Remodelling of Neuromuscular Systems During Insect Metamorphosis

Kent, Karla S.; Consoulas, Christos; Duncan, Karen A.; Johnston, Rebecca M.; Luedeman, Rene; Levine, Richard B.

doi:10.1093/icb/35.6.578

Cited by 22 publications

(7 citation statements)

References 15 publications

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“…At the start of metamorphosis the thoracic muscles of Lepidoptera regress and are later replaced by a set of adult muscles (reviewed by Nü esch, 1985), but many or all of the motor neurons of the adult thoracic muscles persist and are remodeled from those of the larval stage (reviewed by Kent et al, 1995). If the thoracic muscles are denervated just before metamorphosis, the adult thoracic muscles fail to develop normally, and this effect of denervation is taken to indicate that the normal development of the adult thoracic muscles depends on a trophic effect provided by their motor neurons (Nü esch, 1985;Kent et al, 1995).…”

Section: Asl-ir Skeletomotor Neuronsmentioning

confidence: 99%

“…If the thoracic muscles are denervated just before metamorphosis, the adult thoracic muscles fail to develop normally, and this effect of denervation is taken to indicate that the normal development of the adult thoracic muscles depends on a trophic effect provided by their motor neurons (Nü esch, 1985;Kent et al, 1995). Therefore, YXFGLamides possibly have a trophic influence on the development of the adult thoracic muscles.…”

Section: Asl-ir Skeletomotor Neuronsmentioning

confidence: 99%

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Allatostatin‐like‐immunoreactive neurons of the tobacco hornworm, Manduca sexta , and isolation and identification of a new neuropeptide related to cockroach allatostatins

1997

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The YXFGLamide C-terminus serves to define most members of a family of structurally related neuropeptides, the YXFGLamides. These peptides have been identified from the nervous system of various insects and include the allatostatins of cockroaches and crickets, the schistostatins of locusts, and the callatostatins of blowflies. The YXFGLamides have been shown to have various functions, including inhibition of juvenile hormone biosynthesis in cockroaches and crickets and inhibition of contraction of certain insect visceral muscles. We wanted to know if these peptides occur in Manduca sexta and what functions they might have. A new peptide, AKSYNFGLamide, was isolated and identified from M. sexta and has been named "lepidostatin-1"; this is the first YXFGLamide to be found in a lepidopteran, and there are indications that additional YXFGLamides occur in M. sexta. An antiserum to cockroach allatostatins (YXFGLamides) was shown to recognize lepidostatin-1 of M. sexta and was used to map YXFGLamide-immunoreactive neurons in larvae. Because immunoreactive interneurons were found to form an extensive neuropil, YXFGLamides probably function as neuromodulators in M. sexta. Neuroendocrine cells in the brain, abdominal ganglia, and their respective neurohemal organs were YXFGLamide immunoreactive and appear to release YXFGLamides as neurohormones. Immunoreactivity to YXFGLamides and M. sexta diuretic hormone were found to be colocalized and appear to be coreleased in these neuroendocrine cells, indicating that YXFGLamides may be involved in regulation of fluid transport. Innervation of the corpora allata by YXFGLamide-immunoreactive processes was very sparse, suggesting that this innervation does not play an important role in allatostasis. Many thoracic motor neurons were YXFGLamide immunoreactive, suggesting that YXFGLamides may have a myomodulatory or myotrophic function in larvae. However, this immunoreactivity disappeared early in metamorphosis and did not reappear in the adult. The YXFGLamide-immunoreactive neurons in the terminal abdominal ganglion were found to innervate the hindgut, indicating that YXFGLamides may be involved in the control of the rate of myogenic contractions of the larval hindgut.

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Section: Asl-ir Skeletomotor Neuronsmentioning

confidence: 99%

Section: Asl-ir Skeletomotor Neuronsmentioning

confidence: 99%

Allatostatin‐like‐immunoreactive neurons of the tobacco hornworm, Manduca sexta , and isolation and identification of a new neuropeptide related to cockroach allatostatins

1997

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“…The myoblasts initially migrate and legs in lepidoptera), or peripheral nerves (Crossley, aggregate close to the developing tendons, then 1965; Poodry and Schneiderman, 1970;Ursprung align, proliferate, fuse, and eventually differentiate et al, 1972;Lebart-Pedebas, 1990;Bate et al, 1991; into adult leg muscle fibers (Consoulas et al, Currie and Bate, 1991;Fernandes et al, 1991;Fer-1996b). The new muscles are supplied by a persisnandes and VijayRaghavan, 1993;Kent et al, 1995; tent population of larval leg motoneurons Consoulas et al, 1994, 1996b). .…”

Section: Introductionmentioning

confidence: 99%

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

Consoulas

Levine

1997

J. Neurobiol.

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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. © 1997 John Wiley & Sons, Inc. J Neurobiol 32: 531–553, 1997

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“…In the periphery, a period of motorterminal retraction and loss of synaptic boutons is followed by a period of motor-terminal sprouting and the differentiation of a new complement of synaptic boutons. This phenomenon has been particularly well characterized during the metamorphosis of the tobacco hornworm, Manduca sexta, when the muscles of the larval thoracic legs degenerate and new adult leg muscles are formed (Kent et al, 1995;Consoulas et al, 1997). The leg motoneurons, in contrast, survive and are remodeled to innervate the adult leg muscles Levine, 1988, 1993;Consoulas et al, 1996).…”

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confidence: 99%

Remodeling of motor terminals during metamorphosis of the moth Manduca sexta: Expression patterns of two distinct isoforms of Manduca fasciclin II

Knittel

Copenhaver

Kent

2001

J of Comparative Neurology

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During metamorphosis of the moth Manduca sexta, the neuromuscular system of the thoracic legs is reorganized dramatically. Larval leg muscles degenerate at the end of larval life, and new adult leg muscles develop during the ensuing pupal stage. Larval leg motoneurons persist, but undergo substantial remodeling of central and peripheral processes. As part of our on-going investigation of mechanisms underlying the remodeling of motor terminals, we have used antisera generated against Manduca-specific isoforms of the homophilic adhesion molecule fasciclin II (MFas II) to label motor terminals during metamorphosis. Antisera generated against the glycosyl-phosphatidylinositol (GPI) -linked isoform of MFas II (GPI-MFas II) labeled the motor nerves at all stages and seemed to be associated with glial cells ensheathing the peripheral nerves. In addition, the anti-GPI-MFas II antisera labeled regions associated with synaptic boutons at both larval and adult stages. In contrast, antisera generated against a transmembrane isoform of MFas II (TM-MFas II) only labeled specific neuronal processes at discrete intervals during remodeling. Identified leg motoneurons (such as the femoral depressor motoneuron) expressed detectable levels of TM-MFas II in their peripheral processes only during phases of motor-terminal retraction and initial stages of motor-terminal re-growth. Putative modulatory neurons (such as the unpaired median neurons), however, expressed TM-MFas II in their processes during larval stages as well as during remodeling. Use of the isoform-specific anti-MFas II antisera provided a novel method for visualizing remodeling of motor terminals during metamorphosis and helped distinguish different components of the motor nerves and neuromuscular junction.

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Remodelling of Neuromuscular Systems During Insect Metamorphosis

Cited by 22 publications

References 15 publications

Allatostatin‐like‐immunoreactive neurons of the tobacco hornworm, Manduca sexta , and isolation and identification of a new neuropeptide related to cockroach allatostatins

Allatostatin‐like‐immunoreactive neurons of the tobacco hornworm, Manduca sexta , and isolation and identification of a new neuropeptide related to cockroach allatostatins

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

Remodeling of motor terminals during metamorphosis of the moth Manduca sexta: Expression patterns of two distinct isoforms of Manduca fasciclin II

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