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Correlation Between Antioxidative Activities and Metabolite Changes During Cheonggukjang Fermentation

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Correlation Between Antioxidative Activities and Metabolite Changes During Cheonggukjang Fermentation 100858 (121) Biosci. Biotechnol. Biochem., 75 (4), 100858-1–8, 2011 Correlation between Antioxidative Activities and Metabolite Changes during Cheonggukjang Fermentation Jiyoung KIM,1 Jung Nam CHOI,1 Daejung KANG,1 Gun Hee SON,1 Young-Suk KIM,2 y Hyung-Kyoon CHOI,3 Dae Young KWON,4 and Choong Hwan LEE1; 1Department of Bioscience and Biotechnology and Bio/Molecular Informatics Center, Konkuk University, Seoul 143-701, Republic of Korea 2Department of Food Science and Technology, Ewha Woman’s University, Seoul 120-750, Republic of Korea 3College of Pharmacy, Chung-Ang University, Seoul 156-756, Republic of Korea 4Korea Food Research Institute, Songnam 463-746, Republic of Korea Received December 2, 2010; Accepted January 5, 2011; Online Publication, April 22, 2011 [doi:10.1271/bbb.100858] Liquid chromatography mass spectrometry and mul- soybeans and microorganisms, metabolomics is used to tivariate analysis were employed to investigate the identify differences in metabolite composition and to correlation between fermentation time-dependent me- determine the effects of quality control and classifica- tabolite changes in cheonggukjang, a traditional fer- tion.3) Metabolite profiling, one of the metabolomics mented soybean product, and changes in its antioxidant tools used to analyze metabolites in an unbiased manner, activity over 72 h. The metabolite patterns were clearly is an untargeted analytical technique used in chemical distinguishedAdvance not by strains but by fermentation View time, pattern recognition analysis and the identification of into patterns I (0–12 h), II (12–24 h), and III (24–72 h), selected metabolites from crude metabolite mixture which appeared as distinct clusters on principal compo- samples.4) Recently, metabolomic analysis methods nent analysis. The compounds that significantly con- have been established for soybean paste,5) soy sauce,6) tributed to patterns I, II, and III were soyasaponins, and cheonggukjang (CGJ).7,8) These approaches involve isoflavonoid derivatives, and isoflavonoid aglycons re- a wide spectrum of technologies including GC-MS and spectively. Partial least square analysis for metabolite NMR. These previous profiling studies targeted only to antioxidant effects showed correlations between general nutritional factors, such as amino acids, organic the ferric reducing/antioxidant power (FRAP) and acids, and sugars and few studies has conducted func- 2,2-diphenyl-1-picrylhydrazyl (DPPH) assay during tional metabolite profiling. CGJ contains many useful 24–36 h, and 2,20-azinobis (3-ethylbenzothiazoline-6- phytochemicalsProofs and beneficial effects such as anti- sulfonic acid) (ABTS) test and total phenol content oxidative,9,10) anti-tumor,11) anti-diabetic,12) and throm- (TPC) during 36–72 h. Compared with the strong bolytic activity.13) Liquid chromatography-mass spec- negative correlations of glucosylated-isoflavonoids with trometry (LC-MS) has been found to be very suitable for DPPH, ABTS and TPC during fermentation, the recognizing a variety metabolite patterns and character- isoflavonoid aglycon displayed strong positive correla- izing fermented foods.14,15) Recently, metabolic profiling tions with these compounds during fermentation. tools have been combined with bioactivity analysis to identify metabolites that significantly contribute to the Key words: cheonggukjang; metabolite profiling; liquid functional properties of extracts. However, even though chromatography-mass spectrometry (LC-MS); there have been several reports on the relationship antioxidant effects; fermentation between metabolites and bioactivity in soybean and its fermentation product,10,16) no study has directly exam- In Asian and Western countries, traditional soy foods ined changes in the CGJ metabolite profile as a function are consumed frequently in many forms, including soy of fermentation time and looked for correlations with milk, soy beverages, tofu, natto, and miso. Various bioactivities. Hence, in this study, we examined and soybean fermentation products made in Korea such as identified correlations between metabolite profiles and cheonggukjang (fast-fermented bean paste), doenjang antioxidant effects using LC-MS/MS with the goal of (soybean paste), kochujang (fermented red pepper), obtaining basic data on the processing conditions for and ganjang (soy sauce) are produced by processing CGJ fermentation. soybeans with certain microorganisms.1,2) In order to understand better the complex processes that occur Materials and Methods during the production of fermentation products, inte- grated tools are needed to define the metabolic pheno- Chemicals and reagents. DPPH (2,2-diphenyl-1-picrylhydrazyl), type. With the rapid progress of fermentation between ABTS (2,20-azinobis (3-ethylbenzothiazoline-6-sulfonic acid)) dia- y To whom correspondence should be addressed. Tel: +82-2-2049-6177; Fax: +82-2-455-4291; E-mail:[email protected] Abbreviations: FRAP, ferric reducing/antioxidant power; DPPH, 2,2-diphenyl-1-picrylhydrazyl; ABTS, 2,20-azinobis (3-ethylbenzothiazoline-6- sulfonic acid); TPC, total phenol content; LC-MS, liquid chromatography-mass spectrometry; DDS, data-dependent scanning; CID, collision-induced dissociation; XCMS, acronym for various forms (X) of chromatography mass spectrometry; PCA, principal component analysis; PLS, partial least square; PLS-DA, partial least squares discriminant analysis; ANOVA, analysis of variance; MANOVA, multivariate analysis of variance; VIP, variable importance in projection; DDMP, 2,3-dihydro-2,5-dihydroxy-6-methyl-4H-pyran-4-one 100858-2 J. KIM et al. mmonium salt, Ferrozin (5,6-diphenyl-3-(2-pyridyl)-1,2,4-triazine- multiple classes were computed via breakdown and unpaired 40,400-disulfonic acid), NaOH, sodium carbonate, gallic acid, Folin Student’s t-test using Excel (Microsoft). A difference of p < 0:05 Ciocalteu’s phenol reagent, potassium persulfate, dimethyl sulfoxide, was considered significant. Pair-wise metabolite-antioxidant effects p-nitrophenol- -D-glucopyranoside (pNP-Glc), p-nitrophenol (pNP), correlations were calculated by Pearson’s correlation coefficient test and formic acid were obtained from Sigma Chemical. (St. Louis, MO). using R software. Acetonitrile and water used in LC-MS were from Fisher Scientific (Pittsburgh, PA), and were of HPLC grade. Ethanol for extraction Free-radical scavenging ability by use of a stable ABTS radical was from Duksan Chemical (Ansan, Korea). Seven standards, with cation. The ABTS assay was conducted as described by Re et al.19) purities >98%, including daidzin, glycitin, genistein, dadidzein, Seven mM ABTS ammonium was dissolved in potassium phosphate soyasaponon I, II, and IV were from Sigma and Chromadex (Santa buffer (pH 7.4) and then mixed with 2.45 mM of potassium persulfate. Ana, CA). The mixture was maintained at room temperature for 12–16 h in order to allow it to turn into a dark blue solution. The solution was diluted Preparation and extraction of CGJ. Cheonggukjang (CGJ) were with potassium phosphate buffer (pH 7.4) until the absorbance reached given by from the Korea Food Research Institutes (Sungnam, Korea). 0:7 Æ 0:02 at 734 nm, which was measured using a spectrophotometer Three types of CGJ were generated and cooked whole soybeans were (Thermo Electron, Spectronic Genesys 6, Madison WI). One mL of the inoculated with Bacillus licheniformis KCCM 11053P, 11054P, and resulting solution was mixed with 10 mL of the sample and incubated B. amyliquefaciens CH86-1,17) are the most widely used bacilli for for 6 min. The absorbance was then recorded at room temperature. fermented soy foods, and were fermented at 42 C for 0, 12, 24, 36, 48, Results were expressed in mg of trolox equivalents concentration/g of 60, and 72 h. Finally, each CGJ samples (1 g dried powder) were mixed sample. The concentration of standard solutions ranged from 0.03 to with 50 mL of ethanol/water (40:60, v/v) at 25 C with shaking at 0.5 mM. Experiments were carried out in triplicate. 150 rpm for 1 h. The mixture was centrifuged at 5,000 rpm for 10 min at 25 C and then evaporated in vacuo. The extract obtained was Determination of antioxidant activity by DPPH free-radical filtered through a 0.22-mm filter and used for metabolite profiling scavenging assay. DPPH assay was conducted as described by Dietz analysis and evaluating antioxidant activity. et al., with minor modifications.20) Reaction mixtures containing the test samples (10 mL) and 190 mL of a 200-mM DPPH ethanol solution LC-ESI/MS conditions for metabolite profiling. The LC-MS/MS were incubated at room temperature for 30 min in 96-well plates. The instrument consisted of a 212-LC Binary Solvent Delivery System, and absorbance of the DPPH free radical was measured at 515 nm using a aAdvance ProstarÔ 410 AutoSampler, a ProstarÔ 335 photodiode View array microplate reader. Results were expressed in mg of Trolox equivalent detector, which was coupled to the Varian 500-MS ion-trap mass concentration per g of samples. The concentration of the standard spectrometer equipped with an electrospray interface from Varian solutions ranged from 0.0156 to 0.0625 mM. Experiments were carried Technologies (Palo Alto, CA). Chromatographic separation was out in triplicate. performed in a 100 Â 2:0 mm i.d., 3 mm PurSuit XRs C18 column (Varian, Lake Forest, CA) with a MetaGuard 2.0 PurSuit XRs Determination of total phenolics. Total phenol content was C18 guard column (Varian, CA) at a flow rate of 0.2 mL/min. The analyzed as described by Singleton et al.21) The assay conditions were column was maintained at 30 C and eluted with a mobile phase that as follows: A 10-mL sample was added to 0.2 N the Folin-Ciocalteu’s consisted of a combination of A (0.1% v/v formic acid in water) and B phenol reagent (160 mL) in 96 wells. After 3 min, 30 mL of a saturated (0.1% v/v formic acid in acetonitrile). Samples were run with isocratic sodium carbonate solution was added to the mixture, which was then 10% B v/v for the first 2 min, increased to 40% B at 10 min, to 70% at incubated at room temperature for 1 h.
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