Preparation, receptors, bioactivity and bioavailability of γ-glutamyl peptides: A comprehensive review

Aluko, 2015, Antihypertensive peptides from food proteins, Annual Review of Food Science and Technology, 6, 235, 10.1146/annurev-food-022814-015520 Amino, 2016, Structure–CaSR–activity relation of kokumi γ-glutamyl peptides, Chemical and Pharmaceutical Bulletin, 64, 1181, 10.1248/cpb.c16-00293 Bandyopadhyay, 2010, Diverse roles of extracellular calcium-sensing receptor in the central nervous system, Journal of Neuroscience Research, 88, 2073, 10.1002/jnr.22391 Bejjani, 2013, Transport of IRW, an ovotransferrin-derived antihypertensive peptide, in human intestinal epithelial caco-2 cells, Journal of Agricultural and Food Chemistry, 61, 1487, 10.1021/jf302904t Bougle, 2017, Dietary bioactive peptides: Human studies, Critical Reviews in Food Science and Nutrition, 57, 335, 10.1080/10408398.2013.873766 Brennan, 2014, Emerging roles of the extracellular calcium-sensing receptor in nutrient sensing: Control of taste modulation and intestinal hormone secretion, British Journal of Nutrition, 111, S16, 10.1017/S0007114513002250 Broadhead, 2011, Allosteric modulation of the calcium-sensing receptor by γ-glutamyl peptides: Inhibition of PTH secretion, suppression of intracellular cAMP levels, and a common mechanism of action with L-amino acids, Journal of Biological Chemistry, 286, 8786, 10.1074/jbc.M110.149724 Brown, 2001, Extracellular calcium sensing and extracellular calcium signaling, Physiological Reviews, 81, 239, 10.1152/physrev.2001.81.1.239 Chee, 2017, Intervention of dietary dipeptide gamma-L-glutamyl-L-valine (γ-EV) ameliorates inflammatory response in a mouse model of LPS-induced sepsis, Journal of Agricultural and Food Chemistry, 65, 5953, 10.1021/acs.jafc.7b02109 Cheng, 2012, Calcium-sensing receptor inhibits secretagogue-induced electrolyte secretion by intestine via the enteric nervous system, American Journal of Physiology - Gastrointestinal and Liver Physiology, 303, G60, 10.1152/ajpgi.00425.2011 Chen, 2019, Anti-inflammatory effect and cellular uptake mechanism of peptides from common bean (Phaseolus vulga L.) milk and yogurts in Caco-2 mono- and Caco-2/EA.hy926 co-culture models, Journal of Agricultural and Food Chemistry, 67, 8370, 10.1021/acs.jafc.9b03079 Conigrave, 2013, Calcium-sensing receptor (CaSR): Pharmacological properties and signaling pathways, Best Practice & Research Clinical Endocrinology & Metabolism, 27, 315, 10.1016/j.beem.2013.05.010 DeWire, 2007, Beta-arrestins and cell signaling, Annual Review of Physiology, 69, 483, 10.1146/annurev.physiol.69.022405.154749 Ding, 2016, Digestion and absorption of an egg white ACE-inhibitory peptide in human intestinal Caco-2 cell monolayers, International Journal of Food Sciences & Nutrition, 67, 111, 10.3109/09637486.2016.1144722 Ding, 2018, Hydrolysis and transepithelial transport of two corn gluten derived bioactive peptides in human Caco-2 cell monolayers, Food Research International, 106, 475, 10.1016/j.foodres.2017.12.080 Dufner, 2005, The calcium-sensing receptor acts as a modulator of gastric acid secretion in freshly isolated human gastric glands, American Journal of Physiology-gastrointestinal and Liver Physiology, 289, G1084, 10.1152/ajpgi.00571.2004 Dunkel, 2007, Molecular and sensory characterization of gamma-glutamyl peptides as key contributors to the Kokumi taste of edible beans (Phaseolus vulgaris L.), Journal of Agricultural and Food Chemistry, 55, 6712, 10.1021/jf071276u Feng, 2010, Calcium-sensing receptor is a physiologic multimodal chemosensor regulating gastric G-cell growth and gastrin secretion, Proceedings of the National Academy of Sciences, 107, 17791, 10.1073/pnas.1009078107 Frerot, 2013, Identification and quantitation of new glutamic acid derivatives in soy sauce by UPLC/MS/MS, Chemistry and Biodiversity, 10, 1842, 10.1002/cbdv.201300150 Fu, 2016, Angiotensin I–converting enzyme–inhibitory peptides from bovine collagen: Insights into inhibitory mechanism and transepithelial transport, Food Research International, 89, 373, 10.1016/j.foodres.2016.08.037 Gabriel, 2009, The calcium-sensing receptor in taste tissue, Biochemical and Biophysical Research Communications, 378, 414, 10.1016/j.bbrc.2008.11.060 Geng, 2016, Structural mechanism of ligand activation in human calcium-sensing receptor, Elife, 5, 10.7554/eLife.13662 Gerbino, 2018, The different facets of extracellular calcium sensors: Old and new concepts in calcium-sensing receptor signalling and pharmacology, International Journal of Molecular Sciences, 19, 999, 10.3390/ijms19040999 Guha, 2020, Dietary γ-glutamyl valine ameliorates TNF-α-induced vascular inflammation via endothelial calcium-sensing receptors, Journal of Agricultural and Food Chemistry, 68, 9139, 10.1021/acs.jafc.0c04526 Hamamcioglu, 2016, A pilot study to detect oxidative stress in type 2 diabetic patients, Free Radical Biology and Medicine, 96, S62, 10.1016/j.freeradbiomed.2016.04.133 Hirayama, 2014, Development of quantitative method for determination of gamma-glutamyl peptides by capillary electrophoresis tandem mass spectrometry: An efficient approach avoiding matrix effect, Journal of Chromatography A, 1369, 161, 10.1016/j.chroma.2014.10.007 Hofer, 2003, Extracellular calcium sensing and signalling, Nature Reviews Molecular Cell Biology, 4, 530, 10.1038/nrm1154 Hoffner, 2008, [Nε‐(γ‐glutamyl) lysine] as a potential biomarker in neurological diseases: New detection method and fragmentation pathways, Journal of Mass Spectrometry, 43, 456, 10.1002/jms.1331 Hong, 2016, Structural design of oligopeptides for intestinal transport model, Journal of Agricultural and Food Chemistry, 64, 2072, 10.1021/acs.jafc.6b00279 Hua, 2013 Ichinose, 1987, Increase of catecholamines in mouse brain by systemic administration of γ‐glutamyl L-3,4-dihydroxyphenylalanine, Journal of Neurochemistry, 49, 928, 10.1111/j.1471-4159.1987.tb00982.x Itoh, 2012, Production of L-theanine using glutaminase encapsulated in carbon-coated mesoporous silica with high pH stability, Biochemical Engineering Journal, 68, 207, 10.1016/j.bej.2012.07.012 Jain, 2017, Production and characterization of functional properties of protein hydrolysates from egg shell membranes by lactic acid bacteria fermentation, Journal of Food Science and Technology-Mysore, 54, 1062, 10.1007/s13197-017-2530-y Juillerat-Jeanneret, 2014, Dipeptidyl peptidase IV and its inhibitors: Therapeutics for type 2 diabetes and what else?, Journal of Medicinal Chemistry, 57, 2197, 10.1021/jm400658e Kasai, 1986, γ-Glutamyl peptides of Vigna radiata seeds, Phytochemistry, 25, 679, 10.1016/0031-9422(86)88023-2 Kerr, 2010, Effects of γ-glutamyl linker on DPP-IV resistance, duration of action and biological efficacy of acylated glucagon-like peptide-1, Biochemical Pharmacology, 80, 396, 10.1016/j.bcp.2010.04.021 Kitaoka, 1996, Transmural potential changes associated with the in vitro absorption of theanine in the Guinea pig intestine, Bioscience Biotechnology & Biochemistry, 60, 1768, 10.1271/bbb.60.1768 Kumagai, 1988, Synthesis of γ-glutamyl-DOPA from L-glutamine and L-DOPA by γ-glutamyltranspeptidase of Escherichia coli K-12, Agricultural & Biological Chemistry, 52, 1741 Kuroda, 2013, Determination and quantification of the kokumi peptide, γ-glutamyl-valyl-glycine, in commercial soy sauces, Food Chemistry, 141, 823, 10.1016/j.foodchem.2013.03.070 Kuroda, 1997, Vol. 3, 239 Lai, 2008, Autophagy is increased after traumatic brain injury in mice and is partially inhibited by the antioxidant γ-glutamylcysteinyl ethyl ester, Journal of Cerebral Blood Flow and Metabolism, 28, 540, 10.1038/sj.jcbfm.9600551 Li, 2014, β-Arrestin 2 negatively regulates Toll-like receptor 4 (TLR4)-triggered inflammatory signaling via targeting p38 MAPK and interleukin 10, Journal of Biological Chemistry, 289, 23075, 10.1074/jbc.M114.591495 Lin, 2018, Facile immobilization of Bacillus licheniformis γ-glutamyltranspeptidase onto graphene oxide nanosheets and its application to the biocatalytic synthesis of γ-l-glutamyl peptides, International Journal of Biological Macromolecules, 117, 1326, 10.1016/j.ijbiomac.2017.11.153 Lioe, 2006, Evaluation of peptide contribution to the intense umami taste of Japanese soy sauces, Journal of Food Science, 71, S277, 10.1111/j.1365-2621.2006.tb15654.x Liou, 2011, The extracellular calcium-sensing receptor is required for cholecystokinin secretion in response to L-phenylalanine in acutely isolated intestinal I cells, American Journal of Physiology - Gastrointestinal and Liver Physiology, 300, G538, 10.1152/ajpgi.00342.2010 Liu, 2015, Discovery of kokumi peptide from yeast extract by LC-Q-TOF-MS/MS and sensomics approach, Journal of the Science of Food and Agriculture, 95, 3183, 10.1002/jsfa.7058 Mace, 2012, The regulation of K- and L-cell activity by GLUT2 and the calcium-sensing receptor CasR in rat small intestine, Journal of Physiology-London, 590, 2917, 10.1113/jphysiol.2011.223800 Majumder, 2011, Purification and characterisation of angiotensin I converting enzyme (ACE) inhibitory peptides derived from enzymatic hydrolysate of ovotransferrin, Food Chemistry, 126, 1614, 10.1016/j.foodchem.2010.12.039 Marchiando, 2010, Epithelial barriers in homeostasis and disease, Annual Review of Pathology: Mechanisms of Disease, 5, 119, 10.1146/annurev.pathol.4.110807.092135 Matsui, 2004, Tissue distribution of antihypertensive dipeptide, Val-Tyr, after its single oral administration to spontaneously hypertensive rats, Journal of Peptide Science, 10, 535, 10.1002/psc.568 Miyamura, Iida, 2015, Determination and quantification of kokumi peptide, gamma-glutamyl-valyl-glycine, in brewed alcoholic beverages, Journal of Bioscience and Bioengineering, 120, 311, 10.1016/j.jbiosc.2015.01.018 Miyamura, 2016, Quantitative analysis of γ-Glutamyl-valyl-glycine in fish sauces fermented with Koji by LC/MS/MS, Chromatography, 37, 39, 10.15583/jpchrom.2015.034 Muramatsu, 2014, Activation of the gut calcium-sensing receptor by peptide agonists reduces rapid elevation of plasma glucose in response to oral glucose load in rats, American Journal of Physiology - Gastrointestinal and Liver Physiology, 306, G1099, 10.1152/ajpgi.00155.2014 Mütsch-Eckner, 1992, γ-Glutamyl peptides from Allium sativum bulbs, Phytochemistry, 31, 2389, 10.1016/0031-9422(92)83283-5 Mütsch-Eckner, 1992, γ-Glutamyl peptides from Allium sativum bulbs, Phytochemistry, 31, 2389, 10.1016/0031-9422(92)83283-5 Nakajima, 2012, Calcium-sensing receptor mediates dietary peptide-induced CCK secretion in enteroendocrine STC-1 cells, Molecular Nutrition & Food Research, 56, 753, 10.1002/mnfr.201100666 Nakamoto, 2018, Isolation and identification of three γ-glutamyl tripeptides and their putative production mechanism in aged garlic extract, Journal of Agricultural and Food Chemistry, 66, 2891, 10.1021/acs.jafc.7b05480 Nakayama, 1981, Synthesis of γ-glutamylpeptides by γ-glutamylcysteine synthetase from Proteus mirabilis, Agricultural and Biological Chemistry, 45, 2839 Nongonierma, 2013, Inhibition of dipeptidyl peptidase IV and xanthine oxidase by amino acids and dipeptides, Food Chemistry, 141, 644, 10.1016/j.foodchem.2013.02.115 Oakley, 2008, The identification and structural characterization of C7orf24 as γ-glutamyl cyclotransferase an essential enzyme in the γ-glutamyl cycle, Journal of Biological Chemistry, 283, 22031, 10.1074/jbc.M803623200 Oda, 2009, The mRNA distribution of C7orf24, a γ-glutamyl cyclotransferase, in rat tissues, Journal of Histochemistry and Cytochemistry, 57, 1121, 10.1369/jhc.2009.953976 Ohsu, 2010, Involvement of the calcium-sensing receptor in human taste perception, Journal of Biological Chemistry, 285, 1016, 10.1074/jbc.M109.029165 Pacheco, 2008, CaSR stimulates secretion of Wnt5a from colonic myofibroblasts to stimulate CDX2 and sucrase-isomaltase using Ror2 on intestinal epithelia, American Journal of Physiology - Gastrointestinal and Liver Physiology, 295, G748, 10.1152/ajpgi.00560.2007 Phewpan, 2020, Investigation of kokumi substances and bacteria in thai fermented freshwater fish (Pla-ra), Journal of Agricultural and Food Chemistry, 68, 10345, 10.1021/acs.jafc.9b06107 Pierce, 2001, Classical and new roles of β-arrestins in the regulation of G-protein-coupled receptors, Nature Reviews Neuroscience, 2, 727, 10.1038/35094577 Quintana-Cabrera, 2012, γ-Glutamylcysteine detoxifies reactive oxygen species by acting as glutathione peroxidase-1 cofactor, Nature Communications, 3, 1, 10.1038/ncomms1722 Rey, 2010, Extracellular calcium sensing receptor stimulation in human colonic epithelial cells induces intracellular calcium oscillations and proliferation inhibition, Journal of Cellular Physiology, 225, 73, 10.1002/jcp.22198 Rogers, 2012, Loss of the calcium-sensing receptor in colonic epithelium is a key event in the pathogenesis of colon cancer, Clinical Colorectal Cancer, 11, 24, 10.1016/j.clcc.2011.04.003 Romani, 2009, Cardiac microvascular endothelial cells express a functional Ca2+-sensing receptor, Journal of Vascular Research, 46, 73, 10.1159/000140677 Ruat, 2013, Roles of the calcium sensing receptor in the central nervous system, Best Practice & Research Clinical Endocrinology & Metabolism, 27, 429, 10.1016/j.beem.2013.03.001 Saidak, 2009, The role of the calcium-sensing receptor in the development and progression of cancer, Endocrine Reviews, 30, 178, 10.1210/er.2008-0041 Salama, 2015, Glutamyl cysteine dipeptide suppresses ferritin expression and alleviates liver injury in iron-overload rat model, Biochimie, 115, 203, 10.1016/j.biochi.2015.06.006 Salama, 2019, Cadmium-induced hepatocellular injury: Modulatory effects of γ-glutamyl cysteine on the biomarkers of inflammation, DNA damage, and apoptotic cell death, Journal of Trace Elements in Medicine & Biology, 52, 74, 10.1016/j.jtemb.2018.12.003 Sánchez-Vioque, 2011, Determination of γ-glutamyl-S-ethenyl-cysteine in narbon vetch (Vicia narbonensis L.) seeds by high performance liquid chromatography, Animal Feed Science and Technology, 165, 125, 10.1016/j.anifeedsci.2011.02.006 Schreckenberg, 2018, Calcium sensing receptor expression and signalling in cardiovascular physiology and disease, Vascular Pharmacology, 107, 35, 10.1016/j.vph.2018.02.007 Sharma, 2018, L-Theanine: An astounding sui generis integrant in tea, Food Chemistry, 242, 601, 10.1016/j.foodchem.2017.09.046 Shibata, 2017, Isolation and characterization of key contributors to the "kokumi" taste in soybean seeds, Bioscience Biotechnology and Biochemistry, 81, 2168, 10.1080/09168451.2017.1372179 Shimazaki, 2019, Removal of copper in microdroplets by ovomucoid hydrolysates bound to reverse-phase chromatography media within pipette tips, Applied Biochemistry and Biotechnology, 189, 680, 10.1007/s12010-019-03050-w Simbirtsev, 2003, Biological activity of peptide SCV-07 against murine tuberculosis, Russian Journal of Immunology : RJI : Official Journal of Russian Society of Immunology, 8, 11 Sofyanovich, 2019, Multiple pathways for the formation of the γ-glutamyl peptides γ-glutamyl-valine and γ-glutamyl-valyl-glycine in Saccharomyces cerevisiae, PloS One, 14, 10.1371/journal.pone.0216622 Soga, 2011, Serum metabolomics reveals γ-glutamyl dipeptides as biomarkers for discrimination among different forms of liver disease, Journal of hepatology, 55, 896, 10.1016/j.jhep.2011.01.031 Speranza, 2012, γ-Glutamyl transpeptidase-catalyzed synthesis of naturally occurring flavor enhancers, Journal of Molecular Catalysis B: Enzymatic, 84, 65, 10.1016/j.molcatb.2012.03.014 Sugano, 2010, Coexistence of passive and carrier-mediated processes in drug transport, Nature Reviews Drug Discovery, 9, 597, 10.1038/nrd3187 Suzuki, 2002, Improvement of the bitter taste of amino acids through the transpeptidation reaction of bacterial gamma-glutamyltranspeptidase, Journal of Agricultural and Food Chemistry, 50, 313, 10.1021/jf010726u Suzuki, Nakafuji, 2017, New method to produce kokumi seasoning from protein hydrolysates using bacterial enzymes, Journal of Agricultural and Food Chemistry, 65, 10514, 10.1021/acs.jafc.7b03690 Suzuki, 2007, γ-Glutamyl compounds and their enzymatic production using bacterial gamma-glutamyltranspeptidase, Amino Acids, 32, 333, 10.1007/s00726-006-0416-9 Tanaka, 2015, Visualized absorption of anti-atherosclerotic dipeptide, Trp-His, in Sprague-Dawley rats by LC-MS and MALDI-MS imaging analyses, Molecular Nutrition & Food Research, 59, 1541, 10.1002/mnfr.201500075 Tanaka, 2015, Visualized absorption of anti-atherosclerotic dipeptide, Trp-His, in Sprague-Dawley rats by LC-MS and MALDI-MS imaging analyses, Molecular Nutrition & Food Research, 59, 1541, 10.1002/mnfr.201500075 Taylor, 2008, Seed storage protein deficiency improves sulfur amino acid content in common bean (Phaseolus vulgaris L.): Redirection of sulfur from γ-glutamyl-S-methyl-cysteine, Journal of Agricultural and Food Chemistry, 56, 5647, 10.1021/jf800787y Tennakoon, 2016, The calcium-sensing receptor and the hallmarks of cancer, Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1863, 1398, 10.1016/j.bbamcr.2015.11.017 Tfelt-Hansen, 2003, Calcium-sensing receptor stimulates PTHrP release by pathways dependent on PKC, p38 MAPK, JNK, and ERK1/2 in H-500 cells, American Journal of Physiology - Endocrinology And Metabolism, 285, E329, 10.1152/ajpendo.00489.2002 Toelstede, 2009, A series of kokumi peptides impart the long-lasting mouthfulness of matured gouda cheese, Journal of Agricultural and Food Chemistry, 57, 1440, 10.1021/jf803376d Tuthill, 2011, The effect of the immunomodulatory peptide gamma-D-glutamyl-L-tryptophan in leukemia, lymphoma, and head and neck cancer xenograft models, Journal of Clinical Oncology, 29, 10.1200/jco.2011.29.15_suppl.5592 Ueda, 1990, Characteristic flavor constituents in water extract of garlic, Agricultural & Biological Chemistry, 54, 163 Ueda, 1994, Composition of sulfur-containing components in onion and their flavor characters, Bioscience Biotechnology & Biochemistry, 58, 108, 10.1271/bbb.58.108 Wang, 2011, Amino acids stimulate cholecystokinin release through the Ca2+-sensing receptor, American Journal of Physiology - Gastrointestinal and Liver Physiology, 300, G528, 10.1152/ajpgi.00387.2010 Wang, 2006, Association of β-arrestin and TRAF6 negatively regulates Toll-like receptor–interleukin 1 receptor signaling, Nature Immunology, 7, 139, 10.1038/ni1294 Watkins, 2010, Attenuation of radiation- and chemoradiation-induced mucositis using gamma-D-glutamyl-L-tryptophan (SCV-07), Oral Diseases, 16, 655, 10.1111/j.1601-0825.2010.01671.x Xing, 2019, γ-Glutamylvaline prevents low-grade chronic inflammation via activation of a calcium-sensing receptor pathway in 3t3-l1mouse adipocytes, Journal of Agricultural and Food Chemistry, 67, 8361, 10.1021/acs.jafc.9b02334 Xu, 2019, Bioavailability of bioactive peptides derived from food proteins across the intestinal epithelial membrane: A review, Trends in Food Science & Technology, 86, 399, 10.1016/j.tifs.2019.02.050 Xu, 2020, L-Theanine affects intestinal mucosal immunity by regulating short-chain fatty acid metabolism under dietary fiber feeding, Food & Function, 11, 8369, 10.1039/D0FO01069C Xu, 2017, Transepithelial transport of YWDHNNPQIR and its metabolic fate with cytoprotection against oxidative stress in human intestinal Caco-2 cells, Journal of Agricultural and Food Chemistry, 65, 2056, 10.1021/acs.jafc.6b04731 Yang, 2019, Gamma glutamyl peptides: The food source, enzymatic synthesis, kokumi-active and the potential functional properties - a review, Trends in Food Science & Technology, 91, 339, 10.1016/j.tifs.2019.07.022 Yang, 2019, γ-[Glu](n= 1, 2)-Phe/-Met/-Val stimulates gastrointestinal hormone (CCK and GLP-1) secretion by activating the calcium-sensing receptor, Food & Function, 10, 4071, 10.1039/C9FO00313D Yang, 2017, Synthesis and sensory characteristics of kokumi γ-[Glu]n-Phe in the presence of glutamine and phenylalanine: Glutaminase from Bacillus amyloliquefaciens or Aspergillus oryzae as the catalyst, Journal of Agricultural and Food Chemistry, 65, 8696, 10.1021/acs.jafc.7b03419 Yang, 2018, γ-Glu-Met synthesised using a bacterial glutaminase as a potential inhibitor of dipeptidyl peptidase IV, International Journal of Food Science and Technology, 53, 1166, 10.1111/ijfs.13692 Yang, 2018, Comparison of kokumi γ-[Glu](n> 1)-Val and γ-[Glu](n> 1)-Met synthesized through transpeptidation catalyzed by glutaminase from Bacillus amyloliquefaciens, Food Chemistry, 247, 89, 10.1016/j.foodchem.2017.11.096 Yang, 2019, Glutaminase-catalyzed γ-glutamylation to produce CCK secretion-stimulatory γ-[Glu]n-Trp peptides superior to tryptophan, Journal of Functional Foods, 60, 103418, 10.1016/j.jff.2019.103418 Yang, 2014, Emerging roles of dipeptidyl peptidase 4 inhibitors: Anti-inflammatory and immunomodulatory effect and its application in diabetes mellitus, Canadian Journal of Diabetes, 38, 473, 10.1016/j.jcjd.2014.01.008 Zhang, 2015, γ-Glutamyl cysteine and γ-glutamyl valine inhibit TNF-α signaling in intestinal epithelial cells and reduce inflammation in a mouse model of colitis via allosteric activation of the calcium-sensing receptor, Biochimica et Biophysica Acta - Molecular Basis of Disease, 1852, 792, 10.1016/j.bbadis.2014.12.023 Zhang, 2015, γ-Glutamyl-S-allyl-cysteine inhibits hepatic stellate cell proliferation and collagen secretion via a proapoptotic mechanism, European Food Research and Technology, 240, 1271, 10.1007/s00217-015-2453-7