Glycomacropeptide, a low-phenylalanine protein isolated from cheese whey, supports growth and attenuates metabolic stress in the murine model of phenylketonuria

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 7, 2012, Pages

  Solverson, Patrick ^a   Murali, Sangita G ^a   Brinkman, Adam S ^a,b   Nelson, David W ^a   Clayton, Murray K ^a   Yen, Chi Liang Eric ^a   Ney, Denise M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Department Surgery ^*  (United States)

Author keywords

Amino acid metabolism; Cytokines; Energy balance; Indirect calorimetry; Splenomegaly

Indexed keywords

CARBON DIOXIDE; CASEIN; CYTOKINE; GLYCOPROTEIN; OXYGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY MASS; CALORIMETRY; CONTROLLED STUDY; DUAL ENERGY X RAY ABSORPTIOMETRY; ENERGY BALANCE; ENERGY EXPENDITURE; FEMALE; FLUID INTAKE; FOOD INTAKE; GENOTYPE; GROWTH; KIDNEY MASS; LUNG GAS EXCHANGE; MALE; METABOLIC STRESS; MOUSE; NONHUMAN; PHENYLKETONURIA; PRIORITY JOURNAL; PROTEIN ISOLATION; SPLEEN SIZE; WHEY; WILD TYPE;

ABSORPTIOMETRY, PHOTON; AMINO ACIDS; ANIMALS; BODY COMPOSITION; BODY WEIGHT; CASEINS; CHEESE; CYTOKINES; DIET; DIET, PROTEIN-RESTRICTED; ENERGY METABOLISM; GROWTH; MICE; MICE, INBRED C57BL; ORGAN SIZE; OXYGEN CONSUMPTION; PEPTIDE FRAGMENTS; PHENOTYPE; PHENYLKETONURIAS; SPLEEN; SPLENOMEGALY;

EID: 84859461332     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00647.2011     Document Type: Article

References (58)

1. Acheson KJ, Blondel-Lubrano A, Oguey-Araymon S, Beaumont M, Emady-Azar S, Ammon-Zufferey C, Monnard I, Pinaud S, Nielsen-Moennoz C, Bovetto L. Protein choices targeting thermogenesis and metabolism. Am J Clin Nutr 93: 525-534, 2011.
2. Aimutis WR. Bioactive properties of milk proteins with particular focus on anticariogenesis. J Nutr 134: 989S-995S, 2004.
3. Albersen M, Bonthuis M, de Roos NM, van den Hurk DA, Carbasius Weber E, Hendriks MM, de sain-van der Velden MG, de Koning TJ, Visser G. Whole body composition analysis by the BodPod air-displacement plethysmography method in children with phenylketonuria shows a higher body fat percentage. J Inherit Metab Dis Jun 24, 2010.
4. Allen JR, McCauley JC, Waters DL, O'Connor J, Roberts DC, Gaskin KJ. Resting energy expenditure in children with phenylketonuria. Am J Clin Nutr 62: 797-801, 1995.
5. Anderson GH, Tecimer SN, Shah D, Zafar TA. Protein source, quantity, and time of consumption determine the effect of proteins on short-term food intake in young men. J Nutr 134: 3011-3015, 2004.
6. Arnold GL, Vladutiu CJ, Kirby RS, Blakely EM, Deluca JM. Protein insufficiency and linear growth restriction in phenylketonuria. J Pediatr 141: 243-246, 2002.
7. Baer DJ, Stote KS, Paul DR, Harris GK, Rumpler WV, Clevidence BA. Whey protein but not soy protein supplementation alters body weight and composition in free-living overweight and obese adults. J Nutr 141: 1489-1494, 2011.
8. Brody EP. Biological activities of bovine glycomacropeptide. Br J Nutr 84, Suppl 1: S39-S46, 2000.
9. Burton-Freeman BM. Glycomacropeptide (GMP) is not critical to whey-induced satiety, but may have a unique role in energy intake regulation through cholecystokinin (CCK). Physiol Behav 93: 379-387, 2008.
10. Campbell IK, van Nieuwenhuijze A, Segura E, O'Donnell K, Coghill E, Hommel M, Gerondakis S, Villadangos JA, Wicks IP. Differentiation of inflammatory dendritic cells is mediated by NF-kappaB1-depen-dent GM-CSF production in CD4 T cells. J Immunol 186: 5468-5477, 2011.
11. Chabance B, Marteau P, Rambaud JC, Migliore-Samour D, Boynard M, Perrotin P, Guillet R, Jolles P, Fiat AM. Casein peptide release and passage to the blood in humans during digestion of milk or yogurt. Biochimie 80: 155-165, 1998.
12. Colman RJ, Nam G, Huchthausen L, Mulligan JD, Saupe KW. Energy restriction-induced changes in body composition are age specific in mice. J Nutr 137: 2247-2251, 2007.
13. Dangin M, Boirie Y, Garcia-Rodenas C, Gachon P, Fauquant J, Callier P, Ballevre O, Beaufrere B. The digestion rate of protein is an independent regulating factor of postprandial protein retention. Am J Physiol Endocrinol Metab 280: E340-E348, 2001.
14. Donlon J, Levy H, Scriver C. Hyperphenylalaninemia: phenylalanine hydroxylase deficiency. In: Metabolic and Molecular Basis of Inherited Disease, edited by Scriver C, Beaudet A, Sly W, and Valle D. New York: McGraw-Hill, 2007, chapt. 77, p. 1-150.
15. Egle A, Harris AW, Bath ML, O'Reilly L, Cory S. VavP-Bcl2 trans-genic mice develop follicular lymphoma preceded by germinal center hyperplasia. Blood 103: 2276-2283, 2004.
16. Enns GM, Koch R, Brumm V, Blakely E, Suter R, Jurecki E. Suboptimal outcomes in patients with PKU treated early with diet alone: revisiting the evidence. Mol Genet Metab 101: 99-109, 2010.
17. Etzel MR. Manufacture and use of dairy protein fractions. J Nutr 134: 996S-1002S, 2004.
18. Gropper SS, Acosta PB. Effect of simultaneous ingestion of L-amino acids and whole protein on plasma amino acid and urea nitrogen concentrations in humans. JPEN J Parenter Enteral Nutr 15: 48-53, 1991.
19. Hall WL, Millward DJ, Long SJ, Morgan LM. Casein and whey exert different effects on plasma amino acid profiles, gastrointestinal hormone secretion and appetite. Br J Nutr 89: 239-248, 2003.
20. Harding CO, Gillingham MB, Hamman K, Clark H, Goebel-Daghighi E, Bird A, Koeberl DD. Complete correction of hyperphenylalaninemia following liver-directed, recombinant AAV2/8 vector-mediated gene therapy in murine phenylketonuria. Gene Ther 13: 457-462, 2006.
21. Kaiyala KJ, Schwartz MW. Toward a more complete (and less controversial) understanding of energy expenditure and its role in obesity pathogenesis. Diabetes 60: 17-23, 2011.
22. Kelleher SL, Chatterton D, Nielsen K, Lonnerdal B. Glycomacropep-tide and alpha-lactalbumin supplementation of infant formula affects growth and nutritional status in infant rhesus monkeys. Am J Clin Nutr 77: 1261-1268, 2003.
23. Koch R, Burton B, Hoganson G, Peterson R, Rhead W, Rouse B, Scott R, Wolff J, Stern AM, Guttler F, Nelson M, de la Cruz F, Coldwell J, Erbe R, Geraghty MT, Shear C, Thomas J, Azen C. Phenylketonuria in adulthood: a collaborative study. J Inherit Metab Dis 25: 333-346, 2002.
24. Krissansen GW. Emerging health properties of whey proteins and their clinical implications. J Am Coll Nutr 26: 713S-723S, 2007.
25. Laclair CE, Ney DM, MacLeod EL, Etzel MR. Purification and use of glycomacropeptide for nutritional management of phenylketonuria. J Food Sci 74: E199-E206, 2009.
26. Lam SM, Moughan PJ, Awati A, Morton HR. The influence of whey protein and glycomacropeptide on satiety in adult humans. Physiol Behav 96: 162-168, 2009.
27. Li EW, Mine Y. Immunoenhancing effects of bovine glycomacropeptide and its derivatives on the proliferative response and phagocytic activities of human macrophagelike cells, U937. J Agric Food Chem 52: 2704- 2708, 2004.
28. Lim K, van Calcar SC, Nelson KL, Gleason ST, Ney DM. Acceptable low-phenylalanine foods and beverages can be made with glycomacro-peptide from cheese whey for individuals with PKU. Mol Genet Metab 92: 176-178, 2007.
29. Lopez-Posadas R, Requena P, Gonzalez R, Suarez MD, Zarzuelo A, Sanchez de Medina F, Martinez-Augustin O. Bovine glycomacropep-tide has intestinal antiinflammatory effects in rats with dextran sulfate-induced colitis. J Nutr 140: 2014-2019, 2010.
30. Macleod EL, Clayton MK, van Calcar SC, Ney DM. Breakfast with glycomacropeptide compared with amino acids suppresses plasma ghrelin levels in individuals with phenylketonuria. Mol Genet Metab 100: 303-308, 2010.
31. MacLeod EL, Ney DM. Nutritional management of phenylketonuria. Ann Nestle 68: 58-69, 2010.
32. McDonald JD, Bode VC, Dove WF, Shedlovsky A. Pahhph-5: a mouse mutant deficient in phenylalanine hydroxylase. Proc Natl Acad Sci U S A 87: 1965-1967, 1990.
33. McStravick N, Robertson LV, Ripley S, Weetch E, Adams D, Mic-ciche A. Body mass index in adult patients with diet treated phenylketo-nuria (Abstract). J Inherit Metab Dis 33: S107, 2010.
34. Metges CC, El-Khoury AE, Selvaraj AB, Tsay RH, Atkinson A, Regan MM, Bequette BJ, Young VR. Kinetics of L-[1-(13)C]leucine when ingested with free amino acids, unlabeled or intrinsically labeled casein. Am J Physiol Endocrinol Metab 278: E1000-E1009, 2000.
35. Mochizuki S, Mizukami H, Ogura T, Kure S, Ichinohe A, Kojima K, Matsubara Y, Kobayahi E, Okada T, Hoshika A, Ozawa K, Kume A. Long-term correction of hyperphenylalaninemia by AAV-mediated gene transfer leads to behavioral recovery in phenylketonuria mice. Gene Ther 11: 1081-1086, 2004.
36. Nakajima K, Tamura N, Kobayashi-Hattori K, Yoshida T, Hara-Kudo Y, Ikedo M, Sugita-Konishi Y, Hattori M. Prevention of intestinal infection by glycomacropeptide. Biosci Biotechnol Biochem 69: 2294- 2301, 2005.
37. Nelson DW, Gao Y, Spencer NM, Bahn T, Yen CL. Deficiency of the monoacylglycerol acyltransferase MGAT2 increases energy expenditure without high-fat feeding and protects genetically obese mice from excessive weight gain. J Lipid Res 52: 1723-1732, 2011.
38. Ney DM, Gleason ST, van Calcar SC, Macleod EL, Nelson KL, Etzel MR, Rice GM, Wolff JA. Nutritional management of PKU with glyco-macropeptide from cheese whey. J Inherit Metab Dis 32: 32-39, 2009.
39. Ney DM, Hull AK, van Calcar SC, Liu X, Etzel MR. Dietary glyco-macropeptide supports growth and reduces the concentrations of phenyl-alanine in plasma and brain in a murine model of phenylketonuria. J Nutr 138: 316-322, 2008.
40. NIH. Phenylketonuria (PKU): Screening and Management. NIH Consensus Statement. Bethesda, MD: National Institutes of Health, 2000, vol. 17, p. 1-33.
41. NRC. Nutrient Requirements of the Mouse. In: Nutrient Requirements of Laboratory Animals. Washington, DC: National Academy Press, 1995, p. 80-102.
42. Quirk ME, Schmotzer BJ, Singh RH. Predictive equations underestimate resting energy expenditure in female adolescents with phenylketo-nuria. J Am Diet Assoc 110: 922-925, 2010.
43. Raff H, Bruder ED, Jankowski B, Oaks MK, Colman RJ. Growth hormone therapy during neonatal hypoxia in rats: body composition, bone mineral density, and insulin-like growth factor-1 expression. Endocrine 16: 139-143, 2001.
44. Raff H, Bruder ED, Jankowski BM, Colman RJ. Effect of neonatal hypoxia on leptin, insulin, growth hormone and body composition in the rat. Horm Metab Res 33: 151-155, 2001.
45. Requena P, Daddaoua A, Guadix E, Zarzuelo A, Suarez MD, Sanchez de Medina F, Martinez-Augustin O. Bovine glycomacropeptide induces cytokine production in human monocytes through the stimulation of the MAPK and the NF-kappaB signal transduction pathways. Br J Pharmacol 157: 1232-1240, 2009.
46. Requena P, Daddaoua A, Martinez-Plata E, Gonzalez M, Zarzuelo A, Suarez MD, Sanchez de Medina F, Martinez-Augustin O. Bovine glycomacropeptide ameliorates experimental rat ileitis by mechanisms involving downregulation of interleukin 17. Br J Pharmacol 154: 825- 832, 2008.
47. Requena P, Gonzalez R, Lopez-Posadas R, Abadia-Molina A, Suarez MD, Zarzuelo A, de Medina FS, Martinez-Augustin O. The intestinal antiinflammatory agent glycomacropeptide has immunomodulatory actions on rat splenocytes. Biochem Pharmacol 79: 1797-1804, 2010.
48. Rogers QR, Harper AE. Amino acid diets and maximal growth in the rat. J Nutr 87: 267-273, 1965.
49. Royle PJ, McIntosh GH, Clifton PM. Whey protein isolate and glyco-macropeptide decrease weight gain and alter body composition in male Wistar rats. Br J Nutr 100: 88-93, 2008.
50. Santos K, Rocha Wannmacher MCMD, Wajner M. The influence of organic acids on the proliferation of human peripheral lymphocytes activated by concanavalin A and pokeweed mitogen. Int J Immunophar-macol 18: 761-769, 1996.
51. Shimizu K, Ogura H, Goto M, Asahara T, Nomoto K, Morotomi M, Yoshiya K, Matsushima A, Sumi Y, Kuwagata Y, Tanaka H, Shimazu T, Sugimoto H. Altered gut flora and environment in patients with severe SIRS. J Trauma 60: 126-133, 2006.
52. Slocum RH, Cummings JG. Amino acid analysis of physiological samples. In: Techniques in Diagnostic Human Biochemical Genetics: A Laboratory Manual, edited by Hommes FA. New York: Wiley-Liss, 1991, p. 87-126.
53. Surendran S, Campbell GA, Tyring SK, Matalon K, McDonald JD, Matalon R. High levels of orexin A in the brain of the mouse model for phenylketonuria: possible role of orexin A in hyperactivity seen in children with PKU. Neurochem Res 28: 1891-1894, 2003.
54. Van Calcar SC, Macleod EL, Gleason ST, Etzel MR, Clayton MK, Wolff JA, Ney DM. Improved nutritional management of phenylketonuria by using a diet containing glycomacropeptide compared with amino acids. Am J Clin Nutr 89: 1068-1077, 2009.
55. Veldhorst MA, Nieuwenhuizen AG, Hochstenbach-Waelen A, van Vught AJ, Westerterp KR, Engelen MP, Brummer RJ, Deutz NE. Westerterp-Plantenga M.S Dose-dependent satiating effect of whey relative to casein or soy Physiol Behav 96: 675-682, 2009.
56. Veldhorst MA, Nieuwenhuizen AG, Hochstenbach-Waelen A, West-erterp KR, Engelen MP, Brummer RJ, Deutz NE, and Westerterp-Plantenga M.S Effects of complete whey-protein breakfasts versus whey without GMP-breakfasts on energy intake and satiety Appetite 52: 388-395, 2009.
57. Walter JH, White FJ, Hall SK, MacDonald A, Rylance G, Boneh A, Francis DE, Shortland GJ, Schmidt M, Vail A. How practical are recommendations for dietary control in phenylketonuria? Lancet 360: 55-57, 2002.
58. Wang Z, Ying Z, Bosy-Westphal A, Zhang J, Heller M, Later W, Heymsfield SB, Muller MJ. Evaluation of specific metabolic rates of major organs and tissues: comparison between men and women. Am J Hum Biol 23: 333-338, 2011.