Heterogeneity in insulin-stimulated glucose uptake among different muscle groups in healthy lean people and people with obesity.
Adult
Biological Transport
/ drug effects
Biopsy
Female
Fluorodeoxyglucose F18
Glucose
/ metabolism
Glucose Clamp Technique
Humans
Insulin
/ metabolism
Insulin Resistance
/ physiology
Male
Middle Aged
Muscle, Skeletal
/ diagnostic imaging
Obesity
/ diagnostic imaging
Positron-Emission Tomography
Quadriceps Muscle
/ diagnostic imaging
Thinness
/ diagnostic imaging
Glucose disposal
Glucose uptake
Insulin resistance
Perfusion
Journal
Diabetologia
ISSN: 1432-0428
Titre abrégé: Diabetologia
Pays: Germany
ID NLM: 0006777
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
received:
19
08
2020
accepted:
27
11
2020
pubmed:
30
1
2021
medline:
23
2
2022
entrez:
29
1
2021
Statut:
ppublish
Résumé
It has been proposed that muscle fibre type composition and perfusion are key determinants of insulin-stimulated muscle glucose uptake, and alterations in muscle fibre type composition and perfusion contribute to muscle, and consequently whole-body, insulin resistance in people with obesity. The goal of the study was to evaluate the relationships among muscle fibre type composition, perfusion and insulin-stimulated glucose uptake rates in healthy, lean people and people with obesity. We measured insulin-stimulated whole-body glucose disposal and glucose uptake and perfusion rates in five major muscle groups (erector spinae, obliques, rectus abdominis, hamstrings, quadriceps) in 15 healthy lean people and 37 people with obesity by using the hyperinsulinaemic-euglycaemic clamp procedure in conjunction with [ We found: (1) a twofold difference in glucose uptake rates among muscles in both the lean and obese groups (rectus abdominis: 67 [51, 78] and 32 [21, 55] μmol kg Obesity-associated insulin resistance is generalised across all major muscles, and is not caused by alterations in muscle fibre type composition or perfusion. In addition, insulin-stimulated whole-body glucose disposal relative to fat-free mass provides a reliable index of muscle glucose uptake rate.
Identifiants
pubmed: 33511440
doi: 10.1007/s00125-021-05383-w
pii: 10.1007/s00125-021-05383-w
pmc: PMC8336476
mid: NIHMS1723651
doi:
Substances chimiques
Insulin
0
Fluorodeoxyglucose F18
0Z5B2CJX4D
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1158-1168Subventions
Organisme : NIDDK NIH HHS
ID : R01 DK115400
Pays : United States
Organisme : NIAMS NIH HHS
ID : P30 AR074992
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK056341
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK020579
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR002345
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR000448
Pays : United States
Références
Roden M, Shulman GI (2019) The integrative biology of type 2 diabetes. Nature 576(7785):51–60. https://doi.org/10.1038/s41586-019-1797-8
doi: 10.1038/s41586-019-1797-8
pubmed: 31802013
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
Wasserman DH, Ayala JE (2005) Interaction of physiological mechanisms in control of muscle glucose uptake. Clin Exp Pharmacol Physiol 32(4):319–323. https://doi.org/10.1111/j.1440-1681.2005.04191.x
doi: 10.1111/j.1440-1681.2005.04191.x
pubmed: 15810999
James DE, Jenkins AB, Kraegen EW (1985) Heterogeneity of insulin action in individual muscles in vivo: euglycemic clamp studies in rats. Am J Phys 248(5 Pt 1):E567–E574. https://doi.org/10.1152/ajpendo.1985.248.5.E567
doi: 10.1152/ajpendo.1985.248.5.E567
Henriksen EJ, Bourey RE, Rodnick KJ, Koranyi L, Permutt MA, Holloszy JO (1990) Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. Am J Phys 259(4 Pt 1):E593–E598
Megeney LA, Neufer PD, Dohm GL et al (1993) Effects of muscle activity and fiber composition on glucose transport and GLUT-4. Am J Phys 264(4 Pt 1):E583–E593. https://doi.org/10.1152/ajpendo.1993.264.4.E583
doi: 10.1152/ajpendo.1993.264.4.E583
Pataky MW, Wang H, Yu CS et al (2017) High-fat diet-induced insulin resistance in single skeletal muscle fibers is fiber type selective. Sci Rep 7(1):13642. https://doi.org/10.1038/s41598-017-12682-z
doi: 10.1038/s41598-017-12682-z
pubmed: 29057943
pmcid: 5651812
Clerk LH, Rattigan S, Clark MG (2002) Lipid infusion impairs physiologic insulin-mediated capillary recruitment and muscle glucose uptake in vivo. Diabetes 51(4):1138–1145. https://doi.org/10.2337/diabetes.51.4.1138
doi: 10.2337/diabetes.51.4.1138
pubmed: 11916937
Kraegen EW, James DE, Storlien LH, Burleigh KM, Chisholm DJ (1986) In vivo insulin resistance in individual peripheral tissues of the high fat fed rat: assessment by euglycaemic clamp plus deoxyglucose administration. Diabetologia 29(3):192–198. https://doi.org/10.1007/bf02427092
doi: 10.1007/bf02427092
pubmed: 3516775
Conte C, Fabbrini E, Kars M, Mittendorfer B, Patterson BW, Klein S (2012) Multiorgan insulin sensitivity in lean and obese subjects. Diabetes Care 35(6):1316–1321. https://doi.org/10.2337/dc11-1951
doi: 10.2337/dc11-1951
pubmed: 22474039
pmcid: 3357234
Ter Horst KW, Serlie MJ (2020) Normalization of metabolic flux data during clamp studies in humans. Metabolism 104:154168. https://doi.org/10.1016/j.metabol.2020.154168
doi: 10.1016/j.metabol.2020.154168
pubmed: 31982479
Phielix E, Begovatz P, Gancheva S et al (2019) Athletes feature greater rates of muscle glucose transport and glycogen synthesis during lipid infusion. JCI Insight 4(21):e127928. https://doi.org/10.1172/jci.insight.127928
doi: 10.1172/jci.insight.127928
pmcid: 6948766
Camastra S, Gastaldelli A, Mari A et al (2011) Early and longer term effects of gastric bypass surgery on tissue-specific insulin sensitivity and beta cell function in morbidly obese patients with and without type 2 diabetes. Diabetologia 54(8):2093–2102. https://doi.org/10.1007/s00125-011-2193-6
doi: 10.1007/s00125-011-2193-6
pubmed: 21614570
Tirrell TF, Cook MS, Carr JA, Lin E, Ward SR, Lieber RL (2012) Human skeletal muscle biochemical diversity. J Exp Biol 215(Pt 15):2551–2559. https://doi.org/10.1242/jeb.069385
doi: 10.1242/jeb.069385
pubmed: 22786631
pmcid: 3394665
Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 18:111–129
doi: 10.1016/0022-510X(73)90023-3
Smith GI, Yoshino J, Kelly SC et al (2016) High protein intake during weight loss therapy eliminates the weight loss-induced improvement in insulin action in postmenopausal women. Cell Rep 17(3):849–861. https://doi.org/10.1016/j.celrep.2016.09.047
doi: 10.1016/j.celrep.2016.09.047
pubmed: 27732859
pmcid: 5113728
Bryniarski AR, Meyer GA (2019) Brown Fat Promotes Muscle Growth During Regeneration. J Orthop Res 37(8):1817–1826. https://doi.org/10.1002/jor.24324
doi: 10.1002/jor.24324
pubmed: 31042310
pmcid: 6824921
Muzik O, Mangner TJ, Leonard WR, Kumar A, Janisse J, Granneman JG (2013) 15O PET measurement of blood flow and oxygen consumption in cold-activated human brown fat. J Nucl Med 54(4):523–531. https://doi.org/10.2967/jnumed.112.111336
doi: 10.2967/jnumed.112.111336
pubmed: 23362317
Kelley DE, Williams KV, Price JC, Goodpaster B (1999) Determination of the lumped constant for [18F] fluorodeoxyglucose in human skeletal muscle. J Nucl Med 40(11):1798–1804
pubmed: 10565773
Patlak CS, Blasberg RG (1985) Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J Cereb Blood Flow Metab 5(4):584–590. https://doi.org/10.1038/jcbfm.1985.87
doi: 10.1038/jcbfm.1985.87
pubmed: 4055928
Buckinx F, Landi F, Cesari M et al (2018) Pitfalls in the measurement of muscle mass: a need for a reference standard. J Cachexia Sarcopenia Muscle 9(2):269–278. https://doi.org/10.1002/jcsm.12268
doi: 10.1002/jcsm.12268
pubmed: 29349935
pmcid: 5879987
Tanner CJ, Barakat HA, Dohm GL et al (2002) Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 282(6):E1191–E1196. https://doi.org/10.1152/ajpendo.00416.2001
doi: 10.1152/ajpendo.00416.2001
pubmed: 12006347
Lillioja S, Young AA, Culter CL et al (1987) Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 80(2):415–424. https://doi.org/10.1172/JCI113088
doi: 10.1172/JCI113088
pubmed: 3301899
pmcid: 442253
Nyholm B, Qu Z, Kaal A et al (1997) Evidence of an increased number of type IIb muscle fibers in insulin-resistant first-degree relatives of patients with NIDDM. Diabetes 46(11):1822–1828. https://doi.org/10.2337/diab.46.11.1822
doi: 10.2337/diab.46.11.1822
pubmed: 9356032
Holmang A, Brzezinska Z, Bjorntorp P (1993) Effects of hyperinsulinemia on muscle fiber composition and capitalization in rats. Diabetes 42(7):1073–1081. https://doi.org/10.2337/diab.42.7.1073
doi: 10.2337/diab.42.7.1073
pubmed: 8513974
Houmard JA, O’Neill DS, Zheng D, Hickey MS, Dohm GL (1999) Impact of hyperinsulinemia on myosin heavy chain gene regulation. J Appl Physiol (1985) 86(6):1828–1832. https://doi.org/10.1152/jappl.1999.86.6.1828
doi: 10.1152/jappl.1999.86.6.1828
Sylow L, Kleinert M, Richter EA, Jensen TE (2017) Exercise-stimulated glucose uptake—regulation and implications for glycaemic control. Nat Rev Endocrinol 13(3):133–148. https://doi.org/10.1038/nrendo.2016.162
doi: 10.1038/nrendo.2016.162
pubmed: 27739515
Krogh-Madsen R, Thyfault JP, Broholm C et al (2010) A 2-wk reduction of ambulatory activity attenuates peripheral insulin sensitivity. J Appl Physiol (1985) 108(5):1034–1040. https://doi.org/10.1152/japplphysiol.00977.2009
doi: 10.1152/japplphysiol.00977.2009
Albers PH, Pedersen AJ, Birk JB et al (2015) Human muscle fiber type-specific insulin signaling: impact of obesity and type 2 diabetes. Diabetes 64(2):485–497. https://doi.org/10.2337/db14-0590
doi: 10.2337/db14-0590
pubmed: 25187364
Wasserman DH, Wang TJ, Brown NJ (2018) The vasculature in prediabetes. Circ Res 122(8):1135–1150. https://doi.org/10.1161/CIRCRESAHA.118.311912
doi: 10.1161/CIRCRESAHA.118.311912
pubmed: 29650631
pmcid: 5901903
Barrett EJ, Rattigan S (2012) Muscle perfusion: its measurement and role in metabolic regulation. Diabetes 61(11):2661–2668. https://doi.org/10.2337/db12-0271
doi: 10.2337/db12-0271
pubmed: 23093655
pmcid: 3478558
Ferrannini E, Iozzo P, Virtanen KA, Honka MJ, Bucci M, Nuutila P (2018) Adipose tissue and skeletal muscle insulin-mediated glucose uptake in insulin resistance: role of blood flow and diabetes. Am J Clin Nutr 108(4):749–758. https://doi.org/10.1093/ajcn/nqy162
doi: 10.1093/ajcn/nqy162
pubmed: 30239554
Utriainen T, Nuutila P, Takala T et al (1997) Intact insulin stimulation of skeletal muscle blood flow, its heterogeneity and redistribution, but not of glucose uptake in non-insulin-dependent diabetes mellitus. J Clin Invest 100(4):777–785. https://doi.org/10.1172/JCI119591
doi: 10.1172/JCI119591
pubmed: 9259575
pmcid: 508248
Raitakari M, Nuutila P, Ruotsalainen U et al (1996) Evidence for dissociation of insulin stimulation of blood flow and glucose uptake in human skeletal muscle: studies using [15O]H2O, [18F]fluoro-2-deoxy-D-glucose, and positron emission tomography. Diabetes 45(11):1471–1477. https://doi.org/10.2337/diab.45.11.1471
doi: 10.2337/diab.45.11.1471
pubmed: 8866549
Williams KV, Price JC, Kelley DE (2001) Interactions of impaired glucose transport and phosphorylation in skeletal muscle insulin resistance: a dose-response assessment using positron emission tomography. Diabetes 50(9):2069–2079. https://doi.org/10.2337/diabetes.50.9.2069
doi: 10.2337/diabetes.50.9.2069
pubmed: 11522673
Eggleston EM, Jahn LA, Barrett EJ (2007) Hyperinsulinemia rapidly increases human muscle microvascular perfusion but fails to increase muscle insulin clearance: evidence that a saturable process mediates muscle insulin uptake. Diabetes 56(12):2958–2963. https://doi.org/10.2337/db07-0670
doi: 10.2337/db07-0670
pubmed: 17720897
van Raalte DH, van der Palen E, Idema P et al (2020) Peripheral Insulin Extraction in Non-Diabetic Subjects and Type 2 Diabetes Mellitus Patients. Exp Clin Endocrinol Diabetes 128(8):520–527. https://doi.org/10.1055/a-0808-4029
doi: 10.1055/a-0808-4029
pubmed: 30557891
Bertoldo A, Pencek RR, Azuma K et al (2006) Interactions between delivery, transport, and phosphorylation of glucose in governing uptake into human skeletal muscle. Diabetes 55(11):3028–3037. https://doi.org/10.2337/db06-0762
doi: 10.2337/db06-0762
pubmed: 17065339
Goodpaster BH, Bertoldo A, Ng JM et al (2014) Interactions among glucose delivery, transport, and phosphorylation that underlie skeletal muscle insulin resistance in obesity and type 2 Diabetes: studies with dynamic PET imaging. Diabetes 63(3):1058–1068. https://doi.org/10.2337/db13-1249
doi: 10.2337/db13-1249
pubmed: 24222345
pmcid: 3931396
Williams IM, McClatchey PM, Bracy DP, Bonner JS, Valenzuela FA, Wasserman DH (2020) Transendothelial Insulin Transport is Impaired in Skeletal Muscle Capillaries of Obese Male Mice. Obesity (Silver Spring) 28(2):303–314. https://doi.org/10.1002/oby.22683
doi: 10.1002/oby.22683
Sjostrand M, Gudbjornsdottir S, Holmang A, Lonn L, Strindberg L, Lonnroth P (2002) Delayed transcapillary transport of insulin to muscle interstitial fluid in obese subjects. Diabetes 51(9):2742–2748. https://doi.org/10.2337/diabetes.51.9.2742
doi: 10.2337/diabetes.51.9.2742
pubmed: 12196467
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(1):10–16. https://doi.org/10.1172/JCI116932
doi: 10.1172/JCI116932
pubmed: 8282776
pmcid: 293712
Chiu JD, Richey JM, Harrison LN et al (2008) Direct administration of insulin into skeletal muscle reveals that the transport of insulin across the capillary endothelium limits the time course of insulin to activate glucose disposal. Diabetes 57(4):828–835. https://doi.org/10.2337/db07-1444
doi: 10.2337/db07-1444
pubmed: 18223011
Kolterman OG, Insel J, Saekow M, Olefsky JM (1980) Mechanisms of insulin resistance in human obesity: evidence for receptor and postreceptor defects. J Clin Invest 65(6):1272–1284. https://doi.org/10.1172/JCI109790
doi: 10.1172/JCI109790
pubmed: 6997333
pmcid: 371464
Virtanen KA, Iozzo P, Hallsten K et al (2005) Increased fat mass compensates for insulin resistance in abdominal obesity and type 2 diabetes: a positron-emitting tomography study. Diabetes 54(9):2720–2726. https://doi.org/10.2337/diabetes.54.9.2720
doi: 10.2337/diabetes.54.9.2720
pubmed: 16123362
Baron AD, Brechtel G, Wallace P, Edelman SV (1988) Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. Am J Physiol 255(6 Pt 1):E769–E774
pubmed: 3059816
Boersma GJ, Johansson E, Pereira MJ et al (2018) Altered Glucose Uptake in Muscle, Visceral Adipose Tissue, and Brain Predict Whole-Body Insulin Resistance and may Contribute to the Development of Type 2 Diabetes: A Combined PET/MR Study. Horm Metab Res 50(8):627–639. https://doi.org/10.1055/a-0643-4739
doi: 10.1055/a-0643-4739
pubmed: 30001566
Koffert JP, Mikkola K, Virtanen KA et al (2017) Metformin treatment significantly enhances intestinal glucose uptake in patients with type 2 diabetes: Results from a randomized clinical trial. Diabetes Res Clin Pract 131:208–216. https://doi.org/10.1016/j.diabres.2017.07.015
doi: 10.1016/j.diabres.2017.07.015
pubmed: 28778047
Honka H, Makinen J, Hannukainen JC et al (2013) Validation of [18F]fluorodeoxyglucose and positron emission tomography (PET) for the measurement of intestinal metabolism in pigs, and evidence of intestinal insulin resistance in patients with morbid obesity. Diabetologia 56(4):893–900. https://doi.org/10.1007/s00125-012-2825-5
doi: 10.1007/s00125-012-2825-5
pubmed: 23334481
Honka MJ, Latva-Rasku A, Bucci M et al (2018) Insulin-stimulated glucose uptake in skeletal muscle, adipose tissue and liver: a positron emission tomography study. Eur J Endocrinol 178(5):523–531. https://doi.org/10.1530/EJE-17-0882
doi: 10.1530/EJE-17-0882
pubmed: 29535167
pmcid: 5920018