Cited by 825Diabetes, Cardiovascular Risks, and LipoproteinsMetabolism, Diabetes, and CancerAdipokines, Inflammation, and Metabolic Diseases

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Etiology of Insulin Resistance

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Petersen, Kitt Falk, Shulman, Gerald I.·2006·The American Journal of Medicine

DOI 10.1016/j.amjmed.2006.01.009PMC PMC2995525

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Abstract

Type 2 diabetes mellitus is a major cause of morbidity and mortality worldwide, and the prevalence is set to increase dramatically over the coming decades. Understanding the metabolic pathways that lead to type 2 diabetes is therefore an important healthcare objective. Novel investigational techniques based on magnetic resonance spectroscopy (MRS) have allowed real-time insight into the molecular defects in patients with type 2 diabetes, revealing that insulin resistance is a product of decreased insulin-stimulated skeletal muscle glycogen synthesis, which can mostly be attributed to decreased insulin-stimulated glucose transport (Glut 4) activity. This defect appears to be a result of intracellular lipid-induced inhibition of insulin-stimulated insulin-receptor substrate (IRS)-1 tyrosine phosphorylation resulting in reduced IRS-1-associated phosphatidyl inositol 3 kinase activity. The hypothesis that insulin resistance is a result of accumulation of intracellular lipid metabolites (e.g., fatty acyl CoAs, diacylglycerol) in skeletal muscle and hepatocytes is supported by observations in patients and mouse models of lipodystrophy. Furthermore, the increase in hepatic insulin sensitivity observed in patients with type 2 diabetes following weight loss is also accompanied by a significant reduction in intrahepatic fat without any changes in circulating adipocytokines (interleukin-6, resistin, leptin). Finally, recent MRS studies in healthy, lean, elderly subjects and lean insulin-resistant offspring of parents with type 2 diabetes have demonstrated that reduced mitochondrial activity may also lead to increased intramyocellular lipid content and insulin resistance in skeletal muscle in these individuals. In summary, in vivo MRS has proved to be an important tool for elucidating the causal chain of events that causes insulin resistance. Understanding the cellular mechanism(s) of insulin resistance in turn offers the prospect of better targeted and more effective therapeutic interventions for treatment and prevention of type 2 diabetes.

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Background
Distinct cellular pools of perilipin 5 point to roles in lipid trafficking
Bartholomew, S. R., Bell, E. H., Summerfield, T. L. S., Newman, L. C., Miller, E. L., Patterson, B., Niday, Z., Ackerman, W. E., & Tansey, J. T. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2011.10.017 · Cited by 53
“causal, ectopic neutral lipid storage in liver and muscle is emerging as key factors in the etiology of these diseases [2].”
A New Insight into the Roles of MiRNAs in Metabolic Syndrome
Huang, Y., Yan, Y., Xv, W., Ge, Q., Li, C., Zou, H., & Li, Y. (2018) · BioMed Research International · doi:10.1155/2018/7372636 · Cited by 56
“Because obesity causes fat to accumulate not only in adipocytes, but also in muscle and hepatocytes, leading to IR in these organs [24], in recent years, miRNAs have appeared as novel biomarkers for diagnosis of quite a few diseases.”
Background
Grp1 Plays a Key Role in Linking Insulin Signaling to Glut4 Recycling
Li, J., Malaby, A. W., Famulok, M., Sabe, H., Lambright, D. G., & Hsu, V. W. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.03.004 · Cited by 53
“The glucose transporter type 4 (glut4) is expressed selectively in fat and muscle tissues, where it plays a direct role in glucose homeostasis and also has indirect roles in other metabolic events, such as fatty acid biogenesis (Herman and Kahn, 2006; Huang and Czech, 2007; Petersen and Shulman, 2006).”
β-Adrenergic and Atrial Natriuretic Peptide Interactions on Human Cardiovascular and Metabolic Regulation
Birkenfeld, A. L., Boschmann, M., Moro, C., Adams, F., Heusser, K., Tank, J., Diedrich, A., Schroeder, C., Franke, G., Berlan, M., et al. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1084 · Cited by 53
“(22) Finally, increased NEFA concentrations may have led to a secondary increase in gluconeogenesis and a reduced cellular uptake of glucose.(27) Changes in circulating glucose concentration were associated with changes in glucose utilization at the tissue level.”
Background
Evaluating the discriminative power of multi-trait genetic risk scores for type 2 diabetes in a northern Swedish population
The MAGIC investigators, Fontaine‐Bisson, B., Renström, F., Rolandsson, O., Payne, F., Hallmans, G., Barroso, I., & Franks, P. W. (2010) · Diabetologia · doi:10.1007/s00125-010-1792-y · Cited by 51
“For dyslipidaemia, the mechanisms of association with type 2 diabetes primarily involve insulin resistance caused by the infiltration of insulin-sensitive tissues by triacylglycerol and other lipid metabolites [20, 21].”
Background
Tartary buckwheat flavonoids protect hepatic cells against high glucose-induced oxidative stress and insulin resistance via MAPK signaling pathways
Hu, Y., Hou, Z., Liu, D., & Yang, X. (2016) · Food & Function · doi:10.1039/c5fo01467k · Cited by 53
PPAR-α agonism improves whole body and muscle mitochondrial fat oxidation, but does not alter intracellular fat concentrations in burn trauma children in a randomized controlled trial
Cree‐Green, M., Newcomer, B. R., Herndon, D. N., Qian, T., Sun, D., Morio, B., Zwetsloot, J. J., Dohm, G. L., Fram, R. Y., Mlcak, R. P., et al. (2007) · Nutrition & Metabolism · doi:10.1186/1743-7075-4-9 · Cited by 52
“Liver fat (LFAT) and muscle triglycerides (IMCL) were measured using magnetic resonance spectroscopy as described previously [16], except that the settings of the scans were altered to decrease the amount of time in the machine for the patients.”
BackgroundInfluential
Insulin resistance and atherosclerosis: convergence between metabolic pathways and inflammatory nodes
Stöhr, R., & Federici, M. (2013) · Biochemical Journal · doi:10.1042/bj20130121 · Cited by 51
The adipokine/ceramide axis: Key aspects of insulin sensitization
Xia, J. Y., Morley, T. S., & Scherer, P. E. (2013) · Biochimie · doi:10.1016/j.biochi.2013.08.013 · Cited by 52
“Although this study correlated intramyocellular triglyceride to insulin resistance, there have been studies suggesting that other intracellular lipids, mainly diacyglycerol and ceramides play a major role in mediating insulin resistance [3,4].”
Background
Partial Resistance to Peroxisome Proliferator–Activated Receptor-α Agonists in ZDF Rats Is Associated With Defective Hepatic Mitochondrial Metabolism
Satapati, S., He, T., Inagaki, T., Potthoff, M. J., Merritt, M. E., Esser, V., Mangelsdorf, D. J., Kliewer, S. A., Browning, J. D., & Burgess, S. C. (2008) · Diabetes · doi:10.2337/db08-0226 · Cited by 52
“Abnormal mitochondrial metabolism is a key feature of insulin-resistant skeletal muscle (17–20) and has been implicated in human insulin-resistant liver (15,16).”
Background
Links between Childhood Obesity, High-Fat Diet, and Central Precocious Puberty
Calcaterra, V., Magenes, V. C., Hruby, C., Siccardo, F., Mari, A., Cordaro, E., Fabiano, V., & Zuccotti, G. (2023) · Children · doi:10.3390/children10020241 · Cited by 60
Heat shock proteins induction reduces stress kinases activation, potentially improving insulin signalling in monocytes from obese subjects
Simar, D., Jacques, A., & Caillaud, C. (2012) · Cell Stress and Chaperones · doi:10.1007/s12192-012-0336-4 · Cited by 51
Fat in Liver/Muscle Correlates More Strongly With Insulin Sensitivity in Rats Than Abdominal Fat
Lim, S. K., Son, K. R., Song, I. C., Park, H. S., Jin, C. J., Jang, H. C., Park, K. S., Kim, Y., & Lee, H. K. (2008) · Obesity · doi:10.1038/oby.2008.486 · Cited by 53
Insulin promotes iron uptake in human hepatic cell by regulating transferrin receptor-1 transcription mediated by hypoxia inducible factor-1
Biswas, S., Tapryal, N., Mukherjee, R., Kumar, R., & Mukhopadhyay, C. K. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2012.11.003 · Cited by 50
2,3,7,8-Tetrachlorodibenzo-p-Dioxin Impairs an Insulin Signaling Pathway through the Induction of Tumor Necrosis Factor-α in Adipocytes
Nishiumi, S., Yoshida, M., Azuma, T., Yoshida, K., & Ashida, H. (2010) · Toxicological Sciences · doi:10.1093/toxsci/kfq052 · Cited by 50
“Insulin resistance causes a decline in the response to insulin accompanied by defective glucose uptake activity in adipocytes (Petersen and Shulman, 2006).”
Background
Ciliary Neurotrophic Factor Stimulates Muscle Glucose Uptake by a PI3-Kinase–Dependent Pathway That Is Impaired With Obesity
Steinberg, G. R., Watt, M. J., Ernst, M., Birnbaum, M. J., Kemp, B. E., & Jørgensen, S. B. (2009) · Diabetes · doi:10.2337/db08-0659 · Cited by 54
“It is well established that obesity is associated with impaired insulin sensitivity in skeletal muscle, and impaired activation of IRS-1 has been attributed a primary role (28,43).”
Background
HIV protease inhibitors and obesity
Anuurad, E., Bremer, A. A., & Berglund, L. (2010) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e32833dde87 · Cited by 50
From a glucocentric to a lipocentric approach towards metabolic syndrome
Mittra, S., Bansal, V. S., & Bhatnagar, P. K. (2008) · Drug Discovery Today · doi:10.1016/j.drudis.2008.01.006 · Cited by 48
Overnutrition, Hyperinsulinemia and Ectopic Fat: It Is Time for A Paradigm Shift in the Management of Type 2 Diabetes
Janssen, J. A. M. J. L. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105488 · Cited by 70
“This then causes a reduced IRS-1-associated phosphatidyl inositol 3 kinase activity and thereby decreases insulin-stimulated glucose transport (Glut 4) activity (a hallmark of insulin resistance) [81,82].”
BackgroundInfluential
New Opportunities: Harnessing Induced Pluripotency for Discovery in Diabetes and Metabolism
Teo, A. K. K., Wagers, A. J., & Kulkarni, R. N. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.08.010 · Cited by 49
Targeting PGC-1α to control energy homeostasis
Wu, Z., & Boss, O. (2007) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.11.10.1329 · Cited by 50
“A large body of literature implicates dysregulation of fatty acid metabolism [6,7,11] , adipose tissue inflammation [12,13] , increased ER stress [14] ,”
Background
Over-expression of NYGGF4 (PID1) inhibits glucose transport in skeletal myotubes by blocking the IRS1/PI3K/AKT insulin pathway
Wu, W. L., Gan, W., Tong, M., Li, X. L., Dai, J.-Z., Zhang, C. M., & Guo, X. (2010) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2010.11.165 · Cited by 48
“Defects in insulin-stimulated glucose uptake in muscle are suggested to be important early events in the pathogenesis of insulin resistance [9,10].”
Background
Potential Mechanisms of Muscle Mitochondrial Dysfunction in Aging and Obesity and Cellular Consequences
Chanséaume, E., & Morio, B. (2009) · International Journal of Molecular Sciences · doi:10.3390/ijms10010306 · Cited by 50
“Emerging data support the hypothesis that in the particular case of young healthy insulin resistant offspring of parents with type 2 diabetes, alteration in mitochondrial activity would be partly inherited [18-21].”
Background
Human myotubes from myoblast cultures undergoing senescence exhibit defects in glucose and lipid metabolism
Nehlin, J. O., Just, M., Rustan, A. C., & Gaster, M. (2011) · Biogerontology · doi:10.1007/s10522-011-9336-5 · Cited by 53
“mitochondrial function appears to predispose elderly to insulin resistance and type 2 diabetes (Morino et al. 2006; Petersen et al. 2003; Petersen and Shulman 2006).”
Background
In vivo inhibition of focal adhesion kinase causes insulin resistance
Bisht, B., Srinivasan, K. K., & Dey, C. S. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.157107 · Cited by 46
Flaxseed oil prevents trans-10, cis-12-conjugated linoleic acid-induced insulin resistance in mice
Kelley, D. S., Vemuri, M., Adkins, Y. C., Gill, S. H. S., Fedor, D. M., & Mackey, B. E. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114508027451 · Cited by 49
“Dietary factors that contribute to the development of IR and NAFLD include high-fat (saturated and trans -fatty acids) and high-sucrose diets (11–13) .”
Decreased peripheral blood mitochondrial DNA content is related to HbA1c, fasting plasma glucose level and age of onset in Type 2 diabetes mellitus
Xu, F., Zhou, X. M., Shen, F., Pang, R. W. C., & Liu, S. M. (2011) · Diabetic Medicine · doi:10.1111/j.1464-5491.2011.03565.x · Cited by 47
Ionizing Radiation Potentiates High-Fat Diet–Induced Insulin Resistance and Reprograms Skeletal Muscle and Adipose Progenitor Cells
Nylander, V., Ingerslev, L. R., Andersen, E., Fabre, O., Garde, C., Rasmussen, M., Citirikkaya, K., Bæk, J., Christensen, G. L., Aznar, M. C., et al. (2016) · Diabetes · doi:10.2337/db16-0364 · Cited by 47
“be due to a lack of adipose tissue plasticity and consequent lipodystrophy after ionizing radiation (42).”
Background
Tetramethylpyrazine prevents diabetes by activating PI3K/Akt/GLUT-4 signalling in animal model of type-2 diabetes
Rai, U., Kosuru, R., Prakash, S., Singh, S. P., Birla, H., Tiwari, V. K., & Singh, S. K. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.116836 · Cited by 46
The effects of fasting and refeeding with a ‘metabolic preconditioning’ drink on substrate reserves and mononuclear cell mitochondrial function
Awad, S., Stephenson, M. C., Placidi, E., Marciani, L., Constantin‐Teodosiu, D., Gowland, P. A., Spiller, R. E., Fearon, K. C. H., Morris, P. G., Macdonald, I. A., et al. (2010) · Clinical Nutrition · doi:10.1016/j.clnu.2010.01.009 · Cited by 47
Dynamic Tight Glycemic Control During and After Cardiac Surgery Is Effective, Feasible, and Safe
Lecomte, P., Foubert, L. A., Nobels, F. R. E., Coddens, J., Nollet, G., Casselman, F. P. A., Crombrugge, P. V., Vandenbroucke, G., & Cammu, G. (2008) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e318172c557 · Cited by 46
“This leads to decreased insulinstimulated skeletal muscle glycogen synthesis, which can mostly be attributed to decreased glucose transport (Glut 4) receptor sensitivity.(27) Our preliminary data showed that anticipation of changes in insulin sensitivity during key portions of surgery may be more effective for achievi…”
Background
Melatonin and Glucose Metabolism: Clinical Relevance
Lardone, P. J., Álvarez‐Sánchez, N., Guerrero, J. M., & Carrillo‐Vico, A. (2014) · Current Pharmaceutical Design · doi:10.2174/1381612819666131119101032 · Cited by 47
“T2D is preceded by a lengthy asymptomatic stage characterized by hyperglycemia and insulin resistance [136, 137].”
Background
An 8-Week High-Fat Diet Induces Obesity and Insulin Resistance with Small Changes in the Muscle Transcriptome of C57BL/6J Mice
de Wilde, J., Smit, E., Mohren, R., Boekschoten, M. V., de Groot, P., van den Berg, S. A. A., Bijland, S., Voshol, P. J., van Dijk, K. W., de Wit, N. J. W., et al. (2009) · Lifestyle Genomics · doi:10.1159/000308466 · Cited by 47
“Therefore, it has been proposed that not TAG, but lipid intermediates, such as long-chain fatty acyl CoAs, diacylglycerol and ceramides may act as signaling molecules interrupting insulin signaling and glucose metabolism, which eventually results in insulin resistance [”
Background
An islet in distress: β cell failure in type 2 diabetes
Ogihara, T., & Mirmira, R. G. (2010) · Journal of Diabetes Investigation · doi:10.1111/j.2040-1124.2010.00021.x · Cited by 46
Chronological Approach of Diet‐induced Alterations in Muscle Mitochondrial Functions in Rats
Chanséaume, E., Tardy, A.-L., Salles, J., Giraudet, C., Rousset, P., Tissandier, A., Boirie‌, Y., & Morio, B. (2007) · Obesity · doi:10.1038/oby.2007.511 · Cited by 46
Anti-inflammatory and anti-hyperlipidemic effect of Semecarpus anacardium in a High fat diet: STZ-induced Type 2 diabetic rat model
Khan, H. B. H., Vinayagam, K. S., Moorthy, B. T., Shanthi, P., & Sachdanandam, P. (2012) · Inflammopharmacology · doi:10.1007/s10787-011-0109-1 · Cited by 44
Increased Mitochondrial Oxidative Phosphorylation in the Liver Is Associated With Obesity and Insulin Resistance
Buchner, D. A., Yazbek, S. N., Solinas, P., Burrage, L. C., Morgan, M. G., Hoppel, C. L., & Nadeau, J. H. (2010) · Obesity · doi:10.1038/oby.2010.214 · Cited by 47
“Insulin resistance is a key factor in the pathophysiological development of T2D and remains the best indicator of future development of T2D among individuals with a family history of the disease (2).”
Background
The Lyn Kinase Activator MLR-1023 Is a Novel Insulin Receptor Potentiator that Elicits a Rapid-Onset and Durable Improvement in Glucose Homeostasis in Animal Models of Type 2 Diabetes
Ochman, A. R., Lipinski, C. A., Handler, J. A., Reaume, A. G., & Saporito, M. S. (2012) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.192187 · Cited by 45
“Type 2 diabetes (T2D) is a metabolic disease that is driven primarily by insulin receptor insensitivity (Petersen and Shulman, 2006).”
Background
Role of Calpain-10 in the Development of Diabetes Mellitus and Its Complications
Pánico, P., Salazar, A. M., Burns, A. L., & Ostrosky‐Wegman, P. (2014) · Archives of Medical Research · doi:10.1016/j.arcmed.2014.01.005 · Cited by 45
Molecular Genetics of Experimental Hypertension and the Metabolic Syndrome
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The SNARE Protein SNAP23 and the SNARE-Interacting Protein Munc18c in Human Skeletal Muscle Are Implicated in Insulin Resistance/Type 2 Diabetes
Boström, P., Andersson, L. K., Vind, B. F., Håversen, L., Rutberg, M., Wickström, Y., Larsson, E. N. V., Jansson, P., Svensson, M. K. E., Brånemark, R., et al. (2010) · Diabetes · doi:10.2337/db09-1503 · Cited by 44
“Diabetes 59: 1870–1878, 2010 Insulin resistance plays a major role in the development of type 2 diabetes and is highly related to the accumulation of triglycerides in skeletal muscle (1,2).”
Background
Retracted
Relative efficacies of insulin and poly (lactic-co-glycolic) acid encapsulated nano-insulin in modulating certain significant biomarkers in arsenic intoxicated L6 cells
Samadder, A., Das, S., Das, J., & Khuda‐Bukhsh, A. R. (2013) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2013.03.028 · Cited by 43
The induction of miR-96 by mitochondrial dysfunction causes impaired glycogen synthesis through translational repression of IRS-1 in SK-Hep1 cells
Jeong, H.-J., Park, S., Yang, W., & Lee, W. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.03.104 · Cited by 43
“Insulin resistance is defined as a decreased responsiveness of the target tissues to ordinary levels of insulin, and is believed to be a central feature of type 2 diabetes and metabolic syndrome [5,6].”
Background
High-fat and obesogenic diets: current and future strategies to fight obesity and diabetes
Teodoro, J. S., Varela, A. T. I. F., Rolo, A. P., & Palmeira, C. M. (2014) · Genes & Nutrition · doi:10.1007/s12263-014-0406-6 · Cited by 45

Authors: Petersen, K. F., & Shulman, G. I.
Affiliations: Howard Hughes Medical Institute (US)
ORCID: Petersen, Kitt Falk
Shulman, Gerald I.
Venue: The American Journal of Medicine
Publisher: Elsevier BV
Published: 2006-05
Volume: 119
Issue: 5
Pages: S10-S16
ISSN: 0002-9343 (ISSN-L)
DOI: 10.1016/j.amjmed.2006.01.009
PMC: PMC2995525
OpenAlex: W1982488301
Cited by: 825
References: 56
Citations by year: 2026: 19 · 2025: 25 · 2024: 18 · 2023: 26 · 2022: 18 · 2021: 34 · 2020: 31 · 2019: 26 · 2018: 25 · 2017: 27 · 2016: 44 · 2015: 41 · 2014: 55 · 2013: 52 · 2012: 43
FWCI: 10.84
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: The American Journal of Medicine (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Aging (R01AG023686)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK040936)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Keywords: insulin resistance, type 2 diabetes, IRS-1 tyrosine phosphorylation, PI3K signaling, intracellular lipid accumulation, fatty acyl-CoA, diacylglycerol, lipodystrophy, hepatic insulin sensitivity, weight loss, intrahepatic fat, mitochondrial dysfunction, intramyocellular lipid, magnetic resonance spectroscopy, adipokines
MeSH terms: Diabetes Mellitus, Type 2, Humans, Hypoglycemic Agents, Insulin Resistance, Mitochondria, Magnetic Resonance Spectroscopy, Obesity, Phosphoproteins, Weight Loss, Thiazolidinediones, Glucose Transporter Type 4, Insulin Receptor Substrate Proteins

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