory dysfunction for acetylcholinesterase inhibitory activity, J. Ethnopharmacol. 104, 418-422.
13. Mukherjee, P.K., Kumar, V., Mal, M., and Houghton, P.J. (2007) Acetylcholinesterase inhibitors from plants, Phytomedicine 14, 289-300.
14. Vinutha, B., Prashanth, D., Salma, K., Sreeja, S.L., Pratiti, D., Padmaja, R., Radhika, S., Amit, A., Venkateshwarlu, K., and Deepak, M. (2007) Screening of selected Indian medicinal plants for acetylcholinesterase inhibitory activity, J. Ethnopharmacol. 109, 359-363.
15. Gonzalez-Munoz, M.J., Meseguer, I., Sanchez-Reus, M.I., Schultz, A., Olivero, R., Benedi, J., and Sanchez-Muniz, F.J. (2008) Beer consumption reduces cerebral oxidation caused by aluminium toxicity by normalizing gene expression of tumor necrotic factor alpha and several antioxidant enzymes, Food Chem. Toxicol. 46, 1111-1118.
16. Gonzalez-Munoz, M.J., Pena, A., and Meseguer, I. (2008) Role of beer as a possible protective factor in preventing Alzheimer's disease, Food Chem. Toxicol. 46, 49-56.
17. Luchsinger, J.A., Tang M.-X., Siddiqui M., Shea, S., and Mayeux, R. (2004) Alcohol intake and risk of dementia, J. Am. Geriatr. Soc. 52, 540-546.
18. Mukamal, K.J., Kuller, L.H., Fitzpatrick, A.L., LongstrethW.T. Jr,Mittleman, M.A., and Siscovick, D.S. (2003) Prospective study of alcohol consumption and risk of dementia in older adults, J. Am. Med. Assoc. 289, 1405-1413.
19. Collins,M.A.,Neafsey, E.J.,Mukamal, K.J., Gray,M.O., Parks, D.A.,Das, D.K., and Korthuis, R.J. (2009) Alcoholism: alcohol in moderation, cardioprotection, and neuroprotection: epidemiological considerations and mechanistic studies, Clin. Exp. Res. 33, 206-219.
20. Maillard, M.-N., and Berset, C. (1995) Evolution of antioxidant activity during kilning: role of insoluble bound phenolic acids of barley and malt, J. Agric. Food Chem. 43, 1789-1793.
21. Montanari, L., Perretti, G., Natella, F., Guidi, A., and Fantozzi, P. (1999) Organic and phenolic acids in beer, Lebensm. Wiss. Technol. 32, 535-539.
22. Nardini, M., and Ghiselli, A. (2004) Determination of free and bound phenolic acids in beer, Food Chem. 84, 137-143.
23. Yabe, T., Hirahara, H., Harada, N., Ito, N., Nagai, T., Sanagi, T., and Yamada, H. (2010) Ferulic acid induces neural progenitor cell proliferation in vitro and in vivo, Neuroscience 165, 515-524.
24. Cheng,C.Y., Su, S.Y., Tang,N.Y., Ho, T.Y., Chiang, S.Y., and Hsieh,C.L. (2008) Ferulic acid provides neuroprotection against oxidative stress-related apoptosis after cerebral ischemia/reperfusion injury by inhibiting of ICAM-1 mRNA expression in rats, Brain Res. 13, 136-150.
25. Cho, J.Y., Kim, H.S., Kim, D.H., Yan J.J., Suh H.W., and Song, D.K. (2005) Inhibitory effects of long-term administration of ferulic acid on astrocyte activation induced by intracerebroventricular injection of beta-amyloid peptide (1-42) in mice, Prog. Neuro-Psychopharm. 29, 901-907.
26. Schroeter, H., Williams, R.J., Matin, R., Iversen, L., and Rice-Evans, C.A. (2000) Phenolic antioxidants attenuate neuronal cell death following uptake of oxidized low-density lipoprotein, Free Radical Biol. Med. 12, 1222-1233.
27. Kanski, J., Aksenova, M., Stoyanova, A., and Butterfield, D.A. (2002) Ferulic acid antioxidant protection against hydroxyl and peroxyl radical oxidation in synaptosomal and neuronal cell culture systems in vitro: structure-activity studies, J. Nutr. Biochem. 13, 273-281.
28. Zhang, Z., Wei, T., Hou, J., Li, G., Yu, S., and Xin, W. (2003) Iron-induced oxidative damage and apoptosis in cerebellar granule cells: attenuation by tetramethylpyrazine and ferulic acid, Eur. J. Pharmacol. 467, 41-47.
29. Mamiya, T., Kise, M., and Morikawa, K. (2008) Ferulic acid attenuated cognitive deficits and increase in carbonyl proteins induced by buthionine-sulfoximine in mice, Neurosci. Lett. 430, 115-118.
30. Hsieh, M.T., Tsai, F.H., Lin, Y.C., Wang, W.H., and Wu, C.R. (2002) Effects of ferulic acid on the impairment of inhibitory avoidance performance in rats, Planta Med. 68, 754-756.
31. Wenk, G.L., McGann-Gramling, K., Hauss-Wegrzyniak, B., Ronchetti, D., Maucci, R., Rosi, S., Gasparini L., and Ongini E. (2004) Attenuation of chronic neuroinflammation by a nitric oxide-releasing derivative of the antioxidant ferulic acid, J. Neurochem. 89, 484-493.
32. Ellman, G.L., Lourtney D.K., Andres V. and Gmelin, G. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity, Biochem. Pharmacol. 7, 88-95.
33. Rhee, I.K., van Rijn, R.M., and Verpoorte, R. (2003) Qualitative determination of false-positive effects in the acetylcholinesterase assay using thin layer chromatography, Phytochem. Anal. 14, 127-131.
34. Folin, O., and Ciocalteu, V. (1927) On tyrosine and tryptophane determination in proteins, J. Biol. Chem. 27, 627-650.
35. Nardini, M., Cirillo, E., Natella, F., Mencarelli, D., Comisso, A., and Scaccini, C. (2002) Detection of bound phenolic acids: prevention by ascorbic acid and ethylenediaminetetraacetic acid of degradation of phenolic acids during alkaline hydrolysis, Food Chem. 79, 119-124.
36. Floridi, S., Montanari, L., Marconi, O., and Fantozzi, P. (2003) Determination of free phenolic acids in wort and beer by coulometric array detection, J. Agric. Food Chem. 51, 1548-1554.
37. Szwajgier, D., Pielecki, J., and Targoński, Z. (2005) The release of ferulic acid and feruloylated oligosaccharides during wort and beer production, J. Inst. Brew. 111, 372-379.
38. Vanbeneden, N., Delvaux, F., and Delvaux, F.R. (2006) Determination of hydroxycinnamic acids and volatile phenols in wort and beer by isocratic high-performance liquid chromatography using electrochemical detection, J. Chromatogr. A 1136, 237-242.
39. Vanbeneden, N., Gils, F., Delvaux, F., and Delvaux, F.R. (2007) Variability in the release of free and bound hydroxycinnamic acids from diverse malted barley (Hordeum vulgare L.) cultivars during wort production, J. Agric. Food Chem. 55, 11002-11010.
40. Vanbeneden, N., Van Roey, T., Willems, F., Delvaux, F., and Delvaux, F.R. (2008) Release of phenolic flavour precursors during wort production: influence of process parameters and grist composition on ferulic acid release during brewing, Food Chem. 111, 83-91.
41. Savelev, S., Okello, E., Perry, N.S.L., Wilkins, R.M., and Perry, E.K. (2003) Synergistic and antagonistic interactions of anticholinesterase terpenoids in Salvia lavandulaefolia essential oil, Pharmacol. Biochem. Ber. 75, 661-668.
42. Howes, M.-J.R., Perry, N.S.L., and Houghton, P.J. (2003) Plants with traditional uses and activities relevant to the management of Alzheimer's disease and other cognitive disorders, Phytother. Res. 17, 1-18.
43. Wang, H., Zhou, G., Gao, X., Wang, Y., and Yao, W. (2007) Acetylcholinesterase inhibitory-active components of Rhodiola rosea L, Food Chem. 105, 24-27.
44. Miyazawa, M., Watanabe, H., and Kameoka, H. (1997) Inhibition of acetylcholinesterase activity by monoterpenoids with a p-menthane skeleton, J. Agric. Food Chem. 45, 677-679.
45. Yu, L., Haley, S., Perret, J., Harris, M., Wilson, J., and Qian, M. (2002) Free radical scavenging properties of wheat extracts, J. Agric. Food Chem. 50, 1619-1624.
46. Zhou, K., Yin, J.J., and Yu, L.L. (2005) Phenolic acid, tocopherol and carotenoid compositions, and antioxidant functions of hard red winter wheat bran, J. Agric. Food Chem. 53, 3916-3922.
47. Jang, J.-H., Kim, C.-Y., Lim, S.H., Yang, C.H., Song, K.-S., Han, H.S., Lee, H.-K., and Lee, J. (2010) Neuroprotective effects of Triticum aestivum L. (common wheat) against b-amyloid-induced cell death and memory impairments, Phytother. Res. 24, 76-84.
48. Cuvelier, M.E., Richard, H., and Berset, C. (1992) Comparison of the antioxidative activity of some acid-phenols: structure-activity relationship, Biosci. Biotechnol. Biochem. 56, 324-325.
49. Gerhäuser, C. (2005) Beer constituents as potential cancer chemopreventive agents, Eur. J. Cancer 41, 1941-1954.
50. Kikuzaki, H., Hisamoto, M., Hirose, K., Akiyama, K., and Taniguchi, H. (2002) Antioxidant properties of ferulic acid and its related compounds, J. Agric. Food Chem. 50, 2161-2168.
51. Maillard, M.N., Soum, M.H., Boivin, P., and Berset, C. (1996) Antioxidant activity of barley and malt: relationship with phenolic content, Lebensm. Wiss. Technol. 29, 238-244.
52. Nardini, M., D'Aquino, M., Tomassi, G., Gentili, V., Di Felice, M., and Scaccini, C. (1995) Inhibition of human low-density lipoprotein oxidation by caffeic acid and other hydrocinnamic acid derivatives, Free Rad. Biol. Med. 19, 541-552.
53. Itagaki, S., Kurokawa, T., Nakata, C., Saito, Y., Oikawa, S., Kobayashi, M., Hirano, T., and Iseki, K. (2009) In vitro and in vivo antioxidant properties of ferulic acid: A comparative study with other natural oxidation inhibitors, Food Chem. 114, 466-471.
54. 2: insight into mechanisms of neuroprotection and relevance to oxidative stress-related neurodegenerative disorders, Neurochem. Int. 48, 318-327.
55. Liu, Q., and Yao, H. (2007) Antioxidant activities of barley seeds extracts, Food Chem. 12, 732-737.
56. Saija, A., Tomaino, A., Trombetta, D., De Pasquale, A., Uccella, N., Barbuzzi, T., Paolino, D., and Bonina, F. (2000) In vitro and in vivo evaluation of caffeic and ferulic acids as topical photoprotective agents, Int. J. Pharm. 199, 39-47.
57. Fantozzi, P., Montanari, F., Gasbarrini, A., Addolorato, G., Simoncini, M., Nardini, M., Ghiselli, A., and Scaccini, C. (1998) In vitro antioxidant capacity from wort to beer, Lebensm. Wiss. Technol. 31, 221-227.
58. Goupy, P., Hugues, M., Boivin, P., and Amiot, M.J. (1999) Antioxidant composition and activity of barley (Hordeum vulgare) and malt extracts and of isolated phenolic compounds, J. Sci. Food Agric. 79, 1625-1634.
59. Inns, E.L., Buggey, L.A., Booer, C., Nursten, H.E., and Ames, J. (2007) Effect of heat treatment on the antioxidant activity, color, and free phenolic acid profile of malt, J. Agric. Food Chem. 55, 6539-6546.
60. Kim, H.S., Cho, J.Y., Kim, D.H., Yan, J.J., Lee, H.K., Suh, H.W., and Song, D.K. (2004) Inhibitory effects of long-term administration of ferulic acid on microgial activation induced by intracerebroventricular injection of beta-amyloid peptide (1-42) in mice, Biol. Pharm. Bull. 27, 120-121.
61. Yan, J.-J., Cho, J.-Y., Kim, H.-S., Kim, K.-L., Jung, J.-S., Huh, S.-O., Suh, H.-W., Kim, Y.-H., and Song, D.-K. (2001) Protection against b-amyloid peptide toxicity in vivo with long-term administration of ferulic acid, Br. J. Pharmacol. 133, 89-96.
62. Kim, M.J., Choi, S.J., Lim, S.-T., Kim, H.K., Heo, H.J., Kim, E.-K., Jun, W.-J., Cho, H.Y., Kim, Y.J., and Shin, D.H. (2007) Ferulic acid supplementation prevents trimethyltin-induced cognitive deficits in mice, Biosci. Biotechnol. Biochem. 71, 1063-1068.
63. Ho, C.C., Kumaran, A., and Sun Hwang, L. (2009) Bio-assay guided isolation and identification of anti-Alzheimer active compounds from the root of Angelica sinensis, Food Chem. 114, 246-252.
64. Sultana, R. Ravagna, A., Mohmmad-Abdul, H., Calabrese, V., and Butterfield, D.A. (2005) Ferulic acid ethyl ester protects neurons against amyloid beta-peptide(1-42)-induced oxidative stress and neurotoxicity: relationship to antioxidant activity, J. Neurochem. 92, 749-758.
65. Mohmmad Abdul, H., and Butterfield, D.A. (2005) Protection against amyloid beta-peptide (1-42)-induced loss of phospholipids asymmetry in synaptosomal membranes by tricyclodecan-9-xanthogenate (D609) and ferulic acid ethyl ester: implications for Alzheimer's disease, Biochim. Biophys. Acta 1741, 140-148.
66. Jin, Y., Yan, E.-Z., Fan, Y., Zong, Z.-H., Qi, Z.-M., and Li, Z. (2005) Sodium ferulate prevents amyloid-beta-induced neurotoxicity through suppression of p38 MAPK and upregulation of ERK-1/2 and Akt/protein kinase B in rat hippocampus, Acta Pharmacol. Sin. 26, 943-951.
67. Jin, Y., Fan, Y., Yan, E.-Z., Liu, Z., Zong, Z.-H., and Qi, Z.-M. (2006) Effects of sodium ferulate on amyloid-beta-induced MKK3/MKK6-p38 MAPK-Hsp27 signal pathway and apoptosis in rat hippocampus, Acta Pharmacol. Sin. 27, 1309-1316.
68. Jin, Y., Yan, E.-Z., Li, X.-M., Fan, Y., Zhao, Y.-J., Liu, Z., and Liu, W.-Z. (2008) Neuroprotective effect of sodium ferulate and signal transduction mechanisms in the aged rat hippocampus, Acta Pharmacol. Sin. 29, 1399-1408.
69. Karakida, F., Ikeya, Y., Tsunakawa, M., Yamaguchi, T., Ikarashi, Y., Takeda, S., and Aburada,M. (2007) Cerebral protective and cognition-improving effects of sinapic acid in rodents, Biol. Pharm. Bull. 30, 514-519.
70. Scapagnini, G., Foresti, R., Calabrese, V., Giuffrida Stella, A.M., Green, C.J., and Motterlini, R. (2002) Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers, Mol. Pharmacol. 3, 554-561.
71. Bourne, L.C., and Rice-Evans, C. (1998) Bioavailability of ferulic acid, Biochem. Biophys. Res. Commun. 253, 222-227.
72. Ghiselli, A., Natella, F., Guidi, A., Montanari, L., Fantozzi, P., and Scaccini, C. (2000) Beer increases plasma antioxidant capacity in humans, J. Nutr. Biochem. 11, 76-80.
73. Nardini, M., Natella, F., Scaccini, C., and Ghiselli, A. (2006) Phenolic acids from beer are absorbed and extensively metabolized in humans, J. Nutr. Biochem. 17, 14-22.
74. Hollman, P.C., and Katan, M.B. (1998) Bioavailability and health effects of dietary flavonols in man, Arch. Toxicol. 20, 237-248.
75. Nardini, M., Cirillo, E., Natella, F., and Scaccini, C. (2002) Absorption of phenolic acids in humans after coffee consumption, J. Agric. Food Chem. 50, 5735-5741.
76. Nardini, M., Natella, F., Gentili, V., Di Felice, M., and Scaccini, C. (1997) Effect of caffeic acid dietary supplementation on the antioxidant defense system in rat: an in vivo study, Arch. Biochem. Biophys. 342, 157-160.
77. Olthof, M.R., Hollman, P.C., Bujisman, M.N., Van Amelsvoort, J.M., and Katan, M.B. (2003) Chlorogenic acid, quercetin-3-rutinoside and black tea phenols are extensively metabolised in humans, J. Nutr. 133, 1806-1814.
78. Plumb, G.W., Garcia-Conesa, M.T., Kroon, P.A., Rhodes,M., Ridley, S., and Williamson, G. (1999) Metabolism of chlorogenic acid by human plasma, liver, intestine and gut microflora, J. Sci. Food Agric. 79, 390-392.
79. Rechner, A.R., Kuhnle, G., Bremner, P., and Hubbard, G.P. (2002) The metabolic fate of dietary polyphenols in humans, Free Radical Biol. Med. 33, 220-235.
80. Rechner, A.R., Pannala, A.S., and Rice-Evans, C.A. (2001) Caffeic acid derivatives in artichoke extract are metabolized to phenolic acids in vivo, Free Radical Res. 35, 195-202.
81. Rondini, L., Peyrat-Maillard, M.N., Marsset-Baglieri, A., and Berset, C. (2002) Sulfated ferulic acid is the main in vivo metabolite found after short-term ingestion of free ferulic acid in rats, J. Agric. Food Chem. 50, 3037-3041.
82. Couteau, D., McCartney, A.L., Gibson, G.R., Williamson, G., and Faulds, C.B. (2001) Isolation and characterization of human colonic bacteria able to hydrolyze chlorogenic acid, J. Appl. Microbiol. 90, 873-881.
83. Clifford, M.N., Copeland, E.L., Bloxsidge, J.P., and Mitchell, L.A. (2000) Hippuric acid as a major excretion product associated with black tea consumption, Xenobiotica 50, 317-326.
84. Rechner, A.R., Spencer, J.P.E., Kuhnle, G., Hahn, U., and Rice-Evans, C.A. (2001) Novel biomarkers of the bioavailability and metabolism of caffeic acid derivatives in humans, Free Radical Biol. Med. 30, 1213-1222.
85. Gross, M., Pfeiffer, M., Martini, M., Campbell, D., Slavin, J., and Potter, J. (1996) The quantitation of metabolites of quercetin flavonols in human urine, Cancer Epidemiol. Biomarkers Prev. 5, 711-720.