Accumulation and proliferation of adult leg muscle precursors in Manduca are dependent on innervation

Christos Consoulas, Richard B Levine

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

During metamorphosis, the larval thoracic legs of the moth Manduca sexta are replaced by new adult legs. The leg motoneurons do not die after the loss of the larval muscles, but persist to innervate the new adult leg muscles (Kent and Levine, 1988). The adult muscles form from myoblasts that originate in specific production sites within the legs and migrate to the sites of muscle formation, where they accumulate, proliferate, and fuse to form myofibers (Consoulas et al., 1996b). Throughout adult leg muscle development, there is a close association between nerves and the developing muscles, suggesting a role for the nervous system in myogenesis (Consoulas et al., 1996a). This prediction was confirmed and the role of the nervous system clarified in the present study by cutting the larval leg nerves prior to metamorphosis. Although myoblasts were generated and migrated normally in the operated leg, they failed to accumulate in the appropriate regions. The myoblasts did not die, but failed to proliferate and remained in the denervated legs as dispersed cells or as aggregates in inappropriate regions. In about 26% of cases, this resulted in the formation of adult legs that lacked muscles. In the remaining cases, however, delayed regeneration of the leg nerve occurred and small muscles appeared in the more proximal segments of the denervated legs. Each muscle fiber in these operated legs bore motor terminals belonging to axons of the leg nerves which had grown out from the proximal nerve stump and invaded the leg. Following the delayed appearance of motor axons, myoblasts aggregated and underwent proliferation and differentiation into muscle fibers. In a second set of experiments, denervation was performed later, after myoblasts had aggregated to establish anlagen. Myoblast proliferation was reduced but differentiation continued. These observations suggest that motor nerves are essential for both the accumulation of myoblasts into the correct areas of muscle development and the appropriate level of proliferation.

Original languageEnglish (US)
Pages (from-to)531-553
Number of pages23
JournalJournal of Neurobiology
Volume32
Issue number6
DOIs
StatePublished - Jun 5 1997

Fingerprint

Manduca
Leg
Muscles
Myoblasts
Muscle Development
Nervous System
Axons
Nerve Regeneration
Moths
Motor Neurons
Denervation

Keywords

  • accumulation
  • denervation
  • insect
  • migration
  • motor terminals
  • myoblasts
  • myogenesis
  • proliferation
  • regeneration

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Accumulation and proliferation of adult leg muscle precursors in Manduca are dependent on innervation. / Consoulas, Christos; Levine, Richard B.

In: Journal of Neurobiology, Vol. 32, No. 6, 05.06.1997, p. 531-553.

Research output: Contribution to journalArticle

@article{040dc47403054301918d53e999adedcc,
title = "Accumulation and proliferation of adult leg muscle precursors in Manduca are dependent on innervation",
abstract = "During metamorphosis, the larval thoracic legs of the moth Manduca sexta are replaced by new adult legs. The leg motoneurons do not die after the loss of the larval muscles, but persist to innervate the new adult leg muscles (Kent and Levine, 1988). The adult muscles form from myoblasts that originate in specific production sites within the legs and migrate to the sites of muscle formation, where they accumulate, proliferate, and fuse to form myofibers (Consoulas et al., 1996b). Throughout adult leg muscle development, there is a close association between nerves and the developing muscles, suggesting a role for the nervous system in myogenesis (Consoulas et al., 1996a). This prediction was confirmed and the role of the nervous system clarified in the present study by cutting the larval leg nerves prior to metamorphosis. Although myoblasts were generated and migrated normally in the operated leg, they failed to accumulate in the appropriate regions. The myoblasts did not die, but failed to proliferate and remained in the denervated legs as dispersed cells or as aggregates in inappropriate regions. In about 26{\%} of cases, this resulted in the formation of adult legs that lacked muscles. In the remaining cases, however, delayed regeneration of the leg nerve occurred and small muscles appeared in the more proximal segments of the denervated legs. Each muscle fiber in these operated legs bore motor terminals belonging to axons of the leg nerves which had grown out from the proximal nerve stump and invaded the leg. Following the delayed appearance of motor axons, myoblasts aggregated and underwent proliferation and differentiation into muscle fibers. In a second set of experiments, denervation was performed later, after myoblasts had aggregated to establish anlagen. Myoblast proliferation was reduced but differentiation continued. These observations suggest that motor nerves are essential for both the accumulation of myoblasts into the correct areas of muscle development and the appropriate level of proliferation.",
keywords = "accumulation, denervation, insect, migration, motor terminals, myoblasts, myogenesis, proliferation, regeneration",
author = "Christos Consoulas and Levine, {Richard B}",
year = "1997",
month = "6",
day = "5",
doi = "10.1002/(SICI)1097-4695(19970605)32:6<531::AID-NEU1>3.0.CO;2-0",
language = "English (US)",
volume = "32",
pages = "531--553",
journal = "Developmental Neurobiology",
issn = "1932-8451",
publisher = "John Wiley and Sons Inc.",
number = "6",

}

TY - JOUR

T1 - Accumulation and proliferation of adult leg muscle precursors in Manduca are dependent on innervation

AU - Consoulas, Christos

AU - Levine, Richard B

PY - 1997/6/5

Y1 - 1997/6/5

N2 - During metamorphosis, the larval thoracic legs of the moth Manduca sexta are replaced by new adult legs. The leg motoneurons do not die after the loss of the larval muscles, but persist to innervate the new adult leg muscles (Kent and Levine, 1988). The adult muscles form from myoblasts that originate in specific production sites within the legs and migrate to the sites of muscle formation, where they accumulate, proliferate, and fuse to form myofibers (Consoulas et al., 1996b). Throughout adult leg muscle development, there is a close association between nerves and the developing muscles, suggesting a role for the nervous system in myogenesis (Consoulas et al., 1996a). This prediction was confirmed and the role of the nervous system clarified in the present study by cutting the larval leg nerves prior to metamorphosis. Although myoblasts were generated and migrated normally in the operated leg, they failed to accumulate in the appropriate regions. The myoblasts did not die, but failed to proliferate and remained in the denervated legs as dispersed cells or as aggregates in inappropriate regions. In about 26% of cases, this resulted in the formation of adult legs that lacked muscles. In the remaining cases, however, delayed regeneration of the leg nerve occurred and small muscles appeared in the more proximal segments of the denervated legs. Each muscle fiber in these operated legs bore motor terminals belonging to axons of the leg nerves which had grown out from the proximal nerve stump and invaded the leg. Following the delayed appearance of motor axons, myoblasts aggregated and underwent proliferation and differentiation into muscle fibers. In a second set of experiments, denervation was performed later, after myoblasts had aggregated to establish anlagen. Myoblast proliferation was reduced but differentiation continued. These observations suggest that motor nerves are essential for both the accumulation of myoblasts into the correct areas of muscle development and the appropriate level of proliferation.

AB - During metamorphosis, the larval thoracic legs of the moth Manduca sexta are replaced by new adult legs. The leg motoneurons do not die after the loss of the larval muscles, but persist to innervate the new adult leg muscles (Kent and Levine, 1988). The adult muscles form from myoblasts that originate in specific production sites within the legs and migrate to the sites of muscle formation, where they accumulate, proliferate, and fuse to form myofibers (Consoulas et al., 1996b). Throughout adult leg muscle development, there is a close association between nerves and the developing muscles, suggesting a role for the nervous system in myogenesis (Consoulas et al., 1996a). This prediction was confirmed and the role of the nervous system clarified in the present study by cutting the larval leg nerves prior to metamorphosis. Although myoblasts were generated and migrated normally in the operated leg, they failed to accumulate in the appropriate regions. The myoblasts did not die, but failed to proliferate and remained in the denervated legs as dispersed cells or as aggregates in inappropriate regions. In about 26% of cases, this resulted in the formation of adult legs that lacked muscles. In the remaining cases, however, delayed regeneration of the leg nerve occurred and small muscles appeared in the more proximal segments of the denervated legs. Each muscle fiber in these operated legs bore motor terminals belonging to axons of the leg nerves which had grown out from the proximal nerve stump and invaded the leg. Following the delayed appearance of motor axons, myoblasts aggregated and underwent proliferation and differentiation into muscle fibers. In a second set of experiments, denervation was performed later, after myoblasts had aggregated to establish anlagen. Myoblast proliferation was reduced but differentiation continued. These observations suggest that motor nerves are essential for both the accumulation of myoblasts into the correct areas of muscle development and the appropriate level of proliferation.

KW - accumulation

KW - denervation

KW - insect

KW - migration

KW - motor terminals

KW - myoblasts

KW - myogenesis

KW - proliferation

KW - regeneration

UR - http://www.scopus.com/inward/record.url?scp=0031008958&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0031008958&partnerID=8YFLogxK

U2 - 10.1002/(SICI)1097-4695(19970605)32:6<531::AID-NEU1>3.0.CO;2-0

DO - 10.1002/(SICI)1097-4695(19970605)32:6<531::AID-NEU1>3.0.CO;2-0

M3 - Article

C2 - 9183736

AN - SCOPUS:0031008958

VL - 32

SP - 531

EP - 553

JO - Developmental Neurobiology

JF - Developmental Neurobiology

SN - 1932-8451

IS - 6

ER -