Insulin-induced membrane permeability to glucose in human muscles at rest and following exercise.
glucose uptake
insulin sensitivity
microdialysis
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
11
07
2019
accepted:
04
11
2019
pubmed:
8
11
2019
medline:
11
2
2021
entrez:
8
11
2019
Statut:
ppublish
Résumé
Increased insulin action is an important component of the health benefits of exercise, but its regulation is complex and not fully elucidated. Previous studies of insulin-stimulated GLUT4 translocation to the skeletal muscle membrane found insufficient increases to explain the increases in glucose uptake. By determination of leg glucose uptake and interstitial muscle glucose concentration, insulin-induced muscle membrane permeability to glucose was calculated 4 h after one-legged knee-extensor exercise during a submaximal euglycaemic-hyperinsulinaemic clamp. It was found that during submaximal insulin stimulation, muscle membrane permeability to glucose in humans increases twice as much in previously exercised vs. rested muscle and outstrips the supply of glucose, which then becomes limiting for glucose uptake. This methodology can now be employed to determine muscle membrane permeability to glucose in people with diabetes, who have reduced insulin action, and in principle can also be used to determine membrane permeability to other substrates or metabolites. Increased insulin action is an important component of the health benefits of exercise, but the regulation of insulin action in vivo is complex and not fully elucidated. Previously determined increases in skeletal muscle insulin-stimulated GLUT4 translocation are inconsistent and mostly cannot explain the increases in insulin action in humans. Here we used leg glucose uptake (LGU) and interstitial muscle glucose concentration to calculate insulin-induced muscle membrane permeability to glucose, a variable not previously possible to quantify in humans. Muscle membrane permeability to glucose, measured 4 h after one-legged knee-extensor exercise, increased ∼17-fold during a submaximal euglycaemic-hyperinsulinaemic clamp in rested muscle (R) and ∼36-fold in exercised muscle (EX). Femoral arterial infusion of N
Substances chimiques
Insulin
0
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
303-315Informations de copyright
© 2019 The Authors. The Journal of Physiology © 2019 The Physiological Society.
Références
Andersen P, Adams RP, Sjogaard G, Thorboe A & Saltin B (1985). Dynamic knee extension as model for study of isolated exercising muscle in humans. J Appl Physiol 59, 1647-1653.
Baron AD, Tarshoby M, Hook G, Lazaridis EN, Cronin J, Johnson A & Steinberg HO (2000). Interaction between insulin sensitivity and muscle perfusion on glucose uptake in human skeletal muscle: evidence for capillary recruitment. Diabetes 49, 768-774.
Bischoff E (1863). Einige Gewichts- und Trocken-bestimmungen der Organe des menschlichen Körpers. Z Rationelle Med III 20, 75-118.
Bonadonna RC, Saccomani MP, Seely L, Zych KS, Ferrannini E, Cobelli C & DeFronzo RA (1993). Glucose transport in human skeletal muscle. The in vivo response to insulin. Diabetes 42, 191-198.
Bryant NJ, Govers R & James DE (2002). Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol 3, 267-277.
Carson BP, McCormack WG, Conway C, Cooke J, Saunders J, O'Connor WT & Jakeman PM (2015). An in vivo microdialysis characterization of the transient changes in the interstitial dialysate concentration of metabolites and cytokines in human skeletal muscle in response to insertion of a microdialysis probe. Cytokine 71, 327-333.
Cartee GD & Wojtaszewski JF (2007). Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport. Appl Physiol Nutr Metab 32, 557-566.
Castillo C, Bogardus C, Bergman R, Thuillez P & Lillioja S (1994). Interstitial insulin concentrations determine glucose uptake rates but not insulin resistance in lean and obese men. J Clin Invest 93, 10-16.
Cline GW, Petersen KF, Krssak M, Shen J, Hundal RS, Trajanoski Z, Inzucchi S, Dresner A, Rothman DL & Shulman GI (1999). Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes. N Engl J Med 341, 240-246.
Crecelius AR, Kirby BS, Richards JC, Garcia LJ, Voyles WF, Larson DG, Luckasen GJ & Dinenno FA (2011). Mechanisms of ATP-mediated vasodilation in humans: modest role for nitric oxide and vasodilating prostaglandins. Am J Physiol Heart Circ Physiol 301, H1302-H1310.
DeFronzo RA, Tobin JD & Andres R (1979). Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol 237, E214-E223.
Dela F & Stallknecht B (2010). Effect of physical training on insulin secretion and action in skeletal muscle and adipose tissue of first-degree relatives of type 2 diabetic patients. Am J Physiol Endocrinol Metab 299, E80-E91.
Devlin JT, Hirshman M, Horton ED & Horton ES (1987). Enhanced peripheral and splanchnic insulin sensitivity in NIDDM men after single bout of exercise. Diabetes 36, 434-439.
Dombrowski L, Roy D & Marette A (1998). Selective impairment in GLUT4 translocation to transverse tubules in skeletal muscle of streptozotocin-induced diabetic rats. Diabetes 47, 5-12.
Goodyear LJ, Hirshman MF, Napoli R, Calles J, Markuns JF, Ljungqvist O & Horton ES (1996). Glucose ingestion causes GLUT4 translocation in human skeletal muscle. Diabetes 45, 1051-1056.
Goodyear LJ, King PA, Hirshman MF, Thompson CM, Horton ED & Horton ES (1990). Contractile activity increases plasma membrane glucose transporters in absence of insulin. Am J Physiol 258, E667-E672.
Hansen PA, Nolte LA, Chen MM & Holloszy JO (1998). Increased GLUT-4 translocation mediates enhanced insulin sensitivity of muscle glucose transport after exercise. J Appl Physiol (1985) 85, 1218-1222.
Henriksson J (1999). Microdialysis of skeletal muscle at rest. Proc Nutr Soc 58, 919-923.
Henriksson J & Knol M (2005). A single bout of exercise is followed by a prolonged decrease in the interstitial glucose concentration in skeletal muscle. Acta Physiol Scand 185, 313-320.
Henstridge DC, Kingwell BA, Formosa MF, Drew BG, McConell GK & Duffy SJ (2005). Effects of the nitric oxide donor, sodium nitroprusside, on resting leg glucose uptake in patients with type 2 diabetes. Diabetologia 48, 2602-2608.
Hirshman MF, Goodyear LJ, Wardzala LJ, Horton ED & Horton ES (1990). Identification of an intracellular pool of glucose transporters from basal and insulin-stimulated rat skeletal muscle. J Biol Chem 265, 987-991.
Holmang A, Muller M, Andersson OK & Lonnroth P (1998). Minimal influence of blood flow on interstitial glucose and lactate-normal and insulin-resistant muscle. Am J Physiol 274, E446-E452.
Kennedy JW, Hirshman MF, Gervino EV, Ocel JV, Forse RA, Hoenig SJ, Aronson D, Goodyear LJ & Horton ES (1999). Acute exercise induces GLUT4 translocation in skeletal muscle of normal human subjects and subjects with type 2 diabetes. Diabetes 48, 1192-1197.
Kho CM, Enche Ab Rahim SK, Ahmad ZA & Abdullah NS (2017). A review on microdialysis calibration methods: the theory and current related efforts. Mol Neurobiol 54, 3506-3527.
Kingwell B, Formosa M, Muhlmann M, Bradley S & McConell G (2002). Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects. Diabetes 51, 2572-2580.
Kjobsted R, Munk-Hansen N, Birk JB, Foretz M, Viollet B, Bjornholm M, Zierath JR, Treebak JT & Wojtaszewski JF (2017). Enhanced muscle insulin sensitivity after contraction/exercise is mediated by AMPK. Diabetes 66, 598-612.
Klip A & Paquet MR (1990). Glucose transport and glucose transporters in muscle and their metabolic regulation. Diabetes Care 13, 228-243.
Koistinen HA, Galuska D, Chibalin AV, Yang J, Zierath JR, Holman GD & Wallberg-Henriksson H (2003). 5-Amino-imidazole carboxamide riboside increases glucose transport and cell-surface GLUT4 content in skeletal muscle from subjects with type 2 diabetes. Diabetes 52, 1066-1072.
Laakso M, Edelman SV, Brechtel G & Baron AD (1992). Impaired insulin-mediated skeletal muscle blood flow in patients with NIDDM. Diabetes 41, 1076-1083.
Lauritzen HP, Reynet C, Schjerling P, Ralston E, Thomas S, Galbo H & Ploug T (2002). Gene gun bombardment-mediated expression and translocation of EGFP-tagged GLUT4 in skeletal muscle fibres in vivo. Pflugers Arch 444, 710-721.
Lonnroth P, Jansson PA & Smith U (1987). A microdialysis method allowing characterization of intercellular water space in humans. Am J Physiol 253, E228-E231.
Lund S, Holman GD, Schmitz O & Pedersen O (1995). Contraction stimulates translocation of glucose transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin. Proc Natl Acad Sci U S A 92, 5817-5821.
Lund S, Vestergaard H, Andersen PH, Schmitz O, Gotzsche LB & Pedersen O (1993). GLUT-4 content in plasma membrane of muscle from patients with non-insulin-dependent diabetes mellitus. Am J Physiol 265, E889-E897.
MacLean DA, Bangsbo J & Saltin B (1999). Muscle interstitial glucose and lactate levels during dynamic exercise in humans determined by microdialysis. J Appl Physiol (1985) 87, 1483-1490.
Marette A, Burdett E, Douen A, Vranic M & Klip A (1992). Insulin induces the translocation of GLUT4 from a unique intracellular organelle to transverse tubules in rat skeletal muscle. Diabetes 41, 1562-1569.
Mortensen SP, Gonzalez-Alonso J, Nielsen JJ, Saltin B & Hellsten Y (2009). Muscle interstitial ATP and norepinephrine concentrations in the human leg during exercise and ATP infusion. J Appl Physiol (1985) 107, 1757-1762.
Nyberg M, Al-Khazraji BK, Mortensen SP, Jackson DN, Ellis CG & Hellsten Y (2013). Effect of extraluminal ATP application on vascular tone and blood flow in skeletal muscle: implications for exercise hyperemia. Am J Physiol Regul Integr Comp Physiol 305, R281-R290.
Osorio-Fuentealba C, Contreras-Ferrat AE, Altamirano F, Espinosa A, Li Q, Niu W, Lavandero S, Klip A & Jaimovich E (2013). Electrical stimuli release ATP to increase GLUT4 translocation and glucose uptake via PI3Kγ-Akt-AS160 in skeletal muscle cells. Diabetes 62, 1519-1526.
Pappenheimer JR, Renkin EM & Borrero LM (1951). Filtration, diffusion and molecular sieving through peripheral capillary membranes: a contribution to the pore theory of capillary permeability. Am J Physiol 167, 13-46.
Pehmoller C, Brandt N, Birk JB, Hoeg LD, Sjoberg KA, Goodyear LJ, Kiens B, Richter EA & Wojtaszewski JF (2012). Exercise alleviates lipid-induced insulin resistance in human skeletal muscle-signaling interaction at the level of TBC1 domain family member 4. Diabetes 61, 2743-2752.
Pellinger TK, Simmons GH, Maclean DA & Halliwill JR (2010). Local histamine H1- and H2-receptor blockade reduces postexercise skeletal muscle interstitial glucose concentrations in humans. Appl Physiol Nutr Metab 35, 617-626.
Perseghin G, Price TB, Petersen KF, Roden M, Cline GW, Gerow K, Rothman DL & Shulman GI (1996). Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects. N Engl J Med 335, 1357-1362.
Rodnick KJ, Slot JW, Studelska DR, Hanpeter DE, Robinson LJ, Geuze HJ & James DE (1992). Immunocytochemical and biochemical studies of GLUT4 in rat skeletal muscle. J Biol Chem 267, 6278-6285.
Rosdahl H, Hamrin K, Ungerstedt U & Henriksson J (2000). A microdialysis method for the in situ investigation of the action of large peptide molecules in human skeletal muscle: detection of local metabolic effects of insulin. Int J Biol Macromol 28, 69-73.
Rosdahl H, Lind L, Millgard J, Lithell H, Ungerstedt U & Henriksson J (1998). Effect of physiological hyperinsulinemia on blood flow and interstitial glucose concentration in human skeletal muscle and adipose tissue studied by microdialysis. Diabetes 47, 1296-1301.
Ryder JW, Yang J, Galuska D, Rincon J, Bjornholm M, Krook A, Lund S, Pedersen O, Wallberg-Henriksson H, Zierath JR & Holman GD (2000). 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 49, 647-654.
Sahlin K, Broberg S & Katz A (1989). Glucose formation in human skeletal muscle. Influence of glycogen content. Biochem J 258, 911-913.
Scheller D & Kolb J (1991). The internal reference technique in microdialysis: a practical approach to monitoring dialysis efficiency and to calculating tissue concentration from dialysate samples. J Neurosci Methods 40, 31-38.
Shamni O, Cohen G, Gruzman A, Zaid H, Klip A, Cerasi E & Sasson S (2017). Regulation of GLUT4 activity in myotubes by 3-O-methyl-d-glucose. Biochim Biophys Acta Biomembr 1859, 1900-1910.
Sjoberg KA, Frosig C, Kjobsted R, Sylow L, Kleinert M, Betik AC, Shaw CS, Kiens B, Wojtaszewski JFP, Rattigan S, Richter EA & McConell GK (2017). Exercise increases human skeletal muscle insulin sensitivity via coordinated increases in microvascular perfusion and molecular signaling. Diabetes 66, 1501-1510.
Sjoberg KA, Holst JJ, Rattigan S, Richter EA & Kiens B (2014). GLP-1 increases microvascular recruitment but not glucose uptake in human and rat skeletal muscle. Am J Physiol Endocrinol Metab 306, E355-E362.
Sjoberg KA, Rattigan S, Hiscock N, Richter EA & Kiens B (2011). A new method to study changes in microvascular blood volume in muscle and adipose tissue: real-time imaging in humans and rat. Am J Physiol Heart Circ Physiol 301, H450-H458.
Slot JW, Geuze HJ, Gigengack S, Lienhard GE & James DE (1991). Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol 113, 123-135.
Stallknecht B, Larsen JJ, Mikines KJ, Simonsen L, Bulow J & Galbo H (2000). Effect of training on insulin sensitivity of glucose uptake and lipolysis in human adipose tissue. Am J Physiol Endocrinol Metab 279, E376-E385.
Stallknecht B, Simonsen L, Bulow J, Vinten J & Galbo H (1995). Effect of training on epinephrine-stimulated lipolysis determined by microdialysis in human adipose tissue. Am J Physiol 269, E1059-E1066.
Sternlicht E, Barnard RJ & Grimditch GK (1988). Mechanism of insulin action on glucose transport in rat skeletal muscle. Am J Physiol 254, E633-E638.
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.
Treebak JT, Frosig C, Pehmoller C, Chen S, Maarbjerg SJ, Brandt N, MacKintosh C, Zierath JR, Hardie DG, Kiens B, Richter EA, Pilegaard H & Wojtaszewski JF (2009). Potential role of TBC1D4 in enhanced post-exercise insulin action in human skeletal muscle. Diabetologia 52, 891-900.
Vincent MA, Barrett EJ, Lindner JR, Clark MG & Rattigan S (2003). Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. Am J Physiol Endocrinol Metab 285, E123-E129.
Vincent MA, Clerk LH, Lindner JR, Klibanov AL, Clark MG, Rattigan S & Barrett EJ (2004). Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 53, 1418-1423.
Wang H, Arias EB, Pataky MW, Goodyear LJ & Cartee GD (2018). Postexercise improvement in glucose uptake occurs concomitant with greater γ3-AMPK activation and AS160 phosphorylation in rat skeletal muscle. Am J Physiol Endocrinol Metab 315, E859-E871.
Wilson CM & Cushman SW (1994). Insulin stimulation of glucose transport activity in rat skeletal muscle: increase in cell surface GLUT4 as assessed by photolabelling. Biochem J 299, 755-759.
Wojtaszewski JF & Richter EA (2006). Effects of acute exercise and training on insulin action and sensitivity: focus on molecular mechanisms in muscle. Essays Biochem 42, 31-46.
Yazdani S, Jaldin-Fincati JR, Pereira RVS & Klip A (2019). Endothelial cell barriers: Transport of molecules between blood and tissues. Traffic 20, 390-403.