journal article
Jun 01, 1992
Degenerative Changes in the Muscle Fibers of Manduca Sexta During Metamorphosis
Abstract
ABSTRACT
The ultrastructural changes associated with the early stages of degeneration of the larval mesothoracic muscle fibers of Manduca sexta were examined during the prepupal period and on the first day after ecdysis. Over this 5 day period, the muscle fibers decrease in cross-sectional area but increase in apparent surface area compared to the dimensions of early fifth-instar fibers. Large numbers of electrondense granules or droplets are formed and extruded from the muscle cytoplasm into the hemolymph; this process may account for some of the decrease in muscle fiber mass and may represent a developmental mechanism for recycling nutrients. As the fibers shrink, the thick basal lamina is thrown into folds. Phagocytic hemocytes (granulocytes) congregate in clusters over the surface of the degenerating fibers and appear to remove specifically the basal lamina. The timely removal of the thick larval basal lamina may be essential for subsequent fusion of myoblasts to the residual larval myofibers. The contractile elements within the degenerating muscle fibers become disorganized but are not dysfunctional at the end of the first 12 h after the pupal ecdysis. Tracheoles withdraw from intimate contact with each muscle fiber in its clefts and T-tubules and associate in groups adjacent to it. Mitochondria appear to be degenerating. These structural changes are concurrent with a previously observed decline in resting potential and suggest that a significant change in the electrical properties of the muscle fibers should be expected as well.
The ultrastructural changes associated with the early stages of degeneration of the larval mesothoracic muscle fibers of Manduca sexta were examined during the prepupal period and on the first day after ecdysis. Over this 5 day period, the muscle fibers decrease in cross-sectional area but increase in apparent surface area compared to the dimensions of early fifth-instar fibers. Large numbers of electrondense granules or droplets are formed and extruded from the muscle cytoplasm into the hemolymph; this process may account for some of the decrease in muscle fiber mass and may represent a developmental mechanism for recycling nutrients. As the fibers shrink, the thick basal lamina is thrown into folds. Phagocytic hemocytes (granulocytes) congregate in clusters over the surface of the degenerating fibers and appear to remove specifically the basal lamina. The timely removal of the thick larval basal lamina may be essential for subsequent fusion of myoblasts to the residual larval myofibers. The contractile elements within the degenerating muscle fibers become disorganized but are not dysfunctional at the end of the first 12 h after the pupal ecdysis. Tracheoles withdraw from intimate contact with each muscle fiber in its clefts and T-tubules and associate in groups adjacent to it. Mitochondria appear to be degenerating. These structural changes are concurrent with a previously observed decline in resting potential and suggest that a significant change in the electrical properties of the muscle fibers should be expected as well.
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References
52
[1]
Anderson "Pioneer neurones use basal lamina as a substratum for outgrowth in the embryonic grasshopper limb" Development (1988) 10.1242/dev.104.4.601
[2]
Anderson "Spatial and temporal variation in the structure of the basal lamina in embryonic grasshopper limbs during pioneer neurone outgrowth" Development (1989) 10.1242/dev.106.1.185
[3]
Ball "Haemocytes secrete basement membrane components in embryonic locusts" Development (1987) 10.1242/dev.99.2.255
[4]
Beaulaton "Programmed cell death. Cytochemical evidence for accumulation of calcium in mitochondria and its translocation into lysosomes: X-ray microanalysis in metamorphosing insect muscles" Histochem. J (1986) 10.1007/bf01675193
[5]
Beaulaton "Ultrastructural study of the normal degeneration of the intersegmental muscles of Antheraea polyphemus and Manduca sexta (Insecta, Lepidoptera) with particular reference to cellular autophagy" J. Morph (1977) 10.1002/jmor.1051540104
[6]
Beaulaton "Programmed cell death. X-ray microanalysis of calcium and zinc within the electron-dense droplets of the T system in insect muscles" Biol. Cell (1986)
[7]
Bidlack "Evolution of LDH isozymes during programmed cell death" Comp. Biochem. Physiol (1976)
[8]
Casaday "Neurodevelopment in a thoracic ganglion of a moth: identified motor neurones and microanatomical structure" (1975)
[9]
Condic "Removal of the basal lamina in vivo reveals growth cone –basal lamina adhesive interactions and axonal tension in grasshopper embryos" J. Neurosci (1989) 10.1523/jneurosci.09-08-02678.1989
[10]
Crossley "Transformations in the abdominal muscles of the blue blow-fly, Calliphora erythrocephala (Meig), during metamorphosis" J. Embryol. exp. Morph (1965)
[11]
Crossley "The fine structure and mechanism of breakdown of larval intersegmental muscles in the blowfly Calliphora erythrocephala" J. Insect Physiol (1968) 10.1016/0022-1910(68)90174-1
[12]
Crossley "Ultrastructural changes during transition of larval to adult intersegmental muscle at metamorphosis in the blowfly Calliphora erythrocephala. I. Dedifferentiation and myoblast formation" J. Embryol. exp. Morph (1972)
[13]
Crossley "Ultrastructural changes during transition of larval to adult muscle at metamorphosis in the blowfly Calliphora erythrocephala. II. The formation of adult muscle" J. Embryol. exp. Morph (1972)
[14]
Crossley "The morphology and development of the Drosophila muscular system" (1978)
[15]
Djamgoz "Electrophysiological aspects of metabolic pumping in insect muscle" Comp. Biochem. Physiol (1986) 10.1016/0300-9629(86)90606-7
[16]
Dubendorfer "Differentiation in vitro of larval and adult muscles from embryonic cells of Drosophila" Wilhelm Roux’s Archives (1978) 10.1007/bf00848256
[17]
Eaton "Exoskeleton and muscular morphology of the larval thorax of Manduca sexta L. (Lepidoptera: Sphingidae)" Ann. ent. Soc. Am (1982) 10.1093/aesa/75.3.313
[18]
Eigenmann "Untersuchungen fiber die Entwicklung der dorsolongitudinalen Flugmuskeln von Antheraea pernyi Guer" Rev. Suisse Zool (1965) 10.5962/bhl.part.75667
[19]
Finlayson "Normal and induced degeneration of abdominal muscles during metamorphosis in the Lepidoptera" Q. JI microsc. Sci (1956)
[20]
Heinertz "Untersuchungen am thorokalen Nervensystem von Antheraeapolyphemus Cr. (Lepidoptera) unter besonderer Berficksichtigung der Metamorphose" Rev. suisse Zool (1976)
[21]
Huddart "The effects of DNP on the resting potential and ionic content of some insect skeletal muscle fibres" Comp. Biochem. Physiol (1966) 10.1016/0010-406x(66)90204-0
[22]
Jack (1975)
[23]
Jahromi "Structural changes in locust leg muscle fibres in response to tenotomy and joint immobilization" J. Insect Physiol (1979) 10.1016/0022-1910(79)90079-9
[24]
Johnson "An electron microscopic study of flight muscle breakdown in an aphid Megoura viciae" Tissue & Cell (1980) 10.1016/0040-8166(80)90042-7
[25]
Ko "Induction of active zones at ectopic neuromuscular junctions in the frog" J. Neurosci (1989) 10.1523/jneurosci.09-10-03392.1989
[26]
Lebart-Pedebas "Possible migration of imaginai myoblasts from adjacent nerve sheath into the developing flight muscle of Chironomus" Tissue & Cell (1984) 10.1016/0040-8166(84)90008-9
[27]
Lockshin "Degeneration of insect intersegmental muscles: Electrophysiological studies of populations of fibres" J. Insect Physiol (1973) 10.1016/0022-1910(73)90241-2
[28]
Lockshin "Programmed cell death. Cytochemical evidence for lysosomes during the normal breakdown of the intersegmental muscles" J. Ultrastruct (1974) 10.1016/s0022-5320(74)80021-3
[29]
Lockshin "Programmed cell death. Electrophysiological and ultrastructural correlations in metamorphosing muscles of lepidopteran insects" Tissue & Cell (1979) 10.1016/0040-8166(79)90033-8
[30]
Lyonet (1762)
[31]
McLaughlin "Fine-structural changes in a lepidopteran nervous system during metamorphosis" J. Cell Sci (1974) 10.1242/jcs.14.2.369
[32]
Nardi "Morphogenesis in wing imaginai discs: its relationship to changes in the extracellular matrix" Tissue & Cell (1985) 10.1016/0040-8166(85)90026-6
[33]
Nardi "Hemocytes contribute to both the formation and breakdown of the basal lamina in developing wings of Manduca sexta" Tissue & Cell (1989) 10.1016/0040-8166(89)90008-6
[34]
Nystrom "Disruption of active zones in frog neuromuscular junctions following treatment with proteolytic enzymes" J. Neurocytol (1988) 10.1007/bf01735378
[35]
Randall "Ultrastructural and functional changes of a proleg muscle and its innervation in Galleria mellonella (L.) (Lepidoptera: Pyralididae)" J. Morph (1969) 10.1002/jmor.1051280204
[36]
Rees "Effects of denervation on the ultrastructure of insect muscle" J. Cell Sci (1972) 10.1242/jcs.10.3.667
[37]
Rheuben "The resting potential of the moth muscle fibre" J. Physiol., Lond (1972) 10.1113/jphysiol.1972.sp009954
[38]
Rheuben "Comparison of slow larval and fast adult muscle innervated by the same motor neurone" J. exp. Biol (1980) 10.1242/jeb.84.1.103
[39]
Rheuben "Degenerative changes in the structure of neuromuscular junctions of Manduca sexta during metamorphosis" J. exp. Biol (1992) 10.1242/jeb.167.1.119
[40]
Rice "Regulation of proteolysis at the neutrophil-substrate interface by secretory leukoprotease inhibitor" Science (1990) 10.1126/science.2371565
[41]
Sanes "Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites" J. Cell Biol (1978) 10.1083/jcb.78.1.176
[42]
Schaner "Scanning and freeze-fracture study of larval nerves and neuromuscular junctions in Manduca sexta" J. Neurobiol (1985) 10.1002/neu.480160202
[43]
Schwartz "Hormonal control of muscle atrophy and degeneration in the moth Antheraea polyphemus" J. exp. Biol (1984) 10.1242/jeb.111.1.13
[44]
Sonea "Degenerative changes in the function of neuromuscular junctions of Manduca sexta during metamorphosis" J. exp. Biol (1992) 10.1242/jeb.167.1.61
[45]
Stocker "Elektronenmikroskopische Beobachtungen fiber die Fusion myogener Zellen bei Antheraea polyphemus (Lepidoptera)" Experientia (1974) 10.1007/bf01938346
[46]
Tsujimura "Anatomy of external structure and musculature of thoraces in the larva of the lepidopteran Pieris rapae crucivora" J. Morph (1983) 10.1002/jmor.1051770205
[47]
Unnithan "Ultrastructure of juvenile hormone-induced degenerating flight muscles in a bark beetle, Ips paraconfusus" Cell Tissue Res (1977) 10.1007/bf00220652
[48]
Walters "Hemocytes of satumiid silkworms: their behavior in vivo and in vitro in response to diapause, development and injury" J. exp. Zool (1970) 10.1002/jez.1401740407
[49]
Wood "Ultrastructural changes in cockroach leg muscle following unilateral neurotomy. I. Degeneration" J. Ultrastruct. Res (1979) 10.1016/s0022-5320(79)90159-x
[50]
Yamamoto "Mass rearing of the tobacco homworm. 11. Larval rearing and pupation" J. econ. Ent (1969) 10.1093/jee/62.6.1427
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Details
- Published
- Jun 01, 1992
- Vol/Issue
- 167(1)
- Pages
- 91-117
- License
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Cite This Article
Mary B. Rheuben (1992). Degenerative Changes in the Muscle Fibers of Manduca Sexta During Metamorphosis. Journal of Experimental Biology, 167(1), 91-117. https://doi.org/10.1242/jeb.167.1.91
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