Skip to main content Accessibility help
×
Home

Co-ingestion of whole eggs or egg whites with glucose protects against postprandial hyperglycaemia-induced oxidative stress and dysregulated arginine metabolism in association with improved vascular endothelial function in prediabetic men

  • Joshua D. McDonald (a1), Eunice Mah (a1) (a2), Chureeporn Chitchumroonchokchai (a1), Elizabeth J. Reverri (a1), Jinhui Li (a1), Jeff S. Volek (a3), Frederick A. Villamena (a4) and Richard S. Bruno (a1)...

Abstract

Replacing a portion of a glucose challenge with whole eggs (EGG) or egg whites (WHITE) was shown to protect against glucose-induced impairments in vascular function. We hypothesised in the present study that previously observed vasoprotection following co-ingestion of EGG or WHITE with glucose was attributed to limiting postprandial hyperglycaemia-induced oxidative stress that improves NO bioavailability. Prediabetic men completed a randomised, cross-over study in which they ingested isoenergetic meals containing 100 g glucose (GLU), or 75 g glucose with 1·5 EGG, seven WHITE or two egg yolks (YOLK). At 30 min intervals for 3 h, we assessed plasma NO metabolites, the lipid peroxidation biomarker malondialdehyde, antioxidants, arginine and its methylated metabolites (asymmetric dimethylarginine and symmetric dimethylarginine), tetrahydrobiopterin redox status, vasoconstrictors and inflammatory markers. Compared with GLU, malondialdehyde was lower and NO metabolites were greater in EGG and WHITE, but YOLK was not different from GLU. Malondialdehyde was inversely correlated with NO metabolites and vascular function, whereas NO metabolites were positively correlated with vascular function. Compared with GLU, arginine was greater, but asymmetric and symmetric dimethylarginine and angiotensin-II were lower in all egg-based meals. Antioxidants, tetrahydrobiopterin redox status and inflammatory markers did not differ among treatments. Thus, while each egg-based meal improved arginine metabolism, only EGG and WHITE limited lipid peroxidation. This suggests that vasoprotection mediated by EGG and WHITE likely occurs in an NO-dependent manner by improving arginine metabolism and attenuating oxidative stress that otherwise limit NO biosynthesis and bioavailability to the vascular endothelium.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Co-ingestion of whole eggs or egg whites with glucose protects against postprandial hyperglycaemia-induced oxidative stress and dysregulated arginine metabolism in association with improved vascular endothelial function in prediabetic men
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Co-ingestion of whole eggs or egg whites with glucose protects against postprandial hyperglycaemia-induced oxidative stress and dysregulated arginine metabolism in association with improved vascular endothelial function in prediabetic men
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Co-ingestion of whole eggs or egg whites with glucose protects against postprandial hyperglycaemia-induced oxidative stress and dysregulated arginine metabolism in association with improved vascular endothelial function in prediabetic men
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: Professor R. S. Bruno, fax +1 614 292 4339, email bruno.27@osu.edu

References

Hide All
1. Mozaffarian, D, Benjamin, EJ, Go, AS, et al. (2016) Heart disease and stroke statistics-2016 update: a report from the American Heart Association. Circulation 133, e38e360.
2. Loader, J, Montero, D, Lorenzen, C, et al. (2015) Acute hyperglycemia impairs vascular function in healthy and cardiometabolic diseased subjects: systematic review and meta-analysis. Arterioscler Thromb Vasc Biol 35, 20602072.
3. Versari, D, Daghini, E, Virdis, A, et al. (2009) Endothelial dysfunction as a target for prevention of cardiovascular disease. Diabetes Care 32, S314S321.
4. Mah, E, Noh, SK, Ballard, KD, et al. (2011) Postprandial hyperglycemia impairs vascular endothelial function in healthy men by inducing lipid peroxidation and increasing asymmetric dimethylarginine:arginine. J Nutr 141, 19611968.
5. Naseem, KM (2005) The role of nitric oxide in cardiovascular diseases. Mol Aspects Med 26, 3365.
6. Mah, E & Bruno, RS (2012) Postprandial hyperglycemia on vascular endothelial function: mechanisms and consequences. Nutr Res 32, 727740.
7. Harris, RA, Nishiyama, SK, Wray, DW, et al. (2010) Ultrasound assessment of flow-mediated dilation. Hypertension 55, 10751085.
8. Matsuzawa, Y, Kwon, TG, Lennon, RJ, et al. (2015) Prognostic value of flow-mediated vasodilation in brachial artery and fingertip artery for cardiovascular events: a systematic review and meta-analysis. J Am Heart Assoc 4, e002270e002284.
9. Papageorgiou, N, Androulakis, E, Papaioannou, S, et al. (2015) Homoarginine in the shadow of asymmetric dimethylarginine: from nitric oxide to cardiovascular disease. Amino Acids 47, 17411750.
10. Ryoo, S, Lemmon, CA, Soucy, KG, et al. (2006) Oxidized low-density lipoprotein-dependent endothelial arginase II activation contributes to impaired nitric oxide signaling. Circ Res 99, 951960.
11. Boger, RH, Sydow, K, Borlak, J, et al. (2000) LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: involvement of S-adenosylmethionine-dependent methyltransferases. Circ Res 87, 99105.
12. Bode-Boger, SM, Scalera, F, Kielstein, JT, et al. (2006) Symmetrical dimethylarginine: a new combined parameter for renal function and extent of coronary artery disease. J Am Soc Nephrol 17, 11281134.
13. Leiper, J & Vallance, P (1999) Biological significance of endogenous methylarginines that inhibit nitric oxide synthases. Cardiovasc Res 43, 542548.
14. Ito, T, Yufu, K, Mori, A, et al. (1996) Oxidative stress alters arginine metabolism in rat brain: effect of sub-convulsive hyperbaric oxygen exposure. Neurochem Int 29, 187195.
15. Valtonen, P, Laitinen, T, Lyyra-Laitinen, T, et al. (2008) Serum l-homoarginine concentration is elevated during normal pregnancy and is related to flow-mediated vasodilatation. Circ J 72, 18791884.
16. Atzler, D, Schwedhelm, E & Choe, CU (2015) l-Homoarginine and cardiovascular disease. Curr Opin Clin Nutr Metab Care 18, 8388.
17. Vasquez-Vivar, J, Kalyanaraman, B, Martasek, P, et al. (1998) Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci U S A 95, 92209225.
18. Crabtree, MJ, Smith, CL, Lam, G, et al. (2008) Ratio of 5,6,7,8-tetrahydrobiopterin to 7,8-dihydrobiopterin in endothelial cells determines glucose-elicited changes in NO vs. superoxide production by eNOS. Am J Physiol Heart Circ Physiol 294, H1530H1540.
19. Takeda, M, Yamashita, T, Shinohara, M, et al. (2009) Plasma tetrahydrobiopterin/dihydrobiopterin ratio: a possible marker of endothelial dysfunction. Circ J 73, 955962.
20. Day, RT, de Cássia Cavaglieri, R, Tabatabaimir, H, et al. (2010) Acute hyperglycemia rapidly stimulates VEGF mRNA translation in the kidney. Role of angiotensin type 2 receptor (AT2). Cell Signal 22, 18491857.
21. Grassi, D, Desideri, G, Necozione, S, et al. (2012) Protective effects of flavanol-rich dark chocolate on endothelial function and wave reflection during acute hyperglycemia. Hypertension 60, 827832.
22. Loot, AE, Schreiber, JG, Fisslthaler, B, et al. (2009) Angiotensin II impairs endothelial function via tyrosine phosphorylation of the endothelial nitric oxide synthase. J Exp Med 206, 28892896.
23. Ramzy, D, Rao, V, Tumiati, LC, et al. (2006) Elevated endothelin-1 levels impair nitric oxide homeostasis through a PKC-dependent pathway. Circulation 114, I319I326.
24. Esposito, K, Nappo, F, Marfella, R, et al. (2002) Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 106, 20672072.
25. Siti, HN, Kamisah, Y & Kamsiah, J (2015) The role of oxidative stress, antioxidants and vascular inflammation in cardiovascular disease (a review). Vascul Pharmacol 71, 4056.
26. Decode Study Group, The European Diabetes Epidemiology Group (2001) Glucose tolerance and cardiovascular mortality: comparison of fasting and 2-hour diagnostic criteria. Arch Intern Med 161, 397405.
27. McDonald, JD, Chitchumroonchokchai, C, Li, J, et al. (2018) Replacing carbohydrate during a glucose challenge with the egg white portion or whole eggs protects against postprandial impairments in vascular endothelial function in prediabetic men by limiting increases in glycaemia and lipid peroxidation. Br J Nutr 119, 259270.
28. Davalos, A, Miguel, M, Bartolome, B, et al. (2004) Antioxidant activity of peptides derived from egg white proteins by enzymatic hydrolysis. J Food Prot 67, 19391944.
29. Jahandideh, F, Majumder, K, Chakrabarti, S, et al. (2014) Beneficial effects of simulated gastro-intestinal digests of fried egg and its fractions on blood pressure, plasma lipids and oxidative stress in spontaneously hypertensive rats. PLOS ONE 9, e115006.
30. Matoba, N, Usui, H, Fujita, H, et al. (1999) A novel anti-hypertensive peptide derived from ovalbumin induces nitric oxide-mediated vasorelaxation in an isolated SHR mesenteric artery. FEBS Lett 452, 181184.
31. American Diabetes Association (2011) Standards of medical care in diabetes – 2011. Diabetes Care 34, S11S61.
32. U.S. Department of Agriculture, Agricultural Research Service (2016) Nutrient Intakes from Food and Beverages: Mean Amounts Consumed per Individual, by Gender and Age, What We Eat in America, NHANES 2013–2014. Beltsville, MD: U.S. Department of Agriculture, Agricultural Research Service.
33. Bruno, RS, Dugan, CE, Smyth, JA, et al. (2008) Green tea extract protects leptin-deficient, spontaneously obese mice from hepatic steatosis and injury. J Nutr 138, 323331.
34. Gleize, B, Steib, M, André, M, et al. (2012) Simple and fast HPLC method for simultaneous determination of retinol, tocopherols, coenzyme Q(10) and carotenoids in complex samples. Food Chem 134, 25602564.
35. Valdes, C, Arauna, D, Gonzalez, D, et al. (2017) Simplified HPLC methodology for quantifying biological pterins by selective oxidation. J Chromatogr B Analyt Technol Biomed Life Sci 1055–1056, 113118.
36. Biondi, R, Ambrosio, G, De Pascali, F, et al. (2012) HPLC analysis of tetrahydrobiopterin and its pteridine derivatives using sequential electrochemical and fluorimetric detection: application to tetrahydrobiopterin autoxidation and chemical oxidation. Arch Biochem Biophys 520, 716.
37. Bland, JM & Altman, DG (1995) Calculating correlation coefficients with repeated observations: Part 1--correlation within subjects. BMJ 310, 446.
38. Gross, M, Yu, X, Hannan, P, et al. (2003) Lipid standardization of serum fat-soluble antioxidant concentrations: the YALTA study. Am J Clin Nutr 77, 458466.
39. Liu, YF, Oey, I, Bremer, P, et al. (2017) Bioactive peptides derived from egg proteins: a review. Crit Rev Food Sci Nutr (Epublication ahead of print version 22 August 2017).
40. Njike, V, Faridi, Z, Dutta, S, et al. (2010) Daily egg consumption in hyperlipidemic adults--effects on endothelial function and cardiovascular risk. Nutr J 9, 28.
41. Chatzizisis, YS, Coskun, AU, Jonas, M, et al. (2007) Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J Am Coll Cardiol 49, 23792393.
42. Preli, RB, Klein, KP & Herrington, DM (2002) Vascular effects of dietary l-arginine supplementation. Atherosclerosis 162, 115.
43. Mariotti, Fo, Huneau, JFo, Szezepanski, I, et al. (2007) Meal amino acids with varied levels of arginine do not affect postprandial vascular endothelial function in healthy young men. J Nutr 137, 13831389.
44. U.S. Department of Agriculture, Agricultural Research Service (2016) USDA national nutrient database for standard reference, release 28. Nutrient data laboratory home page. https://ndb.nal.usda.gov/ndb/ (accessed May 2018).
45. Atzler, D, Schonhoff, M, Cordts, K, et al. (2016) Oral supplementation with l-homoarginine in young volunteers. Br J Clin Pharmacol 82, 14771485.
46. Moali, C, Boucher, JL, Sari, MA, et al. (1998) Substrate specificity of NO synthases: detailed comparison of l-arginine, homo-l-arginine, their N-omega-hydroxy derivatives, and N-omega-hydroxynor-l-arginine. Biochemistry 37, 1045310460.
47. Michel, T (2013) R is for arginine: metabolism of arginine takes off again, in new directions. Circulation 128, 14001404.
48. Tain, YL & Hsu, CN (2017) Toxic dimethylarginines: asymmetric dimethylarginine (ADMA) and symmetric dimethylarginine (SDMA). Toxins (Basel) 9, E92.
49. Luo, Z, Teerlink, T, Griendling, K, et al. (2010) Angiotensin II and NADPH oxidase increase ADMA in vascular smooth muscle cells. Hypertension 56, 498504.
50. Zobel, EH, von Scholten, BJ, Reinhard, H, et al. (2017) Symmetric and asymmetric dimethylarginine as risk markers of cardiovascular disease, all-cause mortality and deterioration in kidney function in persons with type 2 diabetes and microalbuminuria. Cardiovasc Diabetol 16, 88.
51. Ihlemann, N, Rask-Madsen, C, Perner, A, et al. (2003) Tetrahydrobiopterin restores endothelial dysfunction induced by an oral glucose challenge in healthy subjects. Am J Physiol Heart Circ Physiol 285, H875H882.
52. Keidar, S, Heinrich, R, Kaplan, M, et al. (2002) Oxidative stress increases the expression of the angiotensin-II receptor type 1 in mouse peritoneal macrophages. J Renin Angiotensin Aldosterone Syst 3, 2430.
53. Ruef, J, Moser, M, Kubler, W, et al. (2001) Induction of endothelin-1 expression by oxidative stress in vascular smooth muscle cells. Cardiovasc Pathol 10, 311315.
54. Schleicher, RL, Carroll, MD, Ford, ES, et al. (2009) Serum vitamin C and the prevalence of vitamin C deficiency in the United States: 2003–2004 National Health and Nutrition Examination Survey (NHANES). Am J Clin Nutr 90, 12521263.
55. Kuzkaya, N, Weissmann, N, Harrison, DG, et al. (2005) Interactions of peroxynitrite with uric acid in the presence of ascorbate and thiols: implications for uncoupling endothelial nitric oxide synthase. Biochem Pharmacol 70, 343354.
56. Shatanawi, A, Lemtalsi, T, Yao, L, et al. (2015) Angiotensin II limits NO production by upregulating arginase through a p38 MAPK-ATF-2 pathway. Eur J Pharmacol 746, 106114.
57. DiMarco, DM, Norris, GH, Millar, CL, et al. (2017) Intake of up to 3 eggs per day is associated with changes in HDL function and increased plasma antioxidants in healthy, young adults. J Nutr 147, 323329.
58. Cai, H & Harrison, DG (2000) Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87, 840844.
59. Liddle, RA, Morita, ET, Conrad, CK, et al. (1986) Regulation of gastric emptying in humans by cholecystokinin. J Clin Invest 77, 992996.
60. Brownlee, M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414, 813820.
61. Nishikawa, T, Edelstein, D, Du, XL, et al. (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404, 787790.
62. Daiber, A, Di Lisa, F, Oelze, M, et al. (2017) Crosstalk of mitochondria with NADPH oxidase via reactive oxygen and nitrogen species signalling and its role for vascular function. Br J Pharmacol 174, 16701689.
63. Kobayashi, H, Sasahara, R, Yoda, S, et al. (2017) Egg white hydrolysate inhibits oxidation in mayonnaise and a model system. Biosci Biotechnol Biochem 81, 12061215.
64. Pearce, KL, Clifton, PM & Noakes, M (2011) Egg consumption as part of an energy-restricted high-protein diet improves blood lipid and blood glucose profiles in individuals with type 2 diabetes. Br J Nutr 105, 584592.

Keywords

Type Description Title
WORD
Supplementary materials

McDonald et al. supplementary material
Table S1 and Figures S1-S2

 Word (1.1 MB)
1.1 MB

Co-ingestion of whole eggs or egg whites with glucose protects against postprandial hyperglycaemia-induced oxidative stress and dysregulated arginine metabolism in association with improved vascular endothelial function in prediabetic men

  • Joshua D. McDonald (a1), Eunice Mah (a1) (a2), Chureeporn Chitchumroonchokchai (a1), Elizabeth J. Reverri (a1), Jinhui Li (a1), Jeff S. Volek (a3), Frederick A. Villamena (a4) and Richard S. Bruno (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed