Plastic changes and nitric oxide synthase induction in neurons that innervate the regenerated tail of the lizardGekko gecko: I. Response of spinal motoneurons to tail amputation and regeneration

Cristino, Luigia; Pica, Alessandra; Corte, Francesco Della; Bentivoglio, Marina

doi:10.1002/(sici)1096-9861(20000131)417:1<60::aid-cne5>3.0.co;2-p

Cited by 27 publications

(6 citation statements)

References 32 publications

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“…Neurons re-innervating the regenerating muscle are likely mismatched relative to the original pattern of neuromuscular innervation. In support of this, regenerating motor neurons in geckonid lizards undergo significant changes in size and expression of markers of neuronal identity during tail regeneration (Cristino et al, 2000a; Cristino et al, 2000b). Alterations in muscle redifferentiation also cannot be excluded.…”

Section: Discussionmentioning

confidence: 91%

“…Birth dating experiments suggest that regenerating axons in the lizard tail are not derived from newly born neurons (Duffy, 1992; Alibardi, 1992). Instead, retrograde labeling experiments have shown that most of the newly formed axons in the tail are derived from sprouting of axotomized dorsal root ganglia (DRG) and spinal motor neurons rostral to the breakpoint (Hughes and New, 1959; Duffy, 1992; Cristino et al, 2000a; Cristino et al, 2000b; Cristino et al, 2000c). The expansion in the peripheral innervation field coincides with significant hypertrophy of neuronal cell bodies and altered gene expression in axotomized neurons located in spinal segments just rostral to the autotomy plane (Cristino et al, 2000a; Cristino et al, 2000b).…”

Section: Introductionmentioning

confidence: 99%

“…Instead, retrograde labeling experiments have shown that most of the newly formed axons in the tail are derived from sprouting of axotomized dorsal root ganglia (DRG) and spinal motor neurons rostral to the breakpoint (Hughes and New, 1959; Duffy, 1992; Cristino et al, 2000a; Cristino et al, 2000b; Cristino et al, 2000c). The expansion in the peripheral innervation field coincides with significant hypertrophy of neuronal cell bodies and altered gene expression in axotomized neurons located in spinal segments just rostral to the autotomy plane (Cristino et al, 2000a; Cristino et al, 2000b). In contrast to peripheral nerves, mammals do not regenerate muscle after extensive volumetric muscle loss (Turner and Badylak, 2011), whereas lizards exhibit robust regeneration of entire muscle groups following tail autotomy (Hughes and New, 1959; Alibardi, 1995; Fisher et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Developmental and adult-specific processes contribute to de novo neuromuscular regeneration in the lizard tail

Tokuyama

Fisher

et al. 2018

Developmental Biology

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Peripheral nerves exhibit robust regenerative capabilities in response to selective injury among amniotes, but the regeneration of entire muscle groups following volumetric muscle loss is limited in birds and mammals. In contrast, lizards possess the remarkable ability to regenerate extensive de novo muscle after tail loss. However, the mechanisms underlying reformation of the entire neuromuscular system in the regenerating lizard tail are not completely understood. We have tested whether the regeneration of the peripheral nerve and neuromuscular junctions (NMJs) recapitulate processes observed during normal neuromuscular development in the green anole, Anolis carolinensis. Our data confirm robust axonal outgrowth during early stages of tail regeneration and subsequent NMJ formation within weeks of autotomy. Interestingly, NMJs are overproduced as evidenced by a persistent increase in NMJ density 120 and 250 days post autotomy (DPA). Substantial Myelin Basic Protein (MBP) expression could also be detected along regenerating nerves indicating that the ability of Schwann cells to myelinate newly formed axons remained intact. Overall, our data suggest that the mechanism of de novo nerve and NMJ reformation parallel, in part, those observed during neuromuscular development. However, the prolonged increase in NMJ number and aberrant muscle differentiation hint at processes specific to the adult response. An examination of the coordinated exchange between peripheral nerves, Schwann cells, and newly synthesized muscle of the regenerating neuromuscular system may assist in the identification of candidate molecules that promote neuromuscular recovery in organisms incapable of a robust regenerative response.

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Section: Discussionmentioning

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Developmental and adult-specific processes contribute to de novo neuromuscular regeneration in the lizard tail

Tokuyama

Fisher

et al. 2018

Developmental Biology

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“…In fact, lizard regenerated cord consisted of an epithelial tube, which was primarily made up of ependymal epithelial cells grew from the ependymal cell lining of the injured spinal cord. Most descending neurons of the regenerated spinal cord were confined to the cartilaginous canal, and the functional nerve supply of the regenerated tail might entirely come from the peripheral nerve of the stump (Alibardi, 2010(Alibardi, , 2021Cristino et al, 2000aCristino et al, , 2000bSimpson & Duffy, 1994). The neural stem cells presented in the regenerating spinal cord may be responsible for the lack of dorsal ventral pattern and dorsal root ganglion in the regenerated spinal cord of lizard (Sun et al, 2018).…”

mentioning

confidence: 99%

“…The new peripheral nerve grew distally through the early blastema and continued to extend with the growth of the regenerated tail. No new dorsal root ganglion was regenerated, but the size and cellularity of the last 1-3 ganglion of original caudal stump increased with the expansion of the sensory domain it innervated (Cristino et al, 2000a(Cristino et al, , 2000b. The regenerated motor fibres of the peripheral nerve branch regularly innervated the newly formed muscle bundle and developed a new motor endplate.…”

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confidence: 99%

Neurogenesis in the regenerating tail of tsinling dwarf skinks (Scincella tsinlingensis)

et al. 2023

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Spinal ganglia and peripheral nerves innervate the regenerating tail and muscles of lizards, which provide new opportunities to probe the mechanisms leading to successful functional recovery following spinal cord injury. The regenerated spinal cord and peripheral nerves were detected using immunohistochemistry in original and regenerating tails of Scincella tsinlingensis. Our results showed that positive PCNA, GFAP and SOX2 cells were observed in the ependymal ducts at 15 and 30 days after the autotomy (dpa), with a small number of immunopositive NSE neurons. GFAP and SOX2 positive cells were primarily localized along the regenerated spinal cord after 45 dpa, and the descending nerve of medulla tissue showed positive NSE. Peripheral axons distributed around the muscle and inside the connective tissue and muscle tissue at 15 dpa. The number of axons decreased after 30 dpa. The peripheral axons was mainly distributed between the connective tissue, muscle group and the muscle and epidermis, presenting a radial distribution centred on the cartilage tube at 120 dpa. MBP myelination labelling of the regenerated tail at 30 dpa revealed that the regenerated axons rapidly myelinated along the rostro‐caudal axis. The density of NMJ significantly increased at 120 dpa and 250 dpa. In the second regenerated tails, NMJ density at 250 dpa was still greater than original tails. Overall, these results indicated that neurogenesis was an early event and the ependymal cells were heterogeneous in the regenerated spinal cord of S. tsinlingensis. The regenerated peripheral axons presented a radial distribution centred on the cartilage canal, and the regenerated axons were rapidly myelinated along the rostro‐caudal axis. During the process of regeneration, there were a large number of regenerated neuromuscular joints with high density.

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Nitric oxide synthase in the frog cerebellum: Response of Purkinje neurons to unilateral eighth nerve transection

et al. 2002

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When vestibular damage occurs, nitric oxide synthase (NOS) expression in rat cerebellar flocculus is affected. Since compensation for postural symptoms occurs and Purkinje cells play an important role in movement coordination and motor learning, we analyzed in situ the induction of NOS in the Purkinje cell population of the cerebellum (corpus cerebelli) of frog after unilateral transection of the eighth statoacoustic nerve to gain insight into the role of NO in neural plasticity after injury. Three days after neurectomy, the early effects induced NADPH diaphorase reactivity in most of the Purkinje cells on the ipsilateral side, while on the contralateral side the highest labeling was observed at 15 days. This finding can give information on the dynamics of vestibular compensation, in which NOS involvement was investigated. At 30 days, NADPH diaphorase reactivity was present in a large number of Purkinje cells of the whole cerebellum, while at 60 days a down-regulation for NADPH diaphorase reactivity was evident. A similar trend was observed for NOS-immunoreactivity, which was still present at 60 days in a high percentage of Purkinje cells, mainly on the ipsilateral side. On the basis of cell density evaluations, it was proposed that the early induction of NOS after neurectomy was linked to the degeneration of a part of the Purkinje neurons, while the permanence of NOS labeling might be due to a neuroprotective role of NO in the restoration phase of the vestibular compensation process. Anat Rec 268: 73-83, 2002.

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Plastic changes and nitric oxide synthase induction in neurons that innervate the regenerated tail of the lizardGekko gecko: I. Response of spinal motoneurons to tail amputation and regeneration

Cited by 27 publications

References 32 publications

Developmental and adult-specific processes contribute to de novo neuromuscular regeneration in the lizard tail

Developmental and adult-specific processes contribute to de novo neuromuscular regeneration in the lizard tail

Neurogenesis in the regenerating tail of tsinling dwarf skinks (Scincella tsinlingensis)

Nitric oxide synthase in the frog cerebellum: Response of Purkinje neurons to unilateral eighth nerve transection

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