Modulation of muscle insulin resistance by selective inhibition of GSK-3 in Zucker diabetic fatty rats

Henriksen, Erik J.; Kinnick, Tyson R.; Teachey, Mary K.; O'Keefe, Matthew P.; Ring, David; Johnson, Kirk W.; Harrison, Stephen D.

doi:10.1152/ajpendo.00346.2002

Cited by 108Metabolism, Diabetes, and CancerDiabetes, Cardiovascular Risks, and LipoproteinsNatural Antidiabetic Agents Studies

Modulation of muscle insulin resistance by selective inhibition of GSK-3 in Zucker diabetic fatty rats

Henriksen, Erik J., Kinnick, Tyson R., Teachey, Mary K., O'Keefe, Matthew P., Ring, David, Johnson, Kirk W., Harrison, Stephen D.·2003·American Journal of Physiology-Endocrinology and Metabolism

DOI 10.1152/ajpendo.00346.2002

Open this paper in CoChat — free account

Abstract

A role for elevated glycogen synthase kinase-3 (GSK-3) activity in the multifactorial etiology of insulin resistance is now emerging. However, the utility of specific GSK-3 inhibition in modulating insulin resistance of skeletal muscle glucose transport is not yet fully understood. Therefore, we assessed the effects of novel, selective organic inhibitors of GSK-3 (CT-98014 and CT-98023) on glucose transport in insulin-resistant muscles of Zucker diabetic fatty (ZDF) rats. Incubation of type IIb epitrochlearis and type I soleus muscles from ZDF rats with CT-98014 increased glycogen synthase activity (49 and 50%, respectively, P < 0.05) but did not alter basal glucose transport (2-deoxyglucose uptake). In contrast, CT-98014 significantly increased the stimulatory effects of both submaximal and maximal insulin concentrations in epitrochlearis (37 and 24%) and soleus (43 and 26%), and these effects were associated with increased cell-surface GLUT4 protein. Lithium enhanced glycogen synthase activity and both basal and insulin-stimulated glucose transport in muscles from ZDF rats. Acute oral administration (2 × 30 mg/kg) of CT-98023 to ZDF rats caused elevations in GSK-3 inhibitor concentrations in plasma and muscle. The glucose and insulin responses during a subsequent oral glucose tolerance test were reduced by 26 and 34%, respectively, in the GSK-3 inhibitor-treated animals. Thirty minutes after the final GSK-3 inhibitor treatment, insulin-stimulated glucose transport was significantly enhanced in epitrochlearis (57%) and soleus (43%). Two hours after the final treatment, insulin-mediated glucose transport was still significantly elevated (26%) only in the soleus. These results indicate that specific inhibition of GSK-3 enhances insulin action on glucose transport in skeletal muscle of the insulin-resistant ZDF rat. This unique approach may hold promise as a pharmacological treatment against insulin resistance of skeletal muscle glucose disposal.

Integrity signals

Registry

Crossref · 10.1152/ajpendo.00346.2002

Cites

37 of 37 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

GSK-3 inhibitors increase insulin-stimulated glucose transport in epitrochlearis and soleus muscles from insulin-resistant ZDF rats, but not from insulin-sensitive lean Zucker rats.
“GSK-3 inhibitors increased insulin-stimulated glucose transport in epitrochlearis and soleus muscles from insulin-resistant ZDF rats, but not from insulin-sensitive lean Zucker rats [27,28].”
From Glucocorticoid-induced insulin resistance in skeletal muscles: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor (2005) · cites this paper as [27]
Pharmacological inhibition of GSK-3 with selective inhibitors can improve insulin sensitivity in insulin-resistant muscles from ZDF rats.
“Pharmacological inhibition of GSK-3 with highly selective, reversible, cell-permeable small molecules can improve insulin sensitivity in insulin-resistant muscles from Zucker diabetic fatty (ZDF) rats [27][28][29].”
From Glucocorticoid-induced insulin resistance in skeletal muscles: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor (2005) · cites this paper as [27]
Pharmacological inhibition of GSK-3 increases insulin-stimulated glucose uptake in insulin-resistant skeletal muscles from obese ZDF rats but not in muscle from insulin-sensitive lean ZDF rats.
“Pharmacological inhibition of GSK-3 increases insulin-stimulated glucose uptake in insulin-resistant skeletal muscles from obese ZDF rats but not in muscle from insulin-sensitive lean ZDF rats [27,28].”
From Glucocorticoid-induced insulin resistance in skeletal muscles: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor (2005) · cites this paper as [27]
GSK-3 inhibitors activate glycogen synthase in lean and ZDF rats.
“GSK-3 inhibitors activate glycogen synthase in lean and ZDF rats [27]”
From Glucocorticoid-induced insulin resistance in skeletal muscles: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor (2005) · cites this paper as [27]

Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B
Cross, D. A. E., Alessi, D. R., Cohen, P., Andjelkovich, M., & Hemmings, B. A. (1995) · Nature · doi:10.1038/378785a0 · Cited by 5,244 · see citing works
Insulin Resistance: A Multifaceted Syndrome Responsible for NIDDM, Obesity, Hypertension, Dyslipidemia, and Atherosclerotic Cardiovascular Disease
DeFronzo, R. A., & Ferrannini, E. (1991) · Diabetes Care · doi:10.2337/diacare.14.3.173 · Cited by 4,555 · see citing works
Specificity and mechanism of action of some commonly used protein kinase inhibitors.
Davies, S., Reddy, H., Caivano, M., & Cohen, P. (2000) · Biochemical Journal · doi:10.1042/bj3510095 · Cited by 3,164 · see citing works
A molecular mechanism for the effect of lithium on development.
Klein, P. S., & Melton, D. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8455 · Cited by 2,305 · see citing works
Specificity and mechanism of action of some commonly used protein kinase inhibitors
Davies, S., Reddy, H., Caivano, M., & Cohen, P. (2000) · Biochemical Journal · doi:10.1042/0264-6021:3510095 · Cited by 1,618 · see citing works
Molecular cloning and expression of glycogen synthase kinase‐3/factor A.
Woodgett, J. R. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07419.x · Cited by 1,362 · see citing works
Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells
Stambolic, V., Ruel, L., & Woodgett, J. R. (1996) · Current Biology · doi:10.1016/s0960-9822(02)70790-2 · Cited by 1,321 · see citing works
A rapid filter paper assay for UDPglucose-glycogen glucosyltransferase, including an improved biosynthesis of UDP-14C-glucose
Thomas, J. A., Schlender, K. K., & Larner, J. (1968) · Analytical Biochemistry · doi:10.1016/0003-2697(68)90127-9 · Cited by 1,198 · see citing works
HINDLIMB MUSCLE FIBER POPULATIONS OF FIVE MAMMALS
Ariano, M. A., Edgerton, V. R., & Armstrong, R. B. (1973) · Journal of Histochemistry & Cytochemistry · doi:10.1177/21.1.51 · Cited by 1,118 · see citing works
Role of Insulin Resistance in Human Disease (Syndrome X): An Expanded Definition
Reaven, G. M. (1993) · Annual Review of Medicine · doi:10.1146/annurev.me.44.020193.001005 · Cited by 911 · see citing works
Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription
Coghlan, M. P., Culbert, A. A., Cross, D. A. E., Corcoran, S. L., Yates, J. W., Pearce, N. J., Rausch, O., Murphy, G. J., Carter, P. S., Cox, L. R., et al. (2000) · Chemistry & Biology · doi:10.1016/s1074-5521(00)00025-9 · Cited by 901 · see citing works
Lithium Reduces Tau Phosphorylation by Inhibition of Glycogen Synthase Kinase-3
Hong, M., Chen, D. C. R., Klein, P. S., & Lee, V. M. ‐. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.40.25326 · Cited by 470 · see citing works
Glucose transporter protein content and glucose transport capacity in rat skeletal muscles
Henriksen, E. J., Bourey, R. E., Rodnick, K. J., Koranyi, L. I., Permutt, M. A., & Holloszy, J. O. (1990) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1990.259.4.e593 · Cited by 435 · see citing works
Self-citation
Insulin action and insulin resistance in human skeletal muscle
Zierath, J. R., Krook, A., & Wallberg-Henriksson, H. (2000) · Diabetologia · doi:10.1007/s001250051457 · Cited by 367 · see citing works
Potential role of glycogen synthase kinase-3 in skeletal muscle insulin resistance of type 2 diabetes.
Nikoulina, S. E., Ciaraldi, T. P., Mudaliar, S., Mohideen, P., Carter, L., & Henry, R. R. (2000) · Diabetes · doi:10.2337/diabetes.49.2.263 · Cited by 357 · see citing works
Phosphorylation of insulin receptor substrate 1 by glycogen synthase kinase 3 impairs insulin action
Eldar-Finkelman, H., & Krebs, E. G. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.18.9660 · Cited by 319 · see citing works
Glycogen Synthase from Rabbit Skeletal Muscle; Effect of Insulin on the State of phosphorylation of the Seven Phosphoserine Residues in vivo
Parker, P. J., Caudwell, F. B., & Cohen, P. (1983) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1983.tb07140.x · Cited by 298 · see citing works
Glycogen synthase from rabbit skeletal muscle. Amino acid sequence at the sites phosphorylated by glycogen synthase kinase-3, and extension of the N-terminal sequence containing the site phosphorylated by phosphorylase kinase.
Rylatt, D. B., Aitken, A., Bilham, T., Condon, G. D., Embi, N., & Cohen, P. (1980) · PubMed · Cited by 285 · see citing works
Control of glycogen synthase by hierarchal protein phosphorylation
Roach, P. J. (1990) · The FASEB Journal · doi:10.1096/fasebj.4.12.2168324 · Cited by 270 · see citing works
Insulin responsiveness in skeletal muscle is determined by glucose transporter (Glut4) protein level
Kern, M., Wells, J. A., Stephens, J. M., Elton, C. W., Friedman, J. E., Tapscott, E. B., Pekala, P. H., & Dohm, G. L. (1990) · Biochemical Journal · doi:10.1042/bj2700397 · Cited by 268 · see citing works
Increased glycogen synthase kinase-3 activity in diabetes- and obesity-prone C57BL/6J mice.
Eldar-Finkelman, H., Schreyer, S. A., Shinohara, M. M., LeBoeuf, R. C., & Krebs, E. G. (1999) · Diabetes · doi:10.2337/diabetes.48.8.1662 · Cited by 253 · see citing works
Suitability of 2-deoxyglucose for in vitro measurement of glucose transport activity in skeletal muscle
Hansen, P. A., Gulve, E. A., & Holloszy, J. O. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.76.2.979 · Cited by 234 · see citing works
Effects of a Novel Glycogen Synthase Kinase-3 Inhibitor on Insulin-Stimulated Glucose Metabolism in Zucker Diabetic Fatty (<i>fa</i>/<i>fa</i>) Rats
Cline, G. W., Johnson, K., Regittnig, W., Perret, P., Tozzo, E., Xiao, L., Damico, C., & Shulman, G. I. (2002) · Diabetes · doi:10.2337/diabetes.51.10.2903 · Cited by 228 · see citing works
Self-citation
Inhibition of GSK-3 Selectively Reduces Glucose-6-Phosphatase and Phosphoenolpyruvate Carboxykinase Gene Expression
Lochhead, P. A., Coghlan, M., Rice, S. Q. J., & Sutherland, C. (2001) · Diabetes · doi:10.2337/diabetes.50.5.937 · Cited by 219 · see citing works
The Role of Glycogen Synthase Kinase 3β in Insulin-stimulated Glucose Metabolism
Summers, S. A., Kao, A. W., Kohn, A. D., Backus, G. S., Roth, R. A., Pessin, J. E., & Birnbaum, M. J. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.25.17934 · Cited by 214 · see citing works
Inhibition of Glycogen Synthase Kinase 3 Improves Insulin Action and Glucose Metabolism in Human Skeletal Muscle
Nikoulina, S. E., Ciaraldi, T. P., Mudaliar, S., Carter, L., Johnson, K., & Henry, R. R. (2002) · Diabetes · doi:10.2337/diabetes.51.7.2190 · Cited by 198 · see citing works
Self-citation
Exercise training, glucose transporters, and glucose transport in rat skeletal muscles
Rodnick, K. J., Henriksen, E. J., James, D. E., & Holloszy, J. O. (1992) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1992.262.1.c9 · Cited by 183 · see citing works
Self-citation
Muscle fiber type specificity in insulin signal transduction
Song, X. M., Ryder, J. W., Kawano, Y., Chibalin, A., Krook, A., & Zierath, J. R. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.277.6.r1690 · Cited by 142 · see citing works
Insulin resistance of obese Zucker rats exercise trained at two different intensities
Cortez, M. Y., TORGAN, C. E., Brozinick, J. T., & Ivy, J. L. (1991) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1991.261.5.e613 · Cited by 122 · see citing works
Inhibition of Glycogen-synthase Kinase 3 Stimulates Glycogen Synthase and Glucose Transport by Distinct Mechanisms in 3T3-L1 Adipocytes
Orena, S., Torchia, A. J., & Garofalo, R. S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910002199 · Cited by 109 · see citing works
Epitrochlearis muscle. I. Mechanical performance, energetics, and fiber composition
Нешер, Р., Karl, I. E., Kaiser, K. E., & KIPNIS, D. M. (1980) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1980.239.6.e454 · Cited by 90 · see citing works
Early alterations in soleus GLUT-4, glucose transport, and glycogen in voluntary running rats
Henriksen, E. J., & Halseth, A. E. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.76.5.1862 · Cited by 86 · see citing works
Self-citation
Mechanisms of Multisite Phosphorylation and Inactivation of Rabbit Muscle Glycogen Synthase
Zhang, W. M., DePaoli-Roach, A. A., & Roach, P. J. (1993) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1993.1342 · Cited by 79 · see citing works
Glucose transport: locus of muscle insulin resistance in obese Zucker rats
Sherman, W. M., Katz, A. L., Cutler, C. L., Withers, R. T., & Ivy, J. L. (1988) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1988.255.3.e374 · Cited by 69 · see citing works
Lithium Increases Susceptibility of Muscle Glucose Transport to Stimulation by Various Agents
Tabata, I., Schluter, J. M., Gulve, E. A., et al. (1994) · Diabetes · doi:10.2337/diab.43.7.903 · Cited by 59 · see citing works
Increased response to insulin of glucose metabolism in the 6-day unloaded rat soleus muscle.
Henriksen, E. J., Tischler, M. E., & Johnson, D. G. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)67443-5 · Cited by 58 · see citing works
Self-citation
Effects of lithium and insulin on glycogen synthesis in L6 myocytes: additive effects on inactivation of glycogen synthase kinase-3
Choi, W. S. (2000) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(00)00068-4 · Cited by 23 · see citing works

Flagged first, then by citations

Sorted by citations

Glycogen synthase kinase-3 (GSK3): Inflammation, diseases, and therapeutics
Jope, R. S., Yuskaitis, C. J., & Beurel, E. (2007) · Neurochemical Research · doi:10.1007/s11064-006-9128-5 · Cited by 774 · see citing works
Glucocorticoid-induced insulin resistance in skeletal muscles: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor
Ruzzin, J., Wagman, A. S., & Jensen, J. (2005) · Diabetologia · doi:10.1007/s00125-005-1886-0 · Cited by 243 · see citing works

Kaempferitrin inhibits GLUT4 translocation and glucose uptake in 3T3-L1 adipocytes
Prasad, C. N. V., Mohan, S. S., Banerji, A., et al. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.01.008 · Cited by 38 · see citing works
The interaction of auraptene and other oxyprenylated phenylpropanoids with glucose transporter type 4
Genovese, S., Ashida, H., Yamashita, Y., Nakgano, T., Ikeda, M., Shirasaya, D., Epifano, F., Taddeo, V. A., & Fiorito, S. (2017) · Phytomedicine · doi:10.1016/j.phymed.2017.06.005 · Cited by 16 · see citing works
Poster 71: Goldmann Tonometer Calibration Changes Over Time
Perrigin, J., Perrigin, D., & Jacob, E. S. (2008) · Optometry · doi:10.1016/j.optm.2008.04.078 · Cited by 1 · see citing works
Reduction of Insulin-Stimulated Glucose Uptake in L6 Myotubes by the Protein Kinase Inhibitor SB203580 Is Independent of p38MAPK Activity
Antonescu, C. N., Huang, C., Niu, W., Liu, Z., Eyers, P. A., Heidenreich, K. A., Bilan, P. J., & Klip, A. (2005) · Endocrinology · doi:10.1210/en.2005-0404 · Cited by 79 · see citing works
Prenylated chalcones 4‐hydroxyderricin and xanthoangelol stimulate glucose uptake in skeletal muscle cells by inducing GLUT4 translocation
Kawabata, K., Sawada, K., Ikeda, K., Fukuda, I., Kawasaki, K., Yamamoto, N., & Ashida, H. (2010) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201000267 · Cited by 52 · see citing works

Authors: Henriksen, E. J., Kinnick, T. R., Teachey, M. K., O'Keefe, M. P., Ring, D., Johnson, K. W., & Harrison, S. D.
Affiliations: University of Arizona (US)
Muscle Metabolism Laboratory, Department of Physiology, University of Arizona College of Medicine, Tucson, Arizona 85721; and
Chiron Corporation, Emeryville, California 94608
ORCID: Johnson, Kirk W.
Venue: American Journal of Physiology-Endocrinology and Metabolism
Publisher: American Physiological Society
Published: 2003-05-01
Volume: 284
Issue: 5
Pages: E892-E900
ISSN: 0193-1849 (ISSN-L)
1522-1555
DOI: 10.1152/ajpendo.00346.2002
OpenAlex: W1988605096
Cited by: 108
References: 37
Citations by year: 2024: 3 · 2023: 5 · 2022: 3 · 2021: 1 · 2020: 2 · 2019: 3 · 2018: 1 · 2017: 4 · 2016: 3 · 2015: 1 · 2014: 5 · 2013: 4 · 2012: 4
FWCI: 3.56
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Natural Antidiabetic Agents Studies
Keywords: glycogen synthase kinase-3, GSK3 inhibition, insulin resistance, skeletal muscle glucose transport, GLUT4, glycogen synthase, lithium, Zucker diabetic fatty rats, oral glucose tolerance test
MeSH terms: Administration, Oral, Animals, Biological Transport, Blood Glucose, Cell Membrane, Diabetes Mellitus, Enzyme Inhibitors, Glucose, Glycogen Synthase, Insulin Resistance, Lithium, Male, Monosaccharide Transport Proteins, Muscle Proteins, Obesity, Rats, Zucker, Muscle, Skeletal, Glycogen Synthase Kinase 3, Glucose Transporter Type 4, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Modulation of muscle insulin resistance by selective inhibition of GSK-3 in Zucker diabetic fatty rats

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks