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Frontiers in physiology2023; 14; 1256217; doi: 10.3389/fphys.2023.1256217

Dynamics of training and acute exercise-induced shifts in muscular glucose transporter (GLUT) 4, 8, and 12 expression in locomotion versus posture muscles in healthy horses.

Abstract: Important changes in glucose transporter (GLUT) expression should be expected if the glucose influx plays a pivotal role in fuelling or connecting metabolic pathways that are upregulated in response to exercise. The aim was to assess GLUT4, 8, and 12 dynamics in response to training and acute exercise. Sixteen untrained Standardbred mares (3-4 year) performed an incremental SET at the start and end of 8 weeks harness training. M. pectoralis (PM) and M. vastus lateralis (VL) muscle biopsies were taken before and after each SET, allowing for comparing rest and acute samples in untrained (UT) and trained (T) condition using Western Blot for GLUT quantification and Image Pro v.10 for Blot analysis. Data were normalized against GAPDH. Basal GLUT-levels of PM VL were analysed with the Wilcoxon matched-pairs signed rank test. The effect of acute exercise or training was assessed using the Friedman test with a Dunn's. Basal GLUT4 and GLUT12 protein expression were significantly higher in the VL compared to the PM (P = 0.031 and P = 0.002). Training had no effect on basal GLUT4 expression, neither in the VL ( > 0.9999), nor the PM ( > 0.9999). However, acute exercise in trained condition significantly decreased GLUT4 expression in the VL ( = 0.0148). Neither training nor acute exercise significantly changed total GLUT8 protein expression. Training significantly decreased total GLUT12 protein expression in rest biopsies, only visible in the VL ( = 0.0359). This decrease was even more prominent in the VL after acute exercise in trained condition (P = 0.0025). The important changes seen in GLUT12 expression downregulation, both in response to training and acute exercise in the horse, the downregulation of GLUT4 expression after acute exercise in trained condition and the lack of differential shifts in GLUT8 expression in any of the studied conditions, questions the importance of glucose as substrate to fuel training and exercise in healthy horses. These findings encourage to further explore alternative fuels for their involvement in equine muscular energetics.
Copyright © 2023 Vidal Moreno de Vega, Lemmens, de Meeûs d’Argenteuil, Boshuizen, de Maré, Leybaert, Goethals, de Oliveira, Hosotani, Deforce, Van Nieuwerburgh, Devisscher and Delesalle.
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Publication Date: 2023-08-16 PubMed ID: 37654675PubMed Central: PMC10466803DOI: 10.3389/fphys.2023.1256217Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research aims to understand the changes in expression of glucose transporters (GLUT 4, 8, 12) in horses’ muscles, due to both training and acute exercise, and questions the importance of glucose as a fuel source during horse training and exercise. Using Standardbred mares, the researchers found significant changes specifically in the expression of GLUT 4 and 12, leading to the suggestion of exploring alternative fuels for equine muscular energetics.

Study Design

  • The researches utilized 16 untrained Standardbred mares, aged between 3 to 4 years, subjecting them to an incremental Standardized Exercise Test (SET) at the start and end of an 8-week harness training regime.
  • Muscle biopsies of the M. pectoralis (PM) and M. vastus lateralis (VL) were taken before and after each SET, for comparison between resting and acute exercise samples in both untrained (UT) and trained (T) conditions.
  • Quantification of the GLUT expression was performed using Western Blot, analyzed with Image Pro v.10. Data normalization was done against GAPDH.
  • Statistical analyses involved the Wilcoxon matched-pairs signed rank test for basal GLUT levels, and the Friedman test with a Dunn’s for examining the effect of acute exercise or training.

Findings

  • In resting conditions, GLUT4 and GLUT12 protein expression was found to be significantly higher in the VL as compared to the PM.
  • Training was found to have no effect on the basal expression of GLUT4 in either the VL or PM muscles.
  • However, acute exercise in trained horses was found to decrease GLUT4 expression significantly in the VL muscle.
  • There were no significant changes in total GLUT8 protein expression due to either acute exercise or training.
  • Training led to a significant decrease in total GLUT12 protein expression in resting biopsies, more prominently visible in the VL muscles.
  • This decrease in GLUT12 expression was more pronounced in the VL muscles after acute exercise in trained conditions.

Implications

  • The observed changes in GLUT12 expression – both in response to training and acute exercise in horses, downregulation of GLUT4 expression post acute exercise in trained conditions, and no significant shifts in GLUT8 expression – call for questioning the importance of glucose as a substrate to fuel training and exercise in horses.
  • The findings of this study hint at the potential need to explore alternate fuels, beyond glucose, for their involvement in equine muscular energetics.

Cite This Article

APA
Vidal Moreno de Vega C, Lemmens D, de Meeûs d'Argenteuil C, Boshuizen B, de Maré L, Leybaert L, Goethals K, de Oliveira JE, Hosotani G, Deforce D, Van Nieuwerburgh F, Devisscher L, Delesalle C. (2023). Dynamics of training and acute exercise-induced shifts in muscular glucose transporter (GLUT) 4, 8, and 12 expression in locomotion versus posture muscles in healthy horses. Front Physiol, 14, 1256217. https://doi.org/10.3389/fphys.2023.1256217

Publication

Frontiers in physiology
ISSN: 1664-042X
NlmUniqueID: 101549006
Country: Switzerland
Language: English
Volume: 14
Pages: 1256217
PII: 1256217

Researcher Affiliations

Vidal Moreno de Vega, Carmen
  • Department of Translational Physiology, Infectiology and Public Health, Research Group of Comparative Physiology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Lemmens, Diete
  • Department of Translational Physiology, Infectiology and Public Health, Research Group of Comparative Physiology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
de Meeûs d'Argenteuil, Constance
  • Department of Translational Physiology, Infectiology and Public Health, Research Group of Comparative Physiology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Boshuizen, Berit
  • Department of Translational Physiology, Infectiology and Public Health, Research Group of Comparative Physiology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
  • Wolvega Equine Hospital, Oldeholtpade, Netherlands.
de Maré, Lorie
  • Department of Translational Physiology, Infectiology and Public Health, Research Group of Comparative Physiology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
Leybaert, Luc
  • Department of Basic and Applied Medical Sciences, Faculty of Medicine and Health Sciences, Ghent University, Ghent, Belgium.
Goethals, Klara
  • Biometrics Research Center, Ghent University, Ghent, Belgium.
de Oliveira, Jean Eduardo
  • Cargill R&D Centre Europe, Vilvoorde, Belgium.
Hosotani, Guilherme
  • Cargill R&D Centre Europe, Vilvoorde, Belgium.
Deforce, Dieter
  • Laboratory of Pharmaceutical Biotechnology, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium.
Van Nieuwerburgh, Filip
  • Laboratory of Pharmaceutical Biotechnology, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium.
Devisscher, Lindsey
  • Gut-Liver Immunopharmacology Unit, Department of Basic and Applied Medical Sciences, Liver Research Center Ghent, Ghent University, Ghent, Belgium.
Delesalle, Cathérine
  • Department of Translational Physiology, Infectiology and Public Health, Research Group of Comparative Physiology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.

Conflict of Interest Statement

JO and GH were employed by the Cargill R&D Centre Europe. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 87 references
  1. Abdul-Ghani MA, DeFronzo RA. Pathogenesis of insulin resistance in skeletal muscle.. J Biomed Biotechnol 2010;2010:476279.
    doi: 10.1155/2010/476279pmc: PMC2860140pubmed: 20445742google scholar: lookup
  2. Aerni-Flessner L, Abi-Jaoude M, Koenig A, Payne M, Hruz PW. GLUT4, GLUT1, and GLUT8 are the dominant GLUT transcripts expressed in the murine left ventricle.. Cardiovasc Diabetol 2012 Jun 8;11:63.
    doi: 10.1186/1475-2840-11-63pmc: PMC3416696pubmed: 22681646google scholar: lookup
  3. Arfuso F, Acri G, Piccione G, Sansotta C, Fazio F, Giudice E, Giannetto C. Eye surface infrared thermography usefulness as a noninvasive method of measuring stress response in sheep during shearing: Correlations with serum cortisol and rectal temperature values.. Physiol Behav 2022 Jun 1;250:113781.
    doi: 10.1016/j.physbeh.2022.113781pubmed: 35314176google scholar: lookup
  4. Arfuso F, Giannetto C, Fazio F, Panzera F, Piccione G. Training Program Intensity Induces an Acute Phase Response in Clinically Healthy Horses.. J Equine Vet Sci 2020 May;88:102986.
    doi: 10.1016/j.jevs.2020.102986pubmed: 32303313google scholar: lookup
  5. Arfuso F, Giannetto C, Giudice E, Fazio F, Panzera M, Piccione G. Peripheral Modulators of the Central Fatigue Development and Their Relationship with Athletic Performance in Jumper Horses.. Animals (Basel) 2021 Mar 8;11(3).
    doi: 10.3390/ani11030743pmc: PMC8002136pubmed: 33800520google scholar: lookup
  6. Arfuso F, Giannetto C, Giudice E, Fazio F, Piccione G. Dynamic Change of Free Serum L-carnitine Concentration in Relation to Age, Sex, and Exercise in Anglo-Arabian Thoroughbred Horses.. J Equine Vet Sci 2021 Feb;97:103343.
    doi: 10.1016/j.jevs.2020.103343pubmed: 33478765google scholar: lookup
  7. Arfuso F, Giannetto C, Interlandi C, Giudice E, Bruschetta A, Panzera MF, Piccione G. Dynamic Metabolic Response, Clotting Times and Peripheral Indices of Central Fatigue in Horse Competing in a 44 Km Endurance Race.. J Equine Vet Sci 2021 Nov;106:103753.
    doi: 10.1016/j.jevs.2021.103753pubmed: 34670693google scholar: lookup
  8. Arfuso F, Giudice E, Panzera M, Rizzo M, Fazio F, Piccione G, Giannetto C. Interleukin-1Ra (Il-1Ra) and serum cortisol level relationship in horse as dynamic adaptive response during physical exercise.. Vet Immunol Immunopathol 2022 Jan;243:110368.
    doi: 10.1016/j.vetimm.2021.110368pubmed: 34922262google scholar: lookup
  9. Arnold PK, Finley LWS. Regulation and function of the mammalian tricarboxylic acid cycle.. J Biol Chem 2023 Feb;299(2):102838.
    doi: 10.1016/j.jbc.2022.102838pmc: PMC9871338pubmed: 36581208google scholar: lookup
  10. Barrett MR, Scott Davis M. Conditioning-induced expression of novel glucose transporters in canine skeletal muscle homogenate.. PLoS One 2023;18(5):e0285424.
    doi: 10.1371/journal.pone.0285424pmc: PMC10155965pubmed: 37134107google scholar: lookup
  11. Bazzano M, Giudice E, Rizzo M, Congiu F, Zumbo A, Arfuso F, Di Pietro S, Bruschetta D, Piccione G. Application of a combined global positioning and heart rate monitoring system in jumper horses during an official competition - A preliminary study.. Acta Vet Hung 2016 Jun;64(2):189-200.
    doi: 10.1556/004.2016.019pubmed: 27342090google scholar: lookup
  12. Benomar Y, Naour N, Aubourg A, Bailleux V, Gertler A, Djiane J, Guerre-Millo M, Taouis M. Insulin and leptin induce Glut4 plasma membrane translocation and glucose uptake in a human neuronal cell line by a phosphatidylinositol 3-kinase- dependent mechanism.. Endocrinology 2006 May;147(5):2550-6.
    doi: 10.1210/en.2005-1464pubmed: 16497805google scholar: lookup
  13. Burkuš J, Navarrete Santos A, Schindler M, Babeľová J, Jung JS, Špirková A, Kšiňanová M, Kovaříková V, Fischer B, Koppel J, Fabian D, Čikoš Š. Adiponectin stimulates glucose uptake in mouse blastocysts and embryonic carcinoma cells.. Reproduction 2020 Mar;159(3):227-239.
    doi: 10.1530/REP-19-0251pubmed: 32023207google scholar: lookup
  14. de Laat MA, Clement CK, Sillence MN, McGowan CM, Pollitt CC, Lacombe VA. The impact of prolonged hyperinsulinaemia on glucose transport in equine skeletal muscle and digital lamellae.. Equine Vet J 2015 Jul;47(4):494-501.
    doi: 10.1111/evj.12320pubmed: 24995680google scholar: lookup
  15. de Laat MA, Robinson MA, Gruntmeir KJ, Liu Y, Soma LR, Lacombe VA. AICAR administration affects glucose metabolism by upregulating the novel glucose transporter, GLUT8, in equine skeletal muscle.. Vet J 2015 Sep;205(3):381-6.
    doi: 10.1016/j.tvjl.2015.05.018pubmed: 26116041google scholar: lookup
  16. De Maré L, Boshuizen B, Vidal Moreno de Vega C, de Meeûs C, Plancke L, Gansemans Y, Van Nieuwerburgh F, Deforce D, de Oliveira JE, Hosotani G, Oosterlinck M, Delesalle C. Profiling the Aerobic Window of Horses in Response to Training by Means of a Modified Lactate Minimum Speed Test: Flatten the Curve.. Front Physiol 2022;13:792052.
    doi: 10.3389/fphys.2022.792052pmc: PMC8982777pubmed: 35392373google scholar: lookup
  17. de Meeûs d'Argenteuil C, Boshuizen B, Oosterlinck M, van de Winkel D, De Spiegelaere W, de Bruijn CM, Goethals K, Vanderperren K, Delesalle CJG. Flexibility of equine bioenergetics and muscle plasticity in response to different types of training: An integrative approach, questioning existing paradigms.. PLoS One 2021;16(4):e0249922.
    doi: 10.1371/journal.pone.0249922pmc: PMC8043414pubmed: 33848308google scholar: lookup
  18. de Meeûs d'Argenteuil C, Boshuizen B, Vidal Moreno de Vega C, Leybaert L, de Maré L, Goethals K, De Spiegelaere W, Oosterlinck M, Delesalle C. Comparison of Shifts in Skeletal Muscle Plasticity Parameters in Horses in Three Different Muscles, in Answer to 8 Weeks of Harness Training.. Front Vet Sci 2021;8:718866.
    doi: 10.3389/fvets.2021.718866pmc: PMC8558477pubmed: 34733900google scholar: lookup
  19. DeBosch BJ, Chen Z, Saben JL, Finck BN, Moley KH. Glucose transporter 8 (GLUT8) mediates fructose-induced de novo lipogenesis and macrosteatosis.. J Biol Chem 2014 Apr 18;289(16):10989-10998.
    doi: 10.1074/jbc.M113.527002pmc: PMC4036240pubmed: 24519932google scholar: lookup
  20. Dicks L. M. T., Botha M., Dicks E., Botes M.. The equine gastro-intestinal tract: an overview of the microbiota, disease and treatment.. Livest. Sci. 160, 69–81.
    doi: 10.1016/j.livsci.2013.11.025google scholar: lookup
  21. Duehlmeier R, Hacker A, Widdel-Bigdely A, von Engelhardt W, Sallmann HP. Insulin stimulates GLUT4 translocation in the semitendinosus muscle of Shetland ponies.. Vet J 2010 May;184(2):176-81.
    doi: 10.1016/j.tvjl.2009.01.024pubmed: 19278877google scholar: lookup
  22. Dumba M, Jawad N, McHugh K. Neuroblastoma and nephroblastoma: a radiological review.. Cancer Imaging 2015 Apr 8;15(1):5.
    doi: 10.1186/s40644-015-0040-6pmc: PMC4446071pubmed: 25889326google scholar: lookup
  23. Durham AE, Frank N, McGowan CM, Menzies-Gow NJ, Roelfsema E, Vervuert I, Feige K, Fey K. ECEIM consensus statement on equine metabolic syndrome.. J Vet Intern Med 2019 Mar;33(2):335-349.
    doi: 10.1111/jvim.15423pmc: PMC6430910pubmed: 30724412google scholar: lookup
  24. Essén-Gustavsson B, McMiken D, Karlström K, Lindholm A, Persson S, Thornton J. Muscular adaptation of horses during intensive training and detraining.. Equine Vet J 1989 Jan;21(1):27-33.
    doi: 10.1111/j.2042-3306.1989.tb02085.xpubmed: 2920697google scholar: lookup
  25. Evans PL, McMillin SL, Weyrauch LA, Witczak CA. Regulation of Skeletal Muscle Glucose Transport and Glucose Metabolism by Exercise Training.. Nutrients 2019 Oct 12;11(10).
    doi: 10.3390/nᄐ2432pmc: PMC6835691pubmed: 31614762google scholar: lookup
  26. Fejsáková M., Kottferová J., Dankulincová Z., Haladová E., Matos R., Miňo I.. Some possible factors affecting horse welfare assessment.. Acta Vet. Brno 82, 447–451.
    doi: 10.2754/avb201382040447google scholar: lookup
  27. Filho H. C. M., Manso H. E. C. C. C., Watford M., McKeever K. H.. Abundance of the skeletal muscle Glut-4 glucose transport protein in Standardbred foals during development and exercise.. Comp. Exerc. Physiol. 16, 395–402.
    doi: 10.3920/CEP200008google scholar: lookup
  28. Flores-Opazo M, McGee SL, Hargreaves M. Exercise and GLUT4.. Exerc Sport Sci Rev 2020 Jul;48(3):110-118.
    doi: 10.1249/JES.0000000000000224pubmed: 32568924google scholar: lookup
  29. Gil-Iturbe E, Castilla-Madrigal R, Barrenetxe J, Villaro AC, Lostao MP. GLUT12 expression and regulation in murine small intestine and human Caco-2 cells.. J Cell Physiol 2019 Apr;234(4):4396-4408.
    doi: 10.1002/jcp.27231pubmed: 30352123google scholar: lookup
  30. Gordon M. E., Jerina M. L., Raub R. H., Davison K., Young J., Williamson K. K.. The effects of dietary manipulation and exercise on weight loss and related indices of health in horses.. Comp. Exerc. Physiol. 6, 33–43.
    doi: 10.1017/S1478061509356169google scholar: lookup
  31. Hickner RC, Fisher JS, Hansen PA, Racette SB, Mier CM, Turner MJ, Holloszy JO. Muscle glycogen accumulation after endurance exercise in trained and untrained individuals.. J Appl Physiol (1985) 1997 Sep;83(3):897-903.
    doi: 10.1152/jappl.1997.83.3.897pubmed: 9292478google scholar: lookup
  32. Holman GD. Structure, function and regulation of mammalian glucose transporters of the SLC2 family.. Pflugers Arch 2020 Sep;472(9):1155-1175.
    doi: 10.1007/s00424-020-02411-3pmc: PMC7462842pubmed: 32591905google scholar: lookup
  33. Iwayama K, Tanabe Y, Yajima K, Tanji F, Onishi T, Takahashi H. Preexercise High-Fat Meal Following Carbohydrate Loading Attenuates Glycogen Utilization During Endurance Exercise in Male Recreational Runners.. J Strength Cond Res 2023 Mar 1;37(3):661-668.
    doi: 10.1519/JSC.0000000000004311pubmed: 36165996google scholar: lookup
  34. Jose-Cunilleras E, Hayes KA, Toribio RE, Mathes LE, Hinchcliff KW. Expression of equine glucose transporter type 4 in skeletal muscle after glycogen-depleting exercise.. Am J Vet Res 2005 Mar;66(3):379-85.
    doi: 10.2460/ajvr.2005.66.379pubmed: 15822579google scholar: lookup
  35. Kaneko J. J., Harvey J. W., Bruss M. L.. Clinical biochemistry of domestic animals.. 6th ed. Cambridge: Academic Press.
  36. Katz EB, Stenbit AE, Hatton K, DePinho R, Charron MJ. Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4.. Nature 1995 Sep 14;377(6545):151-5.
    doi: 10.1038/377151a0pubmed: 7675081google scholar: lookup
  37. Kearns CF, McKeever KH, Abe T. Overview of horse body composition and muscle architecture: implications for performance.. Vet J 2002 Nov;164(3):224-34.
    doi: 10.1053/tvjl.2001.0702pubmed: 12505395google scholar: lookup
  38. Klein B. G.. The Physiology of muscle. in Cunninham’s textbook of veterinary Physiology (St.Louis: Elsevier; ), 73–81.
  39. Lacombe VA. Expression and regulation of facilitative glucose transporters in equine insulin-sensitive tissue: from physiology to pathology.. ISRN Vet Sci 2014;2014:409547.
    doi: 10.1155/2014/409547pmc: PMC4060548pubmed: 24977043google scholar: lookup
  40. Lacombe VA, Hinchcliff KW, Devor ST. Effects of exercise and glucose administration on content of insulin-sensitive glucose transporter in equine skeletal muscle.. Am J Vet Res 2003 Dec;64(12):1500-6.
    doi: 10.2460/ajvr.2003.64.1500pubmed: 14672428google scholar: lookup
  41. Lacombe VA, Hinchcliff KW, Kohn CW, Devor ST, Taylor LE. Effects of feeding meals with various soluble-carbohydrate content on muscle glycogen synthesis after exercise in horses.. Am J Vet Res 2004 Jul;65(7):916-23.
    doi: 10.2460/ajvr.2004.65.916pubmed: 15281649google scholar: lookup
  42. Macheda ML, Rogers S, Best JD. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer.. J Cell Physiol 2005 Mar;202(3):654-62.
    doi: 10.1002/jcp.20166pubmed: 15389572google scholar: lookup
  43. Manolescu AR, Witkowska K, Kinnaird A, Cessford T, Cheeseman C. Facilitated hexose transporters: new perspectives on form and function.. Physiology (Bethesda) 2007 Aug;22:234-40.
    doi: 10.1152/physiol.00011.2007pubmed: 17699876google scholar: lookup
  44. Manso Filho H. C., Betros C. L., Gordon M. E., Manso H. E. C. C. C., Watford M., McKeever K. H.. Exercise training, Glut-4 protein abundance and glutamine in skeletal muscle of mature and very old horses.. Comp. Exerc. Physiol. 13, 63–69.
    doi: 10.3920/CEP170003google scholar: lookup
  45. Tremblay F, Dubois MJ, Marette A. Regulation of GLUT4 traffic and function by insulin and contraction in skeletal muscle.. Front Biosci 2003 Sep 1;8:d1072-84.
    doi: 10.2741/1137pubmed: 12957810google scholar: lookup
  46. Martinez E., Maria Z., Periasamy M., Lacombe V.. Abstract 15940: calcium and insulin regulate the novel glucose transporter 8 (GLUT8) in the healthy and diabetic myocardium.. Circulation 130.
    doi: 10.1161/circ.130.suppl_2.15940google scholar: lookup
  47. Matsuo S, Hiasa M, Omote H. Functional characterization and tissue localization of the facilitative glucose transporter GLUT12.. J Biochem 2020 Dec 26;168(6):611-620.
    doi: 10.1093/jb/mvaa090pubmed: 32761185google scholar: lookup
  48. McCutcheon LJ, Geor RJ, Hinchcliff KW. Changes in skeletal muscle GLUT4 content and muscle membrane glucose transport following 6 weeks of exercise training.. Equine Vet J Suppl 2002 Sep;(34):199-204.
    doi: 10.1111/j.2042-3306.2002.tb05418.xpubmed: 12405686google scholar: lookup
  49. Morgan RA, Keen JA, McGowan CM. Treatment of equine metabolic syndrome: A clinical case series.. Equine Vet J 2016 Jul;48(4):422-6.
    doi: 10.1111/evj.12445pubmed: 25808563google scholar: lookup
  50. Morgan R, Keen J, McGowan C. Equine metabolic syndrome.. Vet Rec 2015 Aug 15;177(7):173-9.
    doi: 10.1136/vr.103226pmc: PMC4552932pubmed: 26273009google scholar: lookup
  51. Mueckler M, Thorens B. The SLC2 (GLUT) family of membrane transporters.. Mol Aspects Med 2013 Apr-Jun;34(2-3):121-38.
    doi: 10.1016/j.mam.2012.07.001pmc: PMC4104978pubmed: 23506862google scholar: lookup
  52. Narita H, Tanji K, Miki Y, Mori F, Wakabayashi K. Trehalose intake and exercise upregulate a glucose transporter, GLUT8, in the brain.. Biochem Biophys Res Commun 2019 Jun 30;514(3):672-677.
    doi: 10.1016/j.bbrc.2019.05.017pubmed: 31078265google scholar: lookup
  53. Naylor JM, Kronfeld DS, Acland H. Hyperlipemia in horses: effects of undernutrition and disease.. Am J Vet Res 1980 Jun;41(6):899-905.
    pubmed: 7436077
  54. Nout YS, Hinchcliff KW, Jose-Cunilleras E, Dearth LR, Sivko GS, DeWille JW. Effect of moderate exercise immediately followed by induced hyperglycemia on gene expression and content of the glucose transporter-4 protein in skeletal muscles of horses.. Am J Vet Res 2003 Nov;64(11):1401-8.
    doi: 10.2460/ajvr.2003.64.1401pubmed: 14620777google scholar: lookup
  55. Payne RC, Hutchinson JR, Robilliard JJ, Smith NC, Wilson AM. Functional specialisation of pelvic limb anatomy in horses (Equus caballus).. J Anat 2005 Jun;206(6):557-74.
    doi: 10.1111/j.1469-7580.2005.00420.xpmc: PMC1571521pubmed: 15960766google scholar: lookup
  56. Payne RC, Veenman P, Wilson AM. The role of the extrinsic thoracic limb muscles in equine locomotion.. J Anat 2005 Feb;206(2):193-204.
    doi: 10.1111/j.1469-7580.2005.00353.xpmc: PMC1571467pubmed: 15730484google scholar: lookup
  57. Pratt SE, Geor RJ, Spriet LL, McCutcheon LJ. Time course of insulin sensitivity and skeletal muscle glycogen synthase activity after a single bout of exercise in horses.. J Appl Physiol (1985) 2007 Sep;103(3):1063-9.
    doi: 10.1152/japplphysiol.01349.2006pubmed: 17585040google scholar: lookup
  58. Pujol-Giménez J, Barrenetxe J, González-Muniesa P, Lostao MP. The facilitative glucose transporter GLUT12: what do we know and what would we like to know?. J Physiol Biochem 2013 Jun;69(2):325-33.
    doi: 10.1007/s13105-012-0213-8pubmed: 23385668google scholar: lookup
  59. Pujol-Giménez J, Pérez A, Reyes AM, Loo DD, Lostao MP. Functional characterization of the human facilitative glucose transporter 12 (GLUT12) by electrophysiological methods.. Am J Physiol Cell Physiol 2015 Jun 15;308(12):C1008-22.
    doi: 10.1152/ajpcell.00343.2014pubmed: 25855082google scholar: lookup
  60. Rattigan S, Appleby GJ, Clark MG. Insulin-like action of catecholamines and Ca2+ to stimulate glucose transport and GLUT4 translocation in perfused rat heart.. Biochim Biophys Acta 1991 Sep 3;1094(2):217-23.
    doi: 10.1016/0167-4889(91)90012-Mpubmed: 1909899google scholar: lookup
  61. Reed MJ, Brozinick JT Jr, Lee MC, Ivy JL. Muscle glycogen storage postexercise: effect of mode of carbohydrate administration.. J Appl Physiol (1985) 1989 Feb;66(2):720-6.
    doi: 10.1152/jappl.1989.66.2.720pubmed: 2651386google scholar: lookup
  62. Ricard A, Chanu I. Genetic parameters of eventing horse competition in France.. Genet Sel Evol 2001 Mar-Apr;33(2):175-90.
    doi: 10.1186/1297-9686-33-2-175pmc: PMC2705390pubmed: 11333833google scholar: lookup
  63. Rivero JL, Hill EW. Skeletal muscle adaptations and muscle genomics of performance horses.. Vet J 2016 Mar;209:5-13.
    doi: 10.1016/j.tvjl.2015.11.019pubmed: 26831154google scholar: lookup
  64. Robert C, Valette JP, Pourcelot P, Audigié F, Denoix JM. Effects of trotting speed on muscle activity and kinematics in saddlehorses.. Equine Vet J Suppl 2002 Sep;(34):295-301.
    doi: 10.1111/j.2042-3306.2002.tb05436.xpubmed: 12405704google scholar: lookup
  65. Ryder JW, Yang J, Galuska D, Rincón J, Björnholm M, Krook A, Lund S, Pedersen O, Wallberg-Henriksson H, Zierath JR, Holman GD. Use of a novel impermeable biotinylated photolabeling reagent to assess insulin- and hypoxia-stimulated cell surface GLUT4 content in skeletal muscle from type 2 diabetic patients.. Diabetes 2000 Apr;49(4):647-54.
    doi: 10.2337/diabetes.49.4.647pubmed: 10871204google scholar: lookup
  66. Scheepers A, Joost HG, Schürmann A. The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function.. JPEN J Parenter Enteral Nutr 2004 Sep-Oct;28(5):364-71.
    doi: 10.1177/0148607104028005364pubmed: 15449578google scholar: lookup
  67. Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles.. Physiol Rev 2011 Oct;91(4):1447-531.
    doi: 10.1152/physrev.00031.2010pubmed: 22013216google scholar: lookup
  68. nSeki Y.. Alteration in expression of GLUT4, GLUT8 and GLUT12 in human skeletal muscle after prolonged exercise.. 64th Sci. Sess. Available at: https://professional.diabetes.org/abstract/alteration-expression-glut4-glut8-and-glut12-human-skeletal-muscle-after-prolonged-exercise.n.
  69. Seki Y, Berggren JR, Houmard JA, Charron MJ. Glucose transporter expression in skeletal muscle of endurance-trained individuals.. Med Sci Sports Exerc 2006 Jun;38(6):1088-92.
    doi: 10.1249/01.mss.0000222837.74015.f1pubmed: 16775550google scholar: lookup
  70. Sertié RA, Sertié AL, Giannocco G, Poyares LL, Nunes MT. Acute growth hormone administration increases myoglobin expression and Glut4 translocation in rat cardiac muscle cells.. Metabolism 2014 Dec;63(12):1499-502.
    doi: 10.1016/j.metabol.2014.08.012pubmed: 25306099google scholar: lookup
  71. Shao D, Tian R. Glucose Transporters in Cardiac Metabolism and Hypertrophy.. Compr Physiol 2015 Dec 15;6(1):331-51.
    doi: 10.1002/cphy.c150016pmc: PMC4760112pubmed: 26756635google scholar: lookup
  72. Shi Y, Zhang Y, Ran F, Liu J, Lin J, Hao X, Ding L, Ye Q. Let-7a-5p inhibits triple-negative breast tumor growth and metastasis through GLUT12-mediated warburg effect.. Cancer Lett 2020 Dec 28;495:53-65.
    doi: 10.1016/j.canlet.2020.09.012pubmed: 32946964google scholar: lookup
  73. Singer ER, Barnes J, Saxby F, Murray JK. Injuries in the event horse: training versus competition.. Vet J 2008 Jan;175(1):76-81.
    doi: 10.1016/j.tvjl.2006.11.009pubmed: 17204438google scholar: lookup
  74. Stewart-Hunt L, Geor RJ, McCutcheon LJ. Effects of short-term training on insulin sensitivity and skeletal muscle glucose metabolism in standardbred horses.. Equine Vet J Suppl 2006 Aug;(36):226-32.
    doi: 10.1111/j.2042-3306.2006.tb05544.xpubmed: 17402423google scholar: lookup
  75. Stuart CA, Howell ME, Baker JD, Dykes RJ, Duffourc MM, Ramsey MW, Stone MH. Cycle training increased GLUT4 and activation of mammalian target of rapamycin in fast twitch muscle fibers.. Med Sci Sports Exerc 2010 Jan;42(1):96-106.
    doi: 10.1249/MSS.0b013e3181ad7f36pmc: PMC2796589pubmed: 20010125google scholar: lookup
  76. Stuart CA, Howell ME, Zhang Y, Yin D. Insulin-stimulated translocation of glucose transporter (GLUT) 12 parallels that of GLUT4 in normal muscle.. J Clin Endocrinol Metab 2009 Sep;94(9):3535-42.
    doi: 10.1210/jc.2009-0162pmc: PMC2741719pubmed: 19549745google scholar: lookup
  77. Thorens B, Mueckler M. Glucose transporters in the 21st Century.. Am J Physiol Endocrinol Metab 2010 Feb;298(2):E141-5.
    doi: 10.1152/ajpendo.00712.2009pmc: PMC2822486pubmed: 20009031google scholar: lookup
  78. Valberg SJ, Velez-Irizarry D, Williams ZJ, Pagan JD, Mesquita V, Waldridge B, Maresca-Fichter H. Novel Expression of GLUT3, GLUT6 and GLUT10 in Equine Gluteal Muscle Following Glycogen-Depleting Exercise: Impact of Dietary Starch and Fat.. Metabolites 2023 Jun 1;13(6).
    doi: 10.3390/metabo13060718pmc: PMC10301051pubmed: 37367876google scholar: lookup
  79. Vargas E, Podder V, Carrillo Sepulveda MA. Physiology, Glucose Transporter Type 4.. 2023 Jan;.
    pubmed: 30726007
  80. Waller AP, Burns TA, Mudge MC, Belknap JK, Lacombe VA. Insulin resistance selectively alters cell-surface glucose transporters but not their total protein expression in equine skeletal muscle.. J Vet Intern Med 2011 Mar-Apr;25(2):315-21.
    doi: 10.1111/j.1939-1676.2010.0674.xpubmed: 21314720google scholar: lookup
  81. Waller AP, Lindinger MI. Nutritional aspects of post exercise skeletal muscle glycogen synthesis in horses: a comparative review.. Equine Vet J 2010 Apr;42(3):274-81.
    doi: 10.2746/042516409X479603pubmed: 20486986google scholar: lookup
  82. Walsh D. M., McGowan T., Lamb S. V., Schanbacher B. J., Place N. J., McGowan C. M.. Correlation of plasma insulin concentration with laminitis score in a field study of equine cushing’s disease and equine metabolic syndrome.. J. Equine Vet. Sci. 29, 87–94.
    doi: 10.1016/j.jevs.2008.12.006google scholar: lookup
  83. White SH, Warren LK, Li C, Wohlgemuth SE. Submaximal exercise training improves mitochondrial efficiency in the gluteus medius but not in the triceps brachii of young equine athletes.. Sci Rep 2017 Oct 30;7(1):14389.
    doi: 10.1038/s41598-017-14691-4pmc: PMC5662757pubmed: 29085004google scholar: lookup
  84. Wilson-O'Brien AL, Dehaan CL, Rogers S. Mitogen-stimulated and rapamycin-sensitive glucose transporter 12 targeting and functional glucose transport in renal epithelial cells.. Endocrinology 2008 Mar;149(3):917-24.
    doi: 10.1210/en.2007-0985pubmed: 18039784google scholar: lookup
  85. Wilson-O'Brien AL, Patron N, Rogers S. Evolutionary ancestry and novel functions of the mammalian glucose transporter (GLUT) family.. BMC Evol Biol 2010 May 21;10:152.
    doi: 10.1186/1471-2148-10-152pmc: PMC2890515pubmed: 20487568google scholar: lookup
  86. Zierath JR, Hawley JA. Skeletal muscle fiber type: influence on contractile and metabolic properties.. PLoS Biol 2004 Oct;2(10):e348.
    doi: 10.1371/journal.pbio.0020348pmc: PMC521732pubmed: 15486583google scholar: lookup
  87. Zierler K. Whole body glucose metabolism.. Am J Physiol 1999 Mar;276(3):E409-26.
    doi: 10.1152/ajpendo.1999.276.3.E409pubmed: 10070005google scholar: lookup

Citations

This article has been cited 1 times.
  1. Boshuizen B, De Maré L, Oosterlinck M, Van Immerseel F, Eeckhaut V, De Meeus C, Devisscher L, Vidal Moreno de Vega C, Willems M, De Oliveira JE, Hosotani G, Gansemans Y, Meese T, Van Nieuwerburgh F, Deforce D, Vanderperren K, Verdegaal EL, Delesalle C. Aleurone supplementation enhances the metabolic benefits of training in Standardbred mares: impacts on glucose-insulin dynamics and gut microbiome composition. Front Physiol 2025;16:1565005.
    doi: 10.3389/fphys.2025.1565005pubmed: 40276369google scholar: lookup
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