Milk protein-derived peptides induce 5-HT2C-mediated satiety invivo

International Dairy Journal

Volumn 38, Issue 1, 2014, Pages 55-64

  Schellekens, Harriët ^a   Nongonierma, Alice B ^b   Clarke, Gerard ^a,c   van Oeffelen, Wesley E P A ^a   FitzGerald, Richard J ^b   Dinan, Timothy G ^a,c   Cryan, John F ^a,c  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY OF LIMERICK   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS;

CUMULATIVE FOOD INTAKES; DOSE-DEPENDENT; HUMAN EMBRYONIC KIDNEYS; INTRACELLULAR CALCIUM; INTRAPERITONEAL INJECTIONS; RECEPTOR ACTIVATION; SODIUM CASEINATE; WHEY PROTEIN HYDROLYSATES;

PEPTIDES;

EID: 84901197032     PISSN: 09586946     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.idairyj.2014.04.004     Document Type: Article

References (102)

1. Anderson G.H., Tecimer S.N., Shah D., Zafar T.A. Protein source, quantity, and time of consumption determine the effect of proteins on short-term food intake in young men. Journal of Nutrition 2004, 134:3011-3015.
2. Aronne L.J., Powell A.G., Apovian C.M. Emerging pharmacotherapy for obesity. Expert Opinion on Emerging Drugs 2011, 16:587-596.
3. Aziz A., Anderson G.H. Exendin-4, a GLP-1 receptor agonist, interacts with proteins and their products of digestion to suppress food intake in rats. Journal of Nutrition 2003, 133:2326-2330.
4. Baxter G., Kennett G., Blaney F., Blackburn T. 5-HT2 receptor subtypes: a family re-united?. Trends in Pharmacological Sciences 1995, 16:105-110.
5. Berg K.A., Clarke W.P., Cunningham K.A., Spampinato U. Fine-tuning serotonin2c receptor function in the brain: molecular and functional implications. Neuropharmacology 2008, 55:969-976.
6. Bloom S.R., Kuhajda F.P., Laher I., Pi-Sunyer X., Ronnett G.V., Tan T.M., et al. The obesity epidemic: pharmacological challenges. Molecular Interventions 2008, 8:82-98.
7. Booij L., Merens W., Markus C.R., Van der Does A.J. Diet rich in alpha-lactalbumin improves memory in unmedicated recovered depressed patients and matched controls. Journal of Psychopharmacology 2006, 20:526-535.
8. Boutrou R., Gaudichon C., Dupont D., Jardin J., Airinei G., Marsset-Baglieri A., et al. Sequential release of milk protein-derived bioactive peptides in the jejunum in healthy humans. American Journal of Clinical Nutrition 2013, 97:1314-1323.
9. Bowen J., Noakes M., Clifton P.M. Appetite regulatory hormone responses to various dietary proteins differ by body mass index status despite similar reductions in ad libitum energy intake. Journal of Clinical Endocrinology and Metabolism 2006, 91:2913-2919.
10. Bowen J., Noakes M., Trenerry C., Clifton P.M. Energy intake, ghrelin, and cholecystokinin after different carbohydrate and protein preloads in overweight men. Journal of Clinical Endocrinology and Metabolism 2006, 91:1477-1483.
11. Burns C.M., Chu H., Rueter S.M., Hutchinson L.K., Canton H., Sanders-Bush E., et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 1997, 387:303-308.
12. Burton-Freeman B.M. Glycomacropeptide (GMP) is not critical to whey-induced satiety, but may have a unique role in energy intake regulation through cholecystokinin (CCK). Physiology and Behavior 2008, 93:379-387.
13. Calbet J.A., Holst J.J. Gastric emptying, gastric secretion and enterogastrone response after administration of milk proteins or their peptide hydrolysates in humans. European Journal of Clinical Nutrition 2004, 43:127-139.
14. Cecchini M., Sassi F., Lauer J.A., Lee Y.Y., Guajardo-Barron V., Chisholm D. Tackling of unhealthy diets, physical inactivity, and obesity: health effects and cost-effectiveness. Lancet 2010, 376:1775-1784.
15. Chakrabarti R. Pharmacotherapy of obesity: emerging drugs and targets. Expert Opinion on Therapeutic Targets 2009, 13:195-207.
16. Dalton G.L., Lee M.D., Kennett G.A., Dourish C.T., Clifton P.G. mCPP-induced hyperactivity in 5-HT2C receptor mutant mice is mediated by activation of multiple 5-HT receptor subtypes. Neuropharmacology 2004, 46:663-671.
17. Dalton G.L., Lee M.D., Kennett G.A., Dourish C.T., Clifton P.G. Serotonin 1B and 2C receptor interactions in the modulation of feeding behaviour in the mouse. Psychopharmacology (Berlin) 2006, 185:45-57.
18. Derosa G., Maffioli P. Anti-obesity drugs: a review about their effects and their safety. Expert Opinion on Drug Safety 2012, 11:459-471.
19. Dougkas A., Reynolds C.K., Givens I.D., Elwood P.C., Minihane A.M. Associations between dairy consumption and body weight: a review of the evidence and underlying mechanisms. Nutrition Research Reviews 2011, 1-24.
20. Dutton A.C., Barnes N.M. Anti-obesity pharmacotherapy: future perspectives utilising 5-HT2C receptor agonists. Drug Discovery Today: Therapeutic Strategies 2006, 3:577-583.
21. Figlewicz D.P., Nadzan A.M., Sipols A.J., Green P.K., Liddle R.A., Porte D., et al. Intraventricular CCK-8 reduces single meal size in the baboon by interaction with type-A CCK receptors. American Journal of Physiology 1992, 263:R863-R867.
22. FitzGerald R.J., Murray B.A., Walsh D.J. Hypotensive peptides from milk proteins. Journal of Nutrition 2004, 134:980S-988S.
23. Follenzi A., Naldini L. Generation of HIV-1 derived lentiviral vectors. Methods in Enzymology 2002, 346:454-465.
24. Follenzi A., Naldini L. HIV-based vectors. Preparation and use. Methods in Molecular Medicine 2002, 69:259-274.
25. Foltz M., Meynen E.E., Bianco V., van Platerink C., Koning T.M., Kloek J. Angiotensin converting enzyme inhibitory peptides from a lactotripeptide-enriched milk beverage are absorbed intact into the circulation. Journal of Nutrition 2007, 137:953-958.
26. Froetschel M.A., Azain M.J., Edwards G.L., Barb C.R., Amos H.E. Opioid and cholecystokinin antagonists alleviate gastric inhibition of food intake by premeal loads of casein in meal-fed rats. Journal of Nutrition 2001, 131:3270-3276.
27. Gardner M.L.G. Entry of peptides of dietary origin into the circulation. Nutrition and Health 1983, 2:163-171.
28. Garfield A.S., Heisler L.K. Pharmacological targeting of the serotonergic system for the treatment of obesity. Journal of Physiology 2009, 587:49-60.
29. Gonzalez-Castejon M., Rodriguez-Casado A. Dietary phytochemicals and their potential effects on obesity: a review. Pharmacological Research 2011, 64:438-455.
30. Gooda Sahib N., Saari N., Ismail A., Khatib A., Mahomoodally F., Abdul Hamid A. Plants metabolites as potential antiobesity agents. Scientific World Journal 2012, 2012:8.
31. Halford J.C., Boyland E.J., Blundell J.E., Kirkham T.C., Harrold J.A. Pharmacological management of appetite expression in obesity. Nature Reviews Endocrinology 2010, 6:255-269.
32. Halford J.C., Harrold J.A., Boyland E.J., Lawton C.L., Blundell J.E. Serotonergic drugs: effects on appetite expression and use for the treatment of obesity. Drugs 2007, 67:27-55.
33. Hall W.L., Millward D.J., Long S.J., Morgan L.M. Casein and whey exert different effects on plasma amino acid profiles, gastrointestinal hormone secretion and appetite. British Journal of Nutrition 2003, 89:239-248.
34. Herve C., Beyne P., Jamault H., Delacoux E. Determination of tryptophan and its kynurenine pathway metabolites in human serum by high-performance liquid chromatography with simultaneous ultraviolet and fluorimetric detection. Journal of Chromatography B: Biomedical Sciences and Applications 1996, 675:157-161.
35. Hoyer D., Clarke D.E., Fozard J.R., Hartig P.R., Martin G.R., Mylecharane E.J., et al. International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacological Reviews 1994, 46:157-203.
36. Hoyer D., Hannon J.P., Martin G.R. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacology Biochemistry and Behavior 2002, 71:533-554.
37. Hursel R., van der Zee L., Westerterp-Plantenga M.S. Effects of a breakfast yoghurt, with additional total whey protein or caseinomacropeptide-depleted alpha-lactalbumin-enriched whey protein, on diet-induced thermogenesis and appetite suppression. British Journal of Nutrition 2010, 103:775-780.
38. Jandacek R.J. APD-356 (arena). Current Opinion in Investigational Drugs 2005, 6:1051-1056.
39. Kang J.G., Park C.Y. Anti-obesity drugs: a review about their effects and safety. Journal of Diabetes and Metabolism 2012, 36:13-25.
40. Kawahara Y., Grimberg A., Teegarden S., Mombereau C., Liu S., Bale T.L., et al. Dysregulated editing of serotonin 2C receptor mRNAs results in energy dissipation and loss of fat mass. Journal of Neuroscience 2008, 28:12834-12844.
41. Kennett G.A., Clifton P.G. New approaches to the pharmacological treatment of obesity: can they break through the efficacy barrier?. Pharmacology Biochemistry and Behavior 2010, 97:63-83.
42. Korhonen H. Milk-derived bioactive peptides: from science to applications. Journal of Functional Foods 2009, 1:177-187.
43. Korhonen H., Marnila P., Gill H.S. Bovine milk antibodies for health. British Journal of Nutrition 2000, 84:S135-S146.
44. Kreider R.B., Iosia M., Cooke M., Hudson G., Rasmussen C., Chen H., et al. Bioactive properties and clinical safety of a novel milk protein peptide. Nutrition Journal 2011, 10:99.
45. Kumar M., Verma V., Nagpal R., Kumar A., Behare P.V., Singh B., et al. Anticarcinogenic effect of probiotic fermented milk and chlorophyllin on aflatoxin-B1-induced liver carcinogenesis in rats. British Journal of Nutrition 2012, 107:1006-1016.
46. Lam D.D., Przydzial M.J., Ridley S.H., Yeo G.S., Rochford J.J., O'Rahilly S., et al. Serotonin 5-HT2C receptor agonist promotes hypophagia via downstream activation of melanocortin 4 receptors. Endocrinology 2008, 149:1323-1328.
47. Lonnerdal B. Nutritional and physiologic significance of human milk proteins. American Journal of Clinical Nutrition 2003, 77:1537S-1543S.
48. Luhovyy B.L., Akhavan T., Anderson G.H. Whey proteins in the regulation of food intake and satiety. Journal of the American College of Nutrition 2007, 26:704S-712S.
49. Martin C.K., Redman L.M., Zhang J., Sanchez M., Anderson C.M., Smith S.R., et al. Lorcaserin, a 5-HT(2C) receptor agonist, reduces body weight by decreasing energy intake without influencing energy expenditure. Journal of Clinical Endocrinology and Metabolism 2011, 96:837-845.
50. van Meijl L.E., Vrolix R., Mensink R.P. Dairy product consumption and the metabolic syndrome. Nutrition Research Reviews 2008, 21:148-157.
51. Meisel H., FitzGerald R.J. Biofunctional peptides from milk proteins: mineral binding and cytomodulatory effects. Current Pharmaceutical Design 2003, 9:1289-1295.
52. Miller K.J. Serotonin 5-ht2c receptor agonists: potential for the treatment of obesity. Molecular Interventions 2005, 5:282-291.
53. Morifuji M., Ishizaka M., Baba S., Fukuda K., Matsumoto H., Koga J., et al. Comparison of different sources and degrees of hydrolysis of dietary protein: effect on plasma amino acids, dipeptides, and insulin responses in human subjects. Journal of Agricultural and Food Chemistry 2010, 58:8788-8797.
54. Nagpal R., Behare P., Rana R., Kumar A., Kumar M., Arora S., et al. Bioactive peptides derived from milk proteins and their health beneficial potentials: an update. Food and Function 2011, 2:18-27.
55. Naldini L. Lentiviruses as gene transfer agents for delivery to non-dividing cells. Current Opinion in Biotechnology 1998, 9:457-463.
56. Naldini L., Blomer U., Gallay P., Ory D., Mulligan R., Gage F.H., et al. Invivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996, 272:263-267.
57. Nguyen N., Champion J.K., Ponce J., Quebbemann B., Patterson E., Pham B., et al. Areview of unmet needs in obesity management. Obesity Surgery 2012, 22:956-966.
58. Nieuwenhuizen A.G., Hochstenbach-Waelen A., Veldhorst M.A., Westerterp K.R., Engelen M.P., Brummer R.J., et al. Acute effects of breakfasts containing alpha-lactalbumin, or gelatin with or without added tryptophan, on hunger, 'satiety' hormones and amino acid profiles. British Journal of Nutrition 2009, 101:1859-1866.
59. Niswender C.M., Copeland S.C., Herrick-Davis K., Emeson R.B., Sanders-Bush E. RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. Journal of Biological Chemistry 1999, 274:9472-9478.
60. Nongonierma A.B., FitzGerald R.J. Biofunctional properties of caseinophosphopeptides in the oral cavity. Caries Research 2012, 46:234-267.
61. Nongonierma A.B., FitzGerald R.J. Tryptophan-containing milk protein-derived dipeptides inhibit xanthine oxidase. Peptides 2012, 37:263-272.
62. Nongonierma A.B., FitzGerald R.J. Dipeptidyl peptidase IV inhibitory and antioxidative properties of milk-derived dipeptides and hydrolysates. Peptides 2013, 39:157-163.
63. Nongonierma A.B., Schellekens H., Dinan T.G., Cryan J.F., Fitzgerald R.J. Milk protein hydrolysates activate 5-HT2C serotonin receptors: influence of the starting substrate and isolation of bioactive fractions. Food and Function 2013, 4:728-737.
64. O'Mahony S., Chua A.S., Quigley E.M., Clarke G., Shanahan F., Keeling P.W., et al. Evidence of an enhanced central 5HT response in irritable bowel syndrome and in the rat maternal separation model. Neurogastroenterology and Motility 2008, 20:680-688.
65. O'Neil P.M., Smith S.R., Weissman N.J., Fidler M.C., Sanchez M., Zhang J., et al. Randomized placebo-controlled clinical trial of Lorcaserin for weight loss in type 2 diabetes mellitus: the BLOOM-DM study. Obesity 2012, 20:1426-1436.
66. Obici S. Minireview: molecular targets for obesity therapy in the brain. Endocrinology 2009, 150:2512-2517.
67. Olaghere da Silva U.B., Morabito M.V., Canal C.E., Airey D.C., Emeson R.B., Sanders-Bush E. Impact of RNA editing on functions of the serotonin 2C receptor invivo. Frontiers in Neuroscience 2010, 4:26.
68. Ono T., Morishita S., Murakoshi M. Novel function of bovine lactoferrin in lipid metabolism: visceral fat reduction by enteric-coated lactoferrin. PharmaNutrition 2013, 1:32-34.
69. Ono T., Murakoshi M., Suzuki N., Iida N., Ohdera M., Iigo M., et al. Potent anti-obesity effect of enteric-coated lactoferrin: decrease in visceral fat accumulation in Japanese men and women with abdominal obesity after 8-week administration of enteric-coated lactoferrin tablets. British Journal of Nutrition 2010, 104:1688-1695.
70. Orosco M., Rouch C., Beslot F., Feurte S., Regnault A., Dauge V. Alpha-lactalbumin-enriched diets enhance serotonin release and induce anxiolytic and rewarding effects in the rat. Behavioural Brain Research 2004, 148:1-10.
71. Phelan M., Kerins D. The potential role of milk-derived peptides in cardiovascular disease. Food and Function 2011, 2:153-167.
72. Pilvi T.K., Korpela R., Huttunen M., Vapaatalo H., Mervaala E.M. High-calcium diet with whey protein attenuates body-weight gain in high-fat-fed C57Bl/6J mice. British Journal of Nutrition 2007, 98:900-907.
73. Pilvi T.K., Storvik M., Louhelainen M., Merasto S., Korpela R., Mervaala E.M. Effect of dietary calcium and dairy proteins on the adipose tissue gene expression profile in diet-induced obesity. Journal of Nutrigenetics and Nutrigenomics 2008, 1:240-251.
74. Powell A.G., Apovian C.M., Aronne L.J. New drug targets for the treatment of obesity. Clinical Pharmacology and Therapeutics 2011, 90:40-51.
75. Powell T.M., Khera A. Therapeutic approaches to obesity. Current Treatment Options in Cardiovascular Medicine 2010, 12:381-395.
76. Power O., Jakeman P., FitzGerald R.J. Antioxidative peptides: enzymatic production, invitro and invivo antioxidant activity and potential applications of milk-derived antioxidative peptides. Amino Acids 2013, 44:797-820.
77. Quirós A., Dávalos A., Lasunción M.A., Ramos M., Recio I. Bioavailability of the antihypertensive peptide LHLPLP: transepithelial flux of HLPLP. International Dairy Journal 2008, 18:279-286.
78. Reddy I.M., Kella N.K.D., Kinsella J.E. Structural and conformational basis of the resistance of beta-lactoglobulin to peptic and chymotryptic digestion. Journal of Agricultural and Food Chemistry 1988, 36:737-741.
79. Redman L.M., Ravussin E. Lorcaserin for the treatment of obesity. Drugs Today (Barcelona) 2010, 46:901-910.
80. Ricci-Cabello I., Herrera M.O., Artacho R. Possible role of milk-derived bioactive peptides in the treatment and prevention of metabolic syndrome. Nutrition Reviews 2012, 70:241-255.
81. Rothman R.B., Baumann M.H., Savage J.E., Rauser L., McBride A., Hufeisen S.J., et al. Evidence for possible involvement of 5-HT(2B) receptors in the cardiac valvulopathy associated with fenfluramine and other serotonergic medications. Circulation 2000, 102:2836-2841.
82. le Roux C.W., Bloom S.R. Peptide YY, appetite and food intake. Proceedings of the Nutrition Society 2005, 64:213-216.
83. Satake M., Enjoh M., Nakamura Y., Takano T., Kawamura Y., Arai S., et al. Transepithelial transport of the bioactive tripeptide, Val-Pro-Pro, in human intestinal Caco-2 cell monolayers. Biosciences, Biotechnology and Biochemistry 2002, 66:378-384.
84. Schellekens H., Clarke G., Jeffery I.B., Dinan T.G., Cryan J.F. Dynamic 5-HT2C receptor editing in a mouse model of obesity. PLoS One 2012, 7:e32266.
85. Schellekens H., Dinan T.G., Cryan J.F. Lean mean fat reducing "ghrelin" machine: hypothalamic ghrelin and ghrelin receptors as therapeutic targets in obesity. Neuropharmacology 2009, 58:2-16.
86. Schellekens H., van Oeffelen W.E., Dinan T.G., Cryan J.F. Promiscuous dimerization of the growth hormone secretagogue receptor (GHS-R1a) attenuates ghrelin-mediated signaling. Journal of Biological Chemistry 2013, 288:181-191.
87. Shimizu M., Tsunogai M., Arai S. Transepithelial transport of oligopeptides in the human intestinal cell, Caco-2. Peptides 1997, 18:681-687.
88. Sokolov O.Y., Pryanikova N.A., Kost N.V., Zolotarev Y.A., Ryukert E.N., Zozulya A.A. Reactions between beta-casomorphins-7 and 5-HT2-serotonin receptors. Bulletin of Experimental Biology and Medicine 2005, 140:582-584.
89. Somerville E.M., Horwood J.M., Lee M.D., Kennett G.A., Clifton P.G. 5-HT(2C) receptor activation inhibits appetitive and consummatory components of feeding and increases brain c-fos immunoreactivity in mice. European Journal of Neuroscience 2007, 25:3115-3124.
90. Spellman D., O'Cuinn G., FitzGerald R.J. Bitterness in Bacillus proteinase hydrolysates of whey proteins. Food Chemistry 2009, 114:440-446.
91. Staljanssens D., Van Camp J., Billiet A., De Meyer T., Al Shukor N., De Vos W.H., et al. Screening of soy and milk protein hydrolysates for their ability to activate the CCK1 receptor. Peptides 2012, 34:226-231.
92. Tecott L.H. Serotonin and the orchestration of energy balance. Cell Metabolism 2007, 6:352-361.
93. Tecott L.H., Sun L.M., Akana S.F., Strack A.M., Lowenstein D.H., Dallman M.F., et al. Eating disorder and epilepsy in mice lacking 5-HT2c serotonin receptors. Nature 1995, 374:542-546.
94. Valentino M.A., Lin J.E., Waldman S.A. Central and peripheral molecular targets for antiobesity pharmacotherapy. Clinical Pharmacology and Therapeutics 2010, 87:652-662.
95. Veldhorst M.A., Nieuwenhuizen A.G., Hochstenbach-Waelen A., van Vught A.J., Westerterp K.R., Engelen M.P., et al. Dose-dependent satiating effect of whey relative to casein or soy. Physiology and Behavior 2009, 96:675-682.
96. Vermeirssen V., Deplancke B., Tappenden K.A., Van Camp J., Gaskins H.R., Verstraete W. Intestinal transport of the lactokinin Ala-Leu-Pro-Met-His-Ile-Arg through a Caco-2 Bbe monolayer. Journal of Peptide Science 2002, 8:95-100.
97. Vickers S.P., Clifton P.G., Dourish C.T., Tecott L.H. Reduced satiating effect of d-fenfluramine in serotonin 5-HT(2C) receptor mutant mice. Psychopharmacology (Berlin) 1999, 143:309-314.
98. Vickers S.P., Dourish C.T., Kennett G.A. Evidence that hypophagia induced by d-fenfluramine and d-norfenfluramine in the rat is mediated by 5-HT2C receptors. Neuropharmacology 2001, 41:200-209.
99. Vigna E., Naldini L. Lentiviral vectors: excellent tools for experimental gene transfer and promising candidates for gene therapy. Journal of Gene Medicine 2000, 2:308-316.
100. Virtanen T., Pihlanto A., Akkanen S., Korhonen H. Development of antioxidant activity in milk whey during fermentation with lactic acid bacteria. Journal of Applied Microbiology 2007, 102:106-115.
101. Werry T.D., Loiacono R., Sexton P.M., Christopoulos A. RNA editing of the serotonin 5HT2C receptor and its effects on cell signalling, pharmacology and brain function. Pharmacology and Therapeutics 2008, 119:7-23.
102. Zemel M.B. The role of dairy foods in weight management. Journal of the American College of Nutrition 2005, 24:537S-546S.