Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-28T03:49:09.438Z Has data issue: false hasContentIssue false

Glucagon-like peptide-1 regulation by food proteins and protein hydrolysates

Published online by Cambridge University Press:  19 January 2021

Alba Miguéns-Gómez
Affiliation:
MoBioFood Research Group, Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, c/Marcel·lí Domingo nº1, 43007 Tarragona, Spain
Àngela Casanova-Martí
Affiliation:
MoBioFood Research Group, Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, c/Marcel·lí Domingo nº1, 43007 Tarragona, Spain
M. Teresa Blay
Affiliation:
MoBioFood Research Group, Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, c/Marcel·lí Domingo nº1, 43007 Tarragona, Spain
Ximena Terra
Affiliation:
MoBioFood Research Group, Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, c/Marcel·lí Domingo nº1, 43007 Tarragona, Spain
Raúl Beltrán-Debón
Affiliation:
MoBioFood Research Group, Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, c/Marcel·lí Domingo nº1, 43007 Tarragona, Spain
Esther Rodríguez-Gallego
Affiliation:
MoBioFood Research Group, Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, c/Marcel·lí Domingo nº1, 43007 Tarragona, Spain
Anna Ardévol*
Affiliation:
MoBioFood Research Group, Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, c/Marcel·lí Domingo nº1, 43007 Tarragona, Spain
Montserrat Pinent
Affiliation:
MoBioFood Research Group, Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, c/Marcel·lí Domingo nº1, 43007 Tarragona, Spain
*
*Corresponding author: Anna Ardévol, email anna.ardevol@urv.cat

Abstract

Glucagon-like peptide-1 (GLP-1) is an enterohormone with a key role in several processes controlling body homeostasis, including glucose homeostasis and food intake regulation. It is secreted by the intestinal cells in response to nutrients, such as glucose, fat and amino acids. In the present review, we analyse the effect of protein on GLP-1 secretion and clearance. We review the literature on the GLP-1 secretory effects of protein and protein hydrolysates, and the mechanisms through which they exert these effects. We also review the studies on protein from different sources that has inhibitory effects on dipeptidyl peptidase-4 (DPP4), the enzyme responsible for GLP-1 inactivation, with particular emphasis on specific sources and treatments, and the gaps there still are in knowledge. There is evidence that the protein source and the hydrolytic processing applied to them can influence the effects on GLP-1 signalling. The gastrointestinal digestion of proteins, for example, significantly changes their effectiveness at modulating this enterohormone secretion in both in vivo and in vitro studies. Nevertheless, little information is available regarding human studies and more research is required to understand their potential as regulators of glucose homeostasis.

Type
Review Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

These authors contributed equally to the present review.

References

Rehfeld, JF (1998) The new biology of gastrointestinal hormones. Physiol Rev 78, 10871108.CrossRefGoogle ScholarPubMed
Gunawardene, AR, Corfe, BM & Staton, CA (2011) Classification and functions of enteroendocrine cells of the lower gastrointestinal tract. Int J Exp Pathol 92, 219231.CrossRefGoogle ScholarPubMed
Sternini, C, Anselmi, L & Rozengurt, E (2008) Enteroendocrine cells: a site of “taste” in gastrointestinal chemosensing. Curr Opin Endocrinol Diabetes Obes 15, 7378.CrossRefGoogle ScholarPubMed
Pinent, M, Blay, M, Serrano, J, et al. (2015) Effects of flavanols on the enteroendocrine system: repercussions on food intake. Crit Rev Food Sci Nutr 57, 326334.CrossRefGoogle Scholar
Santos-Hernández, M, Miralles, B, Amigo, L, et al. (2018) Intestinal signaling of proteins and digestion-derived products relevant to satiety. J Agric Food Chem 66, 1012310131.CrossRefGoogle ScholarPubMed
Murphy, KG & Bloom, SR (2006) Gut hormones and the regulation of energy homeostasis. Nature 444, 854859.CrossRefGoogle ScholarPubMed
Le Roux, CW, Aylwin, SJB, Batterham, RL, et al. (2006) Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg 243, 108114.CrossRefGoogle ScholarPubMed
Kreymann, B, Williams, G, Ghatei, MA, et al. (1987) Glucagon-like peptide-1 7-36: a physiological incretin in man. Lancet ii, 13001304.CrossRefGoogle ScholarPubMed
Shaw, JE, Sicree, RA & Zimmet, PZ (2010) Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87, 414.CrossRefGoogle ScholarPubMed
Baggio, LL & Drucker, DJ (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132, 21312157.CrossRefGoogle ScholarPubMed
Vilsbøll, T & Holst, JJ (2004) Incretins, insulin secretion and type 2 diabetes mellitus. Diabetologia 47, 357366.CrossRefGoogle ScholarPubMed
Pick, A, Clark, J, Kubstrup, C, et al. (1998) Role of apoptosis in failure of beta-cell mass compansation for insulin resistance and beta-cell defects in the male Zucker diabetic fatty rat. Diabetes 47, 358364.CrossRefGoogle ScholarPubMed
Farilla, L, Hui, H, Bertolotto, C, et al. (2002) Glucagon-like peptide-1 promotes islet cell growth and inhibits apoptosis in Zucker diabetic rats. Endocrinology 143, 4397–408.CrossRefGoogle ScholarPubMed
Nauck, MA (2011) Incretin-based therapies for type 2 diabetes mellitus: properties, functions, and clinical implications. Am J Med 124, Suppl. 1, S3S18.CrossRefGoogle ScholarPubMed
Filippatos, TD, Athyros, VG & Elisaf, MS (2014) The pharmacokinetic considerations and adverse effects of DDP-4 inhibitors. Expert Opin Drug Metab Toxicol 10, 787812.CrossRefGoogle Scholar
Yu, DMT, Yao, T, Chowdhury, S, et al. (2010) The dipeptidyl peptidase IV family in cancer and cell biology. FEBS J 277, 11261144.CrossRefGoogle ScholarPubMed
Mentlein, R (1999) Dipeptidyl-peptidase IV (CD26) – role in the inactivation of regulatory peptides. Regul Pept 85, 924.CrossRefGoogle ScholarPubMed
Thoma, R, Löffler, B, Stihle, M, et al. (2003) Structural basis of proline-specific exopeptidase activity as observed in human dipeptidyl peptidase-IV. Structure 11, 947959.CrossRefGoogle ScholarPubMed
Havale, SH & Pal, M (2009) Medicinal chemistry approaches to the inhibition of dipeptidyl peptidase-4 for the treatment of type 2 diabetes. Bioorg Med Chem 17, 17831802.CrossRefGoogle Scholar
Holst, JJ (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87, 14091439.CrossRefGoogle ScholarPubMed
Khera, R, Murad, MH, Chandar, AK, et al. (2016) Association of pharmacological treatments for obesity with weight loss and adverse events: a systematic review and meta-analysis. JAMA 315, 2424–2234.CrossRefGoogle ScholarPubMed
Serrano, J, Casanova-Martí, À, Blay, MT, et al. (2017) Strategy for limiting food intake using food components aimed at multiple targets in the gastrointestinal tract. Trends Food Sci Technol 68, 113129.CrossRefGoogle Scholar
Elliott, RM, Morgan, LM, Tredger, JA, et al. (1993) Glucagon-like peptide-1(7-36)amide and glucose-dependent insulino tropic polypeptide secretion in response to nutrient ingestion in man: acute post-prandial and 24-h secretion patterns. J Endocrinol 138, 159166.CrossRefGoogle Scholar
Rocca, AS & Brubaker, PL (1999) Role of the vagus nerve in mediating proximal nutrient-induced glucagon-like peptide-1 secretion. Endocrinology 140, 16871694.CrossRefGoogle ScholarPubMed
Roberge, N & Brubaker, L (1993) Regulation of intestinal proglucagon-derived peptide secretion by glucose-dependent insulinotropic peptide in a novel enteroendocrine loop. Endocrinology 133, 233240.CrossRefGoogle Scholar
Cordier-Bussat, M, Bernard, C, Levenez, F, et al. (1998) Peptones stimulate both the secretion of the incretin hormone glucagon- like peptide 1 and the transcription of the proglucagon gene. Diabetes 47, 10381045.CrossRefGoogle ScholarPubMed
Gorboulev, V, Schürmann, A, Vallon, V, et al. (2012) Na+-d-glucose cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes 61, 187196.CrossRefGoogle ScholarPubMed
Kuhre, RE, Frost, CR, Svendsen, B, et al. (2015) Molecular mechanisms of glucose-stimulated GLP-1 secretion from perfused rat small intestine. Diabetes 64, 370382.CrossRefGoogle ScholarPubMed
Steinert, RE, Gerspach, AC, Gutmann, H, et al. (2011) The functional involvement of gut-expressed sweet taste receptors in glucose-stimulated secretion of glucagon-like peptide-1 (GLP-1) and peptide YY (PYY). Clin Nutr 30, 524532.CrossRefGoogle ScholarPubMed
Kokrashvili, Z, Mosinger, B & Margolskee, RF (2009) T1r3 and α-gustducin in gut regulate secretion of glucagon-like peptide-1. Ann N Y Acad Sci 1170, 9194.CrossRefGoogle ScholarPubMed
Hirasawa, A, Hara, T, Katsuma, S, et al. (2008) Free fatty acid receptors and drug discovery. Biol Pharm Bull 31, 18471851.CrossRefGoogle ScholarPubMed
Reimann, F (2010) Molecular mechanisms underlying nutrient detection by incretin-secreting cells. Int Dairy J 20, 236242.CrossRefGoogle ScholarPubMed
Domínguez Avila, JA, Rodrigo García, J, González Aguilar, GA, et al. (2017) The antidiabetic mechanisms of polyphenols related to increased glucagon-like peptide-1 (GLP1) and insulin signaling. Molecules 22, 903.CrossRefGoogle ScholarPubMed
Casanova-Martí, À, Serrano, J, Blay, MT, et al. (2017) Acute selective bioactivity of grape seed proanthocyanidins on enteroendocrine secretions in the gastrointestinal tract. Food Nutr Res 61, 1321347.CrossRefGoogle ScholarPubMed
González-Abuín, N, Martínez-Micaelo, N, Margalef, M, et al. (2014) A grape seed extract increases active glucagon-like peptide-1 levels after an oral glucose load in rats. Food Funct 5, 23572364.CrossRefGoogle ScholarPubMed
Gonzalez-Abuin, N, Martinez-Micaelo, N, Blay, M, et al. (2014) Grape-seed procyanidins prevent the cafeteria diet-induced decrease of glucagon-like peptide-1 production. J Agric Food Chem 62, 10661072.CrossRefGoogle ScholarPubMed
Pais, R, Gribble, FM & Reimann, F (2016) Signalling pathways involved in the detection of peptones by murine small intestinal enteroendocrine L-cells. Peptides 77, 915.CrossRefGoogle ScholarPubMed
Reimann, F, Williams, L, Da Silva Xavier, G, et al. (2004) Glutamine potently stimulates glucagon-like peptide-1 secretion from GLUTag cells. Diabetologia 47, 15921601.CrossRefGoogle ScholarPubMed
Mace, OJ, Schindler, M & Patel, S (2012) The regulation of K- and L-cell activity by GLUT2 and the calcium-sensing receptor CasR in rat small intestine. J Physiol 590, 29172936.CrossRefGoogle ScholarPubMed
Greenfield, JR, Farooqi, IS, Keogh, JM, et al. (2009) Oral glutamine increases circulating glucagon-like peptide 1, glucagon, and insulin concentrations in lean, obese, and type 2 diabetic subjects. Am J Clin Nutr 89, 106113.CrossRefGoogle ScholarPubMed
Samocha-Bonet, D, Wong, O, Synnott, EL, et al. (2011) Glutamine reduces postprandial glycemia and augments the glucagon-like peptide-1 response in type 2 diabetes patients. J Nutr 141, 12331238.CrossRefGoogle ScholarPubMed
Tolhurst, G, Zheng, Y, Parker, HE, et al. (2011) Glutamine triggers and potentiates glucagon-like peptide-1 secretion by raising cytosolic Ca2+ and cAMP. Endocrinology 152, 405413.CrossRefGoogle ScholarPubMed
Young, SH, Rey, O, Sternini, C, et al. (2010) Amino acid sensing by enteroendocrine STC-1 cells: role of the Na+-coupled neutral amino acid transporter 2. Am J Physiol Cell Physiol 298, 14011413.CrossRefGoogle ScholarPubMed
Mine, Y, Li-Chan, ECY & Jiang, B (2010) Biologically active food proteins and peptides in health: an overview. In Bioactive Proteins and Peptides as Functional Foods and Nutraceuticals, pp. 311 [Mine, Y, Li-Chan, E and Jiang, B, editors]. Oxford: Wiley-Blackwell.CrossRefGoogle Scholar
Bhat, ZF, Kumar, S & Bhat, HF (2015) Bioactive peptides of animal origin: a review. J Food Sci Technol 52, 53775392.CrossRefGoogle ScholarPubMed
Suleria, HAR, Gobe, G, Masci, P, et al. (2016) Marine bioactive compounds and health promoting perspectives; innovation pathways for drug discovery. Trends Food Sci Technol 50, 4455.CrossRefGoogle Scholar
Hsieh, CH, Wang, TY, Hung, CC, et al. (2015) Improvement of glycemic control in streptozotocin-induced diabetic rats by Atlantic salmon skin gelatin hydrolysate as the dipeptidyl-peptidase IV inhibitor. Food Funct 6, 18871892.CrossRefGoogle ScholarPubMed
Huang, SL, Hung, CC, Jao, CL, et al. (2014) Porcine skin gelatin hydrolysate as a dipeptidyl peptidase IV inhibitor improves glycemic control in streptozotocin-induced diabetic rats. J Funct Foods 11, 235242.CrossRefGoogle Scholar
Wang, TY, Hsieh, CH, Hung, CC, et al. (2015) Fish skin gelatin hydrolysates as dipeptidyl peptidase IV inhibitors and glucagon-like peptide-1 stimulators improve glycaemic control in diabetic rats: a comparison between warm- and cold-water fish. J Funct Foods 19, 330340.CrossRefGoogle Scholar
Hsieh, CC, Hernández-Ledesma, B, Fernández-Tomé, S, et al. (2015) Milk proteins, peptides, and oligosaccharides: effects against the 21st century disorders. Biomed Res Int 2015, 146840.CrossRefGoogle ScholarPubMed
Nongonierma, AB & Fitzgerald, RJ (2012) Biofunctional properties of caseinophosphopeptides in the oral cavity. Caries Res 46, 234267.CrossRefGoogle ScholarPubMed
Udenigwe, CC & Aluko, RE (2012) Food protein-derived bioactive peptides: production, processing, and potential health benefits. J Food Sci 77, R11R24.CrossRefGoogle ScholarPubMed
Geraedts, MCP, Troost, FJ, Fischer, MAJG, et al. (2011) Direct induction of CCK and GLP-1 release from murine endocrine cells by intact dietary proteins. Mol Nutr Food Res 55, 476484.CrossRefGoogle ScholarPubMed
Gillespie, AL, Calderwood, D, Hobson, L, et al. (2015) Whey proteins have beneficial effects on intestinal enteroendocrine cells stimulating cell growth and increasing the production and secretion of incretin hormones. Food Chem 189, 120128.CrossRefGoogle ScholarPubMed
Gillespie, AL & Green, BD (2016) The bioactive effects of casein proteins on enteroendocrine cell health, proliferation and incretin hormone secretion. Food Chem 211, 148159.CrossRefGoogle ScholarPubMed
Power-Grant, O, Bruen, C, Brennan, L, et al. (2015) In vitro bioactive properties of intact and enzymatically hydrolysed whey protein: targeting the enteroinsular axis. Food Funct 6, 972980.CrossRefGoogle ScholarPubMed
Hutchison, AT, Feinle-Bisset, C, Fitzgerald, PCE, et al. (2015) Comparative effects of intraduodenal whey protein hydrolysate on antropyloroduodenal motility, gut hormones, glycemia, appetite, and energy intake in lean and obese men. Am J Clin Nutr 102, 13231331.CrossRefGoogle ScholarPubMed
Ryan, AT, Feinle-Bisset, C, Kallas, A, et al. (2012) Intraduodenal protein modulates antropyloroduodenal motility, hormone release, glycemia, appetite, and energy intake in lean men. Am J Clin Nutr 96, 474482.CrossRefGoogle ScholarPubMed
Watson, LE, Phillips, LK, Wu, T, et al. (2019) Differentiating the effects of whey protein and guar gum preloads on postprandial glycemia in type 2 diabetes. Clin Nutr 38, 28272832.CrossRefGoogle ScholarPubMed
Jakubowicz, D, Froy, O, Ahrén, B, et al. (2014) Incretin, insulinotropic and glucose-lowering effects of whey protein pre-load in type 2 diabetes: a randomised clinical trial. Diabetologia 57, 18071811.CrossRefGoogle ScholarPubMed
Bendtsen, LQ, Lorenzen, JK, Gomes, S, et al. (2014) Effects of hydrolysed casein, intact casein and intact whey protein on energy expenditure and appetite regulation: a randomised, controlled, cross-over study. Br J Nutr 112, 14121422.CrossRefGoogle ScholarPubMed
Hall, WL, Millward, DJ, Long, SJ, et al. (2003) Casein and whey exert different effects on plasma amino acid profiles, gastrointestinal hormone secretion and appetite. Br J Nutr 89, 239248.CrossRefGoogle ScholarPubMed
Calbet, JAL & Holst, JJ (2004) Gastric emptying, gastric secretion and enterogastrone response after administration of milk proteins or their peptide hydrolysates in humans. Eur J Nutr 43, 127139.CrossRefGoogle ScholarPubMed
Mortensen, LS, Holmer-Jensen, J, Hartvigsen, ML, et al. (2012) Effects of different fractions of whey protein on postprandial lipid and hormone responses in type 2 diabetes. Eur J Clin Nutr 66, 799805.CrossRefGoogle ScholarPubMed
Overduin, J, Guérin-Deremaux, L, Wils, D, et al. (2015) NUTRALYS® pea protein: characterization of in vitro gastric digestion and in vivo gastrointestinal peptide responses relevant to satiety. Food Nutr Res 59, 2562225631.CrossRefGoogle ScholarPubMed
Häberer, D, Tasker, M, Foltz, M, et al. (2011) Intragastric infusion of pea-protein hydrolysate reduces test-meal size in rats more than pea protein. Physiol Behav 104, 10411047.CrossRefGoogle ScholarPubMed
Higuchi, N, Hira, T, Yamada, N, et al. (2013) Oral administration of corn zein hydrolysate stimulates GLP-1 and GIP secretion and improves glucose tolerance in male normal rats and Goto-Kakizaki rats. Endocrinology 154, 30893098.CrossRefGoogle ScholarPubMed
Hira, T, Mochida, T, Miyashita, K, et al. (2009) GLP-1 secretion is enhanced directly in the ileum but indirectly in the duodenum by a newly identified potent stimulator, zein hydrolysate, in rats. Am J Physiol Gastrointest Liver Physiol 297, G663G671.CrossRefGoogle ScholarPubMed
Ishikawa, Y, Hira, T, Inoue, D, et al. (2015) Rice protein hydrolysates stimulate GLP-1 secretion, reduce GLP-1 degradation, and lower the glycemic response in rats. Food Funct 6, 25252534.CrossRefGoogle ScholarPubMed
Kato, M, Nakanishi, T, Tani, T, et al. (2017) Low-molecular fraction of wheat protein hydrolysate stimulates glucagon-like peptide-1 secretion in an enteroendocrine L cell line and improves glucose tolerance in rats. Nutr Res 37, 3745.CrossRefGoogle Scholar
Chen, W, Hira, T, Nakajima, S, et al. (2018) Wheat gluten hydrolysate potently stimulates peptide-YY secretion and suppresses food intake in rats. Biosci Biotechnol Biochem 80, 19921999.CrossRefGoogle Scholar
Cudennec, B, Balti, R, Ravallec, R, et al. (2015) In vitro evidence for gut hormone stimulation release and dipeptidyl-peptidase IV inhibitory activity of protein hydrolysate obtained from cuttlefish (Sepia officinalis) viscera. Food Res Int 78, 238245.CrossRefGoogle ScholarPubMed
Caron, J, Domenger, D, Belguesmia, Y, et al. (2016) Protein digestion and energy homeostasis: how generated peptides may impact intestinal hormones? Food Res Int 88, 310318.CrossRefGoogle Scholar
Diakogiannaki, E, Pais, R, Tolhurst, G, et al. (2013) Oligopeptides stimulate glucagon-like peptide-1 secretion in mice through proton-coupled uptake and the calcium-sensing receptor. Diabetologia 56, 26882696.CrossRefGoogle ScholarPubMed
Modvig, IM, Kuhre, RE & Holst, JJ (2019) Peptone-mediated glucagon-like peptide-1 secretion depends on intestinal absorption and activation of basolaterally located Calcium-Sensing Receptors. Physiol Rep 7, e14056.CrossRefGoogle ScholarPubMed
Harnedy, PA, Parthsarathy, V, McLaughlin, CM, et al. (2018) Atlantic salmon (Salmo salar) co-product-derived protein hydrolysates: a source of antidiabetic peptides. Food Res Int 106, 598606.CrossRefGoogle ScholarPubMed
Caron, J, Cudennec, B, Domenger, D, et al. (2016) Simulated GI digestion of dietary protein: release of new bioactive peptides involved in gut hormone secretion. Food Res Int 89, 382390.CrossRefGoogle ScholarPubMed
Raka, F, Farr, S, Kelly, J, et al. (2019) Metabolic control via nutrient-sensing mechanisms: role of taste receptors and the gut–brain neuroendocrine axis. Am J Physiol Endocrinol Metab 317, E559E572.CrossRefGoogle ScholarPubMed
Choi, S, Lee, M, Shiu, AL, et al. (2007) Identification of a protein hydrolysate responsive G protein-coupled receptor in enterocytes. Am J Physiol Gastrointest Liver Physiol 292, 98112.CrossRefGoogle ScholarPubMed
Wang, H, Murthy, KS & Grider, JR (2019) Expression patterns of l-amino acid receptors in the murine STC-1 enteroendocrine cell line. Cell Tissue Res 378, 471–83.CrossRefGoogle ScholarPubMed
Le Nevé, B & Daniel, H (2011) Selected tetrapeptides lead to a GLP-1 release from the human enteroendocrine cell line NCI-H716. Regul Pept 167, 1420.CrossRefGoogle ScholarPubMed
Reimer, RA (2006) Meat hydrolysate and essential amino acid-induced glucagon-like peptide-1 secretion, in the human NCI-H716 enteroendocrine cell line, is regulated by extracellular signal-regulated kinase1/2 and p38 mitogen-activated protein kinases. J Endocrinol 191, 159170.CrossRefGoogle ScholarPubMed
Lacroix, IME & Li-Chan, ECY (2012) Dipeptidyl peptidase-IV inhibitory activity of dairy protein hydrolysates. Int Dairy J 25, 97102.CrossRefGoogle Scholar
Mojica, L, Chen, K & de Mejía, EG (2015) Impact of commercial precooking of common bean (Phaseolus vulgaris) on the generation of peptides, after pepsin-pancreatin hydrolysis, capable to inhibit dipeptidyl peptidase-IV. J Food Sci 80, H188H198.CrossRefGoogle ScholarPubMed
Lacroix, IME & Li-Chan, ECY (2013) Inhibition of dipeptidyl peptidase (DPP)-IV and α-glucosidase activities by pepsin-treated whey proteins. J Agric Food Chem 61, 75007506.CrossRefGoogle ScholarPubMed
Silveira, ST, Martínez-Maqueda, D, Recio, I, et al. (2013) Dipeptidyl peptidase-IV inhibitory peptides generated by tryptic hydrolysis of a whey protein concentrate rich in β-lactoglobulin. Food Chem 141, 10721077.CrossRefGoogle Scholar
Nongonierma, AB & FitzGerald, RJ (2013) Dipeptidyl peptidase IV inhibitory properties of a whey protein hydrolysate: influence of fractionation, stability to simulated gastrointestinal digestion and food–drug interaction. Int Dairy J 32, 3339.CrossRefGoogle Scholar
Konrad, B, Anna, D, Marek, S, et al. (2014) The evaluation of dipeptidyl peptidase (DPP)-IV, α-glucosidase and angiotensin converting enzyme (ACE) inhibitory activities of whey proteins hydrolyzed with serine protease isolated from Asian pumpkin (Cucurbita ficifolia). Int J Pept Res Ther 20, 483491.CrossRefGoogle ScholarPubMed
Boots, J-WP (2012) Protein hydrolysate enriched in peptides inhibiting DPP-IV and their use, US Pat. No. 8273710 B2.Google Scholar
Connolly, A, Piggott, CO & FitzGerald, RJ (2014) In vitro α-glucosidase, angiotensin converting enzyme and dipeptidyl peptidase-IV inhibitory properties of brewers’ spent grain protein hydrolysates. Food Res Int 56, 100107.CrossRefGoogle Scholar
Lacroix, IME & Li-Chan, ECY (2014) Isolation and characterization of peptides with dipeptidyl peptidase-IV inhibitory activity from pepsin-treated bovine whey proteins. Peptides 54, 3948.CrossRefGoogle ScholarPubMed
Nongonierma, AB & Fitzgerald, RJ (2014) An in silico model to predict the potential of dietary proteins as sources of dipeptidyl peptidase IV (DPP-IV) inhibitory peptides. Food Chem 165, 489498.CrossRefGoogle Scholar
Lambeir, A, Durinx, C, Scharpé, S, et al. (2003) Dipeptidyl-peptidase IV from bench to bedside: an update on structural properties, functions, and clinical aspects of the enzyme DPP IV. Crit Rev Clin Lab Sci 40, 209294.CrossRefGoogle ScholarPubMed
Power, O, Nongonierma, AB, Jakeman, P, et al. (2014) Food protein hydrolysates as a source of dipeptidyl peptidase IV inhibitory peptides for the management of type 2 diabetes. Proc Nutr Soc 73, 3446.CrossRefGoogle ScholarPubMed
Lan, VTT, Ito, K, Ohno, M, et al. (2015) Analyzing a dipeptide library to identify human dipeptidyl peptidase IV inhibitor. Food Chem 175, 6673.CrossRefGoogle ScholarPubMed
Tominaga, Y, Yokota, S, Tanaka, H, et al. (2012) Dipeptidyl peptidase-4 inhibitor. United States Patent US 2012/0189611.Google Scholar
Uchida, M, Ohshiba, Y & Mogami, O (2011) Novel dipeptidyl peptidase-4-inhibiting peptide derived from β-lactoglobulin. J Pharmacol Sci 117, 6366.CrossRefGoogle ScholarPubMed
Uenishi, H, Kabuki, T, Seto, Y, et al. (2012) Isolation and identification of casein-derived dipeptidyl-peptidase 4 (DPP-4)-inhibitory peptide LPQNIPPL from Gouda-type cheese and its effect on plasma glucose in rats. Int Dairy J 22, 2430.CrossRefGoogle Scholar
Casanova-Martí, À, Bravo, FI, Serrano, J, et al. (2019) Antihyperglycemic effect of a chicken feet hydrolysate via the incretin system: DPP-IV-inhibitory activity and GLP-1 release stimulation. Food Funct 10, 40624070.CrossRefGoogle ScholarPubMed
Wang, Y, Landheer, S, van Gilst, WH, et al. (2012) Attenuation of renovascular damage in Zucker diabetic fatty rat by NWT-03, an egg protein hydrolysate with ACE- and DPP4-inhibitory activity. PLOS ONE 2012, e46781.CrossRefGoogle Scholar
Mochida, T, Hira, T & Hara, H (2010) The corn protein, zein hydrolysate, administered into the ileum attenuates hyperglycemia via its dual action on glucagon-like peptide-1 secretion and dipeptidyl peptidase-IV activity in rats. Endocrinology 151, 30953104.CrossRefGoogle ScholarPubMed
Horner, K, Drummond, E & Brennan, L (2016) Bioavailability of milk protein-derived bioactive peptides: a glycaemic management perspective. Nutr Res Rev 29, 91101.CrossRefGoogle ScholarPubMed
Daniel, H, Spanier, B, Kottra, G, et al. (2006) From bacteria to man: archaic proton-dependent peptide transporters at work. Physiology 21, 93102.CrossRefGoogle Scholar
Wauson, EM, Lorente-Rodríguez, A & Cobb, MH (2013) Minireview: Nutrient sensing by G protein-coupled receptors. Mol Endocrinol 27, 11881197.CrossRefGoogle ScholarPubMed
Kinnamon, SC (2009) Umami taste transduction mechanisms. Am J Clin Nutr 90, 753755.CrossRefGoogle ScholarPubMed