Characterization of unique metabolites in γ-aminobutyric acid-rich cheese by metabolome analysis using liquid chromatography-mass spectrometry.


Journal

Journal of food biochemistry
ISSN: 1745-4514
Titre abrégé: J Food Biochem
Pays: United States
ID NLM: 7706045

Informations de publication

Date de publication:
11 2019
Historique:
received: 04 04 2019
revised: 20 08 2019
accepted: 23 08 2019
pubmed: 7 9 2019
medline: 18 9 2020
entrez: 7 9 2019
Statut: ppublish

Résumé

Fermented dairy products comprise many functional components. Our previous study using fermented milk showed that the γ-aminobutyric acid (GABA)-producing Lactococcus lactis 01-7 strain can produce unique metabolites such as antihypertensive peptides, whereas this study was designed to find the unique metabolites in GABA-rich cheese using the 01-7 strain. Metabolites between cheese ripening with the non-GABA-producing L. lactis 01-1 strain (control) and GABA-rich cheese ripening with a mixture of 01-1 and 01-7 strains were compared. GABA and ornithine were detected in GABA-rich cheese using an amino acid analyzer and citrate was detected in the control cheese using HPLC. Metabolome analysis using LC-MS showed that peptides with unknown function and those with antihypertensive activity were higher in the GABA-rich cheese than in the control cheese. Further analysis of the amount of the YLGY derivatives showed that the amount of YL in the GABA-rich cheese was lower than that in the control. PRACTICAL APPLICATIONS: Clarification of metabolites in cheese contributes to the improvement of cheese ripening, thereby providing consumers with unique cheese with good nutritional and functional characteristics. The use of the 01-7 strain as a cheese starter might provide a functional cheese with antihypertensive-, antioxidative-, and anxiolytic-like activities.

Identifiants

pubmed: 31489647
doi: 10.1111/jfbc.13039
doi:

Substances chimiques

gamma-Aminobutyric Acid 56-12-2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13039

Informations de copyright

© 2019 Wiley Periodicals, Inc.

Références

Contreras, M. M., Sanchez, D., Sevilla, M. A., Recio, I., & Amigo, L. (2013). Resistance of casein-derived bioactive peptides to simulated gastrointestinal digestion. International Dairy Journal, 32, 71-78. https://doi.org/10.1016/j.idairyj.2013.05.008
Conway, V., Gauthier, S. F., & Pouliot, Y. (2013). Antioxidant activities of buttermilk proteins, whey proteins, and their enzymatic hydrolysates. Journal of Agricultural and Food Chemistry, 61, 364-372. https://doi.org/10.1021/jf304309g
Crow, V. L., & Thomas, T. D. (1982). Arginine metabolism in lactic streptococci. Journal of Bacteriology, 150, 1024-1032.
Farkye, N. Y. (1995). Contribution of milk-clotting enzymes and plasmin to cheese ripening. Advances in Experimental Medicine and Biology, 367, 195-207. https://doi.org/10.1007/978-1-4615-1913-3_11
Gómez-Ruiz, J. A., Ramos, M., & Recio, I. (2004). Identification and formation of angiotensin-converting enzyme-inhibitory peptides in Manchego cheese by high-performance liquid chromatography-tandem mass spectrometry. Journal of Chromatography A, 1054, 269-277. https://doi.org/10.1016/j.chroma.2004.05.022
Govindan, B., Johnson, A. J., Viswanathan, G., Ramaswamy, V., Koshy, K. C., & Baby, S. (2018). Secondary metabolites from the unique bamboo, Melocanna baccifera. Natural Product Research, 15, 1-4. https://doi.org/10.1080/14786419.2018.1434647
Hagi, T., Kobayashi, M., & Nomura, M. (2016). Metabolome analysis of milk fermented by γ-aminobutyric acid-producing Lactococcus lactis. Journal of Dairy Science, 99, 994-1001. https://doi.org/10.3168/jds.2015-9945
Hayakawa, K., Kimura, M., & Kamata, K. (2002). Mechanism underlying gamma-aminobutyric acid-induced antihypertensive effect in spontaneously hypertensive rats. European Journal of Pharmacology, 438, 107-113. https://doi.org/10.1016/S0014-2999(02)01294-3
Hayes, M. G., Oliveira, J. C., Mcsweeney, P. L., & Kelly, A. L. (2002). Thermal inactivation of chymosin during cheese manufacture. Journal of Dairy Research, 69, 269-279. https://doi.org/10.1017/S0022029902005472
Ismail, B., & Nielsen, S. S. (2010). Invited review: Plasmin protease in milk: Current knowledge and relevance to dairy industry. Journal of Dairy Science, 93(11), 4999-5009. https://doi.org/10.3168/jds.2010-3122
Kimoto-Nira, H., Moriya, N., Hayakawa, S., Kuramasu, K., Ohmori, H., Yamasaki, S., & Ogawa, M. (2017). Effects of rare sugar D-allulose on acid production and probiotic activities of dairy lactic acid bacteria. Journal of Dairy Science, 100, 5936-5944. https://doi.org/10.3168/jds.2016-12214
Kusano, M., Fukushima, A., Redestig, H., & Saito, K. (2011). Metabolomic approaches toward understanding nitrogen metabolism in plants. Journal of Experimental Botany, 62, 1439-1453. https://doi.org/10.1093/jxb/erq417
Laroute, V., Yasaro, C., Narin, W., Mazzoli, R., Pessione, E., Cocaign-Bousquet, M., & Loubière, P. (2016). GABA production in Lactococcus lactis is enhanced by arginine and co-addition of malate. Frontiers in Microbiology, 7, 1050. https://doi.org/10.3389/fmicb.2016.01050
Li, H., & Cao, Y. (2010). Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids, 39, 1107-1116. https://doi.org/10.1007/s00726-010-0582-7
Lignitto, L., Cavatorta, V., Balzan, S., Gabai, G., Galaverna, G., Novelli, E., … Segato, S. (2010). Angiotensin-converting enzyme inhibitory activity of water-soluble extracts of Asiago d'allevo cheese. International Dairy Journal, 20, 11-17. https://doi.org/10.1016/j.idairyj.2009.07.001
Maier, T. V., Lucio, M., Lee, L. H., VerBerkmoes, N. C., Brislawn, C. J., Bernhardt, J., … Jansson, J. K. (2017). Impact of dietary resistant starch on the human gut microbiome, metaproteome, and metabolome. mBio, 8, e01343-e1417. https://doi.org/10.1128/mBio.01343-17
Marcone, S., Haughton, K., Simpson, P. J., Belton, O., & Fitzgerald, D. J. (2015). Milk-derived bioactive peptides inhibit human endothelial-monocyte interactions via PPAR-γ dependent regulation of NF-κB. Journal of Inflammation, 12, 1. https://doi.org/10.1186/s12950-014-0044-1
Miyake, M., Kirisako, T., Kokubo, T., Miura, Y., Morishita, K., Okamura, H., & Tsuda, A. (2014). Randomised controlled trial of the effects of L-ornithine on stress markers and sleep quality in healthy workers. Nutrition Journal, 13, 53. https://doi.org/10.1186/1475-2891-13-53
Mizushige, T., Sawashi, Y., Yamada, A., Kanamoto, R., & Ohinata, K. (2013). Characterization of Tyr-Leu-Gly, a novel anxiolytic-like peptide released from bovine αS-casein. FASEB Journal, 27, 2911-2917. https://doi.org/10.1096/fj.12-225474
Mozzi, F., Ortiz, M. E., Bleckwedel, J., De Vuyst, L., & Pescuma, M. (2013). Metabolomics as a tool for the comprehensive understanding of fermented and functional foods with lactic acid bacteria. Food Research International, 54, 1152-1161. https://doi.org/10.1016/j.foodres.2012.11.010
Nielsen, S. S. (2002). Plasmin system and microbial proteases in milk: Characteristics, roles, and relationship. Journal of Agricultural and Food Chemistry, 50, 6628-6634. https://doi.org/10.1021/jf0201881
Nomura, M., Kimoto, H., Someya, Y., Furukawa, S., & Suzuki, I. (1998). Production of gamma-aminobutyric acid by cheese starters during cheese ripening. Journal of Dairy Science, 81, 1486-1491. https://doi.org/10.3168/jds.S0022-0302(98)75714-5
Ochi, H., Sakai, Y., Koishihara, H., Abe, F., Bamba, T., & Fukusaki, E. (2013). Monitoring the ripening process of Cheddar cheese based on hydrophilic component profiling using gas chromatography-mass spectrometry. Journal Dairy Science, 96, 7427-7441. https://doi.org/10.3168/jds.2013-6897
Paul, G. K., Gunasekera, S. P., Longley, R. E., & Pomponi, S. A. (2002). Theopederins K and L. Highly potent cytotoxic metabolites from a marine sponge Discodermia species. Journal of Natural Products, 65, 59-61. https://doi.org/10.1021/np0103766
Sagardia, I., Roa-Ureta, R. H., & Bald, C. (2013). A new QSAR model, for angiotensin I-converting enzyme inhibitory oligopeptides. Food Chemistry, 136, 1370-1376. https://doi.org/10.1016/j.foodchem.2012.09.092
Sakurai, N., Ara, T., Enomoto, M., Motegi, T., Morishita, Y., Kurabayashi, A., … Shibata, D. (2014). Tools and databases of the KOMICS web portal for preprocessing, mining, and dissemination of metabolomics data. BioMed Research International, 2014, 194812. https://doi.org/10.1155/2014/194812
Sakurai, N., Ara, T., Kanaya, S., Nakamura, Y., Iijima, Y., Enomoto, M., … Shibata, D. (2013). An application of a relational database system for high-throughput prediction of elemental compositions from accurate mass values. Bioinformatics, 29, 290-291. https://doi.org/10.1093/bioinformatics/bts660
Sánchez-Rivera, L., Martínez-Maqueda, D., Cruz-Huerta, E., Miralles, B., & Recio, I. (2014). Peptidomics for discovery, bioavailability and monitoring of dairy bioactive peptides. Food Research International, 63, 170-181. https://doi.org/10.1016/j.foodres.2014.01.069
Sánchez-Rivera, L., Recio, I., Ramos, M., & Gómez-Ruiz, J. Á. (2013). Short communication: Peptide profiling in cheeses packed using different technologies. Journal of Dairy Science, 96, 3551-3557. https://doi.org/10.3168/jds.2012-6302
Santiago-López, L., Aguilar-Toalá, J. E., Hernández-Mendoza, A., Vallejo-Cordoba, B., Liceaga, A. M., & González-Córdova, A. F. (2018). Invited review: Bioactive compounds produced during cheese ripening and health effects associated with aged cheese consumption. Journal of Dairy Science, 101, 3742-3757. https://doi.org/10.3168/jds.2017-13465
Savijoki, K., Ingmer, H., & Varmanen, P. (2006). Proteolytic systems of lactic acid bacteria. Applied Microbiology and Biotechnology, 71, 394-406. https://doi.org/10.1007/s00253-006-0427-1
Sieber, R., Bütikofer, U., & Bosset, J. O. (1995). Benzoic acid as a natural compound in cultured dairy products and cheese. International Dairy Journal, 5, 227-246. https://doi.org/10.1016/0958-6946(94)00005-A
Smit, G., Smit, B. A., & Engels, W. J. (2005). Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiology Review, 29, 591-610. https://doi.org/10.1016/j.femsre.2005.04.002
Stengel, A., & Taché, Y. (2018). Gut-brain neuroendocrine signaling under conditions of stress-focus on food intake-regulatory mediators. Frontiers in Endocrinology (Lausanne), 9, 498. https://doi.org/10.3389/fendo.2018.00498
Zhao, C. J., Schieber, A., & Gänzle, M. G. (2016). Formation of taste-active amino acids, amino acid derivatives and peptides in food fermentations-A review. Food Research International, 89, 39-47. https://doi.org/10.1016/j.foodres.2016.08.042

Auteurs

Tatsuro Hagi (T)

Animal Products Research Division, Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization (NARO), Ibaraki, Japan.

Hiroyuki Nakagawa (H)

Food Research Institute, National Agriculture and Food Research Organization (NARO), Ibaraki, Japan.

Hideyuki Ohmori (H)

Animal Products Research Division, Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization (NARO), Ibaraki, Japan.

Keisuke Sasaki (K)

Animal Products Research Division, Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization (NARO), Ibaraki, Japan.

Miho Kobayashi (M)

Animal Products Research Division, Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization (NARO), Ibaraki, Japan.

Takumi Narita (T)

Animal Products Research Division, Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization (NARO), Ibaraki, Japan.

Masaru Nomura (M)

Animal Products Research Division, Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization (NARO), Ibaraki, Japan.

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