Advanced Glycation End Products in Infant Formulas Do Not Contribute to Insulin Resistance Associated with Their Consumption

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Klenovics, Kristína Simon ^a,b   Boor, Peter ^b,c   Somoza, Veronika ^d,e   Celec, Peter ^b   Fogliano, Vincenzo ^f   Šebeková, Katarína ^a,b  

^a SLOVAK MEDICAL UNIVERSITY   (Slovakia)

^b Faculty of Natural Sciences   (Slovakia)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d DEUTSCHE FORSCHUNGSANSTALT FÜR LEBENSMITTELCHEMIE   (Germany)

^e UNIVERSITY OF VIENNA   (Austria)

^f UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

8 ISOPROSTANE; ADVANCED GLYCATION END PRODUCT; CELL ADHESION MOLECULE; INSULIN; LEPTIN; LYSINE; MALONALDEHYDE;

AMINO ACID BLOOD LEVEL; ARTICLE; ARTIFICIAL MILK; BREAST MILK; COHORT ANALYSIS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE MARKER; FLUORESCENCE ANALYSIS; FOLLOW UP; FOOD INTAKE; HORMONE BLOOD LEVEL; HORMONE DETERMINATION; HUMAN; INFANT; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEPTIN BLOOD LEVEL; LYSINE BLOOD LEVEL; OXIDATIVE STRESS;

BREAST FEEDING; COHORT STUDIES; CROSS-SECTIONAL STUDIES; DIET; FEMALE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; INFANT; INFANT FORMULA; INFLAMMATION; INSULIN RESISTANCE; LYSINE; MALE; MILK, HUMAN; OXIDATIVE STRESS;

RODENTIA;

EID: 84871776714     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053056     Document Type: Article

References (70)

1. Dabelea D, (2009) The accelerating epidemic of childhood diabetes. Lancet 373: 1999-2000.
2. Dandona P, Aljada A, Bandyopadhyay A, (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25: 4-7.
3. Mericq V, Ong KK, Bazaes R, Pena V, Avila A, et al. (2005) Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational-age children. Diabetologia 48: 2609-2614.
4. Lucas A, Boyes S, Bloom SR, Aynsley-Green A, (1981) Metabolic and endocrine responses to a milk feed in six-day-old term infants: differences between breast and cow's milk formula feeding. Acta Paediatr Scand 70: 195-200.
5. Ginsburg BE, Lindblad BS, Lundsjo A, Persson B, Zetterstrom R, (1984) Plasma valine and urinary C-peptide in breast-fed and artificially fed infants up to 6 months of age. Acta Paediatr Scand 73: 213-217.
6. Madsen AL, Schack-Nielsen L, Larnkjaer A, Molgaard C, Michaelsen KF, (2010) Determinants of blood glucose and insulin in healthy 9-month-old term Danish infants; the SKOT cohort. Diabet Med 27: 1350-1357.
7. Heird WC, (2007) Progress in promoting breast-feeding, combating malnutrition, and composition and use of infant formula, 1981-2006. J Nutr 137: 499S-502S.
8. Leung AKC, Sauve RS, (2005) Breast is best for babies. J Natl Med Assoc 97: 1010-1019.
9. Schack-Nielsen L, Michaelsen KE, (2007) Advances in our understanding of the biology of human milk and its effects on the offspring. J Nutr 137: 503S-510S.
10. Das UN, (2002) The lipids that matter from infant nutrition to insulin resistance. Prostaglandins Leukot Essent Fatty Acids 67: 1-12.
11. Savino F, Fissore MF, Liguori SA, Oggero R, (2009) Can hormones contained in mothers' milk account for the beneficial effect of breast-feeding on obesity in children? Clin Endocrinol (Oxf) 71: 757-765.
12. Kerkhof GF, Leunissen RW, Hokken-Koelega AC, (2012) Early origins of the metabolic syndrome: role of small size at birth, early postnatal weight gain, and adult IGF-I. J Clin Endocrinol Metab 8: 2637-2643.
13. Mericq V, Piccardo C, Cai W, Chen X, Zhu L, et al. (2010) Maternally transmitted and food-derived glycotoxins: a factor preconditioning the young to diabetes? Diabetes Care 33: 2232-2237.
14. Sebekova K, Saavedra G, Zumpe C, Somoza V, Klenovicsova K, et al. (2008) Plasma concentration and urinary excretion of N epsilon-(carboxymethyl)lysine in breast milk- and formula-fed infants. Ann N Y Acad Sci 1126: 177-180.
15. Birlouez-Aragon I, Pischetsrieder M, Leclére J, Morales FJ, Hasenkopf K, et al. (2004) Assessment of protein glycation markers in infant formulas. Food Chemistry 87: 253-259.
16. Delatour T, Hegele J, Parisod V, Richoz J, Maurer S, et al. (2009) Analysis of advanced glycation endproducts in dairy products by isotope dilution liquid chromatography-electrospray tandem mass spectrometry. The particular case of carboxymethyllysine. J Chromatogr A 1216: 2371-2381.
17. Pischetsrieder M, Henle T, (2012) Glycation products in infant formulas: chemical, analytical and physiological aspects. Amino Acids 42: 1111-1118.
18. Sebekova K, Somoza V, (2007) Dietary advanced glycation endproducts (AGEs) and their health effects-PRO. Mol Nutr Food Res 51: 1079-1084.
19. Birlouez-Aragon I, Saavedra G, Tessier FJ, Galinier A, Ait-Ameur L, et al. (2010) A diet based on high-heat-treated foods promotes risk factors for diabetes mellitus and cardiovascular diseases. Am J Clin Nutr 91: 1220-1226.
20. Uribarri J, Cai W, Sandu O, Peppa M, Goldberg T, et al. (2005) Diet-derived advanced glycation end products are major contributors to the body's AGE pool and induce inflammation in healthy subjects. Ann N Y Acad Sci 1043: 461-466.
21. Van Nguyen C, (2006) Toxicity of the AGEs generated from the Maillard reaction: On the relationship of food-AGEs and biological-AGEs. Mol Nutr Food Res 50: 1140-1149.
22. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, et al. (2005) Understanding RAGE, the receptor for advanced glycation end products. J Mol Med (Berl) 83: 876-886.
23. Yan SF, Ramasamy R, Naka Y, Schmidt AM, (2003) Glycation, inflammation, and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circ Res 93: 1159-1169.
24. Buetler TM, Latado H, Leclerc E, Weigle B, Baumeyer A, et al. (2011) Glycolaldehyde-modified beta-lactoglobulin AGEs are unable to stimulate inflammatory signaling pathways in RAGE-expressing human cell lines. Mol Nutr Food Res 55: 291-299.
25. Buetler TM, Leclerc E, Baumeyer A, Latado H, Newell J, et al. (2008) N(epsilon)-carboxymethyllysine-modified proteins are unable to bind to RAGE and activate an inflammatory response. Mol Nutr Food Res 52: 370-378.
26. Cassese A, Esposito I, Fiory F, Barbagallo AP, Paturzo F, et al. (2008) In skeletal muscle advanced glycation end products (AGEs) inhibit insulin action and induce the formation of multimolecular complexes including the receptor for AGEs. J Biol Chem 283: 36088-36099.
27. Miele C, Riboulet A, Maitan MA, Oriente F, Romano C, et al. (2003) Human glycated albumin affects glucose metabolism in L6 skeletal muscle cells by impairing insulin-induced insulin receptor substrate (IRS) signaling through a protein kinase C alpha-mediated mechanism. J Biol Chem 278: 47376-47387.
28. Unoki H, Bujo H, Yamagishi S, Takeuchi M, Imaizumi T, et al. (2007) Advanced glycation end products attenuate cellular insulin sensitivity by increasing the generation of intracellular reactive oxygen species in adipocytes. Diabetes Res Clin Pract 76: 236-244.
29. Zhao Z, Zhao C, Zhang XH, Zheng F, Cai W, et al. (2009) Advanced glycation end products inhibit glucose-stimulated insulin secretion through nitric oxide-dependent inhibition of cytochrome c oxidase and adenosine triphosphate synthesis. Endocrinology 150: 2569-2576.
30. Puddu A, Storace D, Odetti P, Viviani GL, (2010) Advanced glycation end-products affect transcription factors regulating insulin gene expression. Biochem Biophys Res Commun 395: 122-125.
31. Shu TT, Zhu YX, Wang HD, Lin Y, Ma Z, et al. (2011) AGEs Decrease Insulin Synthesis in Pancreatic beta-Cell by Repressing Pdx-1 Protein Expression at the Post-Translational Level. PLoS One 6.
32. Tan KC, Shiu SW, Wong Y, Tam X, (2011) Serum advanced glycation end products (AGEs) are associated with insulin resistance. Diabetes Metab Res Rev 27: 488-492.
33. Uribarri J, Cai W, Ramdas M, Goodman S, Pyzik R, et al. (2011) Restriction of advanced glycation end products improves insulin resistance in human type 2 diabetes: potential role of AGER1 and SIRT1. Diabetes Care 34: 1610-1616.
34. Tahara N, Yamagishi S, Matsui T, Takeuchi M, Nitta Y, et al. (2012) Serum Levels of Advanced Glycation End Products (AGEs) are Independent Correlates of Insulin Resistance in Nondiabetic Subjects. Cardiovascular Therapeutics 30: 42-48.
35. Yonekura H, Yamamoto Y, Sakurai S, Petrova RG, Abedin MJ, et al. (2003) Novel splice variants of the receptor for advanced glycation end-products expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury. Biochem J 370: 1097-1109.
36. Boor P, Celec P, Klenovicsova K, Vlkova B, Szemes T, et al. (2010) Association of biochemical parameters and RAGE gene polymorphisms in healthy infants and their mothers. Clin Chim Acta 411: 1034-1040.
37. Basta G, Sironi AM, Lazzerini G, Del Turco S, Buzzigoli E, et al. (2006) Circulating soluble receptor for advanced glycation end products is inversely associated with glycemic control and S100A12 protein. J Clin Endocrinol Metab 91: 4628-4634.
38. Koyama H, Yamamoto H, Nishizawa Y, (2007) Endogenous Secretory RAGE as a Novel Biomarker for Metabolic Syndrome and Cardiovascular Diseases. Biomark Insights 2: 331-339.
39. Smith DJ, Salmi M, Bono P, Hellman J, Leu T, et al. (1998) Cloning of vascular adhesion protein 1 reveals a novel multifunctional adhesion molecule. J Exp Med 188: 17-27.
40. Lyles GA, Chalmers J, (1992) The metabolism of aminoacetone to methylglyoxal by semicarbazide-sensitive amine oxidase in human umbilical artery. Biochem Pharmacol 43: 1409-1414.
41. Abella A, Marti L, Camps M, Claret M, Fernandez-Alvarez J, et al. (2003) Semicarbazide-sensitive amine oxidase/vascular adhesion protein-1 activity exerts an antidiabetic action in Goto-Kakizaki rats. Diabetes 52: 1004-1013.
42. Li HY, Wei JN, Lin MS, Smith DJ, Vainio J, et al. (2009) Serum vascular adhesion protein-1 is increased in acute and chronic hyperglycemia. Clin Chim Acta 404: 149-153.
43. Li HY, Lin MS, Wei JN, Hung CS, Chiang FT, et al. (2009) Change of serum vascular adhesion protein-1 after glucose loading correlates to carotid intima-medial thickness in non-diabetic subjects. Clin Chim Acta 403: 97-101.
44. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, et al. (2000) Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 85: 2402-2410.
45. Wong SH, Knight JA, Hopfer SM, Zaharia O, Leach CN Jr, et al. (1987) Lipoperoxides in plasma as measured by liquid-chromatographic separation of malondialdehyde-thiobarbituric acid adduct. Clin Chem 33: 214-220.
46. Munch G, Keis R, Wessels A, Riederer P, Bahner U, et al. (1997) Determination of advanced glycation end products in serum by fluorescence spectroscopy and competitive ELISA. Eur J Clin Chem Clin Biochem 35: 669-677.
47. Meltretter J, Pischetsrieder M (2008) Application of mass spectrometry for the detection of glycation and oxidation products in milk proteins. In: Schleicher E, Somoza V, Shieberle P, editors. Maillard Reaction: Recent Advances in Food and Biomedical Sciences. 134-140.
48. Jenness R, (1979) The composition of human milk. Semin Perinatol 3: 225-239.
49. Vlassara H, Striker G, (2007) Glycotoxins in the diet promote diabetes and diabetic complications. Curr Diab Rep 7: 235-241.
50. Ames JM, (2007) Evidence against dietary advanced glycation endproducts being a risk to human health. Mol Nutr Food Res 51: 1085-1090.
51. Miyata T, Kurokawa K, van Ypersele de Strihou C (2000) Relevance of oxidative and carbonyl stress to long-term uremic complications. Kidney Int Suppl 76: S120-125.
52. Park L, Raman KG, Lee KJ, Lu Y, Ferran LJ Jr, et al. (1998) Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med 4: 1025-1031.
53. Nakamura K, Yamagishi SI, Matsui T, Adachi H, Takeuchi M, et al. (2007) Serum levels of soluble form of receptor for advanced glycation end products (sRAGE) are correlated with AGEs in both diabetic and non-diabetic subjects. Clin Exp Med 7: 188-190.
54. Zhang L, Bukulin M, Kojro E, Roth A, Metz VV, et al. (2008) Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J Biol Chem 283: 35507-35516.
55. Klenovicsova K, Krivosikova Z, Gajdos M, Sebekova K, (2011) Association of sVAP-1, sRAGE, and CML with lactation-induced insulin sensitivity in young non-diabetic healthy women. Clin Chim Acta 412: 1842-1847.
56. Havel PJ, (1998) Leptin production and action: relevance to energy balance in humans. Am J Clin Nutr 67: 355-356.
57. Mueller WM, Gregoire FM, Stanhope KL, Mobbs CV, Mizuno TM, et al. (1998) Evidence that glucose metabolism regulates leptin secretion from cultured rat adipocytes. Endocrinology 139: 551-558.
58. Lonnerdal B, Havel PJ, (2000) Serum leptin concentrations in infants: effects of diet, sex, and adiposity. Am J Clin Nutr 72: 484-489.
59. Sebekova K, Krajcovicova-Kudlackova M, Schinzel R, Faist V, Klvanova J, et al. (2001) Plasma levels of advanced glycation end products in healthy, long-term vegetarians and subjects on a western mixed diet. Eur J Nutr 40: 275-281.
60. Fabricius-Bjerre S, Jensen RB, Faerch K, Larsen T, Molgaard C, et al. (2011) Impact of Birth Weight and Early Infant Weight Gain on Insulin Resistance and Associated Cardiovascular Risk Factors in Adolescence. PLoS One 6.
61. Erkekoglu P, Baydar T, (2010) Toxicity of acrylamide and evaluation of its exposure in baby foods. Nutr Res Rev 23: 323-333.
62. Felton JS, Knize MG, Wu RW, Colvin ME, Hatch FT, et al. (2007) Mutagenic potency of food-derived heterocyclic amines. Mutat Res 616: 90-94.
63. Fohgelberg P, Rosen J, Hellenas KE, Abramsson-Zetterberg L, (2005) The acrylamide intake via some common baby food for children in Sweden during their first year of life-an improved method for analysis of acrylamide. Food Chem Toxicol 43: 951-959.
64. Heizmann CW, (2007) The mechanism by which dietary AGEs are a risk to human health is via their interaction with RAGE: arguing against the motion. Mol Nutr Food Res 51: 1116-1119.
65. Lack G, (2012) Update on risk factors for food allergy. J Allergy Clin Immunol 129: 1187-1197.
66. DaVeiga SP, (2012) Epidemiology of atopic dermatitis: a review. Allergy Asthma Proc 33: 227-234.
67. Agostoni C, Grandi F, Gianni ML, Silano M, Torcoletti M, et al. (1999) Growth patterns of breast fed and formula fed infants in the first 12 months of life: an Italian study. Arch Dis Child 81: 395-399.
68. Bulk-Bunschoten AM, van Bodegom S, Reerink JD, de Jong PC, de Groot CJ, (2002) Weight and weight gain at 4 months (The Netherlands 1998): influences of nutritional practices, socio-economic and ethnic factors. Paediatr Perinat Epidemiol 16: 361-369.
69. Gupta M, Zaheer, Jora R, Kaul V, Gupta R, (2010) Breast feeding and insulin levels in low birth weight neonates: a randomized study. Indian J Pediatr 77: 509-513.
70. Bergmann R, Helling R, Heichert C, Scheunemann M, Mading P, et al. (2001) Radio fluorination and positron emission tomography (PET) as a new approach to study the in vivo distribution and elimination of the advanced glycation endproducts N epsilon-carboxymethyllysine (CML) and N epsilon-carboxyethyllysine (CEL). Nahrung 45: 182-188.