Electric field-directed growth and branching of cultured frog nerves

effects of aminoglycosides and polycations

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29 Citations (Scopus)

Abstract

The direction and rate of earliest nerve growth are critical determinants of neuronal architecture. One extrinsic cue that influences these parameters is a small direct current electric field, although the underlying mechanisms are unclear. We have studied the orientation, rate of growth, and branching behavior of embryonic Xenopus spinal neurites exposed to aminoglycoside antibiotics, to raised external cations, to applied direct current electric fields, and to combinations of these treatments. Field-induced cathodal turning and cathodal branching of neurites were blocked by the aminoglycosides, by raised extracellular calcium ([Ca2+]0) and by raised extracellular magnesium ([Mg2+]0). Neomycin together with high external Ca2+, by contrast, induced a reversal in the polarity of turning and branching, with neurites reorienting and branching more frequently anodally. Aminoglycosides decreased neurite growth rates, and for neomycin this was partially reversed by high external Ca2+. Raised [Ca2+]0 alone but not raised [Mg2+]0 altered growth rates in a field-strength dependent manner. Modulation of membrane surface charge may underlie altered galvanotropic orientation and branching. Such an effect is insufficient to explain the changes in growth rates, which may result from additional perturbations to Ca2+ influx and inositol phospholipid metabolism.
Original languageEnglish
Pages (from-to)523-536
Number of pages14
JournalJournal of Neurobiology
Volume26
Issue number4
DOIs
Publication statusPublished - 1 Apr 1995

Fingerprint

Aminoglycosides
Anura
Neurites
Growth
Neomycin
Xenopus
Phosphatidylinositols
Magnesium
Cues
Cations
polycations
Anti-Bacterial Agents
Calcium
Membranes

Keywords

  • Animals
  • Anti-Bacterial Agents
  • Cations, Divalent
  • Cell Division
  • Cells, Cultured
  • Electromagnetic Fields
  • Membrane Potentials
  • Neomycin
  • Neurites
  • Spinal Cord
  • Xenopus laevis
  • Electrical field
  • Surface potential
  • neomycin
  • nerve branching
  • orientation

Cite this

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title = "Electric field-directed growth and branching of cultured frog nerves: effects of aminoglycosides and polycations",
abstract = "The direction and rate of earliest nerve growth are critical determinants of neuronal architecture. One extrinsic cue that influences these parameters is a small direct current electric field, although the underlying mechanisms are unclear. We have studied the orientation, rate of growth, and branching behavior of embryonic Xenopus spinal neurites exposed to aminoglycoside antibiotics, to raised external cations, to applied direct current electric fields, and to combinations of these treatments. Field-induced cathodal turning and cathodal branching of neurites were blocked by the aminoglycosides, by raised extracellular calcium ([Ca2+]0) and by raised extracellular magnesium ([Mg2+]0). Neomycin together with high external Ca2+, by contrast, induced a reversal in the polarity of turning and branching, with neurites reorienting and branching more frequently anodally. Aminoglycosides decreased neurite growth rates, and for neomycin this was partially reversed by high external Ca2+. Raised [Ca2+]0 alone but not raised [Mg2+]0 altered growth rates in a field-strength dependent manner. Modulation of membrane surface charge may underlie altered galvanotropic orientation and branching. Such an effect is insufficient to explain the changes in growth rates, which may result from additional perturbations to Ca2+ influx and inositol phospholipid metabolism.",
keywords = "Animals, Anti-Bacterial Agents, Cations, Divalent, Cell Division, Cells, Cultured, Electromagnetic Fields, Membrane Potentials, Neomycin, Neurites, Spinal Cord, Xenopus laevis, Electrical field, Surface potential, neomycin, nerve branching, orientation",
author = "Lynda Erskine and R Stewart and McCaig, {Colin Darnley}",
year = "1995",
month = "4",
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journal = "Journal of Neurobiology",
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TY - JOUR

T1 - Electric field-directed growth and branching of cultured frog nerves

T2 - effects of aminoglycosides and polycations

AU - Erskine, Lynda

AU - Stewart, R

AU - McCaig, Colin Darnley

PY - 1995/4/1

Y1 - 1995/4/1

N2 - The direction and rate of earliest nerve growth are critical determinants of neuronal architecture. One extrinsic cue that influences these parameters is a small direct current electric field, although the underlying mechanisms are unclear. We have studied the orientation, rate of growth, and branching behavior of embryonic Xenopus spinal neurites exposed to aminoglycoside antibiotics, to raised external cations, to applied direct current electric fields, and to combinations of these treatments. Field-induced cathodal turning and cathodal branching of neurites were blocked by the aminoglycosides, by raised extracellular calcium ([Ca2+]0) and by raised extracellular magnesium ([Mg2+]0). Neomycin together with high external Ca2+, by contrast, induced a reversal in the polarity of turning and branching, with neurites reorienting and branching more frequently anodally. Aminoglycosides decreased neurite growth rates, and for neomycin this was partially reversed by high external Ca2+. Raised [Ca2+]0 alone but not raised [Mg2+]0 altered growth rates in a field-strength dependent manner. Modulation of membrane surface charge may underlie altered galvanotropic orientation and branching. Such an effect is insufficient to explain the changes in growth rates, which may result from additional perturbations to Ca2+ influx and inositol phospholipid metabolism.

AB - The direction and rate of earliest nerve growth are critical determinants of neuronal architecture. One extrinsic cue that influences these parameters is a small direct current electric field, although the underlying mechanisms are unclear. We have studied the orientation, rate of growth, and branching behavior of embryonic Xenopus spinal neurites exposed to aminoglycoside antibiotics, to raised external cations, to applied direct current electric fields, and to combinations of these treatments. Field-induced cathodal turning and cathodal branching of neurites were blocked by the aminoglycosides, by raised extracellular calcium ([Ca2+]0) and by raised extracellular magnesium ([Mg2+]0). Neomycin together with high external Ca2+, by contrast, induced a reversal in the polarity of turning and branching, with neurites reorienting and branching more frequently anodally. Aminoglycosides decreased neurite growth rates, and for neomycin this was partially reversed by high external Ca2+. Raised [Ca2+]0 alone but not raised [Mg2+]0 altered growth rates in a field-strength dependent manner. Modulation of membrane surface charge may underlie altered galvanotropic orientation and branching. Such an effect is insufficient to explain the changes in growth rates, which may result from additional perturbations to Ca2+ influx and inositol phospholipid metabolism.

KW - Animals

KW - Anti-Bacterial Agents

KW - Cations, Divalent

KW - Cell Division

KW - Cells, Cultured

KW - Electromagnetic Fields

KW - Membrane Potentials

KW - Neomycin

KW - Neurites

KW - Spinal Cord

KW - Xenopus laevis

KW - Electrical field

KW - Surface potential

KW - neomycin

KW - nerve branching

KW - orientation

U2 - 10.1002/neu.480260406

DO - 10.1002/neu.480260406

M3 - Article

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SP - 523

EP - 536

JO - Journal of Neurobiology

JF - Journal of Neurobiology

SN - 0022-3034

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ER -