Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-04-30T12:32:13.229Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of dietary carbohydrate restriction and aerobic exercise on retinol binding protein 4 (RBP4) and fatty acid binding protein 5 (FABP5) in middle-aged men with metabolic syndrome

Published online by Cambridge University Press:  14 November 2022

Bahloul Ghorbanian Open the ORCID record for Bahloul Ghorbanian [Opens in a new window] ,
Alexei Wong Open the ORCID record for Alexei Wong [Opens in a new window]  and
Asgar Iranpour Open the ORCID record for Asgar Iranpour [Opens in a new window]
Bahloul Ghorbanian*
Affiliation:
Department of Physical Education, Faculty of Educational Sciences and Psychology, Azarbaijan Shahid Madani University, Tabriz, Iran
Alexei Wong
Affiliation:
Department of Health and Human Performance, Marymount University, Arlington, VA, USA
Asgar Iranpour
Affiliation:
Department of Sports Physiology, Faculty of Educational Sciences and Psychology, University of Mohaghegh Ardabili, Ardabil, Iran
*
*Corresponding author: Dr B. Ghorbanian, email b.gorbanian@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Exercise and dietary interventions have been described to positively affect metabolic syndrome (MetS) via molecular-induced changes. The purpose of this study was to investigate the effects of dietary carbohydrate restriction and aerobic exercise (AE) on retinol binding protein 4 (RBP4) and fatty acid binding protein 5 (FABP5) in middle-aged men with MetS. The study had a randomised, double-blinded, parallel-controlled design. Forty middle-aged men with MetS (age: 53·97 ± 2·85 years, BMI = 31·09 ± 1·04 kg/m2) were randomly assigned to four groups, AE (n 10), ketogenic diet (KD; n 10), AE combined with KD (AE + KD; n 10) or control (C; n 10). RBP4, FABP5, body composition (body mass, BMI and body fat), insulin resistance, insulin sensitivity and MetS factors were evaluated prior to and after the 12-week intervention. AE + KD significantly decreased the body fat percentage (P = 0·006), BMI (P = 0·001), Zmets (P = 0·017), RBP4 (P = 0·017) and the homeostasis model of insulin resistance (HOMA-IR) (P = 0·001) as compared with control group and marginally significantly decreased the Zmets as compared with exercise group (P = 0·086). KD significantly decreased RBP4 levels as compared with control group (P = 0·041). Only the AE intervention (P = 0·045) significantly decreased FABP5 levels. Combining intervention of carbohydrate restriction with AE compared with carbohydrate restriction and AE alone improved RBP4, HOMA-IR as well as different body composition and MetS factors in middle-aged men with MetS.

Keywords

Metabolic syndromeKetogenic dietAerobic exerciseRBP4FABP5
Type
Research Article
Information
British Journal of Nutrition , Volume 130 , Issue 4 , 28 August 2023 , pp. 553 - 563
Check for updates
Copyright
The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

This article was updated on 1st June 2023.

References

Hyde, PN, Sapper, TN, Crabtree, CD, et al. (2019) Dietary carbohydrate restriction improves metabolic syndrome independent of weight loss. JCI Insight 20, 1–8.Google Scholar
Ouchi, N, Parker, JL, Lugus, JJ, et al. (2011) Adipokines in inflammation and metabolic disease. Nat Rev Immunol 11, 85–97.CrossRefGoogle ScholarPubMed
Dludla, P, Nkambule, B, Mazibuko-Mbeje, S, et al. (2020) Adipokines as a therapeutic target by metformin to improve metabolic function: a systematic review of randomized controlled trials. Pharmacol Res Commun 163, 1–5.Google ScholarPubMed
Cho, YM, Youn, BS, Lee, H, et al. (2006) Plasma retinol-binding protein-4 concentrations are elevated in human subjects with impaired glucose tolerance and type 2 diabetes. Diabetes Care 29, 2457–2461.CrossRefGoogle ScholarPubMed
Chang, X, Yan, H, Bian, H, et al. (2015) Serum retinol binding protein 4 is associated with visceral fat in human with nonalcoholic fatty liver disease without known diabetes: a cross-sectional study. Lipids Health Dis 14, 1–8.CrossRefGoogle ScholarPubMed
Chielle, E, Feltez, A & Rossi, E (2017) Influence of obesity on the serum concentration of retinol-binding protein 4 (RBP4) in young adults. J Bras Patol Med Lab 53, 81–86.Google Scholar
McTernan, P & Kumar, S (2007) Retinol binding protein 4 and pathogenesis of diabetes. J Clin Endocrinol Metab 92, 2430–2432.CrossRefGoogle ScholarPubMed
Zimmerman, AW & Veerkamp, JH (2002) New insights into the structure and function of fatty acid-binding proteins. Cell Mol Life Sci 59, 1096–1116.CrossRefGoogle ScholarPubMed
Cao, H, Maeda, K, Gorgun, CZ, et al. (2006) Regulation of metabolic responses by adipocyte/macrophage fatty acid–binding proteins in leptin-deficient mice. Diabetes 55, 1915–1922.CrossRefGoogle ScholarPubMed
Xu, B, Chen, L, Zhan, Y, et al. (2022) The biological functions and regulatory mechanisms of fatty acid binding protein 5 in various diseases. Front Cell Dev Biol 10, 1–6.Google ScholarPubMed
Mongraw-Chaffin, M, Hairston, KG, Hanley, AJ, et al. (2021) Association of visceral adipose tissue and insulin resistance with incident metabolic syndrome independent of obesity status: the IRAS family study. Obesity 29, 1195–1202.CrossRefGoogle ScholarPubMed
Armstrong, EH (2014) The role of fatty acid binding protein 5 (FABP5) in peroxisome proliferator-activated receptor β/δ (PPARβ/δ)-mediated fatty acid and retinoic acid signaling: a structural perspective. Doctoral Dissertation, Emory University.Google Scholar
Taghian, F, Zolfaghari, M & Hedayati, M (2014) Effects of aerobic exercise on serum retinol binding protein4, insulin resistance and blood lipids in obese women. Iran J Public Health 43, 658.Google ScholarPubMed
Zabetian-Targhi, F, Mahmoudi, MJ, Rezaei, N, et al. (2015) Retinol binding protein 4 in relation to diet, inflammation, immunity, and cardiovascular diseases. Adv Nutr 6, 748–762.CrossRefGoogle ScholarPubMed
Shibue, K, Yamane, S, Harada, N, et al. (2015) Fatty acid-binding protein 5 regulates diet-induced obesity via GIP secretion from enteroendocrine K cells in response to fat ingestion. Am J Physiol Endocrinol Metab 308, 583–591.CrossRefGoogle ScholarPubMed
Huang, PL (2009) A comprehensive definition for metabolic syndrome. Dis Model Mech 2, 231–237.CrossRefGoogle ScholarPubMed
Tjønna, AE, Ramos, JS, Pressler, A, et al. (2018) EX-MET study: exercise in prevention on of metabolic syndrome–a randomized multicenter trial: rational and design. BMC Public Health 18, 437.CrossRefGoogle Scholar
Greene, DA, Varley, BJ, Hartwig, TB, et al. (2018) A low-carbohydrate ketogenic diet reduces body mass without compromising performance in powerlifting and Olympic weightlifting athletes. J Strength Cond Res 32, 3373–3382.CrossRefGoogle ScholarPubMed
Vargas, S, Romance, R, Petro, JL, et al. (2018) Efficacy of ketogenic diet on body composition during resistance training in trained men: a randomized controlled trial. J Int Soc Sports Nutr 15, 31.CrossRefGoogle ScholarPubMed
Del Corral, P, Chandler-Laney, PC, Casazza, K, et al. (2009) Effect of dietary adherence with or without exercise on weight loss: a mechanistic approach to a global problem. J Clin Endocrinol Metab 94, 1602–1607.CrossRefGoogle ScholarPubMed
Heyward, VH & Wagner, DR (2004) Applied Body Composition Assessment. Champaign IL: Human Kinetics.Google Scholar
Carroll, JF, Chiapa, AL, Rodriquez, M, et al. (2008) Visceral fat, waist circumference, and BMI: impact of race/ethnicity. Obesity 16, 600–607.CrossRefGoogle ScholarPubMed
Glass, S & Dwyer, GB (2007) ACSM’S Metabolic Calculations Handbook. Baltimore, TX: Lippincott Williams & Wilkins.Google Scholar
Tapking, C, Popp, D, Herndon, DN, et al. (2018) Estimated versus achieved maximal oxygen consumption in severely burned children maximal oxygen consumption in burned children. Burns 44, 2026–2033.CrossRefGoogle ScholarPubMed
Shin, C, Abbott, RD, Lee, H, et al. (2004) Prevalence and correlates of orthostatic hypotension in middle-aged men and women in Korea: the Korean health and genome study. J Hum Hypertens 18, 717–723.CrossRefGoogle ScholarPubMed
Kim, TJ, Kim, HJ, Kim, YB, et al. (2016) Comparison of surrogate markers as measures of uncomplicated insulin resistance in Korean adults. Korean J Fam Med 37, 188.CrossRefGoogle ScholarPubMed
Azali Alamdari, K & Gholami, F (2017) Effect of aerobic training on retinol binding protein-4 and insulin resistance in women with metabolic syndrome. Metab Exer 5, 109–119.Google Scholar
Volek, J, Freidenreich, D, Saenz, C, et al. (2016) Metabolic characteristics of keto-adapted ultra-endurance runners. Metabolism 65, 100–110.CrossRefGoogle ScholarPubMed
Numao, S, Sasai, H, Nomata, Y, et al. (2012) Effects of exercise training on circulating retinol-binding protein 4 and cardiovascular disease risk factors in obese men. Obes Facts 5, 845–855.CrossRefGoogle ScholarPubMed
Syamsunarno, MR, Iso, T, Hanaoka, H, et al. (2013) A critical role of fatty acid binding protein 4 and 5 (FABP4/5) in the systemic response to fasting. PLOS ONE 8, 1–5.CrossRefGoogle ScholarPubMed
Volek, JS, Phinney, SD, Forsythe, CE, et al. (2009) Carbohydrate restriction has a more favorable impact on the metabolic syndrome than a low fat diet. Lipids 44, 297–309.CrossRefGoogle Scholar
Delbari, R, Fathi, R, Talebi Garakani, E, et al. (2013) Changes in FABP5 plasma levels after a period of aerobic exercise with increasing intensity in women with a normal weight and overweight. J Sport Bio Sci 5, 44–52.Google Scholar
Balistreri, CR, Caruso, C & Candore, G (2010) The role of adipose tissue and adipokines in obesity-related inflammatory diseases. Mediators Inflamm 2010, 802078.CrossRefGoogle ScholarPubMed
Ashtary-Larky, D, Bagheri, R, Bavi, H, et al. (2021) Ketogenic diets, physical activity, and body composition: a review. Br J Nutr 127, 1898–1920.CrossRefGoogle ScholarPubMed
Vargas-Molina, S, Petro, JL, Romance, R, et al. (2020) Effects of a KD on body composition and strength in trained women. J Int Soc Sports Nutr 17, 1–4.CrossRefGoogle ScholarPubMed
Ma, S, Huang, Q, Tominaga, T, et al. (2018) An 8-week ketogenic diet alternated interleukin-6, ketolytic and lipolytic gene expression, and enhanced exercise capacity in mice. Nutrients 10, 1–8.Google ScholarPubMed
Holt, SH & Miller, JB (1995) Increased insulin responses to ingested foods are associated with lessened satiety. Appetite 24, 43–54.CrossRefGoogle ScholarPubMed
Boden, G, Sargrad, K, Homko, C, et al. (2005) Effect of a low-carbohydrate diet on appetite, blood glucose levels, and insulin resistance in obese patients with type 2 diabetes. Ann Intern Med 142, 403–411.CrossRefGoogle ScholarPubMed
Westman, EC & Volek, JS (2002) Very-low-carbohydrate weight-loss diets revisited. Cleve Clin J Med 69, 849.Google Scholar
Lee, JW, Lee, HR, Shim, JY, et al. (2008) Abdominal visceral fat reduction is associated with favorable changes of serum retinol binding protein-4 in nondiabetic subjects. Endocr J 55, 81.CrossRefGoogle ScholarPubMed
Lundsgaard, AM, Fritzen, AM & Kiens, B (2018) Molecular regulation of fatty acid oxidation in skeletal muscle during aerobic exercise. Trends Endocrinol Metab 29, 18–30.CrossRefGoogle ScholarPubMed
Durkalec-Michalski, K, Nowaczyk, P & Siedzik, K (2019) Effect of a 4-week KD on exercise metabolism in crossfit-trained athletes. J Int Soc Sports Nutr 16, 16.CrossRefGoogle Scholar
Ebbeling, CB, Knapp, A, Johnson, A, et al. (2022) Effects of a low-carbohydrate diet on insulin-resistant dyslipoproteinemia—a randomized controlled feeding trial. Am J Clin Nutr 115, 154–162.CrossRefGoogle ScholarPubMed
O’Neill, BJ (2020) Effect of low-carbohydrate diets on cardiometabolic risk, insulin resistance, and metabolic syndrome. Curr Opin Endocrinol Diabetes Obes 27, 301–307.CrossRefGoogle ScholarPubMed
Tay, J, Luscombe-Marsh, ND, Thompson, CH, et al. (2015) Comparison of low-and high-carbohydrate diets for type 2 diabetes management: a randomized trial. Am J Clin Nutr 102, 780–790.CrossRefGoogle ScholarPubMed
Maekawa, S, Kawahara, T, Nomura, R, et al. (2014) Retrospective study on the efficacy of a low-carbohydrate diet for impaired glucose tolerance. Diabetes, metabolic syndrome and obesity: targets and therapy. Diabetes Metab Syndr Obes 7, 195–201.CrossRefGoogle Scholar
Amanat, S, Sinaei, E, Panji, M, et al. (2020) A randomized controlled trial on the effects of 12 weeks of aerobic, resistance, and combined exercises training on the serum levels of nesfatin-1, irisin-1 and HOMA-IR. Front Physiol 11, 1–5.CrossRefGoogle ScholarPubMed
Altooq, NJ, Aburowais, SA, Alajaimi, AN, et al. (2021) Low-carbohydrate diet improves the cardiopsychiatry profile of patients with schizophrenia: a pilot study. Heart Mind 5, 80.Google Scholar
Guio de Prada, V, Ortega, JF, Morales-Palomo, F, et al. (2019) Women with metabolic syndrome show similar health benefits from high-intensity interval training than men. PLOS ONE 14, 1–8.CrossRefGoogle ScholarPubMed
Azali Alamdari, K, Yavari, Y & Azarian Sousahab, S (2017) Effect of aerobic training on overall metabolic risk and the atherogenic non-high density lipoprotein cholesterol levels in Tabriz sedentary males by controlling the effect of nutrition. Sci J Rehabil Med 6, 103–112.Google Scholar
Ost, A, Danielsson, A, Liden, M, et al. (2007) Retinol-binding protein-4 attenuates insulin-induced phosphorylation of IRS1 and ERK1/2 in primary human adipocytes. FASEB J 21, 3696–3704.CrossRefGoogle ScholarPubMed
Kotnik, P, Fischer-Posovszky, P & Wabitsch, M (2011) RBP4: a controversial adipokine. Eur J Endocrinol 165, 703–711.CrossRefGoogle ScholarPubMed
Randolph, RK & Ross, AC (1991) Vitamin A status regulates hepatic lecithin: retinol acyltransferase activity in rats. J Biol Chem 266, 16453–16457.CrossRefGoogle ScholarPubMed
Rask, L & Peterson, PA (1976) In vitro uptake of vitamin A from the retinol-binding plasma protein to mucosal epithelial cells from the monkey’s small intestine. J Biol Chem 251, 6360–6366.CrossRefGoogle ScholarPubMed
Kawaguchi, R, Zhong, M, Kassai, M, et al. (2013) Differential and isomerspecific modulation of vitamin A transport and the catalytic activities of the RBP receptor by retinoids. J Membr Biol 246, 647–660.CrossRefGoogle ScholarPubMed
Krzyzanowska, K, Zemany, L, Krugluger, W, et al. (2008) Serum concentrations of retinol-binding protein 4 in women with and without gestational diabetes. Diabetologia 51, 1115–1122.CrossRefGoogle ScholarPubMed
Calibasi-Kocal, G, Mashinchian, O, Basbinar, Y, et al. (2021) Nutritional control of intestinal stem cells in homeostasis and tumorigenesis. Trends Endocrinol Metab 32, 20–35.CrossRefGoogle ScholarPubMed
Graham, T, Yang, Q, Blüher, M, et al. (2006) Retinol-binding protein 4 and insulin resistance in lean, obese, and diabetic subjects. N Engl J Med 354, 2552–2563.CrossRefGoogle ScholarPubMed
Haider, D, Schindler, K, Prager, G, et al. (2007) Serum retinol-binding protein 4 is reduced after weight loss in morbidly obese subjects. J Clin Endocrinol Metab 92, 1168–1171.CrossRefGoogle ScholarPubMed
Vitkova, M, Klimcáková, E, Kovacikova, M, et al. (2007) Plasma levels and adipose tissue messenger ribonucleic acid expression of retinol-binding protein 4 are reduced during calorie restriction in obese subjects but are not related to diet-induced changes in insulin sensitivity. J Clin Endocrinol Metab 92, 2330–2335.CrossRefGoogle Scholar
Napoli, JL (2017) Cellular retinoid binding-proteins, CRBP, CRABP, FABP5: effects on retinoid metabolism, function and related diseases. Pharmacol Ther 173, 19–33.CrossRefGoogle ScholarPubMed
Njelekela, MA, Mpembeni, R, Muhihi, A, et al. (2009) Gender-related differences in the prevalence of cardiovascular disease risk factors and their correlates in urban Tanzania. BMC Cardiovasc Disord 9, 1–8.CrossRefGoogle ScholarPubMed
Fezeu, L, Balkau, B, Kengne, AP, et al. (2007) Metabolic syndrome in a sub-Saharan African setting: central obesity may be the key determinant. Atherosclerosis 193, 70–76.CrossRefGoogle Scholar
Beigh, SH & Jain, S (2012) Prevalence of metabolic syndrome and gender differences. Bioinformation 8, 613.CrossRefGoogle ScholarPubMed