Intermingled cAMP, cGMP and calcium spatiotemporal dynamics in developing neuronal circuits

Averaimo, Stefania; Nicol, Xavier

doi:10.3389/fncel.2014.00376

Cited by 52 publications

(61 citation statements)

References 101 publications

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“…cAMP has been suggested to serve as an important mediator in axonal growth (Averaimo and Nicol, 2014). By using photo-activated adenylyl cyclase (PAC) to locally increment cAMP levels, a recent study revealed that short term elevation of intracellular cAMP induces axonal branching via Protein Kinase A (PKA) activation (Zhou et al 2016).…”

Section: Signaling Mechanisms That Regulate Cytoskeletal Dynamics Durmentioning

confidence: 99%

It takes a village to raise a branch: Cellular mechanisms of the initiation of axon collateral branches

Armijo-Weingart

Gallo

2017

Molecular and Cellular Neuroscience

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The formation of axon collateral branches from the pre-existing shafts of axons is an important aspect of neurodevelopment and the response of the nervous system to injury. This article provides an overview of the role of the cytoskeleton and signaling mechanisms in the formation of axon collateral branches. Both the actin filament and microtubule components of the cytoskeleton are required for the formation of axon branches. Recent work has begun to shed light on how these two elements of the cytoskeleton are integrated by proteins that functionally or physically link the cytoskeleton. While a number of signaling pathways have been determined as having a role in the formation of axon branches, the complexity of the downstream mechanisms and links to specific signaling pathways remain to be fully determined. The regulation of intra-axonal protein synthesis and organelle function are also emerging as components of signal-induced axon branching. Although much has been learned in the last couple of decades about the mechanistic basis of axon branching we can look forward to continue elucidating this complex biological phenomenon with the aim of understanding how multiple signaling pathways, cytoskeletal regulators and organelles are coordinated locally along the axon to give rise to a branch.

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Section: Signaling Mechanisms That Regulate Cytoskeletal Dynamics Durmentioning

confidence: 99%

It takes a village to raise a branch: Cellular mechanisms of the initiation of axon collateral branches

Armijo-Weingart

Gallo

2017

Molecular and Cellular Neuroscience

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“…Crosstalk between second messengers, cyclic nucleotides and Ca 2+ , plays a crucial role in axon pathfinding (Nicol et al, 2011; Averaimo and Nicol, 2014) and modulates the axonal response to Netrin-1 (Hong et al, 2000). We investigated the effects of somatic, axonal, and global Netrin-1 treatments on cyclic nucleotides activity in growth cones and cell bodies with genetically encoded FRET reporters: cGMP reporter cGi500 (Russwurm et al, 2007) or cAMP reporter epac2-camp (Nikolaev et al, 2004).…”

Section: Resultsmentioning

confidence: 99%

Neuronal Cell Bodies Remotely Regulate Axonal Growth Response to Localized Netrin-1 Treatment via Second Messenger and DCC Dynamics

Blasiak

Kilinc

2017

Front. Cell. Neurosci.

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Netrin-1 modulates axonal growth direction and speed. Its best characterized receptor, Deleted in Colorectal Cancer (DCC), is localized to growth cones, but also observed in the cell bodies. We hypothesized that cell bodies sense Netrin-1 and contribute to axon growth rate modulation, mediated by the second messenger system. We cultured mouse cortical neurons in microfluidic devices to isolate distal axon and cell body microenvironments. Compared to isolated axonal treatment, global Netrin-1 treatment decreased the axon elongation rate and affected the dynamics of total and membranous DCC, calcium, and cyclic nucleotides. Signals induced by locally applied Netrin-1 propagated in both anterograde and retrograde directions, demonstrated by the long-range increase in DCC and by the increased frequency of calcium transients in cell bodies, evoked by axonal Netrin-1. Blocking the calcium efflux from endoplasmic reticulum suppressed the membranous DCC response. Our findings support the notion that neurons sense Netrin-1 along their entire lengths in making axonal growth decisions.

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“…Thus, cAMP and cGMP appear to exert opposing influences on neurite aligment to microtopographical features similar to their opposing effects on chemotactive biochemical cues. 63,64 Interestingly, SGSC alignment to the micropatterns, which, like to SGN neurite alignment, depends on RhoA/ ROCK signaling, 21 was likewise disrupted by ryanodine and IP3 receptor inhbitors and by treatment with a cAMP analog. Further, treatment with a cGMP analog enhanced SGSC alignment to micropatterns.…”

Section: Discussionmentioning

confidence: 99%

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

Tuft

et al. 2016

J. Biomed. Mater. Res.

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Objective Micro- and nano-scale 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 [Ca2+]i and cyclic nucleotide levels on the ability of neurites from spiral ganglion neurons (SGNs) to precisely track topographical micropatterns. Approach 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. Main results Elevation of [Ca2+]i by treatment of cultures with elevated potassium reduced neurite alignment to physical microfeatures. Maintenance of cultures in Ca2+-free medium or treatment with the non-selective voltage-gated calcium channel blocker cadmium or L-type Ca2+ 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. Conclusion Manipulation of [Ca2+]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.

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Intermingled cAMP, cGMP and calcium spatiotemporal dynamics in developing neuronal circuits

Cited by 52 publications

References 101 publications

It takes a village to raise a branch: Cellular mechanisms of the initiation of axon collateral branches

It takes a village to raise a branch: Cellular mechanisms of the initiation of axon collateral branches

Neuronal Cell Bodies Remotely Regulate Axonal Growth Response to Localized Netrin-1 Treatment via Second Messenger and DCC Dynamics

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

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