Glucose transporters in rat peripheral nerve: Paranodal expression of GLUT1 and GLUT3

doi:10.1016/S0026-0495(96)90174-2

Metabolism

Volume 45, Issue 12, December 1996, Pages 1466-1473

https://doi.org/10.1016/S0026-0495(96)90174-2 Get rights and content

Abstract

Peripheral nerve depends on glucose oxidation to energize the repolarization of excitable axonal membranes following impulse conduction, hence requiring high-energy demands by the axon at the node of Ranvier. To enter the axon at this site, glucose must be transported from the endoneurial space across Schwann cell plasma membranes and the axolemma. Such transport is likely to be mediated by facilitative glucose transporters. Although immunohistochemical studies of peripheral nerves have detected high levels of the transporter GLUT1 in endoneurial capillaries and perineurium, localization of glucose transporters to Schwann cells or peripheral axons in vivo has not been documented. In this study, we demonstrate that the GLUT1 transporter is expressed in the plasma membrane and cytoplasm of myelinating Schwann cells around the nodes of Ranvier and in the Schmidt-Lanterman incisures, making them potential sites of transcellular glucose transport. No GLUT1 was detected in axonal membranes. GLUT3 mRNA was expressed only at low levels, but GLUT3 polypeptide was barely detected by immunocytochemistry or immunoblotting in peripheral nerve from young adult rats. However, in 13-month-old rats, GLUT3 polypeptide was present in myelinated fibers, endoneurial capillaries, and perineurium. In myelinated fibers, GLUT3 appeared to be preferentially expressed in the paranodal regions of Schwann cells and nodal axons, but was also present in the internodal aspects of these structures. The results of the present study suggest that both Schwann cell GLUT1 and axonal and Schwann cell GLUT3 are involved in the transport of glucose into the metabolically active regions of peripheral axons.

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^☆: Supported by National Institutes of Health Grants No. RO1-DK38304 (D.A.G.), and RO1-DK43884 (A.A.ES.), by the Michigan Diabetes Research and Training Center (P60-DK20572, D.A.G. and A.A.F.S.) and Image Analysis and Molecular Biology Core Laboratories, and the University of Michigan Multipurpose Arthritis Center Molecular Biology Core Laboratory.

^∗: Present address: P.M., Universita Cattolica del Sacro Cuore, 1st Medicina Interna-Servizio di Diabetologia, 00168 Roma, Italy.

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Glucose transporters in rat peripheral nerve: Paranodal expression of GLUT1 and GLUT3☆

Abstract

Brain Res

Kidney Int

J Biol Chem

FEBS Lett

Brain Res

J Biol Chem

Trends Biochem Sci

In vitro studies of substrates and energy production and the effect of insulin on glucose utilization in the neural components of peripheral nerve

Diabetes

The oxygen consumption of mammalian non-myelinated nerve fibers at rest and during activity

J Physiol (Lond)

Microscopic anatomy and function of the connective tissue components of peripheral nerve

The permeability of perineurium to peroxidase after early undernutrition

Acta Neuropathol

Compartments and barriers in the sciatic nerve of the rabbit

Brain Res

Facilitated transport of glucose from blood into peripheral nerve

J Neurochem

The blood-nerve barrier is rich in glucose transporter

J Neurocytol

Glucose transporters of rat peripheral nerve: Differential expression of GLUT-1 gene by Schwann cells and perineurial cells in vivo and in vitro

Diabetes

Expression of glucose transporter 1 in adult and developing human peripheral nerve

Diabetologia

Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain

J Neurocytol

Rows of dimetric particles within the axolemma and juxtaposed particles within glia, incorporated into a new model for the paranodal glial-axonal junction at the node of Ranvier

J Cell Biol

“Axo-glial dysjunction”: A novel structural lesion that accounts for poorly reversible slowing of nerve conduction in the spontaneously diabetic BB-rat

J Clin Invest