Regulation of plasma membrane expansion during axon formation

Quiroga, Santiago; Bisbal, Mariano; Cáceres, Alfredo

doi:10.1002/dneu.22553

Cited by 29 publications

(22 citation statements)

References 114 publications

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“…These signals, frequently in the form of glycoproteins secreted into or presented attached to the extracellular matrix, are ligands for receptors on the surface of the growth cone and trigger a variety of intracellular responses, including membrane remodeling through exocytosis and endocytosis, cytoskeletal reorganization, and modification of protein expression and degradation, both locally in the axon and throughout the neuron. For thorough, recent reviews on growth cone regulation, see “Regulation of plasma membrane expansion during axon formation” on membrane remodeling and addition ( Quiroga et al, 2017 ), “Actin based growth cone motility and guidance” on actin responses in the growth cone ( Omotade et al, 2017 ), “Mechanochemical regulation of growth cone motility” on mechanosensation and mechanotransduction by growth cones ( Kerstein et al, 2015 ), and “Axon Guidance Pathways and the Control of Gene Expression” on regulation of gene expression ( Russell and Bashaw, 2018 ). This review will specifically focus on the mechanisms by which the guidance molecule netrin-1 produces axon guidance responses.…”

Section: Axon Response To the Environmentmentioning

confidence: 99%

“…This section specifically addresses mechanisms associated with either attractive axon guidance or increased axon outgrowth in response to netrin-1 downstream of DCC. Asymmetrical changes in the shape and rate of extension of the growth cone reorient outgrowth during turning; this involves dramatic and regulated remodeling of the plasma membrane ( Quiroga et al, 2017 ) and underlying cytoskeleton ( Dent et al, 2011 ), which is orchestrated by both chemical and mechanical transduction downstream of netrin/DCC, summarized in Figure 5 .…”

Section: Netrin-1 Receptors and Their Mechanismsmentioning

confidence: 99%

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Revisiting Netrin-1: One Who Guides (Axons)

Boyer¹,

Gupton²

2018

Front. Cell. Neurosci.

136

130

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Proper patterning of the nervous system requires that developing axons find appropriate postsynaptic partners; this entails microns to meters of extension through an extracellular milieu exhibiting a wide range of mechanical and chemical properties. Thus, the elaborate networks of fiber tracts and non-fasciculated axons evident in mature organisms are formed via complex pathfinding. The macroscopic structures of axon projections are highly stereotyped across members of the same species, indicating precise mechanisms guide their formation. The developing axon exhibits directionally biased growth toward or away from external guidance cues. One of the most studied guidance cues is netrin-1, however, its presentation in vivo remains debated. Guidance cues can be secreted to form soluble or chemotactic gradients or presented bound to cells or the extracellular matrix to form haptotactic gradients. The growth cone, a highly specialized dynamic structure at the end of the extending axon, detects these guidance cues via transmembrane receptors, such as the netrin-1 receptors deleted in colorectal cancer (DCC) and UNC5. These receptors orchestrate remodeling of the cytoskeleton and cell membrane through both chemical and mechanotransductive pathways, which result in traction forces generated by the cytoskeleton against the extracellular environment and translocation of the growth cone. Through intracellular signaling responses, netrin-1 can trigger either attraction or repulsion of the axon. Here we review the mechanisms by which the classical guidance cue netrin-1 regulates intracellular effectors to respond to the extracellular environment in the context of axon guidance during development of the central nervous system and discuss recent findings that demonstrate the critical importance of mechanical forces in this process.

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Section: Axon Response To the Environmentmentioning

confidence: 99%

Section: Netrin-1 Receptors and Their Mechanismsmentioning

confidence: 99%

Revisiting Netrin-1: One Who Guides (Axons)

Boyer¹,

Gupton²

2018

Front. Cell. Neurosci.

136

130

View full text Add to dashboard Cite

show abstract

“…Regarding growth cone behavior, the close balance between these forces has also been suggested to account for the probabilistic anterograde and retrograde motion of the growth cone ( Shahapure et al, 2010 ). While membrane addition is critical for the process of axonal elongation and blocking membrane addition halts elongation ( Quiroga et al, 2018 ), membrane tension does not appear to be significantly limit the assembly of actin or the advance of the growth cone through large forces.…”

Section: Force and Motionmentioning

confidence: 99%

An Integrated Cytoskeletal Model of Neurite Outgrowth

Miller

Suter

2018

Front. Cell. Neurosci.

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Neurite outgrowth underlies the wiring of the nervous system during development and regeneration. Despite a significant body of research, the underlying cytoskeletal mechanics of growth and guidance are not fully understood, and the relative contributions of individual cytoskeletal processes to neurite growth are controversial. Here, we review the structural organization and biophysical properties of neurons to make a semi-quantitative comparison of the relative contributions of different processes to neurite growth. From this, we develop the idea that neurons are active fluids, which generate strong contractile forces in the growth cone and weaker contractile forces along the axon. As a result of subcellular gradients in forces and material properties, actin flows rapidly rearward in the growth cone periphery, and microtubules flow forward in bulk along the axon. With this framework, an integrated model of neurite outgrowth is proposed that hopefully will guide new approaches to stimulate neuronal growth.

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“…However, there remains a gap in our knowledge regarding the mechanisms downstream of these events that lead to effects on axon growth. The mechanisms regulating developmental axon growth are well‐known and include cytoskeletal reorganization, axon transport, membrane addition, and insertion of guidance molecules onto the growth cone surface (Allen and Chilton, ; Bradke et al, ; Hilton and Bradke, ; Quiroga et al, ), but the extent to which these are involved in mediating the effects of the interventions described above is not known. Cytoskeletal reorganization is clearly an important consideration as demonstrated by the stimulation of CNS regeneration by targeting both the microtubule and actin cytoskeleton (Dergham et al, ; Ruschel et al, ), and the neutralization of growth inhibition by targeting growth cone non‐muscle myosin (Hur et al, ).…”

Section: Introductionmentioning

confidence: 99%

The Virtuous Cycle of Axon Growth: Axonal Transport of Growth‐Promoting Machinery as an Intrinsic Determinant of Axon Regeneration

Petrova

Eva

2018

Developmental Neurobiology

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Injury to the brain and spinal cord has devastating consequences because adult central nervous system (CNS) axons fail to regenerate. Injury to the peripheral nervous system (PNS) has a better prognosis, because adult PNS neurons support robust axon regeneration over long distances. CNS axons have some regenerative capacity during development, but this is lost with maturity. Two reasons for the failure of CNS regeneration are extrinsic inhibitory molecules, and a weak intrinsic capacity for growth. Extrinsic inhibitory molecules have been well characterized, but less is known about the neuron-intrinsic mechanisms which prevent axon re-growth. Key signaling pathways and genetic/epigenetic factors have been identified which can enhance regenerative capacity, but the precise cellular mechanisms mediating their actions have not been characterized. Recent studies suggest that an important prerequisite for regeneration is an efficient supply of growth-promoting machinery to the axon; however, this appears to be lacking from non-regenerative axons in the adult CNS. In the first part of this review, we summarize the evidence linking axon transport to axon regeneration. We discuss the developmental decline in axon regeneration capacity in the CNS, and comment on how this is paralleled by a similar decline in the selective axonal transport of regeneration-associated receptors such as integrins and growth factor receptors. In the second part, we discuss the mechanisms regulating selective polarized transport within neurons, how these relate to the intrinsic control of axon regeneration, and whether they can be targeted to enhance regenerative capacity. © 2018 Wiley Periodicals, Inc. Develop Neurobiol 00: 000-000, 2018.

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Regulation of plasma membrane expansion during axon formation

Abstract: Here, will review current evidence regarding the signaling pathways and mechanisms underlying membrane addition at sites of active growth during axon formation. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 78: 170-180, 2018.

Cited by 29 publications

References 114 publications

Revisiting Netrin-1: One Who Guides (Axons)

Revisiting Netrin-1: One Who Guides (Axons)

An Integrated Cytoskeletal Model of Neurite Outgrowth

The Virtuous Cycle of Axon Growth: Axonal Transport of Growth‐Promoting Machinery as an Intrinsic Determinant of Axon Regeneration

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