Glucose Transporters and Insulin Action — Implications for Insulin Resistance and Diabetes Mellitus

Shepherd, Peter R.; Kahn, Barbara B.

doi:10.1056/nejm199907223410406

Cited by 1,295Metabolism, Diabetes, and CancerPancreatic function and diabetesDiabetes, Cardiovascular Risks, and Lipoproteins

Glucose Transporters and Insulin Action — Implications for Insulin Resistance and Diabetes Mellitus

Shepherd, Peter R., Kahn, Barbara B.·1999·New England Journal of Medicine

DOI 10.1056/nejm199907223410406

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Abstract

Insulin was discovered more than 75 years ago, but only recently have we begun to understand the mechanisms by which insulin promotes the uptake of glucose into cells. This review discusses recent advances, their contribution to our understanding of the pathogenesis of diabetes mellitus, and their implications for the design of new therapies to prevent and treat diabetes and its complications.Role of Glucose Transporters in Maintaining Glucose HomeostasisCarbohydrates, and glucose in particular, are an important source of energy for most living organisms. Tissues such as the brain need glucose constantly, and low blood concentrations of glucose can cause . . .

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In insulin-resistant individuals with T2DM, glucose transport activity is severely impaired.
“In insulin resistant individuals with T2DM, glucose transport activity is severely impaired [156, 181, 182, 187–189].”
From Pathogenesis of insulin resistance in skeletal muscle (2010) · cites this paper as [181]
Activation of insulin signal transduction in skeletal muscle stimulates glucose transport by translocating intracellular GLUT4-containing vesicles to the plasma membrane and activating them after insertion.
“Activation of the insulin signal transduction system in skeletal muscle stimulates glucose transport through a mechanism that involves translocation of a large intracellular pool of glucose transporters (associated with low-density microsomes) to the plasma membrane and their subsequent activation after insertion into the cell membrane [181, 182].”
From Pathogenesis of insulin resistance in skeletal muscle (2010) · cites this paper as [181]

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FGF-21 as a novel metabolic regulator
Kharitonenkov, A., Shiyanova, T. L., Koester, A., Ford, A. M., Micanovic, R., Galbreath, E. J., Sandusky, G. E., Hammond, L. J., Moyers, J. S., Owens, R. A., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23606 · Cited by 2,125 · see citing works
Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes
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Pathogenesis of type 2 diabetes mellitus
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Retinol-Binding Protein 4 and Insulin Resistance in Lean, Obese, and Diabetic Subjects
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Lipid-induced insulin resistance: unravelling the mechanism
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Trends in insulin resistance: insights into mechanisms and therapeutic strategy
Li, M., Chi, X., Wang, Y., Setrerrahmane, S., Xie, W., & Xu, H. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01073-0 · Cited by 939 · see citing works
Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins
Wood, I. S., & Trayhurn, P. (2003) · British Journal of Nutrition · doi:10.1079/bjn2002763 · Cited by 889 · see citing works
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Ritov, V. B., Menshikova, E. V., He, J., Ferrell, R. E., Goodpaster, B. H., & Kelley, D. E. (2005) · Diabetes · doi:10.2337/diabetes.54.1.8 · Cited by 887 · see citing works
Mitochondrial dysfunction in Nash: causes, consequences and possible means to prevent it
Begriche, K., Igoudjil, A., Pessayre, D., & Fromenty, B. (2006) · Mitochondrion · doi:10.1016/j.mito.2005.10.004 · Cited by 753 · see citing works
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Abdul-Ghani, M. A., & DeFronzo, R. A. (2010) · Journal of Biomedicine and Biotechnology · doi:10.1155/2010/476279 · Cited by 670 · see citing works
Insulin effects in muscle and adipose tissue
Dimitriadis, G., Mitrou, P., Lambadiari, V., Maratou, E., & Raptis, S. A. (2011) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(11)70014-6 · Cited by 649 · see citing works
Oxidative stress and the etiology of insulin resistance and type 2 diabetes
Henriksen, E. J., Diamond-Stanic, M. K., & Marchionne, E. M. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.12.005 · Cited by 600 · see citing works
Selective Glycogen Synthase Kinase 3 Inhibitors Potentiate Insulin Activation of Glucose Transport and Utilization In Vitro and In Vivo
Ring, D. B., Johnson, K. W., Henriksen, E. J., Nuss, J. M., Goff, D., Kinnick, T. R., Ma, S. T., Reeder, J. W., Samuels, I., Slabiak, T., et al. (2003) · Diabetes · doi:10.2337/diabetes.52.3.588 · Cited by 532 · see citing works
Invited Review: Effects of acute exercise and exercise training on insulin resistance
Henriksen, E. J. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01219.2001 · Cited by 535 · see citing works
From pre-diabetes to diabetes: diagnosis, treatments and translational research
Khan, R., Chua, Z., Tan, J., Yang, Y., Liao, Z., & Zhao, Y. (2019) · Medicina · doi:10.3390/medicina55090546 · Cited by 484 · see citing works
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Lin, Y., & Sun, Z. (2010) · Journal of Endocrinology · doi:10.1677/joe-09-0260 · Cited by 457 · see citing works
Identification of IRS-1 Ser-1101 as a target of S6K1 in nutrient- and obesity-induced insulin resistance
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Exercise and Physical Activity: Clinical Outcomes and Applications
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NASH: a mitochondrial disease
Pessayre, D., & Fromenty, B. (2005) · Journal of Hepatology · doi:10.1016/j.jhep.2005.03.004 · Cited by 441 · see citing works
Cigarette smoking and diabetes mellitus: evidence of a positive association from a large prospective cohort study
Will, J. C., Galuska, D. A., Ford, E. S., Mokdad, A., & Calle, E. E. (2001) · International Journal of Epidemiology · doi:10.1093/ije/30.3.540 · Cited by 376 · see citing works
AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise
Musi, N., Fujii, N., Hirshman, M. F., Ekberg, I., Fröberg, S., Ljungqvist, O., Thorell, A., & Goodyear, L. J. (2001) · Diabetes · doi:10.2337/diabetes.50.5.921 · Cited by 371 · see citing works
PPARγ activation in adipocytes is sufficient for systemic insulin sensitization
Sugii, S., Olson, P., Sears, D. D., Saberi, M., Atkins, A. R., Barish, G. D., Hong, S.-H., Castro, G. L., Yin, Y.-Q., Nelson, M. C., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912487106 · Cited by 255 · see citing works
Regulation of Postabsorptive and Postprandial Glucose Metabolism by Insulin-Dependent and Insulin-Independent Mechanisms: An Integrative Approach
Dimitriadis, G. D., Maratou, E., Kountouri, A., Board, M., & Lambadiari, V. (2021) · Nutrients · doi:10.3390/nu13010159 · Cited by 241 · see citing works
Imaging Atherosclerotic Plaque Inflammation by Fluorodeoxyglucose With Positron Emission Tomography
Rudd, J. H. F., Narula, J., Strauss, H. W., Virmani, R., Machac, J., Klimas, M., Tahara, N., Fuster, V., Warburton, E. A., Fayad, Z. A., et al. (2010) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2009.12.061 · Cited by 236 · see citing works
Glycated haemoglobin and blood pressure-lowering effect of cinnamon in multi-ethnic Type 2 diabetic patients in the UK: A randomized, placebo-controlled, double-blind clinical trial
Akilen, R., Tsiami, A., Devendra, D., & Robinson, N. (2010) · Diabetic Medicine · doi:10.1111/j.1464-5491.2010.03079.x · Cited by 230 · see citing works
Bipolar disorder and diabetes mellitus: epidemiology, etiology, and treatment implications
Mcintyre, R., Konarski, J., Misener, V., & Kennedy, S. (2005) · Annals of Clinical Psychiatry · doi:10.1080/10401230590932380 · Cited by 203 · see citing works
Glucose toxicity and the development of diabetes in mice with muscle-specific inactivation of GLUT4
Kim, J. K., Zisman, A., Fillmore, J. J., Peroni, O. D., Kotani, K., Perret, P., Zong, H., Dong, J., Kahn, C. R., Kahn, B. B., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci10294 · Cited by 202 · see citing works
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Regulation of Skeletal Muscle Glucose Transport and Glucose Metabolism by Exercise Training
Evans, P. L., McMillin, S. L., Weyrauch, L. A., & Witczak, C. A. (2019) · Nutrients · doi:10.3390/nu11102432 · Cited by 190 · see citing works
Disruption of CXC Motif Chemokine Ligand-14 in Mice Ameliorates Obesity-induced Insulin Resistance
Nara, N., Nakayama, Y., Okamoto, S., Tamura, H., Kiyono, M., Muraoka, M., Tanaka, K., Taya, C., Shitara, H., Ishii, R., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700412200 · Cited by 176 · see citing works
Insulin signaling and glucose transport in insulin resistant human skeletal muscle
Karlsson, H. K. R., & Zierath, J. R. (2007) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-007-0030-9 · Cited by 159 · see citing works
Effect of Oral Creatine Supplementation on Human Muscle GLUT4 Protein Content After Immobilization
Eijnde, B. O. '., Ursø, B., Richter, E. A., Greenhaff, P. L., & Hespel, P. (2001) · Diabetes · doi:10.2337/diabetes.50.1.18 · Cited by 162 · see citing works
Coordinated patterns of gene expression for substrate and energy metabolism in skeletal muscle of diabetic mice
Yechoor, V. K., Patti, M.-E., Saccone, R., & Kahn, C. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.142301999 · Cited by 156 · see citing works
Genetic Predisposition for Type 2 Diabetes, but Not for Overweight/Obesity, Is Associated with a Restricted Adipogenesis
Arner, P., Arner, E., Hammarstedt, A., & Smith, U. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018284 · Cited by 146 · see citing works
Phytotherapy in diabetes: Review on potential mechanistic perspectives
El-Abhar, H. S., & Schaalan, M. F. (2014) · World Journal of Diabetes · doi:10.4239/wjd.v5.i2.176 · Cited by 145 · see citing works
Glucose metabolism in lymphoid and inflammatory cells and tissues
Calder, P. C., Dimitriadis, G., & Newsholme, P. (2007) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0b013e3281e72ad4 · Cited by 143 · see citing works
Exercise training and the antioxidant α-lipoic acid in the treatment of insulin resistance and type 2 diabetes
Henriksen, E. J. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.04.002 · Cited by 136 · see citing works
Relation of self-rated measures of physical activity to multiple risk factors of insulin resistance syndrome in young adults
Gustat, J., Srinivasan, S. R., Elkasabany, A., & Berenson, G. S. (2002) · Journal of Clinical Epidemiology · doi:10.1016/s0895-4356(02)00427-4 · Cited by 135 · see citing works
Metabolic and molecular basis of insulin resistance
Bajaj, M., & DeFronzo, R. A. (2003) · Journal of Nuclear Cardiology · doi:10.1016/s1071-3581(03)00520-8 · Cited by 131 · see citing works
Cinnamon in glycaemic control: Systematic review and meta analysis
Akilen, R., Tsiami, A., Devendra, D., & Robinson, N. (2012) · Clinical Nutrition · doi:10.1016/j.clnu.2012.04.003 · Cited by 124 · see citing works
Impact of blood glucose, diabetes, insulin, and obesity on standardized uptake values in tumors and healthy organs on 18F-FDG PET/CT
Büsing, K. A., Schönberg, S. O., Brade, J., & Wasser, K. (2013) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2012.10.014 · Cited by 111 · see citing works
Oxidative Stress, Glucose Metabolism, and the Prevention of Type 2 Diabetes: Pathophysiological Insights
Shah, S., Iqbal, M., Karam, J., Salifu, M., & McFarlane, S. I. (2007) · Antioxidants & Redox Signaling · doi:10.1089/ars.2007.1629 · Cited by 115 · see citing works
Muscle glycogen inharmoniously regulates glycogen synthase activity, glucose uptake, and proximal insulin signaling
Jensen, J., Jebens, E., Brennesvik, E. O., Ruzzin, J., Soos, M. A., Engebretsen, E. M. L., O'Rahilly, S., & Whitehead, J. P. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00330.2005 · Cited by 114 · see citing works
Chronic central leptin infusion restores hyperglycemia independent of food intake and insulin level in streptozotocin‐induced diabetic rats
Hidaka, S., Yoshimatsu, H., Kondou, S., Tsuruta, Y., Oka, K., Noguchi, H., Okamoto, K., Sakino, H., Teshima, Y., Okeda, T., et al. (2002) · The FASEB Journal · doi:10.1096/fj.01-0164com · Cited by 108 · see citing works
Oxidative stress impairs nuclear proteins binding to the insulin responsive element in the GLUT4 promoter
Pessler, D., Rudich, A., & Bashan, N. (2001) · Diabetologia · doi:10.1007/s001250100024 · Cited by 82 · see citing works
Effect of creatine supplementation on creatine and glycogen content in rat skeletal muscle
Op ‘t Eijnde, B., Richter, E. A., Henquin, J. ‐., Kiens, B., & Hespel, P. (2001) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2001.00786.x · Cited by 79 · see citing works
Oxidant stress and skeletal muscle glucose transport: Roles of insulin signaling and p38 MAPK
Kim, J. S., Saengsirisuwan, V., Sloniger, J. A., Teachey, M. K., & Henriksen, E. J. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2006.05.031 · Cited by 78 · see citing works
Management of side effects of androgen deprivation therapy
Grossmann, M., & Zajac, J. D. (2011) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2011.05.004 · Cited by 69 · see citing works
Interactions of Impaired Glucose Transport and Phosphorylation in Skeletal Muscle Insulin Resistance
Williams, K. V., Price, J. C., & Kelley, D. E. (2001) · Diabetes · doi:10.2337/diabetes.50.9.2069 · Cited by 61 · see citing works
Vascular Endothelial Growth Factor: A Novel Endocrine Defensive Response to Hypoglycemia
Dantz, D., Bewersdorf, J., Fruehwald-Schultes, B., Kern, W., Jelkmann, W., Born, J., Fehm, H. L., & Peters, A. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.2.8215 · Cited by 56 · see citing works
Increased adipose tissue aromatase activity improves insulin sensitivity and reduces adipose tissue inflammation in male mice
Ohlsson, C., Hammarstedt, A., Vandenput, L., Saarinen, N., Ryberg, H., Windahl, S. H., Farman, H. H., Jansson, J.-O., Movérare-Skrtic, S., Smith, U., et al. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00093.2017 · Cited by 55 · see citing works
The Degree of Menstrual Disturbance Is Associated With the Severity of Insulin Resistance in PCOS
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Kaempferitrin inhibits GLUT4 translocation and glucose uptake in 3T3-L1 adipocytes
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Authors: Shepherd, P. R., & Kahn, B. B.
Affiliations: University College London (GB)
Beth Israel Deaconess Medical Center (US)
ORCID: Shepherd, Peter R.
Kahn, Barbara B.
Venue: New England Journal of Medicine
Publisher: Massachusetts Medical Society
Published: 1999-07-22
Volume: 341
Issue: 4
Pages: 248-257
ISSN: 0028-4793 (ISSN-L)
1533-4406
DOI: 10.1056/nejm199907223410406
OpenAlex: W2327640792
Cited by: 1,295
References: 123
Citations by year: 2026: 19 · 2025: 25 · 2024: 29 · 2023: 28 · 2022: 41 · 2021: 46 · 2020: 50 · 2019: 47 · 2018: 44 · 2017: 47 · 2016: 40 · 2015: 54 · 2014: 68 · 2013: 71 · 2012: 54
FWCI: 3.11
Type: journal article
Language: en
Open access: closed
Locations: New England Journal of Medicine (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (DK 43051, R01DK043051)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Keywords: glucose transporters, insulin action, insulin resistance, diabetes mellitus, glucose homeostasis, glucose uptake, insulin signaling, diabetes pathogenesis, diabetes treatment
MeSH terms: Animals, Biological Transport, Diabetes Mellitus, Glucose, Hemostasis, Humans, Insulin, Insulin Resistance, Intracellular Membranes, Monosaccharide Transport Proteins, Muscle Proteins, Signal Transduction, Adipocytes, Muscle, Skeletal, Glucose Transporter Type 4

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Glucose Transporters and Insulin Action — Implications for Insulin Resistance and Diabetes Mellitus

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