Int J Sports Med 2021; 42(14): 1260-1267
DOI: 10.1055/a-1480-7692
Physiology & Biochemistry

Circulating MicroRNA Responses to Postprandial Lipemia with or without Prior Exercise

Catherine B. Springer
1   Department of Kinesiology, University of Maryland School of Public Health, College Park, United States
,
Ryan M. Sapp
1   Department of Kinesiology, University of Maryland School of Public Health, College Park, United States
,
William S. Evans
1   Department of Kinesiology, University of Maryland School of Public Health, College Park, United States
,
James M. Hagberg
1   Department of Kinesiology, University of Maryland School of Public Health, College Park, United States
,
Steven J. Prior
1   Department of Kinesiology, University of Maryland School of Public Health, College Park, United States
2   Department of Veterans Affairs, Baltimore Veterans Affairs Geriatric Research, Education and Clincial Center, Baltimore, United States
› Institutsangaben
Funding: This research was supported by an American College of Sports Medicine Foundation grant and the University of Maryland Department of Kinesiology Graduate Research Initiative Fund. S.J.P. was supported, in part, by the Baltimore Veterans Affairs Medical Center Geriatric Research, Education, and Clinical Center.

Abstract

Repeated exposure to a high-fat meal triggers inflammation and oxidative stress, contributing to the onset of cardiometabolic diseases. Regular exercise prevents cardiometabolic diseases and a prior bout of acute endurance exercise can counteract the detrimental cardiovascular effects of a subsequent high-fat meal. Circulating microRNAs (ci-miRs) are potential mediators of these vascular effects through regulation of gene expression at the posttranscriptional level. Therefore, we investigated the expression of ci-miRs related to vascular function (miR-21, miR-92a, miR-126, miR-146a, miR-150, miR-155, miR-181b, miR-221, miR-222) in plasma from healthy, recreationally to highly active, Caucasian adult men after a high-fat meal with (EX) and without (CON) a preceding bout of cycling exercise. Ci-miR-155 was the only ci-miR for which there was a significant interaction effect of high-fat meal and exercise (p=0.050). Ci-miR-155 significantly increased in the CON group at two (p=0.007) and four hours (p=0.010) after the high-fat meal test, whereas it significantly increased in the EX group only four hours after the meal (p=0.0004). There were significant main effects of the high-fat meal on ci-miR-21 (p=0.01), ci-miR-126 (p=0.02), ci-miR-146a (p=0.02), ci-miR-181b (p=0.02), and ci-miR-221 (p=0.008). Collectively, our results suggest that prior exercise does not prevent high-fat meal-induced increases in vascular-related ci-miRs.



Publikationsverlauf

Eingereicht: 11. Dezember 2020

Angenommen: 03. April 2021

Artikel online veröffentlicht:
11. Juni 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Benjamin EJ, Muntner P, Alonso A. et al. Heart disease and stroke statistics-2019 Update: A Report From the American Heart Association 2019. Circulation 2019; 139: e56-e528
  • 2 Tyldum GA, Schjerve IE, Tjønna AE. et al. Endothelial dysfunction induced by post-prandial lipemia. complete protection afforded by high-intensity aerobic interval exercise. J Am Coll Cardiol 2009; 53: 200-206
  • 3 Michael AGJ, Guillermo G-C. Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ Res 2016; 176: 139-148
  • 4 Lusis AJ. Atherosclerosis Aldons. Nature 2010; 407: 233-241
  • 5 Tóth PP, Potter D, Ming EE. Prevalence of lipid abnormalities in the United States: The National Health and Nutrition Examination Survey 2003–2006. J Clin Lipidol 2012; 6: 325-330
  • 6 Gill JMR, Al-Mamari A, Ferrell WR. et al. Effects of prior moderate exercise on postprandial metabolism and vascular function in lean and centrally obese men. J Am Coll Cardiol 2004; 44: 2375-2382
  • 7 Simionescu N, Niculescu LS, Sanda GM. et al. Analysis of circulating microRNAs that are specifically increased in hyperlipidemic and/or hyperglycemic sera. Mol Biol Rep 2014; 41: 5765-5773
  • 8 Lin X, Zhan JK, Wang YJ. et al. Function, role, and clinical application of micrornas in vascular aging. Biomed Res Int 2016; 2016: 6021394
  • 9 Sapp RM, Hagberg JM. Circulating microRNAs: Advances in exercise physiology. Curr Opin Physiol 2019; 10: 1-9
  • 10 Sapp RM, Shill DD, Roth SM. et al. Circulating microRNAs in acute and chronic exercise: More than mere biomarkers. J Appl Physiol (1985) 2017; 122: 702-717
  • 11 Marin T, Gongol B, Chen Z. et al. Mechanosensitive microRNAs – role in endothelial responses to shear stress and redox state. Free Radic Biol Med 2013; 64: 61-68
  • 12 Chen CF, Huang J, Li H. et al. MicroRNA-221 regulates endothelial nitric oxide production and inflammatory response by targeting adiponectin receptor 1. Gene 2015; 565: 246-251
  • 13 Xue Y, Wei Z, Ding H. et al. MicroRNA-19b/221/222 induces endothelial cell dysfunction via suppression of PGC-1α in the progression of atherosclerosis. Atherosclerosis 2015; 241: 671-681
  • 14 Celic T, Meuth V, Six I. et al. The miR-221/222 cluster is a key player in vascular biology via the fine-tuning of endothelial cell physiology. Curr Vasc Pharmacol 2017; 15: 40-46
  • 15 Yamakuchi M, Hashiguchi T. Endothelial cell aging: How miRNAs contribute?. J Clin Med 2018; 7: 170
  • 16 Chistiakov DA, Orekhov AN, Bobryshev YV. The role of miR-126 in embryonic angiogenesis, adult vascular homeostasis, and vascular repair and its alterations in atherosclerotic disease. J Mol Cell Cardiol 2016; 97: 47-55
  • 17 Donaldson CJ, Lao KH, Zeng L. The salient role of microRNAs in atherogenesis. J Mol Cell Cardiol 2018; 122: 98-113
  • 18 Luo XY, Zhu XQ, Li Y. et al. MicroRNA-150 restores endothelial cell function and attenuates vascular remodeling by targeting PTX3 through the NF-κB signaling pathway in mice with acute coronary syndrome. Cell Biol Int 2018; 42: 1170-1181
  • 19 Yang LX, Liu G, Zhu GF. et al. MicroRNA-155 inhibits angiotensin II-induced vascular smooth muscle cell proliferation. J Renin Angiotensin Aldosterone Syst 2014; 15: 109-116
  • 20 Virtue A, Johnson C, Lopez-Pastraña J. et al. MicroRNA-155 deficiency leads to decreased atherosclerosis, increased white adipose tissue obesity, and non-alcoholic fatty liver disease a novel mouse model of obesity paradox. J Biol Chem 2017; 292: 1267-1287
  • 21 Wang Z, Zhu H, Shi H. et al. Exosomes derived from M1 macrophages aggravate neointimal hyperplasia following carotid artery injuries in mice through miR-222/CDKN1B/CDKN1C pathway. Cell Death Dis 2019; 10: 422
  • 22 Mahesh G, Biswas R. MicroRNA-155: A master regulator of inflammation. J Interferon Cytokine Res 2019; 39: 321-330
  • 23 Nazari-jahantigh M, Wei Y, Noels H. et al. MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J Clin Invest 2012; 122: 4190-4202
  • 24 Cheng HS, Njock MS, Khyzha N. et al. Noncoding RNAs regulate NF-κB signaling to modulate blood vessel inflammation. Front Genet 2014; 5: 422
  • 25 Dlouhá D, Hubácek JA. Regulatory RNAs and cardiovascular disease - With a special focus on circulating MicroRNAs. Physiol Res 2017; 66: S21-S38
  • 26 Olivieri F, Rippo MR, Procopio AD. et al. Circulating inflamma-miRs in aging and age-related diseases. Front Genet 2013; 4: 121
  • 27 Wang L, Zhang H, Rodriguez S. et al. Notch-dependent repression of miR-155 in the bone marrow niche regulate hematopoiesis in an NF-kB dependent manner. Cell Stem Cell 2015; 15: 51-65
  • 28 Sun C, Alkhoury K, Wang YI. et al. IRF-1 and miRNA126 modulate VCAM-1 expression in response to a high fat meal. Circ Res 2012; 111: 1054-1064
  • 29 Hsieh CH, Rau CS, Wu SC. et al. Weight-reduction through a low-fat diet causes differential expression of circulating microRNAs in obese C57BL/6 mice. BMC Genomics 2015; 16: 699
  • 30 Nasias D, Evangelakos I, Nidris V. et al. Significant changes in hepatic transcriptome and circulating miRNAs are associated with diet-induced metabolic syndrome in apoE3L.CETP mice. J Cell Physiol 2019; 234: 20485-20500
  • 31 Quintanilha BJ, Pinto Ferreira LR, Ferreira FM. et al. Circulating plasma microRNAs dysregulation and metabolic endotoxemia induced by a high-fat high-saturated diet. Clin Nutr 2020; 39: 554-562
  • 32 Jenkins NT, Landers RQ, Thakkar SR. et al. Prior endurance exercise prevents postprandial lipaemia-induced increases in reactive oxygen species in circulating CD31±cells. J Physiol 2011; 589: 5539-5553
  • 33 Brandauer J, Landers-Ramos RQ, Jenkins NT. et al. Effects of prior acute exercise on circulating cytokine concentration responses to a high-fat meal. Physiol Rep 2013; 1: e00040
  • 34 Bae J-H, Bassenge E, Kim K-B. et al. Postprandial hypertriglyceridemia impairs endothelial function by enhanced oxidant stress. Atherosclerosis 2001; 155: 517-523
  • 35 Wallace JP, Johnson B, Padilla J. et al. Postprandial lipaemia, oxidative stress and endothelial function: A review. Int J Clin Pract 2010; 64: 389-403
  • 36 Nair VD, Ge Y, Li S. et al. Sedentary and trained older men have distinct circulating exosomal microRNA profiles at baseline and in response to acute exercise. Front Physiol 2020; 11: 605
  • 37 Li F, Bai M, Xu J. et al. Long-term exercise alters the profiles of circulating micro-RNAs in the plasma of young women. Front Physiol 2020; 11: 372
  • 38 Barber JL, Zellars KN, Barringhaus KG. et al. The effects of regular exercise on circulating cardiovascular-related MicroRNAs. Sci Rep 2019; 9: 7527
  • 39 Fernández-Sanjurjo M, Úbeda N, Fernández-García B. et al. Exercise dose affects the circulating microRNA profile in response to acute endurance exercise in male amateur runners. Scand J Med Sci Sports 2020; 30: 1896-1907
  • 40 Sawada S, Kon M, Wada S. et al. Profiling of circulating micrornas after a bout of acute resistance exercise in humans. PLoS One 2013; 8: e70823
  • 41 Sapp RM, Chesney CA, Eagan LE. et al. Changes in circulating microRNA and arterial stiffness following high-intensity interval and moderate intensity continuous exercise. Physiol Rep 2020; 8: e14431
  • 42 Jackson AS, Pollock ML. Generalized equations for predicting body density of men. Br J Nutr 1978; 40: 497-504
  • 43 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
  • 44 Petitt DS, Cureton KJ. Effects of prior exercise on postprandial lipemia: A quantitative review. Metabolism 2003; 52: 418-424
  • 45 Chamorro-Jorganes A, Araldi E, Suárez Y. MicroRNAs as pharmacological targets in endothelial cell function and dysfunction. Pharmacol Res 2013; 75: 15-27
  • 46 Russo A, Bartolini D, Mensà E. et al. Physical activity modulates the overexpression of the inflammatory miR-146a-5p in obese patients. IUBMB Life 2018; 70: 1012-1022
  • 47 Cook-Mills JM, Marchese ME, Abdala-Valencia H. Vascular cell adhesion molecule-1 expression and signaling during disease: Regulation by reactive oxygen species and antioxidants. Antioxid Redox Signal 2011; 15: 1607-1638
  • 48 Sharma S, Eghbali M. Influence of sex differences on microRNA gene regulation in disease. Biol Sex Differ 2014; 5: 3
  • 49 Ameling S, Kacprowski T, Chilukoti RK. et al. Associations of circulating plasma microRNAs with age, body mass index and sex in a population-based study. BMC Med Genomics 2015; 8: 61
  • 50 Cui C, Yang W, Shi J. et al. Identification and analysis of human sex-biased MicroRNAs. Genomics Proteomics Bioinformatics 2018; 16: 200-211
  • 51 Sapp RM, Landers-Ramos RQ, Shill DD. et al. Sex-specific alterations in blood-borne factos in physically inactive individuals are detrimental to endothelial cell functions. J Appl Physiol (1985) 2020; 129: 664-674
  • 52 Lopez S, Bermudez B. Montserrat-de la Paz S, et al. A microRNA expression signature of the postprandial state in response to a high-saturated-fat challenge. J Nutr Biochem 2018; 57: 45-55
  • 53 Mathiyalagan P, Liang Y, Kim D. et al. Angiogenic mechanisms of human CD34+ stem cell exosomes in the repair of ischemic hindlimb. Circ Res 2017; 120: 1466-1476
  • 54 Mocharla P, Briand S, Giannotti G. et al. AngiomiR-126 expression and secretion from circulating CD34+ and CD14+ PBMCs: Role for proangiogenic effects and alterations in type 2 diabetics. Blood 2013; 121: 226-236
  • 55 Zhang J, Zhao F, Yu X. et al. MicroRNA-155 modulates the proliferation of vascular smooth muscle cells by targeting endothelial nitric oxide synthase. Int J Mol Med 2015; 35: 1708-1714
  • 56 Wahl P, Wehmeier UF, Jansen FJ. et al. Acute effects of different exercise protocols on the circulating vascular microRNAs -16, -21, and -126 in trained subjects. Front Physiol 2016; 7: 643
  • 57 Uhlemann M, Möbius-Winkler S, Fikenzer S. et al. Circulating microRNA-126 increases after different forms of endurance exercise in healthy adults. Eur J Prev Cardiol 2014; 21: 484-491
  • 58 Schmitz B, Schelleckes K, Nedele J. et al. Dose-response of High-Intensity Training (HIT) on atheroprotective miRNA-126 levels. Front Physiol 2017; 8: 349
  • 59 Banzet S, Chennaoui M, Girard O. et al. Changes in circulating microRNAs levels with exercise modality. J Appl Physiol (1985) 2013; 115: 1237-1244
  • 60 Baggish AL, Hale A, Weiner RB. et al. Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J Physiol 2011; 589: 3983-3994
  • 61 D’souza RF, Woodhead JST, Zeng N. et al. Circulatory exosomal miRNA following intense exercise is unrelated to muscle and plasma miRNA abundances. Am J Physiol Endocrinol Metab 2018; 315: E723-E733
  • 62 Guescini M, Canonico B, Lucertini F. et al. Muscle releases alpha-sarcoglycan positive extracellular vesicles carrying miRNAs in the bloodstream. PLoS One 2015; 10:: e0125094
  • 63 Mayr B, Müller EE, Schäfer C. et al. Exercise responsive micro ribonucleic acids identify patients with coronary artery disease. Eur J Prev Cardiol 2019; 26: 348-355
  • 64 Nielsen S, Akerstrom T, Rinnov A. et al. The miRNA plasma signature in response to acute aerobic exercise and endurance training. PLoS One 2014; 9: e87308
  • 65 Ramos AE, Lo C, Estephan LE. et al. Specific circulating microRNAs display dose-dependent responses to variable intensity and duration of endurance exercise. Am J Physiol Heart Circ Physiol 2018; 315: H273-H283
  • 66 Schmitz B, Niehues H, Lenders M. et al. Effects of high-intensity interval training on microvascular glycocalyx and associated microRNAs. Am J Physiol Heart Circ Physiol 2019; 316: H1538-H1551
  • 67 Schmitz B, Rolfes F, Schelleckes K. et al. Longer work/rest intervals during High-Intensity Interval Training (HIIT) lead to elevated levels of miR-222 and miR-29c. Front Physiol 2018; 9: 395
  • 68 Alexy T, Rooney K, Weber M. et al. TNF-α alters the release and transfer of microparticle-encapsulated miRNAs from endothelial cells. Physiol Genomics 2014; 46: 833-840
  • 69 Lee DY, Chiu JJ. Atherosclerosis and flow: Roles of epigenetic modulation in vascular endothelium. J Biomed Sci 2019; 26: 56
  • 70 Padilla J, Simmons GH, Bender SB. et al. Vascular effects of exercise: endothelial adaptations beyond active muscle beds. Physiology (Bethesda) 2011; 26: 132-145
  • 71 Green DJ, Hopman MTE, Padilla J. et al. Vascular adaptation to exercise in humans: Role of hemodynamic stimuli. Physiol Rev 2017; 97: 495-528
  • 72 Schmitz B, Breulmann FL, Jubran B. et al. A three-step approach identifies novel shear stress-sensitive endothelial microRNAs involved in vasculoprotective effects of high-intensity interval training (HIIT). Oncotarget 2019; 10: 3625-3640