Cited by 343Liver Disease Diagnosis and TreatmentMetabolism, Diabetes, and CancerDiabetes, Cardiovascular Risks, and Lipoproteins

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Resolving the Paradox of Hepatic Insulin Resistance

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Santoleri, Dominic, Titchenell, Paul M.·2019·Cellular and Molecular Gastroenterology and Hepatology

DOI 10.1016/j.jcmgh.2018.10.016PMC PMC6369222

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Abstract

Insulin resistance is associated with numerous metabolic disorders, such as obesity and type II diabetes, that currently plague our society. Although insulin normally promotes anabolic metabolism in the liver by increasing glucose consumption and lipid synthesis, insulin-resistant individuals fail to inhibit hepatic glucose production and paradoxically have increased liver lipid synthesis, leading to hyperglycemia and hypertriglyceridemia. Here, we detail the intrahepatic and extrahepatic pathways mediating insulin's control of glucose and lipid metabolism. We propose that the interplay between both of these pathways controls insulin signaling and that mis-regulation between the 2 results in the paradoxic effects seen in the insulin-resistant liver instead of the commonly proposed deficiencies in particular branches of only the direct hepatic pathway.

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Figure 1 PI3K/Akt signaling in hepatocytes. Insulin binds to and activates the insulin receptor on the liver surface after a meal. After activation, the receptor recruits and activates IRS, which then activates PI3K. PI3K phosphorylates the signaling lipid molecule PIP2 into PIP3 in a process that is opposed by PTEN. PIP3 activates 3-phosphoinositide-dependent protein kinase 1 (PDK1), which phosphorylates Akt at Thr308. To fully activate Akt, mTORC2 also must phosphorylate it at Ser473. From Akt, different pathways for controlling glucose and lipid homeostasis branch out. Glycogen synthesis is induced through Akt inhibition of GSK3. In addition, Akt can promote glycogen synthesis in a manner independent of GSK3, such as activation of GYS2 by glucose-6-phosphate (G6P). Akt inhibition of TSC activates mTORC1, which in turn activates the lipogenic gene program through activation of SREBP1c and Gck, which phosphorylates glucose to G6P, which feeds into glycolysis and glycogen synthesis. In addition, G6P activates ChREBP, which activates lipogenesis along with SREBP1c. Akt inhibits FoxO1, resulting in an inhibition of gluconeogenesis by suppressing expressing of the proteins glucose-6-phosphatase (G6pc) and Pck1. Externally, FFAs can promote gluconeogenesis and contribute to insulin resistance by being taken up by the liver and converted to Acetyl-CoA, which activates pyruvate carboxylase.CC BY-NC-ND · PubMed Central

Figure 2 Indirect insulin effects on the liver. Insulin can block gluconeogenesis and glycogenolysis in the liver through several indirect pathways. Its secretion from the pancreatic β cells inhibits glucagon secretion in neighboring α cells. In the adipose tissue, insulin inhibits lipolysis, which reduces the levels of circulating FFAs, which promote glucose production. Finally, insulin signaling in the hypothalamus and central nervous system acts on Agrp neurons to signal through the hepatic vagus branch to inhibit HGP.CC BY-NC-ND · PubMed Central

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1 retracted

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Background
Metabolic Derangement in Non-Alcoholic Fatty Liver Disease: Opportunities for Early Diagnostic and Prognostic Markers
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Preliminary results of dulaglutide treatment in patients with non-alcoholic fatty liver disease (DEMOS study)
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“Основными последствиями этих процессов выступают гипергликемия, гипертриглицеридемия и усиленная аккумуляция жира в гепатоцитах [6].”
Hepatocyte androgen receptor in females mediates androgen-induced hepatocellular glucose mishandling and systemic insulin resistancePreprint
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“The liver plays a major role in 74 determining systemic insulin resistance and metabolism[22] and its function is altered in women[23] and mice[24] 75 with hyperandrogenemia.”
Background
Investigation of the potential connections between NAFLD-associated Alzheimer's disease: bioinformatics analysis of shared genesPreprint
Bhattacharya, I., Bhattacharya, T., Sahu, A., Das, P., Sarkar, S., Prasanna, V. S., Sreed, R., Ravichandiran, V., & Arumugam, S. (2024) · Research Square · doi:10.21203/rs.3.rs-4667019/v1 · Cited by 2
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Polyethylene glycol loxenatide modulates lipid metabolism and insulin resistance through lncRNA steroid receptor RNA activator/cellular nucleic acid binding protein/Rho‐associated coiled‐coil kinase 2 axis in type 2 diabetes mellitus
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“Insulin-resistant individuals fail to repress hepatic glucose production while increasing lipid synthesis, resulting in hyperglycemia and hypertriglyceridemia 7 .”
Analysis of Exosomal miRNA and Hepatic mRNA Expression in the Dysregulation of Insulin Action in Perimenopausal Mice
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“Several lines of evidence have demonstrated that the impairment of this biological process has adverse e ﬀ ects on hepatic insulin resistance, increasing the risk of diabetes or other metabolic disease [59].”
Macrophage Plg-RKT expression promotes diet-induced obesity and metabolic dysfunction-associated steatotic liver disease
Miles, L. A., Bai, H., Chakrabarty, S., Baik, N., Zhang, Y., Parmer, R. J., & Samad, F. (2025) · Journal of Thrombosis and Haemostasis · doi:10.1016/j.jtha.2025.09.020 · Cited by 1
Transkingdom network analysis reveals the dominant role of ileal microbiota in host metabolism over colonic microbiota in diet-induced obesity
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“The liver plays a central role in glucose/lipid metabolism (11).”
The Prickly Solution to Metabolic Syndrome: A Multitarget View on the Opuntia ficus-indica Fruit Phytocomplex
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“Concurrently, hepatic IR fails to suppress gluconeogenesis and dysregulates lipid synthesis, promoting metabolic in-flexibility [16].”
Emerging Approaches for the Treatment of Metabolic Dysfunction-Associated Steatotic Liver Disease: The Application of Nanomedicines
Shi, T., Yue, H., Wang, W., Gao, Y., Xu, S., Gao, J., & Yin, C. (2026) · International Journal of Nanomedicine · doi:10.2147/ijn.s603396 · Cited by 1
“The liver serves as a pivotal metabolic organ alongside skeletal muscle and adipose tissue 114 and is regulated primarily by the insulin signaling pathway IRS/PI3K/AKT/FoxO1, 115 which also modulates the cell cycle, growth, and apoptosis.”
Hepatic Lipoprotein Production, Cardiometabolic Phenotypes, and Subtypes of Steatotic Liver Disease
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Nobiletin ameliorates hepatic insulin resistance by modulating the gut–liver axis
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Insulin resistance in the 21st century: new takes on an old problem—2025 Diabetes, Diabetes Care, and Diabetologia Expert Forum
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Metabolic dysfunction-associated fatty liver disease from definition to complications
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Pathophysiology of Type 2 Diabetes: A General Overview of Glucose and Insulin Homeostasis
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Analyze the Efficacy of Silymarin in Treating Newly Diagnosed Cases of Type 2 Diabetes Mellitus by Contrasting its Effects on Glycemic Control and Insulin Resistance
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Effects of marine phenolics on diabetes, obesity, and metabolic syndrome
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Complexity in Hepatic Insulin Resistance – Unraveling the Role of Ubiquitin-Specific Protease 14 in Protein Homeostasis of Metabolic Transcription Factors
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FETAL METABOLIC PROGRAMMING IN THE ETIOLOGY OF POLYCYSTIC OVARIAN SYNDROME
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GRg1 Ameliorates Insulin Resistance Through Activation of the PI3K/AKT/GSK-3β Pathway in HepG2 Cells
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“The liver, which is responsible for glucose synthesis and metabolism, and hepatic insulin resistance, characterized by suppressed insulin-dependent cellular glucose consumption (Santoleri & Titchenell, 2019), plays a central role in insulin resistance (Jia et al., 2020; Petersen & Shulman, 2018).”
Background
FACTORES DE RIESGO IMPLICADOS EN LA RESISTENCIA A LA INSULINA: UN ANÁLISIS BIBLIOGRÁFICO.
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Gene Expression Pattern of PI3K/AKT Pathway Based on Insulin Resistance and Vitamin D Toward the Understanding of T2DM PathogenesisPreprint
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Heterocyclic amines and arylamine N-acetyltransferase 2 polymorphism in pathogenesis of insulin resistance.
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Identification of glucose and insulin patterns during A 5-H glucose tolerance test and association with cardiometabolic risk factors
Crespo-Morfin, P. B., Aguilar-Salinas, C. A., Almeda‐Valdés, P., Alfaro-Pastrana, R., Bello‐Chavolla, O. Y., Cano-Castillo, J., Gomez-Perez, F. J., & Cruz‐Bautista, I. (2022) · Revista de investigaci�n Cl�nica · doi:10.24875/ric.22000039
“Hepatic insulin resistance can be present in fasting conditions and during the first minutes of an OGTT 30 .”
Background
Correlation of Prediabetes and Metabolic Syndrome in Rural Population of Dinanath
Gulzar, A., Rashid, N., Siddiqi, M. F., Arif, Z., Ali, R., & Uddin, M. A. (2022) · Pakistan Journal of Medical and Health Sciences · doi:10.53350/pjmhs22166232
FBP1 is a nonenzymatic safety valve that curtails AKT activation to prevent insulin hyperresponsivenessPreprint
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Hepatic Lipid Droplet-Associated Proteome Changes Distinguish Dietary-Induced Fatty Liver from Insulin Resistance in Male MicePreprint
Woerkom, A. V., Harney, D. J., Nagarajan, S. R., Hakeem-Sanni, M. F., Lin, J., Hooke, M., Pulpitel, T., Cooney, G., Larance, M., Saunders, D., et al. (2023) · bioRxiv · doi:10.1101/2023.03.09.531813
Leptin and the Intersection of Cardiovascular Disease, Metabolism, and Adipose Tissue
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Endocrine
Cywes, R., Kajee, H., Wellington, N., Cucuzzella, M. T., Riley, K., Isaacs, D. M., Pataguana, N., Lake, I., Rauch, L., McKelvey, S., et al. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-821617-0.00010-3
Bioenergetic and redox signaling in hepatic steatosis models: Integrative analysis of nutritional, hormonal, and inflammatory stimuli
Kakimoto, P. A. (2021) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.46.2021.tde-10082023-115406
Study of Lipid Profiles Levels and Some Parameters of Glucose Monitoring As Predictive Indicators of Recurrent MI in Patients Undergoing Elective Percutaneous Coronary Intervention (PCI)
Jasim, R. H., & Lefta, A. A. (2023) · Journal of Kufa for Chemical Sciences · doi:10.36329/jkcm/2022/v2.i9.13287
Resistencia a la insulina, hepatopatía grasa y su asociación con las proteínas acarreadoras de IGF
Guzmán, C., Mendoza-Domínguez, G., & Bautista-Ubaldo, M. G. (2023) · Revista Mexicana de Endocrinología Metabolismo y Nutrición · doi:10.24875/rme.22000056
Modelling of postprandial glucose and insulin dynamics
van Sloun, B. (2023) · doi:10.26481/dis.20231027bs
The Correlations Between Level of Zonulin, Leptin and Anthropometric Indicators in Patients with Metabolic-associated Fatty Liver Disease in Combination with Type 2 Diabetes mellitus
Didyk, O. K., & Chernyavskyi, V. V. (2023) · Family medicine European practices · doi:10.30841/2786-720x.3.2023.289347
Multi-layered proteomics identifies insulin-induced upregulation of the EphA2 receptor via the ERK pathway and dependent on low IGF1R levelPreprint
Jørgensen, S. H., Emdal, K. B., Pedersen, A.-K., Axelsen, L. N., Kildegaard, H. F., Damozay, D., Pedersen, T. Å., Grønborg, M., Slaaby, R., Nielsen, P. K., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.14.571674
Akdeniz diyeti ve Non alkolik yağlı karaciğer hastalığı
Bektaş, A., & Ulusoy, M. (2023) · Troia Medical Journal · doi:10.55665/troiamedj.1363991
Additional file 1 of Transcriptome sequencing and metabolome analysis reveal the metabolic reprogramming of partial hepatectomy and extended hepatectomy
Li, Z., Peng, B., Chen, S., Li, J., Hu, K., Liao, L., Xie, Q., Yao, M., Liang, L., Tomlinson, S., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24104254
Additional file 1 of Integrated analysis of differentially expressed long noncoding RNAs and mRNAs associated with high-fat diet-induced hepatic insulin resistance in mice
Zhou, Z., Zhao, X., Chen, L., Li, Y., Chen, Z., Wang, Y., Zhou, Z., & Chu, X. (2020) · Figshare · doi:10.6084/m9.figshare.12511466
Additional file 3 of Transcriptome sequencing and metabolome analysis reveal the metabolic reprogramming of partial hepatectomy and extended hepatectomy
Li, Z., Peng, B., Chen, S., Li, J., Hu, K., Liao, L., Xie, Q., Yao, M., Liang, L., Tomlinson, S., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24104260
Additional file 5 of Transcriptome sequencing and metabolome analysis reveal the metabolic reprogramming of partial hepatectomy and extended hepatectomy
Li, Z., Peng, B., Chen, S., Li, J., Hu, K., Liao, L., Xie, Q., Yao, M., Liang, L., Tomlinson, S., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24104266
Additional file 2 of Integrated analysis of differentially expressed long noncoding RNAs and mRNAs associated with high-fat diet-induced hepatic insulin resistance in mice
Zhou, Z., Zhao, X., Chen, L., Li, Y., Chen, Z., Wang, Y., Zhou, Z., & Chu, X. (2020) · Figshare · doi:10.6084/m9.figshare.12511472
Additional file 11 of Transcriptome sequencing and metabolome analysis reveal the metabolic reprogramming of partial hepatectomy and extended hepatectomy
Li, Z., Peng, B., Chen, S., Li, J., Hu, K., Liao, L., Xie, Q., Yao, M., Liang, L., Tomlinson, S., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24104284
Additional file 5 of Integrated analysis of differentially expressed long noncoding RNAs and mRNAs associated with high-fat diet-induced hepatic insulin resistance in mice
Zhou, Z., Zhao, X., Chen, L., Li, Y., Chen, Z., Wang, Y., Zhou, Z., & Chu, X. (2020) · Figshare · doi:10.6084/m9.figshare.12511493
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Metabolic-Dysfunction-Associated Fatty Liver Disease and Hepatic Insulin Resistance: A Type 2 Diabetes Mellitus-like in the liver - A Systematic ReviewPreprint
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Mathematical Modelling of MASLD ‐ Towards Digital Twins in Liver Disease
Simonsson, C. (2024) · Linköping studies in science and technology. Dissertations · doi:10.3384/9789180757348
Effects of biomaterial-incubated pancreatic islet transplantation on liver dysfunction of STZ-diabetic ratsPreprint
Nemati, M., Nemati, F., Hosseinzadeh, Z., & Ghaffari, M. K. (2024) · Research Square · doi:10.21203/rs.3.rs-5434832/v1
Intergrated Compositional Analysis, Pharmacodynamics and in Vivo Pharmacokinetics of Guizhi-Huangqi Herb Pair in Diabetic Liver InjuryPreprint
Jia, N., Li, J., Cui, Y. M., Li, Y., Li, X., & Chu, X. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5208281

Authors: Santoleri, D., & Titchenell, P. M.
Affiliations: University of Pennsylvania (US)
Corresponding author: Titchenell, Paul M.
ORCID: Santoleri, Dominic
Titchenell, Paul M.
Venue: Cellular and Molecular Gastroenterology and Hepatology
Publisher: Elsevier BV
Published: 2019
Volume: 7
Issue: 2
Pages: 447-456
ISSN: 2352-345X (ISSN-L)
DOI: 10.1016/j.jcmgh.2018.10.016
PMC: PMC6369222
OpenAlex: W2899043265
Cited by: 336
References: 102
Citations by year: 2026: 35 · 2025: 57 · 2024: 61 · 2023: 63 · 2022: 51 · 2021: 40 · 2020: 24 · 2019: 5
FWCI: 2.57
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Cellular and Molecular Gastroenterology and Hepatology (publishedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institutes of Health (K01 DK111715, P30 DK19525)
Topics: Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
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
Keywords: hepatic insulin resistance, insulin signaling, hepatic glucose production, hepatic lipid synthesis, hypertriglyceridemia, hyperglycemia, type 2 diabetes, obesity, glucose metabolism, lipid metabolism
MeSH terms: Animals, Humans, Insulin, Insulin Resistance, Liver, Models, Biological, Signal Transduction, Lipid Metabolism

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Resolving the Paradox of Hepatic Insulin Resistance

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