Positive and negative regulation of glucose uptake by hyperosmotic stress

doi:10.1016/S1262-3636(07)70071-X

Diabetes & Metabolism

Volume 29, Issue 6, December 2003, Pages 566-575

https://doi.org/10.1016/S1262-3636(07)70071-X Get rights and content

Summary

This review will provide insight on the current understanding of the intracellular signaling mechanisms by which hyperosmolarity mimics insulin responses such as Glut 4 translocation and glucose transport but also antagonizes insulin effects. Glucose uptake induced by insulin is largely dependent on the PI 3-kinase/PKB pathway. In both adipocyte and muscle cells, hyperosmolarity promotes glucose uptake by multiple mechanisms which do not require PI 3-kinase/PKB pathway but are dependent on the cell type. In muscle, osmotic stress induces glucose uptake by stimulation of AMP-Kinase and/or inhibition of Glut 4 endocytosis. In adipocytes, activation of Gab1-dependent signaling pathway plays an important role in osmotic stress-mediated glucose uptake. Apart of its insulin-like effects, hyperosmolarity can lead to cellular insulin resistance mediated by both prevention of PKB activation and inhibition of the Insulin Receptor Substrate-1 (IRS1) function. Serine phosphorylation and degradation of IRS1 negatively regulate its functions. Understanding how osmotic stress induces glucose transport or mediates insulin resistance may provide novel targets for strategies to enhance glucose transport or to prevent insulin resistance.

Résumé

Régulation positive et négative du transport du glucose par le stress hyperosmolaire

Le stress hyperosmolaire a un double effet: il mime l'effet de l'insuline sur la translocation des transporteurs de glucose Glut 4 et sur le transport du glucose, mais il inhibe aussi les effets de l'insuline sur ces mêmes paramètres. Cette revue décrit les mécanismes intracellulaires par lesquels ces effets s'exercent. La captation de glucose induite par l'insuline est largement dépendante de la stimulation de la voie PI 3-kinase/PKB dans le muscle et l'adipocyte. Si l'hyperosmolarité induit également la captation de glucose, cet effet s'exerce par de multiples mécanismes qui sont indépendants de cette voie PI 3-kinase/PKB et qui diffèrent dans le muscle squelettique et dans l'adipocyte. Dans les lignées musculaires, l'augmentation du transport de glucose en réponse à un stress hyperosmolaire implique l'activation de l'AMP-Kinase et également une inhibition de l'endocytose des transporteurs de glucose Glut 4. Dans les lignées adipocytaires, c'est l'activation d'une voie dépendante de Gab-1 qui explique l'effet de l'hyperosmolarité. Indépendamment de ses effets insulinomimétiques, l'hyperosmolarité provoque également une insulinorésistance au niveau cellulaire qui s'explique d'une part par une désactivation de la PKB et d'autre part par une inhibition de la fonction d'IRS1. Cette rétrorégulation du signal insulinique est due à court terme à une phosphorylation d'IRS1 sur des résidus sérine et à long terme à une dégradation d'IRS1, deux processus que l'on retrouve dans l'insulinorésistance. Une meilleure connaissance des voies stimulées par le stress hyperosmolaire pour augmenter le transport de glucose ainsi que des mécanismes mis en jeu dans l'apparition de l'insulinorésistance peut fournir de nouvelles pistes et cibles thérapeutiques du diabète et de l'insulinorésistance.

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ReviewPositive and negative regulation of glucose uptake by hyperosmotic stress

Summary

Résumé

Insulin signalling and the regulation of glucose and lipid metabolism

Nature

Insulin signaling pathways in time and space

Trends Cell Biol

Molecular mechanisms of insulin-stimulated glucose uptake in adipocytes

Diabetes Metab

Insulin regulation of glucose uptake: a complex interplay of intracellular signalling pathways

Diabetologia

Intracellular signaling in contracting skeletal muscle

J Appl Physiol

Hypoxia stimulates glucose transport in insulin-resistant human skeletal muscle

Diabetes

Stimulation of glucose transport in skeletal muscle by hypoxia

J Appl Physiol

A role for AMP – activated protein kinase in contraction – and hypoxia-regulated glucose transport in skeletal muscle

Mol Cell

Mechanisms of adaptation of glucose transporters to changes in the oxidative chain of muscle and fat cells

Am J Physiol

Rapid stimulation of glucose transport by mitochondrial uncoupling depends in part on cytosolic Ca2+ and cPKC

Am J Physiol

Phosphatidylinositol 3-kinase and the actin network are not required for the stimulation of glucose transport caused by mitochondrial uncoupling: comparison with insulin action

Biochem J

Cellular mechanism of metformin action involves glucose transporter translocation from an intracellular pool to the plasma membrane in L6 muscle cells

Endocrinology

Role of AMP-activated protein kinase in mechanism of metformin action

J Clin Invest

Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes

Diabetes

Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase

Nat Med

Osmotic shock stimulates GLUT4 translocation in 3T3L1 adipocytes by a novel tyrosine kinase pathway

J Biol Chem

Phosphoinositide 3-kinase is required for insulin-induced but not for growth hormone- or hyperosmolarity-induced glucose uptake in 3T3-L1 adipocytes

Mol Endocrinol

The osmotic shock-induced glucose transport pathway in 3T3-L1 adipocytes is mediated by Gab-1 and requires Gab-1-associated phosphatidylinositol 3-kinase activity for full activation

J Biol Chem

Activation of glucose transport by AMP-activated protein kinase via stimulation of nitric oxide synthase

Diabetes

A Crk-II/TC10 signaling pathway is required for osmotic shock-stimulated glucose transport

J Biol Chem

Inactivation and dephosphorylation of protein kinase Bα (PKBα) promoted by hyperosmotic stress

EMBO J

Osmotic shock inhibits insulin signaling by maintaining Akt/protein kinase B in an inactive dephosphorylated state

Mol Cell Biol

Stimulation of MAPK cascades by insulin and osmotic shock: lack of an involvement of p38 mitogen-activated protein kinase in glucose transport in 3T3-L1 adipocytes

Diabetes

Hyperosmotic shock induces both activation and translocation of glucose transporters in mammalian cells

Pflugers Arch

Hyperosmotic stress inhibits IRS1 function by distinct mechanisms in 3T3-L1 adipocytes

J Biol Chem

Hyperosmolarity reduces GLUT4 endocytosis and increases its exocytosis from a VAMP2-independent pool in L6 muscle cells

J Biol Chem

Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism

Diabetes

Characterization of the role of the AMP-activated protein kinase in the stimulation of glucose transport in skeletal muscle cells

Biochem J

Activation of the ERK pathway and atypical protein kinase C isoforms in exercise – and aminoimidazole-4-carboxamide-1-beta-D-riboside (AICAR) – stimulated glucose transport

J Biol Chem

Sorbitol activates atypical protein kinase C and GLUT4 glucose transporter translocation/glucose transport through proline-rich tyrosine kinase-2, the extracellular signal-regulated kinase pathway and phospholipase D

Biochem J

Function and dysfunction of aPKC isoforms for glucose transport in insulin-sensitive and insulin-resistant states

Am J Physiol Endocrinol Metab

Activation of AMPK is essential for AICAR-induced glucose uptake by skeletal muscle but not adipocytes

Am J Physiol Endocrinol Metab

5-aminoimidazole-4-carboxamide ribonucleoside (AICAR) inhibits insulin-stimulated glucose transport in 3T3-L1 adipocytes

Diabetes

A GRB2-associated docking protein in EGF- and insulin-receptor signalling

Nature

Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis

Nature

Maintenance of genomic integrity in mammalian kidney cells exposed to hyperosmotic stress

Comp Biochem Physiol A Mol Integr Physiol

Crk family adaptors-signalling complex formation and biological roles

Oncogene

Distinct cellular effects and interactions of the Rho-family GTPase TC10

Curr Biol

Review
Positive and negative regulation of glucose uptake by hyperosmotic stress

Rapid stimulation of glucose transport by mitochondrial uncoupling depends in part on cytosolic Ca2⁺ and cPKC