Regeneration of descending projections to the spinal motor neurons after spinal hemisection in the goldfish

Takeda, Akihito; Goris, Richard C.; Funakoshi, Kengo

doi:10.1016/j.brainres.2007.04.020

Cited by 25 publications

(12 citation statements)

References 20 publications

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“…Methimazole‐treated animals also recovered function. Recovery of the startle reflex, a strong indicator of functional regeneration of ascending and descending pathways in anamniotic spinal cord (Zottoli & Freemer, 2006; Takeda et al. , 2007), was virtually as rapid in methimazole‐treated tadpoles as in those without drug treatment; both groups were essentially normal with respect to this behavior at 2 weeks.…”

Section: Resultsmentioning

confidence: 99%

Metamorphosis and the regenerative capacity of spinal cord axons in Xenopus laevis

Gibbs

Chittur

Szaro

2010

European Journal of Neuroscience

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Throughout the vertebrate subphylum, the regenerative potential of central nervous system axons is greatest in embryonic stages and declines as development progresses. For example, Xenopus laevis can functionally recover from complete transection of the spinal cord as a tadpole but is unable to do so after metamorphosing into a frog. Neurons of the reticular formation and raphe nucleus are among those that regenerate axons most reliably in tadpole and that lose this ability after metamorphosis. To identify molecular factors associated with the success and failure of spinal cord axon regeneration, we pharmacologically manipulated thyroid hormone (TH) levels using methimazole or triiodothyronine, to either keep tadpoles in a permanently larval state or induce precocious metamorphosis, respectively. Following complete spinal cord transection, serotonergic axons crossed the lesion site and tadpole swimming ability was restored when metamorphosis was inhibited, but these events failed to occur when metamorphosis was prematurely induced. Thus, the metamorphic events controlled by TH led directly to the loss of regenerative potential. Microarray analysis identified changes in hindbrain gene expression that accompanied regeneration-permissive and -inhibitory conditions, including many genes in the permissive condition that have been previously associated with axon outgrowth and neuroprotection. These data demonstrate that changes in gene expression occur within regenerating neurons in response to axotomy under regeneration-permissive conditions in which normal development has been suspended, and they identify candidate genes for future studies of how central nervous system axons can successfully regenerate in some vertebrates.

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Section: Resultsmentioning

confidence: 99%

Metamorphosis and the regenerative capacity of spinal cord axons in Xenopus laevis

Gibbs

Chittur

Szaro

2010

European Journal of Neuroscience

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“…Anamniotes such as cyclostomes (Rovainen 1976; Wood and Cohen 1979; Armstrong et al 2003; Shifman et al 2007), certain fish (Coggeshall and Youndblood 1983; Dervan and Roberts 2003; Takeda et al 2007; Reimer et al 2008), anuran larvae (Lorente de Nó 1921; Michel and Reier 1979; Beattie et al 1990; Gibbs and Szaro 2006), and tailed amphibians (Piatt 1955; Butler and Ward 1965; Stensaas 1983; Davis et al 1990; Chevallier et al 2004; Mchedlishvili et al 2007) are able to repair their damaged spinal cords and to recover some of the functions lost by injury. In addition, we have recently reported that an amniote vertebrate (the fresh-water turtle, Trachemys dorbignyi ) also exhibits outstanding self-repairing capabilities after the complete transection of the spinal cord.…”

Section: Introductionmentioning

confidence: 99%

Cell proliferation and cytoarchitectural remodeling during spinal cord reconnection in the fresh-water turtle Trachemys dorbignyi

et al. 2011

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In fresh-water turtles, the bridge connecting the proximal and caudal stumps of transected spinal cords consists of regenerating axons running through a glial cellular matrix. To understand the process leading to the generation of the scaffold bridging the lesion, we analyzed the mitotic activity triggered by spinal injury in animals maintained alive for 20–30 days after spinal cord transection. Flow cytometry and bromodeoxyuridine (BrdU)-labeling experiments revealed a significant increment of cycling cells around the lesion epicenter. BrdU-tagged cells maintained a close association with regenerating axons. Most dividing cells expressed the brain lipid-binding protein (BLBP). Cells with BrdU-positive nuclei expressed glial fibrillary acidic protein. As spinal cord regeneration involves dynamic cell rearrangements, we explored the ultra-structure of the bridge and found cells with the aspect of immature oligodendrocytes forming an embryonic-like microenvironment. These cells supported and ensheathed regenerating axons that were recognized by immunocytological and electron-microscopical procedures. Since functional recovery depends on proper impulse transmission, we examined the anatomical axon-glia relationships near the lesion epicenter. Computer-assisted three-dimensional models revealed helical axon-glial junctions in which the intercellular space appeared to be reduced (5–7 nm). Serial-sectioning analysis revealed that fibril-containing processes provided myelinating axon sheaths. Thus, disruption of the ependymal layer elicits mitotic activity predominantly in radial glia expressing BLBP on the lateral aspects of the ependyma. These cycling cells seem to migrate and contribute to the bridge providing the main support and sheaths for regenerating axons.

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“…However, exceptions occur during embryonic life: in marsupial embryos, the transected cord heals as development proceeds, leading to restoration of functions (Saunders et al,1998). In a number of other vertebrates like cyclostomes (Rovainen,1976; Wood and Cohen,1979; Armstrong et al,2003; reviewed by Shifman et al,2007), some teleosts (Dervan and Roberts,2003; Takeda et al,2007), and tailed amphibians (Piatt,1955; Stensaas,1983; Davis et al,1990; Chevallier et al,2004), the spinal cord seems to have self‐repairing mechanisms that lead to total or partial recovery of sensory‐motor functions. According to Stensaas (1983), “urodeles thus constitute the most advanced phylogenetic group in which functional regeneration occurs following lesions that interrupt ascending and descending pathways of the spinal cord.”…”

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confidence: 99%

Neural reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi

Rehermann

Marichal

Russo

et al. 2009

J of Comparative Neurology

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This paper provides the first evidence that fresh water turtles are able to reconnect their completely transected spinal cord leading to some degree of recovery of the motor functions lost after injury. Videographic analysis showed that some turtles (5 out of 11) surviving more than 20 days after injury were able to initiate stepping locomotion. However the stepping movements were slower than those of normal animals and swimming patterns were not restored. Even though just 45% of the injured turtles recovered their stepping patterns, all showed axonal sprouting beyond the lesion site. Immunocytochemical and electron microscope images revealed the occurrence of regrowing axons crossing the severed region. A major contingent of the axons reconnecting the cord originated from sensory neurons lying in dorsal ganglia adjacent to the lesion site. The axons bridging the damaged region traveled on a cellular scaffold consisting of BLBP and GFAP positive cells and processes. Serotonergic varicose nerve fibers and endings were found at early stages of the healing process at the epicenter of the lesion. Interestingly, the glial scar commonly found in the damaged central nervous system of mammals was absent. In contrast GFAP and BLBP positive processes were found running parallel to the main axis of the cord accompanying the crossing axons.

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Regeneration of descending projections to the spinal motor neurons after spinal hemisection in the goldfish

Cited by 25 publications

References 20 publications

Metamorphosis and the regenerative capacity of spinal cord axons in Xenopus laevis

Metamorphosis and the regenerative capacity of spinal cord axons in Xenopus laevis

Cell proliferation and cytoarchitectural remodeling during spinal cord reconnection in the fresh-water turtle Trachemys dorbignyi

Neural reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi

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