Enhanced antioxidant activity for apple juice fermented with lactobacillus plantarum ATCC14917

Molecules

Volumn 24, Issue 1, 2019, Pages

  Li, Zhongxi ^a,b   Teng, Jing ^a,b   Lyu, Yilu ^c   Hu, Xiaoqian ^a,b   Zhao, Yueliang ^a,b   Wang, Mingfu ^a,b,d  

^a SHANGHAI OCEAN UNIVERSITY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c Changle No 2 Middle School   (China)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Antioxidant activity; Apple phenolics; Lactobacillus plantarum ATCC14917 fermentation; LC MS MS

Indexed keywords

1,1-DIPHENYL-2-PICRYLHYDRAZYL; 2,2'-AZINO-DI-(3-ETHYLBENZOTHIAZOLINE)-6-SULFONIC ACID; ANTIOXIDANT; BENZOTHIAZOLE DERIVATIVE; BIPHENYL DERIVATIVE; FLAVONOID; FRUCTOSE; GLUCOSE; PHENOL DERIVATIVE; PICRIC ACID; SCAVENGER; SULFONIC ACID DERIVATIVE;

ANIMAL; CELL SURVIVAL; CHEMISTRY; DRUG EFFECT; FERMENTATION; FRUIT AND VEGETABLE JUICE; LACTOBACILLUS PLANTARUM; MALUS; METABOLISM; MOUSE; PH; RAW 264.7 CELL LINE;

ANIMALS; ANTIOXIDANTS; BENZOTHIAZOLES; BIPHENYL COMPOUNDS; CELL SURVIVAL; FERMENTATION; FLAVONOIDS; FREE RADICAL SCAVENGERS; FRUCTOSE; FRUIT AND VEGETABLE JUICES; GLUCOSE; HYDROGEN-ION CONCENTRATION; LACTOBACILLUS PLANTARUM; MALUS; MICE; PHENOLS; PICRATES; RAW 264.7 CELLS; SULFONIC ACIDS;

EID: 85059228854     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules24010051     Document Type: Article

References (55)

1. Liaudanskas, M.; Viškelis, P.; Jakštas, V.; Raudonis, R.; Kviklys, D.; Milašius, A.; Janulis, V. Application of an Optimized HPLC Method for the Detection of Various Phenolic Compounds in Apples from Lithuanian Cultivars. J. Chem. 2014, 2014. [CrossRef]
2. Kelly,W.;Wu, X.; Liu, R.H. Antioxidant activity of apple peels. J. Agric. Food Chem. 2003, 51, 609-614.
3. Wojdyo, A.; Oszmiá nski, J.; Laskowski, P. Polyphenolic Compounds and Antioxidant Activity of New and Old Apple Varieties. J. Agric. Food Chem. 2008, 56, 6520-6530. [CrossRef] [PubMed]
4. Fevrier, H.; Le Quere, J.; Le Bail, G.; Guyot, S. Polyphenol profile, PPO activity and pH variation in relation to colour changes in a series of red-fleshed apple juices. LWT-Food Sci. Technol. 2017, 85, 353-362. [CrossRef]
5. Eberhardt, M.V.; Lee, C.Y.; Liu, R.H. Antioxidant activity of fresh apples. NATURE 2000, 405, 903-904. [CrossRef]
6. Thilakarathna, S.H.; Rupasinghe, H.P.V.; Needs, P.W. Apple peel bioactive rich extracts effectively inhibit in vitro human LDL cholesterol oxidation. Food Chem. 2013, 138, 463-470. [CrossRef] [PubMed]
7. Bao, M.; Shen, J.; Jia, Y.; Li, F.; Ma, W.; Shen, H.; Shen, L.; Lin, X.; Zhang, L.; Dong, X. Apple polyphenol protects against cigarette smoke-induced acute lung injury. Nutrition 2013, 29, 235-243. [CrossRef]
8. Francini, A.; Sebastiani, L. Phenolic Compounds in Apple (Malus x domestica Borkh.): Compounds Characterization and Stability during Postharvest and after Processing. Antioxidants 2013, 2, 181-193. [CrossRef]
9. van Duynhoven, J.; Vaughan, E.E.; Jacobs, D.M.; Kemperman, R.A.; van Velzen, E.J.J.; Gross, G.; Roger, L.C.; Possemiers, S.; Smilde, A.K.; Doré, J.; et al. Metabolic fate of polyphenols in the human superorganism. Proc. Natl. Acad. Sci. USA 2011, 108, 4531-4538. [CrossRef]
10. DuPont, M.S.; Bennett, R.N.; Mellon, F.A.; Williamson, G. Polyphenols from Alcoholic Apple Cider Are Absorbed, Metabolized and Excreted by Humans. Nutrition 2002, 132, 172-175. [CrossRef]
11. Borges, G.; Lean, M.E.J.; Roberts, S.A.; Crozier, A. Bioavailability of dietary (poly)phenols: A study with ileostomists to discriminate between absorption in small and large intestine. Food and Funct. 2013, 2013, 754-762. [CrossRef] [PubMed]
12. Wu, X.; Pittman, H.E.; Prior, R.L. Fate of anthocyanins and antioxidant capacity in contents of the gastrointestinal tract of weanling pigs following black raspberry consumption. J. Agric. Food Chem. 2006, 54. [CrossRef] [PubMed]
13. Perez-Jimenez, J.; Diaz-Rubio, M.; Saura-Calixto, F. Non-extractable polyphenols, a major dietary antioxidant: Occurrence, metabolic fate and health effects. Nutr. Res. Rev. 2013, 26, 118-129. [CrossRef] [PubMed]
14. Hervert-Hernandez, D.; Goni, I. Dietary Polyphenols and Human Gut Microbiota: A Review. Food Rev. Int. 2011, 27, 154-169. [CrossRef]
15. Avila, M.; Hidalgo, M.; Sánchez-Moreno, C.; Pelaez, C.; Requena, T.; Pascual-Teresa, S. De Bioconversion of anthocyanin glycosides by Bifidobacteria and Lactobacillus. Food Res. Int. 2009, 42, 1453-1461. [CrossRef]
16. Fritsch, C.; Jänsch, A.; Ehrmann, M.A.; Toelstede, S.; Vogel, R.F. Characterization of Cinnamoyl Esterases from Different Lactobacilli and Bifidobacteria. Curr. Microbiol. 2017, 74, 247-256. [CrossRef] [PubMed]
17. Esteban-Torres, M.; Reverón, I.; Mancheño, J.M.; de las Rivas, B.; Muñoz, R. Characterization of a Feruloyl Esterase from Lactobacillus plantarum. Appl. Environ. Microb. 2013, 79, 5130-5136. [CrossRef] [PubMed]
18. Sánchez-Patán, F.; Tabasco, R.; Monagas, M.; Requena, T.; Peláez, C.; Moreno-Arribas, M.V.; Bartolomé, B. Capability of Lactobacillus plantarum IFPL935 To Catabolize Flavan-3-ol Compounds and Complex Phenolic Extracts. J. Agric. Food Chem. 2012, 60, 7142-7151. [CrossRef]
19. Rodriguez, H.; Curiel, J.A.; Landete, J.M.; de las Rivas, B.; López de Felipe, F.; Gomez-Cordoves, C.; Mancheno, J.M.; Munoz, R. Food phenolics and lactic acid bacteria. Int. J. Food Microbio. 2009, 132, 79-90. [CrossRef]
20. Rossi, M.; Amaretti, A.; Leonardi, A.; Raimondi, S.; Simone, M.; Quartieri, A. Potential Impact of Probiotic Consumption on the Bioactivity of Dietary Phytochemicals. J. Agric. Food Chem. 2013, 61, 9551-9558. [CrossRef]
21. Pereira-Caro, G.; Oliver, C.M.; Weerakkody, R.; Singh, T.; Conlon, M.; Borges, G.; Sanguansri, L.; Lockett, T.; Roberts, S.A.; Crozier, A. Chronic administration of a microencapsulated probiotic enhances the bioavailability of orange juice flavanones in humans. Free Radical Biol. Med. 2015, 84, 206-214. [CrossRef] [PubMed]
22. Chiou, Y.; Wu, J.; Huang, Q.; Shahidi, F.; Wang, Y.; Ho, C.; Pan, M. Metabolic and colonic microbiota transformation may enhance the bioactivities of dietary polyphenols. J. Funct. Foods 2014, 7, 3-25. [CrossRef]
23. Zhao, D.; Shah, N. Antiradical and tea polyphenol-stabilizing ability of functional fermented soymilk-tea beverage. Food Chem. 2014, 158, 262-269. [CrossRef] [PubMed]
24. Zhao, D.; Shah, N. Lactic acid bacterial fermentation modified phenolic composition in tea extracts and enhanced their antioxidant activity and cellular uptake of phenolic compounds following in vitro digestion. J. Func. Foods 2016, 20, 182-194. [CrossRef]
25. Mukerji, P.; Roper, J.M.; Stahl, B.; Smith, A.B.; Burns, F.; Rae, J.C.; Yeung, N.; Lyra, A.; Svärd, L.; Saarinen, M.T.; et al. Safety evaluation of AB-LIFE®(Lactobacillus plantarum CECT 7527, 7528 and 7529): Antibiotic resistance and 90-day repeated-dose study in rats. Food Chem. Toxicol. 2016, 92, 117-128. [CrossRef] [PubMed]
26. Valero-Cases, E.; Nuncio-Jáuregui, N.; Frutos, M.J. Influence of Fermentation with Different Lactic Acid Bacteria and in Vitro Digestion on the Biotransformation of Phenolic Compounds in Fermented Pomegranate Juices. J. Agric. Food Chem. 2017, 65, 6488-6496. [CrossRef]
27. Fessard, A.; Kapoor, A.; Patche, J.; Assemat, S.; Hoarau, M.; Bourdon, E.; Bahorun, T.; Remize, F. Lactic fermentation as an efficient tool to enhance the antioxidant activity of tropical fruit juices and teas. Microorganisms 2017, 5, 23. [CrossRef]
28. Yang, J.; Ji, Y.; Park, H.; Lee, J.; Park, S.; Yeo, S.; Shin, H.; Holzapfel,W.H. Selection of functional lactic acid bacteria as starter cultures for the fermentation of Korean leek (Allium tuberosum Rottler ex Sprengel.). Int. J. Food Microbiol. 2014, 191, 164-171. [CrossRef] [PubMed]
29. Filannino, P.; Cavoski, I.; Thlien, N.; Vincentini, O.; De Angelis, M.; Silano, M.; Gobbetti, M.; Di Cagno, R. Lactic acid fermentation of cactus cladodes (Opuntia ficus-indica L.) generates flavonoid derivatives with antioxidant and anti-inflammatory properties. PLoS ONE 2016, 11.
30. Mousavi, Z.E.; Mousavi, S.M.; Razavi, S.H.; Emam-Djomeh, Z.; Kiani, H. Fermentation of pomegranate juice by probiotic lactic acid bacteria. World J. Microbiol. Biotechnol. 2010, 27, 123-128. [CrossRef]
31. Kandler, O.; Weiss, N. Genus lactobacillus. In Bergey's Manual of Systematic Bacteriology; Holt, J.G., Ed.; Williams and Wilkins: Baltimore, MD, USA, 1986; Volume 2, p. 1219.
32. Kaprasob, R.; Kerdchoechuen, O.; Laohakunjit, N.; Sarkar, D.; Shetty, K. Fermentation-based biotransformation of bioactive phenolics and volatile compounds from cashew apple juice by select lactic acid bacteria. Process Biochem. 2017, 59, 141-149. [CrossRef]
33. Espirito-Santo, A.P.; Carlin, F.; Renard, C.M.G.C. Apple, grape or orange juice: Which one offers the best substrate for lactobacilli growth?-A screening study on bacteria viability, superoxide dismutase activity, folates production and hedonic characteristics. Food Res. Int. 2015, 78, 352-360. [CrossRef] [PubMed]
34. Senanayake, S.P.J.N. Green tea extract: Chemistry, antioxidant properties and food applications-A review. J. Funct. Foods 2013, 5, 1529-1541. [CrossRef]
35. Gan, R.; Shah, N.;Wang, M.; Lui,W.; Corke, H. Fermentation alters antioxidant capacity and polyphenol distribution in selected edible legumes. Int. J. Food Sci. Technol. 2016, 51, 875-884. [CrossRef]
36. Kwaw, E.; Ma, Y.; Tchabo,W. Effect of lactobacillus strains on phenolic profile, color attributes and antioxidant activities of lactic-acid-fermented mulberry juice. Food Chem. 2018, 250, 148-154. [CrossRef] [PubMed]
37. Hashemi, S.M.B.; Mahmoodi, M. Fermentation of Barberry Juice to Produce Probiotic Beverage. Curr. Nutr. Food Sci. 2017, 13, 204-211.
38. Othman, N.B.; Roblain, D.; Chammen, N.; Thonart, P.; Hamdi, M. Antioxidant phenolic compounds loss during the fermentation of Chétoui olives. Food Chem. 2009, 116, 662-669. [CrossRef]
39. Mousavia, Z.E.; Mousavia, S.M.; Razavia, S.H.; Hadinejada, M.; Emam-Djomeha, Z.; Mirzapoura, M. Effect of Fermentation of Pomegranate Juice by Lactobacillus plantarum and Lactobacillus acidophilus on the Antioxidant Activity and Metabolism of Sugars, Organic Acids and Phenolic Compounds. Food Biotechnol. 2013, 27, 1-13. [CrossRef]
40. Cai, Y.Z.; Sun, M.; Xing, J.; Luo, Q.; Corke, H. Structure-radical scavenging activity relationships of phenolic compounds from traditional Chinese medicinal plants. Life Sci. 2006, 78, 2872-2888. [CrossRef]
41. Rainha, N.; Koci, K.; Coelho, A.V.; Lima, E.; Baptista, J.; Fernandes-Ferreira, M. HPLC-UV-ESI-MS analysis of phenolic compounds and antioxidant properties of Hypericum undulatum shoot cultures and wild-growing plants. Phytochemistry 2013, 86, 83-91. [CrossRef]
42. Dueñas, M.; Fernández, D.; Hernández, T.; Estrella, I.; Muñoz, R. Bioactive phenolic compounds of cowpeas (Vigna sinensis L.). Modifications by fermentation with natural microflora and with Lactobacillus plantarum ATCC 14917. J. Sci. Food Agr. 2005, 85, 297-304. [CrossRef]
43. Muñoz, R.; de las Rivas, B.; de Felipe, F.L.; Reverón, I.; Santamaría, L.; Esteban-Torres, M.; Curiel, J.A.; Rodríguez, H.; Landete, J.M. Biotransformation of phenolics by Lactobacillus plantarum in fermented foods. In Fermented Foods in Health and Disease Prevention; Frías, J., Martinez-Villaluenga, C., Peñas, E., Eds.; Academic Press: Cambridge, MA, USA, 2016; Volume 4, pp. 63-68. ISBN 978-0-12-802309-9.
44. Wolfe, K.L.; Liu, R.H. Cellular Antioxidant Activity (CAA) Assay for Assessing Antioxidants, Foods, and Dietary Supplements. J. Agric. Food Chem. 2007, 55, 8896-8907. [CrossRef] [PubMed]
45. Valko, M.; Leibfritz, D.; Moncol, J.; Cronin, M.T.D.; Mazur, M.; Telser, J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39, 44-84. [CrossRef] [PubMed]
46. Pereira, A.L.F.; Maciel, T.C.; Rodrigues, S. Probiotic beverage from cashew apple juice fermented with Lactobacillus casei. Food Res. Int. 2011, 44, 1276-1283. [CrossRef]
47. Hurst, W.J.; Martin, R.A., Jr.; Zoumas, B.L. Application of HPLC to characterization of individual carbohydrates in foods. J. Food Sci. 1979, 44, 892-895. [CrossRef]
48. Morales-de La Peña, M.; Salvia-Trujillo, L.; Rojas-Graü, M.A.; Martín-Belloso, O. Impact of high intensity pulsed electric field on antioxidant properties and quality parameters of a fruit juice-soymilk beverage in chilled storage. LWT-Food Sci. Technol. 2010, 43, 872-881. [CrossRef]
49. Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 1999, 26, 1231-1237. [CrossRef]
50. Cicco, N.; Lanorte, M.T.; Paraggio, M.; Viggiano, M.; Lattanzio, V. A reproducible, rapid and inexpensive Folin-Ciocalteu micro-method in determining phenolics of plant methanol extracts. Microchem. J. 2009, 91, 107-110. [CrossRef]
51. Kwaw, E.; Ma, Y.; Tchabo, W.; Apaliya, M.T.; Xiao, L.; Li, X.; Hu, M. Effect of fermentation parameters and their optimization on the phytochemical properties of lactic-acid-fermented mulberry juice. J. Food Meas. Charact. 2017, 11, 1462-1473. [CrossRef]
52. Tsao, R.; Yang, R.; Young, J.C.; Zhu, H. Polyphenolic profiles in eight apple cultivars using high-performance liquid chromatography (HPLC). J. Agric. Food Chem. 2003, 51, 6347-6353. [CrossRef]
53. Del Rio, D.; Stewart, A.J.; Mullen,W.; Burns, J.; Lean, M.E.; Brighenti, F.; Crozier, A. HPLC-MSn analysis of phenolic compounds and purine alkaloids in green and black tea. J. Agric. Food Chem. 2004, 52, 2807-2815. [CrossRef] [PubMed]
54. Dou, J.; Lee, V.S.; Tzen, J.T.; Lee, M.R. Identification and comparison of phenolic compounds in the preparation of oolong tea manufactured by semifermentation and drying processes. J. Agric. Food Chem. 2007, 55, 7462-7468. [CrossRef] [PubMed]
55. Teng, J.; Li, Y.; Yu,W.; Zhao, Y.; Hu, X.; Tao, N.-P.;Wang, M. Naringenin, a common flavanone, inhibits the formation of AGEs in bread and attenuates AGEs-induced oxidative stress and inflammation in RAW264.7 cells. Food Chem. 2018, 269, 35-42. [CrossRef] [PubMed]