Cited by 733Metabolism, Diabetes, and CancerPancreatic function and diabetesAdipokines, Inflammation, and Metabolic Diseases

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Insulin Signaling in Health and Disease

White, Morris F.·2003·Science

DOI 10.1126/science.1092952

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Abstract

The signaling pathways used by insulin have been identified [M. White, Insulin Signaling Pathway, Sci. STKE (Connections Map, as seen November 2003), http://stke.sciencemag.org/cgi/cm/cmp_12069]. Now our challenge is to understand how the failure of these signals is associated with obesity and the progressive failure of pancreatic beta cells that leads to diabetes. Whether better management of chronic inflammation can improve insulin action is an important area of investigation. Drugs that stimulate IRS2 (insulin receptor substrate protein 2) synthesis or signaling might be a good starting point. This knowledge will lead to rational strategies that prevent or cure diabetes.

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M. White Insulin Signaling Pathway Sci. STKE (Connections Map as seen November 2003) http://stke.sciencemag.org/cgi/cm/cmp_12069.
G. S. Hotamisligil, B. M. Spiegelman, Science259, 87 (1999).
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Background
Retracted
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Background
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Background
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Background
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Method
Retracted
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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“The receptors for insulin and IGF1 are tyrosine kinases that recruit and phosphorylate various proteins to generate physiological responses (White, 2003).”
CDK4 is an essential insulin effector in adipocytes
Lagarrigue, S., López‐Mejía, I. C., Denechaud, P., Escoté, X., Castillo‐Armengol, J., Jiménez, V., Chavey, C., Giralt, A., Lai, Q., Zhang, L., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci81480 · Cited by 76
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Background
Retracted
H 2 O 2 -Induced Phosphorylation of ERK1/2 and PKB Requires Tyrosine Kinase Activity of Insulin Receptor and c-Src
Mehdi, M. Z., Pandey, N. R., Pandey, S., & Srivastava, A. K. (2005) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.1014 · Cited by 75
Insulin resistance and hepatitis C: an evolving story
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“Unlike other receptor tyrosine kinases, most functions of the insulin receptor require accessory molecules known as insulin receptor substrates (IRSs) (1e4) to engage multiple downstream signalling pathways.(4) 5 Insulin binding results in autophosphorylation of the receptor and tyrosine phosphorylation of intracellul…”
Background
Ophiopogonin D alleviates high‐fat diet‐induced metabolic syndrome and changes the structure of gut microbiota in mice
Chen, S., Li, X., Liu, L., Liu, C., & Han, X. (2017) · The FASEB Journal · doi:10.1096/fj.201700741rr · Cited by 75
“Proinflammatory cytokines, particularly TNF-a, promote the serine phosphorylation of insulin receptor substrate 1, a critical step to induce insulin resistance (52).”
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Inositol - An effective growth promotor?
Lee, S. A., & Bedford, M. R. (2016) · World s Poultry Science Journal · doi:10.1017/s0043933916000660 · Cited by 80
“Stimulation of the IP3K signalling pathway generates PtdIns(3,4,5)P3, leading to the activation of the Akt (protein kinase B) cascade, which regulates cellular functions such as cell survival and metabolism (White, 2003).”
Background
β‐cell mass in people with type 2 diabetes
Cho, J., Kim, J., Shin, J., Shin, J., & Yoon, K. (2011) · Journal of Diabetes Investigation · doi:10.1111/j.2040-1124.2010.00072.x · Cited by 69
Identification of the tyrosine phosphatase PTP-MEG2 as an antagonist of hepatic insulin signaling
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“Binding of insulin to its cognate receptor stimulates receptor tyrosine kinase activity, resulting in the phosphorylation of several substrates, including insulin receptor substrate (IRS) proteins (White, 2003).”
The role of insulin receptor signaling in zebrafish embryogenesis
Toyoshima, Y., Monson, C., Duan, C., Wu, Y., Gao, C., Yakar, S., Sadler, K. C., & LeRoith, D. (2008) · Endocrinology · doi:10.1210/en.2008-0329 · Cited by 72
Neuronal stress signaling and eIF2α phosphorylation as molecular links between Alzheimer's disease and diabetes
Lourenco, M. V., Ferreira, S. T., & Felice, F. G. D. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.003 · Cited by 74
Voluntary exercise prevents the obese and diabetic metabolic syndrome of the melanocortin‐4 receptor knockout mouse
Haskell‐Luevano, C., Schaub, J. W., Andreasen, A., Haskell, K. R., Moore, M. C., Koerper, L. M., Rouzaud, F., Baker, H. V., Millard, W. J., Walter, G., et al. (2009) · The FASEB Journal · doi:10.1096/fj.08-109686 · Cited by 72
“The leptin and insulin hormones signal in the hypothalamic neurons through the phosphatidylinositol 3-kinase pathway that is inhibited by phosphatase with tensin homology (Pten) (49, 50).”
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CNS-targets in control of energy and glucose homeostasis
Kleinridders, A., Könner, A. C., & Brüning, J. C. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2009.10.006 · Cited by 74
Dual role of the coactivator TORC2 in modulating hepatic glucose output and insulin signaling
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“Hepatic IRS2 expression is often reduced in mouse models of Type II diabetes, reflecting in part the inhibitory effects of hyperinsulinemia on expression of the IRS2 gene (Brady, 2004; White, 2003).”
Background
The IRS/PI3K/Akt signaling pathway mediates olanzapine-induced hepatic insulin resistance in male rats
Ren, L., Zhou, X., Huang, X., Wang, C., & Li, Y. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.12.015 · Cited by 71
The brown adipose cell: a model for understanding the molecular mechanisms of insulin resistance
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Insulin Signal Mimicry as a Mechanism for the Insulin-Like Effects of Vanadium
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“Once activated, IR-PTK can phosphorylate several cytosolic insulin receptor substrates (IRSs and Shc), which serve as docking sites for Src homology (SH)-2 domain-containing signaling molecules (23), triggering the activation of two key signaling pathways (Fig.”
Background
The Repression of IRS2 Gene by ATF3, a Stress-Inducible Gene, Contributes to Pancreatic β-Cell Apoptosis
Li, D., Yin, X. H., Zmuda, E. J., Wolford, C. C., Dong, X. C., White, M. F., & Hai, T. (2007) · Diabetes · doi:10.2337/db07-0717 · Cited by 67
“Although the IRS family of proteins includes IRS1–IRS6 and other proteins such as GAB1, GAB2, and CBL (2,3), the majority of the insulin action appears to be mediated by IRS1 and IRS2 (rev.”
Background
Cellular inflammatory responses: Novel insights for obesity and insulin resistance
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Insulin signaling and life span
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“Most, if not all, insulin signals are produced or modulated through tyrosine phosphorylation of IRS1 or its homolog IRS2 or other scaffold proteins [ 136 ].”
Background
Untitled work
(2008) · doi:10.1016/j.cmet.2008.06.010 · Cited by 67
“…of insulin (and IGF) receptors by (1) providing a juxtamembrane localiza- tion signal for PIP3 generation, (2) amplify- Cell Me ing the signal engendered by receptor autophosphorylation, and (3) engaging a panoply of substrates that account for the diverse actions of insulin (White, 2003).”
Background
A high-carbohydrate diet in the immediate postnatal life of rats induces adaptations predisposing to adult-onset obesity
Srinivasan, M., Mitrani, P., Sadhanandan, G., Dodds, C., Shbeir‐ElDika, S., Thamotharan, S., Ghanim, H., Dandona, P., Devaskar, S. U., & Patel, M. S. (2008) · Journal of Endocrinology · doi:10.1677/joe-08-0021 · Cited by 66
“Hormone binding to the IR results in rapid autophosphorylation of the receptor followed by tyrosine phosphorylation of IR substrate proteins, inducing an activation of the downstream pathways such as the MAPK and PI3K cascades (White 2003).”
Background
Molecular Profiling of Pancreatic Neuroendocrine Tumors in Sporadic and Von Hippel-Lindau Patients
Speisky, D., Ducès, A., Bièche, I., Rebours, V., Hammel, P. R., Sauvanet, A., Richard, S., Bédossa, P., Vidaud, M., Murat, A., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-2759 · Cited by 68
Effects of insulin on the skin: possible healing benefits for diabetic foot ulcers
Emanuelli, T., Burgeiro, A., & Carvalho, E. (2016) · Archives of Dermatological Research · doi:10.1007/s00403-016-1686-z · Cited by 67
“Besides regulating glucose and lipid metabolism, insulin is involved in processes including protein synthesis, mitochondrial biogenesis, growth, autophagy, proliferation, differentiation, and migration [153].”
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Amino Acid Sensing via General Control Nonderepressible-2 Kinase and Immunological Programming
Battu, S., Minhas, G., Mishra, A., & Khan, N. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01719 · Cited by 69
“mTOR being a central regulator of amino acid and insulin signaling (97, 98), under amino acid abundance, it phosphorylates IRS1 (at serine 307) and inhibits the downstream insulin signaling (99, 100).”
Background
Synergistic activation of the insulin receptor via two distinct sites
Li, J., Park, J., Mayer, J. P., Webb, K. J., Uchikawa, E., Wu, J., Liu, S., Zhang, X., Stowell, M. H. B., Choi, E., et al. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00750-6 · Cited by 65
Potential health concerns of dietary phosphorus: cancer, obesity, and hypertension
Anderson, J. J. B. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12208 · Cited by 66
Energy balance, insulin‐related genes and risk of colon and rectal cancer
Slattery, M. L., Murtaugh, M. A., Caan, B. J., Ma, K.-N., Neuhausen, S. L., & Samowitz, W. S. (2005) · International Journal of Cancer · doi:10.1002/ijc.20843 · Cited by 62
Therapeutic neovascularization for coronary disease: current state and future prospects
Lassaletta, A. D., Chu, L. M., & Sellke, F. W. (2011) · Basic Research in Cardiology · doi:10.1007/s00395-011-0200-1 · Cited by 64
“Like VEGF, insulin has a tyrosine kinase receptor and shares many downstream components with the VEGF angiogenic pathway [17, 27, 93, 106].”
Background
IRS2 Signaling in LepR-b Neurons Suppresses FoxO1 to Control Energy Balance Independently of Leptin Action
Sadagurski, M., Leshan, R. L., Patterson, C. M., Rozzo, A., Kuznetsova, A., Skorupski, J. C., Jones, J. C., DePinho, R. A., Myers, M. G., & White, M. F. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.04.011 · Cited by 66
Global Assessment of Regulation of Phosphorylation of Insulin Receptor Substrate-1 by Insulin In Vivo in Human Muscle
Yi, Z., Langlais, P. R., Filippis, E. A. D., Luo, M., Flynn, C. R., Schroeder, S., Weintraub, S. T., Mapes, R., & Mandarino, L. J. (2007) · Diabetes · doi:10.2337/db06-1355 · Cited by 65
“3 Introduction Through the efforts of a large number of investigators, many of the details of insulin signaling have been defined on a molecular level (1).”
Background
Insulin-signaling Pathway Regulates the Degradation of Amyloid β-protein via Astrocytes
Yamamoto, N., Ishikuro, R., Tanida, M., Suzuki, K., Ikeda‐Matsuo, Y., & Sobue, K. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.06.018 · Cited by 65
Central amygdala nucleus (Ce) gene expression linked to increased trait-like Ce metabolism and anxious temperament in young primates
Fox, A. S., Oler, J. A., Shelton, S. E., Nanda, S. A., Davidson, R. J., Roseboom, P. H., & Kalin, N. H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206723109 · Cited by 57
“In the periphery, IRS2 regulates insulin sensitivity and in the brain IRS2 impacts multiple functions including reward (58), memory (59, 60), and energy homeostasis (61, 62).”
Background
Decreased osteoclastogenesis and high bone mass in mice with impaired insulin clearance due to liver-specific inactivation to CEACAM1
Huang, S., Kaw, M., Harris, M., Ebraheim, N. A., McInerney, M. F., Najjar, S. M., & Lecka‐Czernik, B. (2010) · Bone · doi:10.1016/j.bone.2009.12.020 · Cited by 63
“Insulin action on bone may involve direct signaling through the insulin receptor, activation of bone anabolic IGF-1 signaling by binding to IGF-1 receptor, or synergistic effects with other anabolic agents such as parathyroid hormone (PTH) [21,24].”
Knockdown of TRPC3 with siRNA coupled to carbon nanotubes results in decreased insulin‐mediated glucose uptake in adult skeletal muscle cells
Lanner, J. T., Bruton, J. D., Assefaw‐Redda, Y., Andronache, Z., Zhang, S., Severa, D., Zhang, Z., Melzer, W., Zhang, S., Katz, A., et al. (2009) · The FASEB Journal · doi:10.1096/fj.08-116814 · Cited by 62
The Reciprocal Stability of FOXO1 and IRS2 Creates a Regulatory Circuit that Controls Insulin Signaling
Guo, S., Dunn, S. L., & White, M. F. (2006) · Molecular Endocrinology · doi:10.1210/me.2006-0092 · Cited by 64
“Type 2 diabetes emerges when nutrient homeostasis is dysregulated by peripheral insulin resistance and pancreatic -cell failure (1, 39).”
Background
Depletion of Mitochondrial DNA Causes Impaired Glucose Utilization and Insulin Resistance in L6 GLUT4myc Myocytes
Park, S. Y., Choi, G. H., Choi, H. I., Ryu, J., Jung, C. Y., & Lee, W. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m409399200 · Cited by 61
Insulin mediated novel therapies for the treatment of Alzheimer's disease
Dubey, S. K., Lakshmi, K. K., Krishna, K. V., Agrawal, M., Singhvi, G., Saha, R. N., Saraf, S., Saraf, S., Shukla, R., & Alexander, A. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117540 · Cited by 62
Type 2 Diabetes (T2DM) and Parkinson’s Disease (PD): a Mechanistic Approach
Sabari, S. S., Balasubramani, K., Iyer, M., Babu, H. W. S., Venkatesan, D., Gopalakrishnan, A. V., Narayanaswamy, A., Kumar, N. S., & Vellingiri, B. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03359-y · Cited by 64
“Therefore, understanding the role of insulin and its signalling pathway is essential to investigate, in T2DM and PD [20].”
Background
Genetic Inactivation of Pyruvate Dehydrogenase Kinases Improves Hepatic Insulin Resistance Induced Diabetes
Tao, R., Xiong, X., Harris, R. A., White, M. F., & Dong, X. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071997 · Cited by 60
“Insulin receptor substrates (Irs) play an essential role in the insulin signal transduction through a direct mediation of insulin receptor activities [19].”
Background
Insulin Therapy for Gestational Diabetes Mellitus Does Not Fully Protect Offspring From Diet-Induced Metabolic Disorders
Zhu, H., Chen, B., Cheng, Y., Zhou, Y. X., Yan, Y., Luo, Q., Jiang, Y., Sheng, J., Ding, G., & Huang, H. (2019) · Diabetes · doi:10.2337/db18-1151 · Cited by 63
“Defective insulin secretion and action are twomajor results of diabetes (49,50).”
Background
IRS‐2 branch of IGF‐1 receptor signaling is essential for appropriate timing of myelination
Freude, S., Leeser, U., Müller, M., Hettich, M. M., Udelhoven, M., Schilbach, K., Tobe, K., Kadowaki, T., Köhler, C. N., Schröder, H., et al. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05631.x · Cited by 59
Insulin Resistance in Non-Obese Subjects Is Associated with Activation of the JNK Pathway and Impaired Insulin Signaling in Skeletal Muscle
Masharani, U. B., Maddux, B. A., Li, X., Sakkas, G. K., Mulligan, K. M., Schambelan, M., Goldfine, I. D., & YOUNGREN, J. F. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019878 · Cited by 62
“[8,9].”
Involvement of insulin receptor substrates in cognitive impairment and Alzheimer’s disease
Taguchi, A., Tanokashira, D., & Fukuokaya, W. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.253535 · Cited by 57
“…the biological effects of insulin/IGF1 signaling (IIS) on glucose or lipid metabolism are mediated via insulin receptor substrate (IRS)1 and IRS2 (White, 2003) whereas the tyrosine kinase activation of IR/IGF1R stimulates the phosphorylation of other scaffold proteins such as SH2B, GABs, DOCKs,…”
Nutritional approaches for managing obesity-associated metabolic diseases
Botchlett, R. E., Woo, S., Liu, M., Pei, Y., Guo, X., Li, H., & Wu, C. (2017) · Journal of Endocrinology · doi:10.1530/joe-16-0580 · Cited by 65
“Inflammation/proinflammatory cytokines are widely known to interfere with the insulin signaling pathway, including suppression/interference of IRS-1 and IRS-2 (White 2003).”
Background
Therapeutic Mechanisms of Herbal Medicines Against Insulin Resistance: A Review
Li, J., Bai, L., Wei, F., Zhao, J., Wang, D., Xiao, Y., Yan, W., & Wei, J. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00661 · Cited by 61
“Insulin activates the PI3K/Akt pathway, which is responsible for glucose uptake, and the MAPK pathway, which is critical for IR (Saltiel and Kahn, 2001).”
BackgroundInfluential

Authors: White, M. F.
Affiliations: Joslin Diabetes Center (US)
Corresponding author: White, Morris F.
ORCID: White, Morris F.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2003-12-05
Volume: 302
Issue: 5651
Pages: 1710-1711
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1092952
OpenAlex: W2115177689
Cited by: 733
References: 19
Citations by year: 2026: 7 · 2025: 17 · 2024: 13 · 2023: 21 · 2022: 24 · 2021: 35 · 2020: 32 · 2019: 30 · 2018: 36 · 2017: 35 · 2016: 39 · 2015: 47 · 2014: 35 · 2013: 39 · 2012: 50
FWCI: 9.65
Type: journal article
Language: en
Open access: closed
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Keywords: insulin signaling, insulin resistance, obesity, type 2 diabetes, pancreatic beta-cell failure, chronic inflammation, insulin receptor substrate 2
MeSH terms: Animals, Diabetes Mellitus, Diabetes Mellitus, Type 1, Diabetes Mellitus, Type 2, Humans, Inflammation, Insulin, Insulin Resistance, Islets of Langerhans, Models, Biological, Obesity, Phosphoproteins, Phosphorylation, Receptor, Insulin, Somatomedins, Signal Transduction, Cytokines, Intracellular Signaling Peptides and Proteins, Mice, Insulin Receptor Substrate Proteins

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Insulin Signaling in Health and Disease

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