Neurons and ecdysteroids promote the proliferation of myogenic cells cultured from the developing adult legs of Manduca sexta

Developmental Biology

Volumn 173, Issue 1, 1996, Pages 51-68

  Luedeman, René ^a   Levine, Richard B ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL PROLIFERATION; INSECT; LEG; METAMORPHOSIS; MUSCLE CELL; MUSCLE DEVELOPMENT; NERVE CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA; INSECTA; MANDUCA SEXTA;

EID: 0030020537     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1996.0006     Document Type: Article

References (63)

1. Ball, E. E., Ho, R. K., and Goodman, C. S. (1985). Muscle development in the grasshopper embryo. I. Muscles, nerves, and apodemes in the metathoracic leg. Dev. Biol. 111, 383-398.
2. Ball, E. E., and Goodman, C. S. (1985a). Muscle development in the grasshopper embryo. II. Syncytial origin of the extensor tibiae muscle pioneers. Dev. Biol. 111, 399-416.
3. Ball, E. E., and Goodman, C. S. (1985b). Muscle development in the grasshopper embryo. III. Sequential origin of the flexor tibiae muscle pioneers. Dev. Biol. 111, 417-424.
4. Bate, M. (1990). The embryonic development of larval muscles in Drosophila. Development 110, 791-804.
5. Bate, M., Rushton, E., and Currie, D. A. (1991). Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 113, 79-89.
6. Bermudez, I., Lees, G., Botham, R. P., and Beadle, D. J. (1986). Myogenesis and neuromuscular junction formation in cultures of Periplaneta americana myoblasts and neurons. Dev. Biol. 116, 467-476.
7. Bischoff, R., and Holtzer, H. (1969). Mitosis and the processes of differentiation of myogenic cells in vitro. J. Cell Biol. 41, 188-200.
8. Bollenbacher, W. E., Smith, S. L., Goodman, W., and Gilbert, L. I. (1981). Ecdysteroid titer during the larval-pupal-adult development of the tobacco hornworm, Manduca sexta. Gen. Comp. Endocrinol. 44, 302-306.
9. Broadie, K. S., and Bate, M. (1993a). Development of larval muscle properties in the embryonic myotubes of Drosophila melanogaster. J. Neurosci. 13, 167-180.
10. Broadie, K. S., and Bate, M. (1993b). Muscle development is independent of innervation during Drosophila embryogenesis. Development 119, 533-543.
11. Broadie, K. S., and Bate, M. (1993c). Innervation directs receptor synthesis and localization in Drosophila embryo synaptogenesis. Nature 361, 350-353.
12. Broadie, K. S., and Bate, M. (1993d). Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis. Neuron 11, 607-619.
13. Buckley, P. A., and Konigsberg, I. R. (1974). Myogenic fusion and the postmitotic gap. Dev. Biol. 37, 193-212.
14. Clegg, C. H., Linkhart, T. A., Olwin, B. B., and Hauschka, S. D. (1987). Growth factor control of skeletal muscle differentiation: Commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor. J. Cell Biol. 105, 949-956.
15. Consoulas, C., Kent, K. S., Anezaki, M., and Levine, R. B. Development of adult thoracic leg muscles during metamorphosis of the hawkmoth Manduca sexta. Submitted for publication.
16. Consoulas, C., Kent, K. S., and Levine, R. B. Remodeling of the peripheral processes and presynaptic terminals of leg motoneurons during metamorphosis of the hawkmoth, Manduca sexta. Submitted for publication.
17. Currie, D. A., and Bate, M. (1991). The development of adult abdominal muscles in Drosophila: Myoblasts express twist and are associated with nerves. Development 113, 91-102.
18. Currie, D. A., and Bate, M. (1995). Innervation is essential for the development and differentiation of a sex-specific adult muscle in Drosophila melanogaster. Development 121, 2549-2557.
19. Cusella-De Angelis, M. G., Molinari, S., Le Donne, A., Coletta, M., Vivarelli, E., Bouche, M., Molinaro, M., Ferrari, S., and Cossu, G. (1994). Differential response of embryonic and fetal myoblasts to TGFβ: A possible regulatory mechanism of skeletal muscle histogenesis. Development 120, 925-933.
20. Donoghue, M. J., and Sanes, J. R. (1994). All muscles are not created equal. Trends Genet. 10, 396-401.
21. Fernandes, J., Bate, M., and Vijayraghavan, K. (1991). Development of the indirect flight muscles of Drosophila. Development 113, 67-77.
22. Fernandes, J., and Keshishian, H. (1995) Neuromuscular development in Drosophila: Insights from embryos and pupae. Curr. Opin. Neurobiol. 5, 10-18.
23. Fernandes, J., and VijayRaghavan, K. (1993). Development of indirect flight muscle innervation in Drosophila melanogaster. Development 118, 215-227.
24. Gorczyca, M., Augart, C., and Budnik, V. (1993). Insulin-like receptor and insulin-like peptide are localized at neuromuscular junctions in Drosophila. J. Neurosci. 13, 3692-3704.
25. Hall, Z. W., and Sanes, J. R. (1993). Synaptic structure and development: The neuromuscular junction. Neuron 10, 99-122.
26. Harris, A. J. (1981). Embryonic growth and innervation of rat skeletal muscles. I. Neural regulation of fiber numbers. Philos. Trans. R. Soc. London, Ser. B 293, 257-277.
27. Hayashi, J. H., and Hildebrand, J. G. (1990). Insect olfactory neurons in vitro: Morphological and physiological characterization of cells from the developing antennal lobes of Manduca sexta. J. Neurosci. 10, 848-859.
28. Hayashi, J. H., and Levine, R. B. (1992). Calcium and Potassium currents in leg motoneurons during postembryonic development in the hawkmoth Manduca sexta. J. Exp. Biol. 171, 15-42.
29. Hegstrom, C. D., and Truman, J. W. (1996). Steroid control of muscle remodeling during metamorphosis in Manduca sexta. J. Neurobiol., in press.
30. Hummon, M. R., and Costello, W. J. (1987). Induced disruption in the connectivity of an identified neuron in the Drosophila temperature sensitive mutant, shibire. J. Neurosci. 7, 3633-3638.
31. Johansen, J., Halpern, M. E., and Keshishian, H. (1989). Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. J. Neurosci. 9, 4318-4332.
32. Kent, K. S., and Levine, R. B. (1988). Neural control of leg movements in a metamorphic insect: Persistence of the larval leg motoneurons to innervate the adult legs of Manduca sexta. J. Comp. Neurol. 276, 30-43.
33. Kent, K. S., Consoulas, C., Duncan, K., Johnston, R. M., Luedeman, R., and Levine, R. B. (1995) Remodeling of neuromuscular systems during insect metamorphosis. Amer. Zool., in press.
34. Konigsberg, I. R. (1963). Clonal analysis of myogenesis. Science 140, 1273-1284.
35. Lawrence, P. A., and Johnston, P. (1986). The muscle patterns of a segment of Drosophila may be determined by neurons and not by contributing muscles. Cell 45, 505-513.
36. Levine, R. B., Fahrbach, S. E., and Weeks, J. C. (1991). Steroid hormones and the reorganization of the nervous system during insect metamorphosis. Seminars in the Neurosciences. 3, 437-447.
37. Levine, R. B., Morton, D. B., and Restifo, L. L. (1995). Remodeling of the insect nervous system. Curr. Op. Neurobiol. 5, 28-35.
38. Levine, R. B., and Truman, J. W. (1985). Dendritic reorganization of abdominal motoneurons during metamorphosis of the moth, Manduca sexta. J. Neurosci. 5, 2424-2431.
39. Lough, J., and Bischoff, R. (1976). Differential sensitivity to 5-bromodeoxyuridine during the S phase of synchronized myogenic cells. Devl. Biol. 50, 457-475.
40. Miller, J. B., and Stockdale, F. E. (1987). What muscle cells know that nerves don't tell them. Trends Neurosci. 10, 325-330.
41. Nüesch, H. (1985). Control of muscle development. In "Comparative Insect Physiology, Biochemistry and Pharmacology" (Kerkut, G. A., and Gilbert, L. I., Eds.), Vol. 2, pp. 425-452. Pergamon, Oxford.
42. Ocalan, M., Goodman, S. L., Kuhl, U., Hauschka, S. D., and von der Mark, K. (1988). Laminin alters cell shape and stimulates motility and proliferation of murine skeletal myoblasts. Dev. Biol. 125, 158-167.
43. Olson, E. N. (1992). Interplay between proliferation and differentiation within the myogenic lineage. Dev. Biol. 154, 261-272.
44. Olson, E. N., Stenberg, E., Hu, J. S., Spizz, G., and Wilcox, C. (1986). Regulation of myogenic differentiation by the type β transforming growth factor. J. Cell Biol. 103, 1799-1855.
45. Ontell, M. P., Hughes, D., Hauschka, S. D., and Ontell, M. (1992). Transient neonatal denvervation alters the proliferative capacity of myosatellite cells in dystrophic (129ReJdy/dy)muscle. J. Neurobiol. 23, 407-419.
46. O'Shea, M., and Adams, M. E. (1981). Pentapeptide (proctolin) associated with an identified neuron. Science 213, 567-569.
47. Prugh, J., Della Croce, K., and Levine, R. B. (1992). Effects of the steroid hormone, 20-hydroxyecdysone, on the growth of neurites by identified insect motoneurons in vitro. Dev. Biol. 154, 331-347.
48. Rapraeger, A. C., Krufka, A., and Olwin, B. B. (1991). Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252, 1705-1708.
49. Ratner, N. Hong, D., Lieberman, M. A., Bunge, R. P., and Glaser, L. (1988). The neuronal cell-surface molecule mitogenic for Schwann cells is a heparin-binding protein. Proc. Natl. Acad. Sci. USA 85, 6992-6996.
50. Ross, J. J., Duxon, M. J., and Harris, A. J. (1987). Neural determination of muscle fiber numbers in embryonic rat lumbrical muscles. Development 100, 395-409.
51. Salkoff, L., and Wyman, R. (1983). Ion currents in Drosophila flight muscle. J. Physiol. (London) 337, 687-709.
52. Sanes, J. R., and Hildebrand, J. G. (1976). Structure and development of antennae in a moth, Manduca sexta. Dev. Biol. 51, 282-299.
53. Seecof, R. L., Gerson, I., Donady, J. J., and Teplitz, R. L. (1973). Drosophila myogenesis in vitro:The genesis of "small" myocytes and myotubes. Dev. Biol. 35, 250-261.
54. Selleck, S. B., Gonzalex, C., Glover, D. M., and White, K. (1992). Regulation of G1-S transition in postembryonic neuronal precursors by axon ingrowth. Nature 355, 253-255.
55. Stockdale, F. E. (1992). Myogenic cell lineages. Dev. Biol. 154, 284-298.
56. Stocker, R. F., and Nüesch, H. (1975). Ultrastructural studies on neuromuscular contacts and the formation of junctions in the flight muscles of Anteraea polyphemus (Lep.) I. Normal adult development. Cell. Tissue Res. 159, 245-266.
57. Templeton, T. J., and Hauschka, S. D. (1992). FGF-mediated aspects of skeletal muscle growth and differentiation are controlled by a high affinity receptor, FGFR1. Dev. Biol. 154, 169-181.
58. Thorn, R. S., and Truman, J. W. (1989). Neuronal respecification during the metamorphosis of the genital segments in the tobacco hornworm moth, Manduca sexta. J. Comp. Neurol. 284, 489-503.
59. Tolbert, L. P., Matsumoto, S. G., and Hildebrand, J. G. (1983). Development of synapses in the antennal lobe of the moth Manduca sexta during metamorphosis. J. Neurosci. 3, 1158-1175.
60. Trimmer, B. A., and Weeks, J. C. (1993). Muscarinic acetylcholine receptors modulate the excitability of an identified insect motoneuron. J. Neurophysiol. 69, 1821-1836.
61. Truman, J. W., and Reiss, S. E. (1995). Neuromuscular metamorphosis in the moth Manduca sexta: hormonal regulation of synapse loss and remodeling. J. Neurosci. 15, 4815-4826.
62. Volk, T., and VijayRaghavan, K. (1994). A central role for epidermal segment border cells in the induction of muscle patterning in the Drosophila embryo. Development 120, 59-70.
63. Weeks, J. C., and Levine, R. B. (1990). Postembryonic neuronal plasticity and its hormonal control during insect metamorphosis. Annu. Rev. Neurosci. 13, 183-194.