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

Minami A. Tokuyama, Cindy Xu, Rebecca E. Fisher, Norma Wilson-Rawls, Kenro Kusumi, Jason Newbern

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)287-296
Number of pages10
JournalDevelopmental Biology
Volume433
Issue number2
DOIs
StatePublished - Jan 15 2018

Fingerprint

Lizards
Neuromuscular Junction
Tail
Regeneration
Muscles
Peripheral Nerves
Schwann Cells
Myelin Basic Protein
Birds
Axons
Mammals
Neurons
Wounds and Injuries

Keywords

  • de novo
  • Lizard
  • Neuromuscular junction
  • Regeneration
  • Reptile

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

Cite this

Developmental and adult-specific processes contribute to de novo neuromuscular regeneration in the lizard tail. / Tokuyama, Minami A.; Xu, Cindy; Fisher, Rebecca E.; Wilson-Rawls, Norma; Kusumi, Kenro; Newbern, Jason.

In: Developmental Biology, Vol. 433, No. 2, 15.01.2018, p. 287-296.

Research output: Contribution to journalArticle

@article{4ab35d9d04054ed2a35eb0be3fddfb9c,
title = "Developmental and adult-specific processes contribute to de novo neuromuscular regeneration in the lizard tail",
abstract = "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.",
keywords = "de novo, Lizard, Neuromuscular junction, Regeneration, Reptile",
author = "Tokuyama, {Minami A.} and Cindy Xu and Fisher, {Rebecca E.} and Norma Wilson-Rawls and Kenro Kusumi and Jason Newbern",
year = "2018",
month = "1",
day = "15",
doi = "10.1016/j.ydbio.2017.10.003",
language = "English (US)",
volume = "433",
pages = "287--296",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - Developmental and adult-specific processes contribute to de novo neuromuscular regeneration in the lizard tail

AU - Tokuyama, Minami A.

AU - Xu, Cindy

AU - Fisher, Rebecca E.

AU - Wilson-Rawls, Norma

AU - Kusumi, Kenro

AU - Newbern, Jason

PY - 2018/1/15

Y1 - 2018/1/15

N2 - 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.

AB - 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.

KW - de novo

KW - Lizard

KW - Neuromuscular junction

KW - Regeneration

KW - Reptile

UR - http://www.scopus.com/inward/record.url?scp=85040541221&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85040541221&partnerID=8YFLogxK

U2 - 10.1016/j.ydbio.2017.10.003

DO - 10.1016/j.ydbio.2017.10.003

M3 - Article

C2 - 29291978

AN - SCOPUS:85040541221

VL - 433

SP - 287

EP - 296

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 2

ER -