Differential effects of dietary protein sources on postprandial low-grade inflammation after a single high fat meal in obese non-diabetic subjects

Jens Holmer-Jensen, Toni Karhu, Lene S Mortensen, Steen B Pedersen, Karl-Heinz Herzig, Kjeld Hermansen, Jens Holmer-Jensen, Toni Karhu, Lene S Mortensen, Steen B Pedersen, Karl-Heinz Herzig, Kjeld Hermansen

Abstract

Background: Obesity is a state of chronic low-grade inflammation. Chronic low-grade inflammation is associated with the pathophysiology of both type-2 diabetes and atherosclerosis. Prevention or reduction of chronic low-grade inflammation may be advantageous in relation to obesity related co-morbidity. In this study we investigated the acute effect of dietary protein sources on postprandial low-grade inflammatory markers after a high-fat meal in obese non-diabetic subjects.

Methods: We conducted a randomized, acute clinical intervention study in a crossover design. We supplemented a fat rich mixed meal with one of four dietary proteins - cod protein, whey isolate, gluten or casein. 11 obese non-diabetic subjects (age: 40-68, BMI: 30.3-42.0 kg/m2) participated and blood samples were drawn in the 4 h postprandial period. Adiponectin was estimated by ELISA methods and cytokines were analyzed by multiplex assay.

Results: MCP-1 and CCL5/RANTES displayed significant postprandial dynamics. CCL5/RANTES initially increased after all meals, but overall CCL5/RANTES incremental area under the curve (iAUC) was significantly lower after the whey meal compared with the cod and casein meals (P = 0.0053). MCP-1 was initially suppressed after all protein meals. However, the iAUC was significantly higher after whey meal compared to the cod and gluten meals (P = 0.04).

Conclusion: We have demonstrated acute differential effects on postprandial low grade inflammation of four dietary proteins in obese non-diabetic subjects. CCL5/RANTES initially increased after all meals but the smallest overall postprandial increase was observed after the whey meal. MCP-1 was initially suppressed after all 4 protein meals and the whey meal caused the smallest overall postprandial suppression.

Trial registration: ClinicalTrials.gov ID: NCT00863564.

Figures

Figure 1
Figure 1
The plot show mean (+SEM) responses for CCL5/RANTES in plasma in the 4 h postprandial period after the four meals consumed by 11 obese non-diabetic subjects. Meals consisted of an energy-free soup plus 80 g fat (from butter) and 45 g carbohydrate consumed with either 45 g cod protein, 45 g whey protein, 45 g gluten or 45 g casein.
Figure 2
Figure 2
The plot show mean (+SEM) responses for MCP-1 in plasma in the 4 h postprandial period after the four meals consumed by 11 obese non-diabetic subjects. Meals consisted of an energy-free soup plus 80 g fat (from butter) and 45 g carbohydrate consumed with either 45 g cod protein, 45 g whey protein, 45 g gluten or 45 g casein.

References

    1. Biro FM, Wien M. Childhood obesity and adult morbidities. Am J Clin Nutr. 2010;91:1499S–1505S. doi: 10.3945/ajcn.2010.28701B.
    1. Schelbert KB. Comorbidities of obesity. Prim Care. 2009;36:271–285. doi: 10.1016/j.pop.2009.01.009.
    1. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 1993;259:87–91. doi: 10.1126/science.7678183.
    1. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286:327–334. doi: 10.1001/jama.286.3.327.
    1. Ridker PM, Buring JE, Cook NR, Rifai N. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14 719 initially healthy American women. Circulation. 2003;107:391–397. doi: 10.1161/01.CIR.0000055014.62083.05.
    1. Libby P, Ridker PM, Hansson GK. Leducq Transatlantic Network on Atherothrombosis. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol. 2009;54:2129–2138. doi: 10.1016/j.jacc.2009.09.009.
    1. Danesh J, Wheeler JG, Hirschfield GM, Eda S, Eiriksdottir G, Rumley A, Lowe GD, Pepys MB, Gudnason V. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N Engl J Med. 2004;350:1387–1397. doi: 10.1056/NEJMoa032804.
    1. Danesh J, Kaptoge S, Mann AG, Sarwar N, Wood A, Angleman SB, Wensley F, Higgins JP, Lennon L, Eiriksdottir G, Rumley A, Whincup PH, Lowe GD, Gudnason V. Long-Term Interleukin-6 Levels and Subsequent Risk of Coronary Heart Disease: Two New Prospective Studies and a Systematic Review. PLoS Med. 2008;5:e78. doi: 10.1371/journal.pmed.0050078.
    1. Wang P, Mariman E, Renes J, Keijer J. The secretory function of adipocytes in the physiology of white adipose tissue. J Cell Physiol. 2008;216:3–13. doi: 10.1002/jcp.21386.
    1. Yudkin JS, Stehouwer CD, Emeis JJ, Coppack SW. C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol. 1999;19:972–978. doi: 10.1161/01.ATV.19.4.972.
    1. Festa A, D'Agostino R Jr, Williams K, Karter AJ, Mayer-Davis EJ, Tracy RP, Haffner SM. The relation of body fat mass and distribution to markers of chronic inflammation. Int J Obes Relat Metab Disord. 2001;25:1407–1415. doi: 10.1038/sj.ijo.0801792.
    1. Park HS, Park JY, Yu R. Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-alpha and IL-6. Diabetes Res Clin Pract. 2005;69:29–35. doi: 10.1016/j.diabres.2004.11.007.
    1. Fain JN. Release of inflammatory mediators by human adipose tissue is enhanced in obesity and primarily by the nonfat cells: a review. Mediators Inflamm. 2010;2010:513948.
    1. Ito A, Suganami T, Miyamoto Y, Yoshimasa Y, Takeya M, Kamei Y, Ogawa Y. Role of MAPK phosphatase-1 in the induction of monocyte chemoattractant protein-1 during the course of adipocyte hypertrophy. J Biol Chem. 2007;282:25445–25452. doi: 10.1074/jbc.M701549200.
    1. Sell H, Eckel J. Monocyte chemotactic protein-1 and its role in insulin resistance. Curr Opin Lipidol. 2007;18:258–262. doi: 10.1097/MOL.0b013e3281338546.
    1. Herder C, Baumert J, Thorand B, Koenig W, de Jager W, Meisinger C, Illig T, Martin S, Kolb H. Chemokines as risk factors for type 2 diabetes: results from the MONICA/KORA Augsburg study, 1984-2002. Diabetologia. 2006;49:921–929. doi: 10.1007/s00125-006-0190-y.
    1. Niu J, Kolattukudy PE. Role of MCP-1 in cardiovascular disease: molecular mechanisms and clinical implications. Clin Sci (Lond) 2009;117:95–109. doi: 10.1042/CS20080581.
    1. Aukrust P, Halvorsen B, Yndestad A, Ueland T, Oie E, Otterdal K, Gullestad L, Damas JK. Chemokines and cardiovascular risk. Arterioscler Thromb Vasc Biol. 2008;28:1909–1919. doi: 10.1161/ATVBAHA.107.161240.
    1. van Oostrom AJ, Rabelink TJ, Verseyden C, Sijmonsma TP, Plokker HW, De Jaegere PP, Cabezas MC. Activation of leukocytes by postprandial lipemia in healthy volunteers. Atherosclerosis. 2004;177:175–182. doi: 10.1016/j.atherosclerosis.2004.07.004.
    1. Alipour A, van Oostrom AJ, Izraeljan A, Verseyden C, Collins JM, Frayn KN, Plokker TW, Elte JW, Cabezas MC. Leukocyte Activation by Triglyceride-Rich Lipoproteins. Arterioscler Thromb Vasc Biol. 2008.
    1. Bouwens M, Grootte Bromhaar M, Jansen J, Muller M, Afman LA. Postprandial dietary lipid-specific effects on human peripheral blood mononuclear cell gene expression profiles. Am J Clin Nutr. 2010;91:208–217. doi: 10.3945/ajcn.2009.28586.
    1. Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC, Jung S, Littman DR, Weber C, Ley K. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med. 2003;9:61–67. doi: 10.1038/nm810.
    1. Koenen RR, von Hundelshausen P, Nesmelova IV, Zernecke A, Liehn EA, Sarabi A, Kramp BK, Piccinini AM, Paludan SR, Kowalska MA, Kungl AJ, Hackeng TM, Mayo KH, Weber C. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med. 2009;15:97–103. doi: 10.1038/nm.1898.
    1. Veillard NR, Kwak B, Pelli G, Mulhaupt F, James RW, Proudfoot AE, Mach F. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ Res. 2004;94:253–261. doi: 10.1161/01.RES.0000109793.17591.4E.
    1. Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, Perrard JL, Sweeney JF, Peterson LE, Chan L, Smith CW, Ballantyne CM. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation. 2007;115:1029–1038. doi: 10.1161/CIRCULATIONAHA.106.638379.
    1. Galland L. Diet and inflammation. Nutr Clin Pract. 2010;25:634–640. doi: 10.1177/0884533610385703.
    1. Amar J, Burcelin R, Ruidavets JB, Cani PD, Fauvel J, Alessi MC, Chamontin B, Ferrieres J. Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr. 2008;87:1219–1223.
    1. Heinonen MV, Laaksonen DE, Karhu T, Karhunen L, Laitinen T, Kainulainen S, Rissanen A, Niskanen L, Herzig KH. Effect of diet-induced weight loss on plasma apelin and cytokine levels in individuals with the metabolic syndrome. Nutr Metab Cardiovasc Dis. 2009;19:626–633. doi: 10.1016/j.numecd.2008.12.008.
    1. van Dijk SJ, Feskens EJ, Bos MB, Hoelen DW, Heijligenberg R, Bromhaar MG, de Groot LC, de Vries JH, Muller M, Afman LA. A saturated fatty acid-rich diet induces an obesity-linked proinflammatory gene expression profile in adipose tissue of subjects at risk of metabolic syndrome. Am J Clin Nutr. 2009;90:1656–1664. doi: 10.3945/ajcn.2009.27792.
    1. Rogowski O, Shapira I, Steinvil A, Berliner S. Low-grade inflammation in individuals with the hypertriglyceridemic waist phenotype: another feature of the atherogenic dysmetabolism. Metabolism. 2009;58:661–667. doi: 10.1016/j.metabol.2009.01.005.
    1. Margioris AN. Fatty acids and postprandial inflammation. Curr Opin Clin Nutr Metab Care. 2009;12:129–137. doi: 10.1097/MCO.0b013e3283232a11.
    1. Jimenez-Gomez Y, Lopez-Miranda J, Blanco-Colio LM, Marin C, Perez-Martinez P, Ruano J, Paniagua JA, Rodriguez F, Egido J, Perez-Jimenez F. Olive oil and walnut breakfasts reduce the postprandial inflammatory response in mononuclear cells compared with a butter breakfast in healthy men. Atherosclerosis. 2009;204:e70–6. doi: 10.1016/j.atherosclerosis.2008.09.011.
    1. Myhrstad MC, Narverud I, Telle-Hansen VH, Karhu T, Bodtker Lund D, Herzig KH, Makinen M, Halvorsen B, Retterstol K, Kirkhus B, Granlund L, Holven KB, Ulven SM. Effect of the fat composition of a single high-fat meal on inflammatory markers in healthy young women. Br J Nutr. 2011. pp. 1–10.
    1. Huffman KM, Orenduff MC, Samsa GP, Houmard JA, Kraus WE, Bales CW. Dietary carbohydrate intake and high-sensitivity C-reactive protein in at-risk women and men. Am Heart J. 2007;154:962–968. doi: 10.1016/j.ahj.2007.07.009.
    1. Arya F, Egger S, Colquhoun D, Sullivan D, Pal S, Egger G. Differences in postprandial inflammatory responses to a 'modern' v. traditional meat meal: a preliminary study. Br J Nutr. 2010;104:724–728. doi: 10.1017/S0007114510001042.
    1. Zemel MB, Sun X, Sobhani T, Wilson B. Effects of dairy compared with soy on oxidative and inflammatory stress in overweight and obese subjects. Am J Clin Nutr. 2010;91:16–22. doi: 10.3945/ajcn.2009.28468.
    1. Panagiotakos DB, Pitsavos CH, Zampelas AD, Chrysohoou CA, Stefanadis CI. Dairy products consumption is associated with decreased levels of inflammatory markers related to cardiovascular disease in apparently healthy adults: the ATTICA study. J Am Coll Nutr. 2010;29:357–364.
    1. Nilsson M, Stenberg M, Frid AH, Holst JJ, Bjorck IM. Glycemia and insulinemia in healthy subjects after lactose-equivalent meals of milk and other food proteins: the role of plasma amino acids and incretins. Am J Clin Nutr. 2004;80:1246–1253.
    1. Pal S, Ellis V, Ho S. Acute effects of whey protein isolate on cardiovascular risk factors in overweight, post-menopausal women. Atherosclerosis. 2010;212:339–344. doi: 10.1016/j.atherosclerosis.2010.05.032.
    1. Mortensen LS, Hartvigsen ML, Brader LJ, Astrup A, Schrezenmeir J, Holst JJ, Thomsen C, Hermansen K. Differential effects of protein quality on postprandial lipemia in response to a fat-rich meal in type 2 diabetes: comparison of whey, casein, gluten, and cod protein. Am J Clin Nutr. 2009;90:41–48. doi: 10.3945/ajcn.2008.27281.
    1. Lehto SM, Niskanen L, Herzig KH, Tolmunen T, Huotari A, Viinamaki H, Koivumaa-Honkanen H, Honkalampi K, Ruotsalainen H, Hintikka J. Serum chemokine levels in major depressive disorder. Psychoneuroendocrinology. 2010;35:226–232. doi: 10.1016/j.psyneuen.2009.06.007.
    1. Rabe-Hesketh S. Multilevel and longitudinal modeling using Stata. Texas: Stata Press; 2008.
    1. Alipour A, Elte JW, van Zaanen HC, Rietveld AP, Cabezas MC. Postprandial inflammation and endothelial dysfuction. Biochem Soc Trans. 2007;35:466–469. doi: 10.1042/BST0350466.
    1. Grewal IS, Rutledge BJ, Fiorillo JA, Gu L, Gladue RP, Flavell RA, Rollins BJ. Transgenic monocyte chemoattractant protein-1 (MCP-1) in pancreatic islets produces monocyte-rich insulitis without diabetes: abrogation by a second transgene expressing systemic MCP-1. J Immunol. 1997;159:401–408.
    1. Krohn R, Raffetseder U, Bot I, Zernecke A, Shagdarsuren E, Liehn EA, van Santbrink PJ, Nelson PJ, Biessen EA, Mertens PR, Weber C. Y-box binding protein-1 controls CC chemokine ligand-5 (CCL5) expression in smooth muscle cells and contributes to neointima formation in atherosclerosis-prone mice. Circulation. 2007;116:1812–1820. doi: 10.1161/CIRCULATIONAHA.107.708016.
    1. Braunersreuther V, Steffens S, Arnaud C, Pelli G, Burger F, Proudfoot A, Mach F. A novel RANTES antagonist prevents progression of established atherosclerotic lesions in mice. Arterioscler Thromb Vasc Biol. 2008;28:1090–1096. doi: 10.1161/ATVBAHA.108.165423.
    1. Braunersreuther V, Zernecke A, Arnaud C, Liehn EA, Steffens S, Shagdarsuren E, Bidzhekov K, Burger F, Pelli G, Luckow B, Mach F, Weber C. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2007;27:373–379.
    1. Breland UM, Michelsen AE, Skjelland M, Folkersen L, Krohg-Sorensen K, Russell D, Ueland T, Yndestad A, Paulsson-Berne G, Damas JK, Oie E, Hansson GK, Halvorsen B, Aukrust P. Raised MCP-4 levels in symptomatic carotid atherosclerosis: an inflammatory link between platelet and monocyte activation. Cardiovasc Res. 2010;86:265–273. doi: 10.1093/cvr/cvq044.
    1. Kraaijeveld AO, de Jager SC, de Jager WJ, Prakken BJ, McColl SR, Haspels I, Putter H, van Berkel TJ, Nagelkerken L, Jukema JW, Biessen EA. CC chemokine ligand-5 (CCL5/RANTES) and CC chemokine ligand-18 (CCL18/PARC) are specific markers of refractory unstable angina pectoris and are transiently raised during severe ischemic symptoms. Circulation. 2007;116:1931–1941. doi: 10.1161/CIRCULATIONAHA.107.706986.
    1. Kobusiak-Prokopowicz M, Orzeszko J, Mazur G, Mysiak A, Orda A, Poreba R, Mazurek W. Chemokines and left ventricular function in patients with acute myocardial infarction. Eur J Intern Med. 2007;18:288–294. doi: 10.1016/j.ejim.2007.02.001.
    1. Jones KL, Maguire JJ, Davenport AP. Chemokine receptor CCR5: from AIDS to atherosclerosis. Br J Pharmacol. 2011;162:1453–1469. doi: 10.1111/j.1476-5381.2010.01147.x.
    1. Bursill CA, Castro ML, Beattie DT, Nakhla S, van der Vorst E, Heather AK, Barter PJ, Rye KA. High-density lipoproteins suppress chemokines and chemokine receptors in vitro and in vivo. Arterioscler Thromb Vasc Biol. 2010;30:1773–1778. doi: 10.1161/ATVBAHA.110.211342.
    1. Herder C, Peltonen M, Koenig W, Kraft I, Muller-Scholze S, Martin S, Lakka T, Ilanne-Parikka P, Eriksson JG, Hamalainen H, Keinanen-Kiukaanniemi S, Valle TT, Uusitupa M, Lindstrom J, Kolb H, Tuomilehto J. Systemic immune mediators and lifestyle changes in the prevention of type 2 diabetes: results from the Finnish Diabetes Prevention Study. Diabetes. 2006;55:2340–2346. doi: 10.2337/db05-1320.
    1. De Caterina R, Massaro M. Omega-3 fatty acids and the regulation of expression of endothelial pro-atherogenic and pro-inflammatory genes. J Membr Biol. 2005;206:103–116. doi: 10.1007/s00232-005-0783-2.
    1. Adkins Y, Kelley DS. Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids. J Nutr Biochem. 2010;21:781–792. doi: 10.1016/j.jnutbio.2009.12.004.
    1. Clare DA, Swaisgood HE. Bioactive milk peptides: a prospectus. J Dairy Sci. 2000;83:1187–1195. doi: 10.3168/jds.S0022-0302(00)74983-6.
    1. Otani H, Hata I. Inhibition of proliferative responses of mouse spleen lymphocytes and rabbit Peyer's patch cells by bovine milk caseins and their digests. J Dairy Res. 1995;62:339–348. doi: 10.1017/S0022029900031034.
    1. Aihara K, Ishii H, Yoshida M. Casein-derived tripeptide, Val-Pro-Pro (VPP), modulates monocyte adhesion to vascular endothelium. J Atheroscler Thromb. 2009;16:594–603. doi: 10.5551/jat.729.
    1. Vordenbaumen S, Braukmann A, Petermann K, Scharf A, Bleck E, von Mikecz A, Jose J, Schneider M. Casein alpha s1 is expressed by human monocytes and upregulates the production of GM-CSF via p38 MAPK. J Immunol. 2011;186:592–601. doi: 10.4049/jimmunol.1001461.
    1. Dandona P, Aljada A, Mohanty P, Ghanim H, Hamouda W, Assian E, Ahmad S. Insulin inhibits intranuclear nuclear factor kappaB and stimulates IkappaB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect? J Clin Endocrinol Metab. 2001;86:3257–3265. doi: 10.1210/jc.86.7.3257.
    1. Aljada A, Ghanim H, Saadeh R, Dandona P. Insulin inhibits NFkappaB and MCP-1 expression in human aortic endothelial cells. J Clin Endocrinol Metab. 2001;86:450–453. doi: 10.1210/jc.86.1.450.
    1. Ghanim H, Korzeniewski K, Sia CL, Abuaysheh S, Lohano T, Chaudhuri A, Dandona P. Suppressive effect of insulin infusion on chemokines and chemokine receptors. Diabetes Care. 2010;33:1103–1108. doi: 10.2337/dc09-2193.

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