Neuroprotective effects of digested polyphenols from wild blackberry species

European Journal of Nutrition

Volumn 52, Issue 1, 2013, Pages 225-236

  Tavares, Lucélia ^a   Figueira, Inês ^a   McDougall, Gordon J ^b   Vieira, Helena L A ^a,c,d   Stewart, Derek ^b,e   Alves, Paula M ^a,c   Ferreira, Ricardo B ^a,f   Santos, Cláudia N ^a,c  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c INSTITUTO DE BIOLOGIA EXPERIMENTAL E TECNOLÓGICA   (Portugal)

^d NOVA MEDICAL SCHOOL   (Portugal)

^e HERIOT WATT UNIVERSITY   (United Kingdom)

^f INSTITUTO SUPERIOR DE AGRONOMIA   (Portugal)

Author keywords

Caspase activity; Glutathione balance; In vitro digestion; Neurodegenerative diseases; Wild blackberries

Indexed keywords

CASPASE 3; CASPASE 7; GLUTATHIONE; PLANT EXTRACT; POLYPHENOL DERIVATIVE; REACTIVE OXYGEN METABOLITE; RUBUS BRIGANTINUS EXTRACT; RUBUS VAGABUNDUS EXTRACT; UNCLASSIFIED DRUG;

ARTICLE; BLACKBERRY; CELL LEVEL; CHEMICAL COMPOSITION; CONTROLLED STUDY; DIGESTION; ENZYME ACTIVATION; FOOD INTAKE; HUMAN; HUMAN CELL; IN VITRO DIGESTION; METABOLITE; MODEL; MODULATION; MOLECULAR MECHANICS; NEUROBLASTOMA CELL; NEUROPROTECTION; RUBUS BRIGANTINUS; RUBUS VAGABUNDUS;

APOPTOSIS; CASPASE 3; CASPASE 7; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; FRUIT; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; MASS SPECTROMETRY; NEUROPROTECTIVE AGENTS; PHYSICOCHEMICAL PHENOMENA; PLANT EXTRACTS; POLYPHENOLS; REACTIVE OXYGEN SPECIES; ROSACEAE;

RUBUS; RUBUS MOLUCCANUS;

EID: 84872713036     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-012-0307-7     Document Type: Article

References (59)

1. Lau FC, Shukitt-Hale B, Joseph JA (2006) Beneficial effects of berry fruit polyphenols on neuronal and behavioral aging. J Agric Food Chem 86:2251-2255 (Pubitemid 44690143)
2. Beking K, Vieira A (2010) Flavonoid intake and disability-adjusted life years due to Alzheimer's and related dementias: a population-based study involving twenty-three developed countries. Public Health Nutr 13:1403-1409
3. Wimo A, Jonsson L, Gustavsson A, McDaid D, Ersek K, Georges J, Gulacsi L, Karpati K, Kenigsberg P, Valtonen H (2011) The economic impact of dementia in Europe in 2008-cost estimates from the Eurocode project. Int J Geriatr Psychiatry 26:825-832
4. Maiese K, Chong ZZ, Hou J, Shang YC (2009) New strategies for Alzheimer's disease and cognitive impairment. Oxid Med Cell Longev 2:279-289
5. Dumont M, Beal MF (2011) Neuroprotective strategies involving ROS in Alzheimer disease. Free Radic Biol Med 51:1014-1026
6. Williams P, Sorribas A, Howes MJR (2011) Natural products as a source of Alzheimer's drug leads. Nat Prod Rep 28:48-77
7. de Rijk MC, Breteler MM, den Breeijen JH, Launer LJ, Grobbee DE, van der Meche FG, Hofman A (1997) Dietary antioxidants and Parkinson disease. The Rotterdam study. Arch Neurol 54:762-765
8. Di Matteo V, Esposito E (2003) Biochemical and therapeutic effects of antioxidants in the treatment of Alzheimer's disease, Parkinson's disease, and amyotrophic lateral sclerosis. Curr Drug Targets CNS Neurol Disord 2:95-107
9. Dai Q, Borenstein AR, Wu Y, Jackson JC, Larson EB (2006) Fruit and vegetable juices and Alzheimer's disease: the Kame project. Am J Med 119:751-759 (Pubitemid 44308471)
10. Seeram NP (2008) Berry fruits: compositional elements, biochemical activities, and the impact of their intake on human health, performance, and disease. J Agric Food Chem 56:627-629 (Pubitemid 351300222)
11. Shukitt-Hale B, Lau FC, Joseph JA (2008) Berry fruit supplementation and the aging brain. J Agric Food Chem 56:636-641 (Pubitemid 351300224)
12. Dai J, Patel JD, Mumper RJ (2007) Characterization of blackberry extract and its antiproliferative and anti-inflammatory properties. J Med Food 10:258-265 (Pubitemid 47105670)
13. Wang SY, Jiao H (2000) Scavenging capacity of berry crops on superoxide radicals, hydrogen peroxide, hydroxyl radicals, and singlet oxygen. J Agric Food Chem 48:5677-5684
14. Shukitt-Hale B, Cheng V, Joseph JA (2009) Effects of blackberries on motor and cognitive function in aged rats. Nutr Neurosci 12:135-140
15. Joseph JA, Kowatch MA, Maki T, Roth GS (1990) Selective cross-activation/inhibition of second messenger systems and the reduction of age-related deficits in the muscarinic control of dopamine release from perifused rat striata. Brain Res 537:40-48
16. Rutz S, Majchrzak M, Siedschlag V, Barbelivien A, Harati H, Rothmaier AK, Feuerstein TJ, Jackisch R, Cassel JC (2009) The modulation of striatal dopamine release correlates with water-maze performance in aged rats. Neurobiol Aging 30:957-972
17. Ramassamy C (2006) Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. Eur J Pharmacol 545:51-64
18. Castroviejo S (ed) (1986-2007) Flora Ibérica. Plantas vasculares de la Península Ibérica e Islas Baleares. Real Jardín Botánico, CSIC, Madrid
19. Tavares L, Fortalezas S, Carrilho C, McDougall GJ, Stewart D, Ferreira RB, Santos CN (2010) Antioxidant and antiproliferative properties of strawberry tree tissues. J Berry Res 1:3-12
20. Tavares L, Figueira I, Macedo D, McDougall GJ, Leitão MC, Vieira HLA, Stewart D, Alves PM, Ferreira RB, Santos CN (2012) Neuroprotective effect of blackberry (Rubus sp.) polyphenols is potentiated after simulated gastrointestinal digestion. Food Chem 131:1443-1452
21. Tavares L, Carrilho D, Tyagi M, Barata D, Serra AT, Duarte CMM, Duarte RO, Feliciano RP, Bronze MR, Chicau P, Espírito-Santo MD, Ferreira RB, dos Santos CN (2010) Antioxidant capacity of Macaronesian traditional medicinal plants. Molecules 15:2576-2592
22. Queiroga CS, Almeida AS, Martel C, Brenner C, Alves PM, Vieira HL (2010) Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis. J Biol Chem 285:17077-17088
23. Wang H, Joseph JA (1999) Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 27:612-616 (Pubitemid 29408648)
24. Wolfe KL, Liu RH (2007) Cellular antioxidant activity (CAA) assay for assessing antioxidants, foods, and dietary supplements. J Agric Food Chem 55:8896-8907 (Pubitemid 350105534)
25. Kand'ar R, Zakova P, Lotkova H, Kucera O, Cervinkova Z (2007) Determination of reduced and oxidized glutathione in biological samples using liquid chromatography with fluorimetric detection. J Pharm Biomed Anal 43:1382-1387 (Pubitemid 46282398)
26. Bensadoun A, Weinstein D (1976) Assay of proteins in the presence of interfering materials. Anal Biochem 70:241-250
27. Wolfe KL, Kang X, He X, Dong M, Zhang Q, Liu RH (2008) Cellular antioxidant activity of common fruits. J Agric Food Chem 56:8418-8426
28. McDougall GJ, Fyffe S, Dobson P, Stewart D (2005) Anthocyanins from red wine-their stability under simulated gastrointestinal digestion. Phytochemistry 66:2540-2548 (Pubitemid 41562285)
29. McDougall GJ, Fyffe S, Dobson P, Stewart D (2007) Anthocyanins from red cabbage-stability to simulated gastrointestinal digestion. Phytochemistry 68:1285-1294 (Pubitemid 46602458)
30. Perez-Vicente A, Gil-Izquierdo A, Garcia-Viguera C (2002) In vitro gastrointestinal digestion study of pomegranate juice phenolic compounds, anthocyanins, and vitamin C. J Agric Food Chem 50:2308-2312 (Pubitemid 34275303)
31. Gil-Izquierdo A, Gil MI, Ferreres F (2002) Effect of processing techniques at industrial scale on orange juice antioxidant and beneficial health compounds. J Agric Food Chem 50:5107-5114 (Pubitemid 34925098)
32. Deaville ER, Green RJ, Mueller-Harvey I, Willoughby I, Frazier RA (2007) Hydrolyzable tannin structures influence relative globular and random coil protein binding strengths. J Agric Food Chem 55:4554-4561 (Pubitemid 46932655)
33. Mertz C, Cheynier V, Gunata Z, Brat P (2007) Analysis of phenolic compounds in two blackberry species (Rubus glaucus and Rubus adenotrichus) by high-performance liquid chromatography with diode array detection and electrospray ion trap mass spectrometry. J Agric Food Chem 55:8616-8624 (Pubitemid 350013107)
34. Mullen W, Yokota T, Lean MEJ, Crozier A (2003) Analysis of ellagitannins and conjugates of ellagic acid and quercetin in raspberry fruits by LC-MSn. Phytochemistry 64:617-624 (Pubitemid 37168986)
35. Ayoub NA (2010) A trimethoxyellagic acid glucuronide from Conocarpus erectus leaves: isolation, characterization and assay of antioxidant capacity. Pharm Biol 48:328-332
36. Manach C, Williamson G, Morand C, Scalbert A, Remesy C (2005) Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr 81:230S-242S
37. Jung KA, Kwak MK (2010) The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 15:7266-7291
38. Lee C, Park GH, Kim CY, Jang JH (2011) [6]-Gingerol attenuates beta-amyloid-induced oxidative cell death via fortifying cellular antioxidant defense system. Food Chem Toxicol 49:1261-1269
39. Lu YH, Su MY, Huang HY, Lin L, Yuan CG (2010) Protective effects of the citrus flavanones to PC12 cells against cytotoxicity induced by hydrogen peroxide. Neurosci Lett 484:6-11
40. Pavlica S, Gebhardt R (2010) Protective effects of flavonoids and two metabolites against oxidative stress in neuronal PC12 cells. Life Sci 86:79-86
41. Ballatori N, Krance SM, Notenboom S, Shi S, Tieu K, Hammond CL (2009) Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 390:191-214
42. Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radic Biol Med 43:883-898 (Pubitemid 47223636)
43. Artal-Sanz M, Tavernarakis N (2005) Proteolytic mechanisms in necrotic cell death and neurodegeneration. FEBS Lett 579:3287-3296 (Pubitemid 40804676)
44. Spencer JP, Schroeter H, Kuhnle G, Srai SK, Tyrrell RM, Hahn U, Rice-Evans C (2001) Epicatechin and its in vivo metabolite, 3′-O-methyl epicatechin, protect human fibroblasts from oxidative-stress-induced cell death involving caspase-3 activation. Biochem J 354:493-500 (Pubitemid 32269712)
45. Garnier P, Ying W, Swanson RA (2003) Ischemic preconditioning by caspase cleavage of poly(ADP-ribose) polymerase-1. J Neurosci 23:7967-7973 (Pubitemid 37082448)
46. McLaughlin B, Hartnett KA, Erhardt JA, Legos JJ, White RF, Barone FC, Aizenman E (2003) Caspase 3 activation is essential for neuroprotection in preconditioning. Proc Natl Acad Sci USA 100:715-720 (Pubitemid 36126118)
47. Tanaka H, Yokota H, Jover T, Cappuccio I, Calderone A, Simionescu M, Bennett MV, Zukin RS (2004) Ischemic preconditioning: neuronal survival in the face of caspase-3 activation. J Neurosci 24:2750-2759 (Pubitemid 38380952)
48. Mandel S, Amit T, Reznichenko L, Weinreb O, Youdim MB (2006) Green tea catechins as brain-permeable, natural iron chelators-antioxidants for the treatment of neurodegenerative disorders. Mol Nutr Food Res 50:229-234 (Pubitemid 43325663)
49. Andres-Lacueva C, Shukitt-Hale B, Galli RL, Jauregui O, Lamuela-Raventos RM, Joseph JA (2005) Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr Neurosci 8:111-120 (Pubitemid 40959652)
50. Kalt W, Blumberg JB, McDonald JE, Vinqvist-Tymchuk MR, Fillmore SAE, Graf BA, O'Leary JM, Milbury PE (2008) Identification of anthocyanins in the liver, eye, and brain of blueberry-fed pigs. J Agric Food Chem 56:705-712 (Pubitemid 351300234)
51. Mullen W, Larcombe S, Arnold K, Welchman H, Crozier A (2009) Use of accurate mass full scan mass spectrometry for the analysis of anthocyanins in berries and berry-fed tissues. J Agric Food Chem 58:3910-3915
52. Milbury PE, Kalt W (2010) Xenobiotic metabolism and berry flavonoid transport across the blood-brain barrier. J Agric Food Chem 58:3950-3956
53. Son TG, Camandola S, Mattson MP (2008) Hormetic dietary phytochemicals. Neuromolecular Med 10:236-246
54. Cho MJ, Howard LR, Prior RL, Clark JR (2004) Flavonoid glycosides and antioxidant capacity of various blackberry, blueberry and red grape genotypes determined by high-performance liquid chromatography/mass spectrometry. J Sci Food Agric 84:1771-1782 (Pubitemid 39270702)
55. Jordheim M, Enerstvedt KH, Andersen OM (2011) Identification of cyanidin 3-O-beta-(6″-(3-Hydroxy-3-methylglutaroyl)glucoside) and other anthocyanins from wild and cultivated blackberries. J Agric Food Chem 59:7436-7440
56. Gasperotti M, Masuero D, Vrhovsek U, Guella G, Mattivi F (2010) Profiling and accurate quantification of Rubus ellagitannins and ellagic acid conjugates using direct UPLC-Q-TOF HDMS and HPLC-DAD analysis. J Agric Food Chem 58:4602-4616
57. Kool MM, Comeskey DJ, Cooney JM, McGhie TK (2010) Structural identification of the main ellagitannins of a boysenberry (Rubus loganbaccus × baileyanus Britt.) extract by LC-ESI-MS/MS,MALDI-TOF-MS and NMR spectroscopy. Food Chem 119:1535-1543
58. Cho MJ, Howard LR, Prior RL, Clark JR (2005) Flavonol glycosides and antioxidant capacity of various blackberry and blueberry genotypes determined by high-performance liquid chromatography/mass spectrometry. J Sci Food Agric 85:2149-2158 (Pubitemid 41426309)
59. Hager TJ, Howard LR, Liyanage R, Lay JO, Prior RL (2008) Ellagitannin composition of blackberry as determined by HPLC-ESI-MS and MALDI-TOF-MS. J Agric Food Chem 56:661-669 (Pubitemid 351300228)