Intracellular calcium and cyclic nucleotide levels modulate neurite guidance by microtopographical substrate features

Shufeng Li; Bradley Tuft; Linjing Xu; Marc Polacco; Joseph C Clarke; C Allan Guymon; Marlan R Hansen

doi:10.1002/jbm.a.35738

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Intracellular calcium and cyclic nucleotide levels modulate neurite guidance by microtopographical substrate features

Journal article

Peer reviewed

Intracellular calcium and cyclic nucleotide levels modulate neurite guidance by microtopographical substrate features

Shufeng Li, Bradley Tuft, Linjing Xu, Marc Polacco, Joseph C Clarke, C Allan Guymon and Marlan R Hansen

Journal of biomedical materials research. Part A, Vol.104(8), pp.2037-2048

08/2016

DOI: 10.1002/jbm.a.35738

PMCID: PMC5258117

PMID: 27062708

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http://doi.org/10.1002/jbm.a.35738View

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Abstract

Micro- and nanoscale surface features have emerged as potential tools to direct neurite growth into close proximity with next generation neural prosthesis electrodes. However, the signaling events underlying the ability of growth cones to respond to topographical features remain largely unknown. Accordingly, this study probes the influence of [Ca(2+) ]i and cyclic nucleotide levels on the ability of neurites from spiral ganglion neurons (SGNs) to precisely track topographical micropatterns. Photopolymerization and photomasking were used to generate micropatterned methacrylate polymer substrates. Dissociated SGN cultures were plated on the micropatterned surfaces. Calcium influx and release from internal stores were manipulated by elevating extracellular K(+) , maintenance in calcium-free media, or bath application of various calcium channel blockers. Cyclic nucleotide activity was increased by application of cpt-cAMP or 8-Br-cGMP. Elevation of [Ca(2+) ]i by treatment of cultures with elevated potassium reduced neurite alignment to physical microfeatures. Maintenance of cultures in Ca(2+) -free medium or treatment with the non-selective voltage-gated calcium channel blocker cadmium or L-type Ca(2+) channel blocker nifedipine did not signficantly alter SGN neurite alignment. By contrast, ryanodine or xestospongin C, which block release of internal calcium stores via ryanodine-sensitive channels or inositol-1,4,5-trisphosphate receptors respectively, each significantly decreased neurite alignment. Cpt-cAMP significantly reduced neurite alignment while 8-Br-cGMP significantly enhanced neurite alignment. Manipulation of [Ca(2+) ]i or cAMP levels significantly disrupts neurite guidance while elevation of cGMP levels increases neurite alignment. The results suggest intracellular signaling pathways similar to those recruited by chemotactic cues are involved in neurite guidance by topographical features. © 2016 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 104A: 2037-2048, 2016.

Membrane Potentials - drug effects

Cell Survival - drug effects

Calcium - metabolism

Rats

Spiral Ganglion - cytology

Macrocyclic Compounds - pharmacology

Animals

Cyclic GMP - metabolism

Axon Guidance - drug effects

Intracellular Space - metabolism

Polymers - chemistry

Oxazoles - pharmacology

Cyclic AMP - metabolism

Ryanodine - pharmacology

Details

Title: Subtitle: Intracellular calcium and cyclic nucleotide levels modulate neurite guidance by microtopographical substrate features
Creators: Shufeng Li - Department of Otolaryngology, Eye & ENT Hospital of Fudan University, Shanghai, 200031, China
Bradley Tuft - Department of Chemical and Biochemical Engineering, University of Iowa, Iowa City, Iowa, 52242
Linjing Xu - Department of Otolaryngology-Head and Neck Surgery, University of Iowa, Iowa City, Iowa, 52242
Marc Polacco - Department of Otolaryngology-Head and Neck Surgery, University of Iowa, Iowa City, Iowa, 52242
Joseph C Clarke - Department of Otolaryngology-Head and Neck Surgery, University of Iowa, Iowa City, Iowa, 52242
C Allan Guymon - Department of Chemical and Biochemical Engineering, University of Iowa, Iowa City, Iowa, 52242
Marlan R Hansen - Department of Neurosurgery, University of Iowa, Iowa City, Iowa, 52242
Resource Type: Journal article
Publication Details: Journal of biomedical materials research. Part A, Vol.104(8), pp.2037-2048
DOI: 10.1002/jbm.a.35738
PMID: 27062708
PMCID: PMC5258117
NLM abbreviation: J Biomed Mater Res A
ISSN: 1549-3296
eISSN: 1552-4965
Publisher: United States
Grant note: R01 DC012578 / NIDCD NIH HHS P30 DC010362 / NIDCD NIH HHS
Language: English
Date published: 08/2016
Academic Unit: Molecular Physiology and Biophysics; Chemical and Biochemical Engineering; Neurosurgery; Otolaryngology
Record Identifier: 9984006465402771

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