Routing of transported materials in the dorsal root and nerve fiber branches of the dorsal root ganglion

Ochs, Sidney; Erdman, John P.; Jersild, Ralph A.; McAdoo, V.

doi:10.1002/neu.480090606

Cited by 94 publications

(29 citation statements)

References 32 publications

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“…A mechanism of routing that has been suggested is that the organelles destined for each branch of the axonal tree are synthesized at separate sites in the cell body, so that the site of synthesis determines the destination of the organelles (Ochs et al, 1978). This evidently cannot be true in our experiments, since the routing of [3H]serotonin indicates that old, as well as new, vesicles are routed.…”

Section: Routing Of Neurotransmittermentioning

confidence: 68%

Routing of transmitter and other changes in fast axonal transport after transection of one branch of the bifurcate axon of an identified neuron

Aletta¹,

Goldberg²

1984

J. Neurosci.

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The regulation of the quantities and types of organelles that leave the neuronal cell body destined for use in the axon and its terminals is not well understood. We had previously found that transport of transmitter undergoes a precise down regulation when most of one branch of the bifurcate axon of an identified serotonergic neuron was removed. We have now investigated further the nature of the regulatory event and the reason for its initiation by eliminating portions of the axonal tree of this neuron. We find that the down regulation is more likely to be due to the loss of synapses than of axon because transport of [3H]serotonin decreases as much when an axonal branch is transected distally as after a proximal transection. Transport of [3H]fucosyl glycoprotein, which normally is associated with the serotonergic vesicle in this axon, decreases to the same extent as transport of [3H]serotonin following proximal transection. The glycoprotein down regulation occurs much more rapidly, possibly due to an inhibition of vesicle synthesis. A secondary rise in transport of [3H] fucosyl glycoprotein 3 days to 2 weeks after axotomy suggests that the radiolabeled glycoprotein has undergone a redistribution into organelles not normally labeled and transported in intact neurons in large amounts, since [3H]serotonin transport remains stably diminished during this period. We also describe here a case of routing of rapidly transported material. When one axonal branch is cut far from the point of bifurcation (-10 mm), ["Hlserotonin is directed away from the branch lacking its synaptic terminals and into the remaining intact branch even though the transected branch is physically capable of transporting its normal amount of [3H]serotonin. We suggest that the presence of synaptic endings influences both the export of transmitter vesicles from the cell body and the partitioning of vesicles among axon collaterals.Fast axonal transport supplies axon collaterals and terminals with newly synthesized organelles and macromolecules from the cell body of the neuron (Ochs, 1982). The collaterals and terminals are themselves incapable of synthesizing these materials. In a healthy mature

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Section: Routing Of Neurotransmittermentioning

confidence: 68%

Routing of transmitter and other changes in fast axonal transport after transection of one branch of the bifurcate axon of an identified neuron

Aletta¹,

Goldberg²

1984

J. Neurosci.

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“…Conjectures about the functional role of the axonal reticulum have largely centered on a likely role in axoplasmic transport (Droz et al, 1975;Ochs et al, 1978;Rambourg and Droz, 1980;Tsukita and Ishikawa, 1980;Papasozemenos et al, 1983;Price et al, 1991), evidence that ionic conditions are critical (Duce and Keen, 1978;Lindsey et al, 1981), and that axonal reticulum export signals control the number of ion channel proteins or G-protein-coupled receptors (Ma et al, 2001), which in some circumstances may be associated with the lysosomal system (Broadwell and Cataldo, 1984). Mechanisms of particular relevance might be the receptive properties selectively expressed in distal nociceptive endings, which include the tetrodotoxin-resistant sodium channel (Fang et al, 2002) and the capsaicin channel (VR1; Caterina,et al, 2000).…”

Section: The Axonal Reticulum and Granular Matrixmentioning

confidence: 99%

Nociceptor structural specialization in canine and rodent testicular “free” nerve endings

Kruger¹,

Kavookjian

Kumazawa

et al. 2003

J of Comparative Neurology

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The receptive fields (RFs) of polymodal nociceptor units of canine testis consist of small fascicles of branching axons ending as clusters within the thin vascular layer overlying the seminiferous tubules. This propitious arrangement enabled serial reconstruction of electron micrographs of a flat, punctate zone, identified during recording of impulse discharge of a single physiologically characterized nociceptor "unit." The RFs showed multiple axons, with some branching and sequential vesicle-containing swellings, similar to what have been called terminals and assumed to constitute impulse generating sites in other tissues. Consistent with this interpretation is the local presence of: (1) clusters of small mitochondria, (2) glycogen granules, and (3) sectors of axolemma denuded of Schwann cell processes and thus "free" endings directly contacting the epithelial basal lamina. The most distal sectors showed additional morphologic properties: (1) zones of vesicles embedded in an extensive granular matrix, (2) preterminal arrays of "axonal reticulum" derived from the smooth endoplasmic reticulum displacing axonal cytoskeletal elements, (3) a variety of sizes and electron lucency in clear, spherical vesicles and a few granular or dense-core vesicles, and (4) specialization in the last Schwann cell of the fascicle. These latter features may reflect differences in the specialized receptor mechanisms of nociceptors that are difficult to detect without extensive serial electron microscopic analysis. Alternatively, these features may constitute a regional specialization of the testis. The term free nerve ending is perhaps an insufficient and inaccurate descriptor of the morphology of nociceptors. These findings are considered in the context of their possible relation to the sensitized vanilloid receptor mechanism unique to nociceptors.

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“…In the latter case it would be assumed that the loss of supply of trophic substance by the centrally directed axons in the dorsal roots was quantitatively relatively small and thus the cell does not show an "injury response." The lesser role of the central relative to the peripheral process could be due, in part, to the disproportionate loss of axoplasmic volume between the central and peripheral axons after axotomy because the central axons are of smaller diameter (7) and the flow of axoplasm is slower than in the large peripherally directed axons (8,9).…”

mentioning

confidence: 99%

Developing dorsal root ganglion neurons require trophic support from their central processes: evidence for a role of retrogradely transported nerve growth factor from the central nervous system to the periphery.

Yip¹,

Johnson²

1984

Proc. Natl. Acad. Sci. U.S.A.

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Injury to the peripheral processes produces a profound cell loss (40-50%) in the dorsal root ganglion of newborn rats. Although division of central processes produces littie or no cellular change in sensory ganglion of adult animals, no Information has been available on the effect of dorsal root section in developing dorsal root ganglion. We show that 6 days after dorsal rhizotomy on newborn rats, there is a 50% decrease in neuronal number in L5 dorsal root ganglion. A combined central and peripheral lesion of the sensory process results in a greater decrease in neuronal number (70%). Both of these effects can be prevented by the concomitant treatment with nerve growth factor. We also demonstrate that 12'I-labeled nerve growth factor is retrogradely transported with high selectivity from the spinal cord to the dorsal root ganglion via the dorsal roots. The results indicate that trophic support for developing sensory neurons is provided through the central processes. This is presumably due to the uptake and retrograde transport of a trophic factor by the terminals of the central processes. The data suggest that nerve growth factor may be the trophic factor. (7) and the flow of axoplasm is slower than in the large peripherally directed axons (8, 9).Populations of developing neurons come under the influence of their peripheral fields and are able to make compensatory adjustments according to the sizes of the afferent input they receive (10-12) and the efferent output they project (13-16). The adjustments are made by way of corresponding alterations in cell number and size within the developing neuronal population. The sensory ganglion is unique in the sense that its target areas include both central neurons in the spinal cord and the innervated organs in the periphery. Despite the lack of morphological alteration reported after sectioning of the central process in adult animals, it is possible that developing DRG neurons receive trophic support from both central and peripheral target zones.Nerve growth factor (NGF) has long been thought to act as a trophic factor transferring information from the peripheral target organs to the innervating sympathetic and sensory neurons. Our recent findings (17) have demonstrated that eliminating the peripheral target influence by crushing the sciatic nerve in the newborn rat resulted in a substantial loss (40-50%) of neurons in L5 DRG. Treatment with NGF prevented the decrease in neuronal number of the axotomized DRG. In the present study, we examine the effects of central process axotomy on the survival of the neonatal neurons to evaluate the relative roles of central and peripheral contacts on the development of the DRG neurons and to determine if exogenous NGF can prevent the observed deleterious effects of central axonal injury.

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Routing of transported materials in the dorsal root and nerve fiber branches of the dorsal root ganglion

Cited by 94 publications

References 32 publications

Routing of transmitter and other changes in fast axonal transport after transection of one branch of the bifurcate axon of an identified neuron

Routing of transmitter and other changes in fast axonal transport after transection of one branch of the bifurcate axon of an identified neuron

Nociceptor structural specialization in canine and rodent testicular “free” nerve endings

Developing dorsal root ganglion neurons require trophic support from their central processes: evidence for a role of retrogradely transported nerve growth factor from the central nervous system to the periphery.

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