Muscular carnosine is a marker for cardiorespiratory fitness and cardiometabolic risk factors in men with type 1 diabetes.
Cardiometabolic risk factors
Lipoproteins
Magnetic resonance spectroscopy
Muscle carnosine
Physical exercise
Type 1 diabetes
Journal
European journal of applied physiology
ISSN: 1439-6327
Titre abrégé: Eur J Appl Physiol
Pays: Germany
ID NLM: 100954790
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
13
04
2021
accepted:
04
03
2022
pubmed:
18
3
2022
medline:
28
5
2022
entrez:
17
3
2022
Statut:
ppublish
Résumé
Muscle is an essential organ for glucose metabolism and can be influenced by metabolic disorders and physical activity. Elevated muscle carnosine levels have been associated with insulin resistance and cardiometabolic risk factors. Little is known about muscle carnosine in type 1 diabetes (T1D) and how it is influenced by physical activity. The aim of this study was to characterize muscle carnosine in vivo by proton magnetic resonance spectroscopy ( 16 men with T1D (10 athletes/6 sedentary) and 14 controls without diabetes (9/5) were included. Body composition by DXA, cardiorespiratory capacity (VO Subjects with T1D presented higher carnosine CR levels compared to controls. T1D patients with a lower VO Elevated muscle carnosine levels in persons with T1D and their effect on atherogenic lipoproteins can be modulated by physical activity.
Identifiants
pubmed: 35298695
doi: 10.1007/s00421-022-04929-z
pii: 10.1007/s00421-022-04929-z
doi:
Substances chimiques
Biomarkers
0
Lipoproteins
0
Carnosine
8HO6PVN24W
Creatine
MU72812GK0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1429-1440Subventions
Organisme : Department of Universities, Research and Information Society of the Government of Catalonia
ID : 2014_SRG_520
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abbasoğlu L, Kalaz EB, Soluk-Tekkeşin M, Olgaç V, Doğru-Abbasoğlu S, Uysal M (2012) Beneficial effects of taurine and carnosine in experimental ischemia/reperfusion injury in testis. Pediatr Surg Int 28(11):1125–1131. https://doi.org/10.1007/s00383-012-3168-5
doi: 10.1007/s00383-012-3168-5
pubmed: 22961384
Baguet A, Everaert I, De Naeyer H, Reyngoudt H, Stegen S, Beeckman S, Achten E, Vanhee L, Volkaert A, Petrovic M, Taes Y, Derave W (2011) Effects of sprint training combined with vegetarian or mixed diet on muscle carnosine content and buffering capacity. Eur J Appl Physiol 111:2571–2580. https://doi.org/10.1007/s00421-011-1877-4
doi: 10.1007/s00421-011-1877-4
pubmed: 21373871
Balling M, Afzal S, Varbo A, Langsted A, Davey Smith G, Nordestgaard BG (2020) VLDL cholesterol accounts for one-half of the risk of myocardial infarction associated with apoB-containing lipoproteins. J Am Coll Cardiol 76:2725–2735. https://doi.org/10.1016/j.jacc.2020.09.610
doi: 10.1016/j.jacc.2020.09.610
pubmed: 33272366
Befroy DE, Petersen KF, Dufour S, Mason GF, de Graaf RA, Rothman DL, Shulman GI (2007) Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56:1376–1381. https://doi.org/10.2337/db06-0783
doi: 10.2337/db06-0783
pubmed: 17287462
Bergman BC, Howard D, Schauer IE, Maahs DM, Snell-Bergeon JK, Eckel RH, Perreault L, Rewers M (2012) Features of hepatic and skeletal muscle insulin resistance unique to type 1 diabetes. J Clin Endocrinol Metab 97:1663–1672. https://doi.org/10.1210/jc.2011-3172
doi: 10.1210/jc.2011-3172
pubmed: 22362823
pmcid: 3339891
Boldyrev AA, Aldini G, Derave W (2013) Physiology and pathophysiology of carnosine. Physiol Rev 93:1803–1845. https://doi.org/10.1152/physrev.00039.2012
doi: 10.1152/physrev.00039.2012
pubmed: 24137022
Borghouts LB, Keizer HA (2000) Exercise and insulin sensitivity: a review. Int J Sports Med 21:1–12. https://doi.org/10.1055/s-2000-8847
doi: 10.1055/s-2000-8847
pubmed: 10683091
Botteri G, Montori M, Gumà A, Pizarro J, Cedó L, Escolà-Gil JC, Li D, Barroso E, Palomer X, Kohan AB, Vázquez-Carrera M (2017) VLDL and apolipoprotein CIII induce ER stress and inflammation and attenuate insulin signalling via toll-like receptor 2 in mouse skeletal muscle cells. Diabetologia 60:2262–2273. https://doi.org/10.1007/s00125-017-4401-5
doi: 10.1007/s00125-017-4401-5
pubmed: 28835988
pmcid: 6078195
Brugnara L, Vinaixa M, Murillo S, Samino S, Rodriguez MA, Beltran A, Lerin C, Davison G, Correig X, Novials A (2012) Metabolomics approach for analyzing the effects of exercise in subjects with type 1 diabetes mellitus. PLoS ONE 7(7):e40600. https://doi.org/10.1371/journal.pone.0040600
doi: 10.1371/journal.pone.0040600
pubmed: 22792382
pmcid: 3394718
Brugnara L, Mallol R, Ribalta J, Vinaixa M, Murillo S, Casserras T, Guardiola M, Vallvé JC, Kalko SG, Correig X, Novials A (2015) Improving assessment of lipoprotein profile in type 1 diabetes by 1H NMR Spectroscopy. PLoS ONE 10(8):e0136348. https://doi.org/10.1371/journal.pone.0136348
doi: 10.1371/journal.pone.0136348
pubmed: 26317989
pmcid: 4552656
Church TS, Blair SN, Cocreham S, Johannsen N, Johnson W, Kramer K, Mikus CR, Myers V, Nauta M, Rodarte RQ, Sparks L, Thompson A, Earnest CP (2010) Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial. JAMA 304:2253–2262. https://doi.org/10.1001/jama.2010.1710
doi: 10.1001/jama.2010.1710
pubmed: 21098771
pmcid: 3174102
Cytospcape: an open source platform for complex analysis and visualization (2020). http://cytoscape.org/ . Accessed Dec 2020
da Eira SV, Painelli VS, Shinjo SK, Ribeiro Pereira W, Cilli EM, Sale C, Gualano B, Otaduy MC, Artioli GG (2020) Magnetic resonance spectroscopy as a non-invasive method to quantify muscle carnosine in humans: a comprehensive validity assessment. Sci Rep 10(1):4908. https://doi.org/10.1038/s41598-020-61587-x
doi: 10.1038/s41598-020-61587-x
Dalla-Riva J, Stenkula KG, Petrlova J, Lagerstedt JO (2013) Discoidal HDL and apoA-I-derived peptides improve glucose uptake in skeletal muscle. J Lipid Res 54:1275–1282. https://doi.org/10.1194/jlr.M032904
doi: 10.1194/jlr.M032904
pubmed: 23471027
pmcid: 3653404
de Courten B, Kurdiova T, de Courten MP, Belan V, Everaert I, Vician M, Teede H, Gasperikova D, Aldini G, Derave W, Ukropec J, Ukropcova B (2015) Muscle carnosine is associated with cardiometabolic risk factors in humans. PLoS ONE 10(10):e0138707. https://doi.org/10.1371/journal.pone.0138707
doi: 10.1371/journal.pone.0138707
pubmed: 26439389
pmcid: 4595442
Duan Y, Li F, Tan B, Yao K, Yin Y (2017) Metabolic control of myofibers: promising therapeutic target for obesity and type 2 diabetes. Obes Rev 18:647–659. https://doi.org/10.1111/obr.12530
doi: 10.1111/obr.12530
pubmed: 28391659
Dubé JJ, Amati F, Stefanovic-Racic M, Toledo FG, Sauers SE, Goodpaster BH (2008) Exercise-induced alterations in intramyocellular lipids and insulin resistance: the athlete’s paradox revisited. Am J Physiol Endocrinol Metab 294:E882–E888. https://doi.org/10.1152/ajpendo.00769.2007
doi: 10.1152/ajpendo.00769.2007
pubmed: 18319352
Egan B, Zierath JR (2013) Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab 17:162–184. https://doi.org/10.1016/j.cmet.2012.12.012
doi: 10.1016/j.cmet.2012.12.012
pubmed: 23395166
DeFronzo RA, Tripathy D (2009) Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32(Suppl 2):S157–S163. https://doi.org/10.2337/dc09-S302
doi: 10.2337/dc09-S302
pubmed: 19875544
pmcid: 2811436
Gualano B, Everaert I, Stegen S, Artioli GG, Taes Y, Roschel H, Achten E, Otaduy MC, Junior AH, Harris R, Derave W (2012) Reduced muscle carnosine content in type 2, but not in type 1 diabetic patients. Amino Acids 43:21–24. https://doi.org/10.1007/s00726-011-1165-y
doi: 10.1007/s00726-011-1165-y
pubmed: 22120670
IPAQ. International physical activity questionnaire. http://www.ipaq.ki.se/ , https://sites.google.com/site/theipaq/
Kamei J, Ohsawa M, Miyata S, Tanaka S (2008) Preventive effect of L-carnosine on changes in the thermal nociceptive threshold in streptozotocin-induced diabetic mice. Eur J Pharmacol 600(1–3):83–86. https://doi.org/10.1016/j.ejphar.2008.10.002
doi: 10.1016/j.ejphar.2008.10.002
pubmed: 18930724
Kaul K, Apostolopoulou M, Roden M (2015) Insulin resistance in type 1 diabetes mellitus. Metab Clin Exp 64:1629–1639. https://doi.org/10.1016/j.metabol.2015.09.002
doi: 10.1016/j.metabol.2015.09.002
pubmed: 26455399
Kodama S, Saito K, Tanaka S, Maki M, Yachi Y, Asumi M, Sugawara A, Totsuka K, Shimano H, Ohashi Y, Yamada N, Sone H (2009) Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis. JAMA 301:2024–2035. https://doi.org/10.1001/jama.2009.681
doi: 10.1001/jama.2009.681
pubmed: 19454641
Krššák M, Lindeboom L, Schrauwen-Hinderling V, Szczepaniak LS, Derave W, Lundbom J, Befroy D, Schick F, Machann J, Kreis R, Boesch C (2021) Proton magnetic resonance spectroscopy in skeletal muscle: experts’ consensus recommendations. NMR Biomed 34(5):e4266. https://doi.org/10.1002/nbm.4266
doi: 10.1002/nbm.4266
pubmed: 32022964
Lawler JM, Barnes WS, Wu G, Song W, Demaree S (2002) Direct antioxidant properties of creatine. Biochem Biophys Res Commun 290:47–52. https://doi.org/10.1006/bbrc.2001.6164
doi: 10.1006/bbrc.2001.6164
pubmed: 11779131
Lyerly GW, Sui X, Lavie CJ, Church TS, Hand GA, Blair SN (2009) The association between cardiorespiratory fitness and risk of all-cause mortality among women with impaired fasting glucose or undiagnosed diabetes mellitus. Mayo Clin Proc 84:780–786. https://doi.org/10.1016/S0025-6196(11)60487-4
doi: 10.1016/S0025-6196(11)60487-4
pubmed: 19720775
pmcid: 2735427
Machann J, Häring H, Schick F, Stumvoll M (2004) Intramyocellular lipids and insulin resistance. Diabetes Obes Metab 6:239–248. https://doi.org/10.1111/j.1462-8902.2004.00339.x
doi: 10.1111/j.1462-8902.2004.00339.x
pubmed: 15171747
Mallol R, Amigó N, Rodríguez MA, Heras M, Vinaixa M, Plana N, Rock E, Ribalta J, Yanes O, Masana L, Correig X (2015) Liposcale: a novel advanced lipoprotein test based on 2D diffusion-ordered H NMR spectroscopy. J Lipid Res 56:737–746. https://doi.org/10.1194/jlr.D050120
doi: 10.1194/jlr.D050120
pubmed: 25568061
pmcid: 4340320
Matthews JJ, Dolan E, Swinton PA, Santos L, Artioli GG, Turner MD, Elliott-Sale KJ, Sale C (2021) Effect of carnosine or β-alanine supplementation on markers of glycemic control and insulin resistance in humans and animals: a systematic review and meta-analysis. Adv Nutr (bethesda, MD) 12(6):2216–2231. https://doi.org/10.1093/advances/nmab087
doi: 10.1093/advances/nmab087
Meex RC, Schrauwen-Hinderling VB, Moonen-Kornips E, Schaart G, Mensink M, Phielix E, van de Weijer T, Sels JP, Schrauwen P, Hesselink MK (2010) Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity. Diabetes 59:572–579. https://doi.org/10.2337/db09-1322
doi: 10.2337/db09-1322
pubmed: 20028948
Monaco C, Hughes MC, Ramos SV, Varah NE, Lamberz C, Rahman FA, McGlory C, Tarnopolsky MA, Krause MP, Laham R, Hawke TJ, Perry C (2018) Altered mitochondrial bioenergetics and ultrastructure in the skeletal muscle of young adults with type 1 diabetes. Diabetologia 61(6):1411–1423. https://doi.org/10.1007/s00125-018-4602-6
doi: 10.1007/s00125-018-4602-6
pubmed: 29666899
Oberbach A, Bossenz Y, Lehmann S, Niebauer J, Adams V, Paschke R, Schön MR, Blüher M, Punkt K (2006) Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 29:895–900. https://doi.org/10.2337/diacare.29.04.06.dc05-1854
doi: 10.2337/diacare.29.04.06.dc05-1854
pubmed: 16567834
Ozdemir MS, Reyngoudt H, De Deene Y, Sazak HS, Fieremans E, Delputte S, D’Asseler Y, Derave W, Lemahieu I, Achten E (2007) Absolute quantification of carnosine in human calf muscle by proton magnetic resonance spectroscopy. Phys Med Biol 52:6781–6794. https://doi.org/10.1088/0031-9155/52/23/001
doi: 10.1088/0031-9155/52/23/001
pubmed: 18029975
Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664–671. https://doi.org/10.1056/NEJMoa031314
doi: 10.1056/NEJMoa031314
pubmed: 14960743
pmcid: 2995502
Petersen KF, Dufour S, Savage DB, Bilz S, Solomon G, Yonemitsu S, Cline GW, Befroy D, Zemany L, Kahn BB, Papademetris X, Rothman DL, Shulman GI (2007) The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci USA 104:12587–12594. https://doi.org/10.1073/pnas.0705408104
doi: 10.1073/pnas.0705408104
pubmed: 17640906
pmcid: 1924794
Pfister F, Riedl E, Wang Q, vom Hagen F, Deinzer M, Harmsen MC, Molema G, Yard B, Feng Y, Hammes HP (2011) Oral carnosine supplementation prevents vascular damage in experimental diabetic retinopathy. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol 28(1):125–136. https://doi.org/10.1159/000331721
doi: 10.1159/000331721
R project for statistical computing. https://www.r-project.org/ . Accessed Dec 2020
Richter EA, Hargreaves M (2013) Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev 93:993–1017. https://doi.org/10.1152/physrev.00038.201
doi: 10.1152/physrev.00038.201
pubmed: 23899560
Ripley EM, Clarke GD, Hamidi V, Martinez RA, Settles FD, Solis C, Deng S, Abdul-Ghani M, Tripathy D, DeFronzo RA (2018) Reduced skeletal muscle phosphocreatine concentration in type 2 diabetic patients: a quantitative image-based phosphorus-31 MR spectroscopy study. Am J Physiol Endocrinol Metab 315(2):E229–E239. https://doi.org/10.1152/ajpendo.00426.2017
doi: 10.1152/ajpendo.00426.2017
pubmed: 29509433
pmcid: 6139498
Ross R, Blair SN, Arena R, Church TS, Després JP, Franklin BA, Haskell WL, Kaminsky LA, Levine BD, Lavie CJ, Myers J, Niebauer J, Sallis R, Sawada SS, Sui X, Wisløff U, American Heart Association Physical Activity Committee of the Council on Lifestyle and Cardiometabolic Health, Council on Clinical Cardiology, Council on Epidemiology and Prevention, Council on Cardiovascular and Stroke Nursing, and Stroke Council (2016) Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the American Heart Association. Circulation 134:e653–e699. https://doi.org/10.1161/CIR.0000000000000461
doi: 10.1161/CIR.0000000000000461
pubmed: 27881567
Saunders B, Elliott-Sale K, Artioli GG, Swinton PA, Dolan E, Roschel H, Sale C, Gualano B (2017) β-alanine supplementation to improve exercise capacity and performance: a systematic review and meta-analysis. Br J Sports Med 51(8):658–669. https://doi.org/10.1136/bjsports-2016-096396
doi: 10.1136/bjsports-2016-096396
pubmed: 27797728
Sietsema KE, Stringer WW, Sue DY, Ward S (2021) Wasserman & Whipp’s: principles of exercise testing and interpretation: including pathophysiology and clinical applications. Wolters Kluwer Health, Philadelphia (Kindle edition. Library of Congress Control Number: 2020905821)
Sluik D, Buijsse B, Muckelbauer R, Kaaks R, Teucher B, Johnsen NF et al (2012) Physical activity and mortality in individuals with diabetes mellitus: a prospective study and meta-analysis. Arch Intern Med 172:1285–1295. https://doi.org/10.1001/archinternmed.2012.3130
doi: 10.1001/archinternmed.2012.3130
pubmed: 22868663
Srikanthan P, Singhal A, Lee CC, Nagarajan R, Wilson N, Roberts CK, Hahn TJ, Thomas MA (2012) Characterization of intra-myocellular lipids using 2D localized correlated spectroscopy and abdominal fat using MRI in type 2 diabetes. Magn Reson Insights 5:29–36. https://doi.org/10.4137/MRI.S10489
doi: 10.4137/MRI.S10489
pubmed: 23471581
Stefan D, Cesare FD, Andrasescu A, Pop E, Lazarie A, Vescovo E, Strbak O, Williams S, Starcuk Z, Cabanas M, van Ormondt D, Graveron-Demilly D (2009) Quantitation of magnetic resonance spectroscopy signals: the jMRUI software package. Meas Sci Technol 20:104035. https://doi.org/10.1088/0957-0233/20/10/104035
doi: 10.1088/0957-0233/20/10/104035
Stegen S, Everaert I, Deldicque L, Vallova S, de Courten B, Ukropcova B, Ukropec J, Derave W (2015) Muscle histidine-containing dipeptides are elevated by glucose intolerance in both rodents and men. PLoS ONE 10(3):e0121062. https://doi.org/10.1371/journal.pone.0121062
doi: 10.1371/journal.pone.0121062
pubmed: 25803044
pmcid: 4372406
Thorell A, Hirshman MF, Nygren J, Jorfeldt L, Wojtaszewski JF, Dufresne SD, Horton ES, Ljungqvist O, Goodyear LJ (1999) Exercise and insulin cause GLUT-4 translocation in human skeletal muscle. Am J Physiol 277:E733–E741. https://doi.org/10.1152/ajpendo.1999.277.4.E733
doi: 10.1152/ajpendo.1999.277.4.E733
pubmed: 10516134
Tikkanen-Dolenc H, Wadén J, Forsblom C, Harjutsalo V, Thorn LM, Saraheimo M, Elonen N, Rosengård-Bärlund M, Gordin D, Tikkanen HO, Groop PH, FinnDiane Study Group (2017) Frequent and intensive physical activity reduces risk of cardiovascular events in type 1 diabetes. Diabetologia 60:574–580. https://doi.org/10.1007/s00125-016-4189-8
doi: 10.1007/s00125-016-4189-8
pubmed: 28013340
van de Weijer T, Schrauwen-Hinderling VB (2019) Application of magnetic resonance spectroscopy in metabolic research. Biochim Biophys Acta Mol Basis Dis 1865:741–748. https://doi.org/10.1016/j.bbadis.2018.09.013
doi: 10.1016/j.bbadis.2018.09.013
pubmed: 30261288
Wu G (2020) Important roles of dietary taurine, creatine, carnosine, anserine and 4-hydroxyproline in human nutrition and health. Amino Acids 52:329–360. https://doi.org/10.1007/s00726-020-02823-6
doi: 10.1007/s00726-020-02823-6
pubmed: 32072297
pmcid: 7088015
Zierath JR, Krook A, Wallberg-Henkinsson H (2000) Insulin action and insulin resistance in human skeletal muscle. Diabetologia 43:821–935. https://doi.org/10.1007/s001250051457
doi: 10.1007/s001250051457
pubmed: 10952453