Glia‐to‐axon communication: Enrichment of glial proteins transferred to the squid giant axon

Sheller, Rebecca A.; Tytell, Michael; Smyers, Mark E.; Bittner, George D.

doi:10.1002/jnr.490410305

Cited by 24 publications

(19 citation statements)

References 59 publications

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“…In later studies, the synthesis of axoplasmic proteins by the isolated giant axon of Loligo pealii was confirmed (3), and the question of their cellular localization was addressed (104,200,201,277,303). At the end of a series of experiments, the conclusion was reached that the axoplasmic proteins synthesized by the isolated giant axon were entirely derived from periaxonal glia (the glia-neuron protein transfer hypothesis).…”

Section: The Squid Giant Axonmentioning

confidence: 99%

“…157). While the latter data were severely criticized (193), and the possibility of glia-to-neuron transfer of RNA was largely forgotten, the concept of the glia-neuron unit was revived in studies of the local synthesis of proteins in isolated giant axons of crayfish (30,147) and squid (104,200,201,277,303). The squid data were taken to support the idea that locally synthesized axonal proteins exclusively derive from periaxonal glia, although later experiments demonstrated this view to be incorrect (see sects.…”

Section: The Local System Of Gene Expression In Axons and Nerve Tmentioning

confidence: 99%

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Local Gene Expression in Axons and Nerve Endings: The Glia-Neuron Unit

Giuditta¹,

Chun²,

Eyman³

et al. 2008

Physiological Reviews

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Neurons have complex and often extensively elongated processes. This unique cell morphology raises the problem of how remote neuronal territories are replenished with proteins. For a long time, axonal and presynaptic proteins were thought to be exclusively synthesized in the cell body, which delivered them to peripheral sites by axoplasmic transport. Despite this early belief, protein has been shown to be synthesized in axons and nerve terminals, substantially alleviating the trophic burden of the perikaryon. This observation raised the question of the cellular origin of the peripheral RNAs involved in protein synthesis. The synthesis of these RNAs was initially attributed to the neuron soma almost by default. However, experimental data and theoretical considerations support the alternative view that axonal and presynaptic RNAs are also transcribed in the flanking glial cells and transferred to the axon domain of mature neurons. Altogether, these data suggest that axons and nerve terminals are served by a distinct gene expression system largely independent of the neuron cell body. Such a local system would allow the neuron periphery to respond promptly to environmental stimuli. This view has the theoretical merit of extending to axons and nerve terminals the marginalized concept of a glial supply of RNA (and protein) to the neuron cell body. Most long-term plastic changes requiring de novo gene expression occur in these domains, notably in presynaptic endings, despite their intrinsic lack of transcriptional capacity. This review enlightens novel perspectives on the biology and pathobiology of the neuron by critically reviewing these issues.

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Section: The Squid Giant Axonmentioning

confidence: 99%

Section: The Local System Of Gene Expression In Axons and Nerve Tmentioning

confidence: 99%

Local Gene Expression in Axons and Nerve Endings: The Glia-Neuron Unit

Giuditta¹,

Chun²,

Eyman³

et al. 2008

Physiological Reviews

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“…A variety of evidence, mainly from experiments on squid giant axons, demonstrated that the axoplasmic RNAs are partially transferred from extra-axonal glia (Edstrom et al 1969;Gainer et al 1977;Lasek et al 1977;Cutillo et al 1983;Rapallino et al 1988;Buchheit & Tytell, 1992). However, the glial-axonal transfer of proteins did not appear to involve the conventional secretory exocytic and endocytic pathways (Sheller et al 1995).…”

Section: Polyribosomal Clusters In the First Internodementioning

confidence: 99%

Beyond the initial axon segment of the spinal motor axon: fasciculated microtubules and polyribosomal clusters

Li¹,

Cheng²,

Li³

et al. 2005

Journal of Anatomy

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Dense undercoating, microtubular fascicles and scattered polyribosomal clusters have until now been considered to be the three structural features of the initial segment, and were thought not to extend beyond the initial segment into the myelinated parts of the axon. The aim of the present study was to make clear whether there is a sudden change in morphology between the unmyelinated and myelinated part. We followed spinal motor axons from the initial segment to the first internode by conventional electron microscopy and serial sectioning, and found that the microtubular fascicles and polyribosomal clusters do exist in the internodal axoplasm. The fasciculated microtubules were observed mainly in the first paranode. The polyribosomal clusters were found along the course of the first internode at a random distance, however, they occurred mainly in the proximal part of the first internode. The proportion of sections in which ribosomes were found, i.e. the incidence of ribosomes, in the first 30-µ m-long portion was 71 ± 24% (mean ± SD, n = 4), and significantly different from that in the second 30-µ m-long portion (3.2 ± 1.3%) (mean ± SD, n = 4) ( P < 0.005). The more distal part of the first internode was not investigated.

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“…The transfer of HSPs and other proteins may involve nonconventional secretion in which cytosolic proteins that lack the signal sequences required for Golgimediated secretion are translocated across the glial plasmalemma (Hightower and Guidon, 1989;Mignatti et al, 1992;Sheller et al, 1995) and then across the axolemma (Sheller et al, 1995). Because HSPs are essential molecular chaperons that assist other proteins in crossing cellular membranes, this intercellular transfer may be aided by induced members of the HSP 70 family that are secreted by the glia in response to a stress or by some constitutive members of the HSP 70 family that are present normally in the cytoplasm of the axon and/or glia.…”

Section: Proposed Mechanism Of Glia-to-axon Transfermentioning

confidence: 99%

Heat-shock proteins in axoplasm: High constitutive levels and transfer of inducible isoforms from glia

et al. 1998

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To characterize heat-shock proteins (HSPs) of the 70-kDa family in the crayfish medial giant axon (MGA), we analyzed axoplasmic proteins separately from proteins of the glial sheath. Several different molecular weight isoforms of constitutive HSP 70s that were detected on immunoblots were approximately 1-3% of the total protein in the axoplasm of MGAs. To investigate inducible HSPs, MGAs were heat shocked in vitro or in vivo, then the axon was bathed in radiolabeled amino acid for 4 hours. After either heat-shock treatment, protein synthesis in the glial sheath was decreased compared with that of control axons, and newly synthesized proteins of 72 kDa, 84 kDa, and 87 kDa appeared in both the axoplasm and the sheath. Because these radiolabeled proteins were present in MGAs only after heat-shock treatments, we interpreted the newly synthesized proteins of 72 kDa, 84 kDa, and 87 kDa to be inducible HSPs. Furthermore, the 72-kDa radiolabeled band in heat-shocked axoplasm and glial sheath samples comigrated with a band possessing HSP 70 immunoreactivity. The amount of heat-induced proteins in axoplasm samples was greater after a 2-hour heat shock than after a 1-hour heat shock. These data indicate that MGA axoplasm contains relatively high levels of constitutive HSP 70s and that, after heat shock, MGA axoplasm obtains inducible HSPs of 72 kDa, 84 kDa, and 87 kDa from the glial sheath. These constitutive and inducible HSPs may help MGAs maintain essential structures and functions following acute heat shock.

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Glia‐to‐axon communication: Enrichment of glial proteins transferred to the squid giant axon

Cited by 24 publications

References 59 publications

Local Gene Expression in Axons and Nerve Endings: The Glia-Neuron Unit

Local Gene Expression in Axons and Nerve Endings: The Glia-Neuron Unit

Beyond the initial axon segment of the spinal motor axon: fasciculated microtubules and polyribosomal clusters

Heat-shock proteins in axoplasm: High constitutive levels and transfer of inducible isoforms from glia

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