Developmental plasticity of neuropeptide expression in motoneurons of the moth, Manduca sexta: Steroid hormone regulation

Journal of Neurobiology

Volumn 29, Issue 1, 1996, Pages 99-114

  Witten, Jane L ^a,b   Truman, James W ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

developmental plasticity; FMRFamide peptides; motoneurons; neuropeptides; steroid hormones

Indexed keywords

NEUROPEPTIDE;

ANIMAL TISSUE; ARTICLE; HORMONAL REGULATION; LEPIDOPTERA; MOTONEURON; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANIMALS; ECDYSTERONE; FMRFAMIDE; INVERTEBRATE HORMONES; LARVA; METAMORPHOSIS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MOTHS; MOTOR NEURONS; NEUROPEPTIDES;

EID: 0030045585     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199601)29:1<99::AID-NEU8>3.0.CO;2-2     Document Type: Article

References (70)

1. ADAMS, M. A. and O'SHEA, M. (1983). Peptide cotransmitter at a neuromuscular junction. Science 221: 286-289.
2. AMOS, T. M. and MESCE, K. A. (1994). Reorganization of the ventral nerve cord in the moth Manduca sexta (L.) (Lepidoptera: Sphingidae). Int. J. Insect Morphol. Embryol. 23:21-37.
3. BARKER, D. L., HERBERT, E., HILDEBRAND, J. G., and KRAVITZ, E. (1972). Acetylcholine and lobster sensory neurons. J. Physiol. Lond. 226:205-229.
4. BELL, R. A. and JOACHIM, F. G. (1976). Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann. Entomol. Soc. Am 69:365-373.
5. BISHOP, C. A., WINE, J. J., NAGY, F., and O'SHEA, M. (1987). Physiological consequences of a peptide cotransmitter in a crayfish nerve-muscle preparation. J Neurosci. 7:1769-1779.
6. BLACK, I. B. and PATTERSON, P. H. (1980). Developmental regulation of neurotransmitter phenotype. Curr. Top. Dev. Biol 15:27-40.
7. BLACKBURN, M. E., KINGAN, T. G., RAINA, A. K., and MA, M. C. (1992). Colocalization and differential expression of PBAN- and FMRFamide-like immunoreactivity in the subesophageal ganglion of Helicoverpa zea (Lepidoptera: Noctuidae) during development. Arch. Insect Biochem. Physiol. 21:225-238.
8. BOOKER, R. and TRUMAN, J. W. (1987). Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. I. Neuroblast arrays and the fate of their progeny during metamorphosis. J. Comp. Neurol. 255:548-559.
9. BOWEN, M. F., BOLLENBACHER, W. E., and GILBERT, L. I. (1984). In vitro studies on the role of the brain and prothoracic glands in the pupal diapause of Manduca sexta. J. Exp. Biol. 108:9-24.
10. BREEDLOVE, S. M. (1992). Sexual dimorphism in the vertebrate nervous system. J. Neurosci 12:4133-4142.
11. COTTRELL, G. A., SCHOT, L. P. C., and DOCKRAY, G. F. (1983). Identification and probable role of a single neurone containing the Helix FMRFamide. Nature 304:638-640.
12. DAVIS, N. D., HOMBERG, U., DIRCKSEN, H., LEVINE, R. B., and HILDEBRAND, J. G. (1993). Crustacean cardioactive peptide-immunoreactive neurons in the hawkmoth, Manduca sexta, and changes in their immunoreactivity during postembryonic development. J. Comp. Neurol. 338:612-627.
13. EPHRUSSI, B. and BEADLE, A. W. (1936). A technique of transplantation for Drosophila. Am. Nat. 70:218-225.
14. EVANS, P. D. and MYERS, C. M. (1986). The modulatory actions of FMRFamide and related peptides on locust skeletal muscle. J. Exp. Biol. 126:403-422.
15. FISHMAN, R. B. and BREEDLOVE, S. M. (1988). Neonatal androgen maintains sexually dimorphic perineal muscles in the absence of innervation. Muscle Nerve 11:553-560.
16. FONAGY, A., SCHOOFS, L., PROOST, P., VANDAMME, J., BUEDS, H., and DELOOF, A. (1992). Isolation, primary structure, and synthesis of neomyosuppressin, a myoinhibiting neuropeptide from the grey fleshfly, Neobellierria-Bullata. Comp. Biochem. Physiol. 102C: 239-245.
17. FONTAINE, B., KLARSFELD, A., HOKFELT, T., and CHANGEUX, J.-P. (1986). Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increases the number of acetylcholine receptors in primary cultures of chick embryo myotubes. Neurosci. Lett. 71:59-65.
18. FUJISAWA, Y., SHIMODA, M., KIGUCHI, K., ICHIKAWA, T., and FUJITA, N. (1993). Inhibitory effect of a neuropeptide, ManducaFLRFamide, on the midgut activity of the Sphingid moth, Agrius convolvuvi. Zool. Sci. 10:773-777.
19. HOLMAN, G. M., COOK, B. J., and NACHMAN, R. J. (1986). Isolation, primary structure and synthesis of leucomyosuppressin, an insect neuropeptide that inhibits spontaneous contractions of the cockroach hindgut. Comp. Biochem. Physiol. 85C:329-333.
20. HOMBERG, U. and HILDEBRAND, J. G. (1994). Postembryonic development of γ-aminobutyric acid-like immunoreactivity in the brain of the sphinx moth Manduca sexta. J. Comp. Neurol. 339:132-149.
21. HYATT-SACHS, H., SCHREIBER, R. C., BENNETT, T. A., and ZIGMOND, R. E. (1993). Phenotypic plasticity in adult sympathetic ganglia in vivo: effects of deafferentiation and axotomy on the expression of vasoactive intestinal peptide. J. Neurosci. 13:1642-1653.
22. KENT, K. S. and LEVINE, R. B. (1988). Neural control of leg movements in a metamorphic insect: persistence of the larval leg motor neurons to innervate the adult legs of Manduca sexta. J. Comp. Neurol. 276:30-43.
23. KINGAN, T., TEPLOW, D. P., PHILLIPS, J. M., RIEHM, J. P. J., RAO, K. R., HILDEBRAND, J. G., HOMBERG, U., KAMMER, A. E., JARDINE, I., GRIFFIN, P. R., and HUNT, D. F. (1990). A new peptide in the FMRFamide family isolated from the CNS of the hawkmoth, Manduca sexta. Peptides 11:849-856.
24. LANDIS, S. C. (1988). Target regulation of neurotransmitter phenotype. Trends Neurosci. 13:344-350.
25. LANDIS, S. C. and KEEFE, D. (1983). Evidence for neurotransmitter plasticity in vivo. II. Immunocytochemical studies of rat sweat gland innervation during development. Dev. Biol. 126:129-138.
26. LANDIS, S. C., SCHWAB, M., and SIEGEL, R. E. (1988). Evidence for transmitter plasticity in vivo: developmental changes in the properties of cholinergic sympathetic neurons. Dev. Biol. 98:349-372.
27. LEBLANC, G. and LANDIS, S. C. (1986). Development of choline acetyltransferase activity in the cholinergic sympathetic innervation of sweat glands. J. Neurosci. 6:260-265.
28. 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.
29. LEVINE, R. B., FAHRBACH, S. E., and WEEKS, J. C. (1991). Steroid hormones and the reorganization of the nervous system during insect metamorphosis. Semin. Neurosci. 3:437-447.
30. LOI, P. K. and TUBLITZ, N. J. (1993). Hormonal control of transmitter plasticity in insect peptidergic neurons: I. Steroid regulation of the decline in cardioacceleratory peptide 2 (CAP2) expression. J. Exp. Biol. 181: 175-194.
31. LU, B., FU, W-M., GREENGARD, P., and POO, M-M. (1993). Calcitonin gene-related peptide potentiates synaptic responses at developing neuromuscular junction. Nature 363:76-79.
32. MARDER, E., CALABRESE, R. L., NUSBAUM, M. P., and TRIMMER, B. (1987). Distribution and partial characterization of FMRFamide-like peptides in the stomatogastric nervous systems of the rock crab. Cancer borealis, and the spiny lobster, Panulirus interruptus. J. Comp. Neurol. 259:150-163.
33. MATTEOLI, M., BALBI, S., SALA, C., CHINI, B., CIMINO, M., VITRAGALLO, M., and FUMAGALLI, G. (1990). Developmentally regulated expression of calcitonin gene-related peptide at mammalian neuromuscular junction. J. Mol. Neurosci. 2:175-184.
34. MELTZER, Y. L. (1971). Hormonal and Attractant Pesticide Technology. Noyes Data Corp., Park Ridge, NJ.
35. MILDE, J. J. and WALLSTEIN, M. (1995). Inhibitory effects of FLRFamide on motor neurons in the central nervous system of the moth, Manduca sexta. In: Gottingen Neurobiology Report. N. Elsner and R. Menzel, Eds. Thieme, Stuttgart, p. 661.
36. MILES, K., GREENGARD, P., HUGANIR, R. L. (1989). Calcitonin gene-related peptide regulates phosphorylation of the nicotinic acetylchotine receptor in rat myotubes. Neuron 2:1517-1524.
37. NAMBU, J. R., MURPHY-ERDOSH, C., ANDREWS, P. C., FEISTNER, G. J., and SCHELLER, R. H. (1988). Isolation and characterization of a Drosophila neuropeptide gene. Neuron 1:55-61.
38. NEW, H. V. and MUDGE, A. W. (1989). Calcitonin generelated peptide regulates muscle acetylcholine receptor synthesis. Nature 323:809-811.
39. NICHOLS, R. (1992a). Isolation and expression of the Drosophila drosulfakinin neural peptide gene product, DKS-I. Mol. Cell. Neurosci. 3:342-347.
40. NICHOLS, R. (1992b). Isolation and structural characterization of Drosophila TDVDHVFLRFamide and FMRFamide-containing neural peptides. J. Mol. Neurosci. 3:213-218.
41. NICHOLS, R., SCHNEUWLY, S. A., and DIXON, J. E. (1988). Identification and characterization of a Drosophila homologue to the vertebrate neuropeptide cholecystokinin. J. Biol. Chem. 263:12167-12170.
42. NORRIS, B. J. and CALABRESE, R. L. (1987). Identification of motor neurons that contain a FMRFamide-like peptide and the effects of FMRFamide of longitudinal muscle in the Medicinal Leech, Hirudo medicinalis. J. Comp. Neurol. 266:95-11.
43. PATTERSON, P. H. and CHUN, L. L. Y. (1977). The induction of acetylcholine synthesis in primary cultures of dissociated rat sympathetic neurons. II. Developmental aspects. Dev. Biol. 60:473-481.
44. POPPER, P. and MICEVYCH, P. E. (1989). The effect of castration on calcitonin gene-related peptide in spinal motoneurons. Neuroendocrinology 50:338-343.
45. POTTER, D. D., LANDIS, S. C., MATSUMOTO, S. G., and FURSHPAN, E. J. (1986). Synaptic functions in rat sympathetic neurons in microcultures II: Adrenergic/ cholinergic dual status and plasticity. J. Neurosci. 6: 1080-1098.
46. PRESCOTT, D. J., HILDEBRAND, J. G., SANES, J. R., and JEWETT, S. (1977). Biochemical and developmental studies of acetylcholine metabolism in the central nervous system of the moth, Manduca sexta. Comp. Biochem. Physiol. 56C:77-84.
47. RIDDIFORD, L. M. (1988). Hormone action on the cellular level. In: Comprehensive Insect Physiology, Biochemistry and Pharmacology, GA Kerkut and L. I. Gilbert, Eds. Pergamon Press, New York.
48. ROBB, S., and EVANS, P. D. (1994). The modulatory effect of Schisto FLRF amide on heart and skeletal muscle in the locust Schistocerca gregaria. J. Exp. Biol. 197:437-442.
49. ROBB, S., PACKMAN, L. C., and EVANS, P. D. (1989). Isolation, primary structure and bioactivity of SchistoFLRFamide neuropeptide from the locust, Schistocerca gregaria. Biochem. Biophys. Res. Commun. 160: 850-856.
50. SANES, J. R. and HILDEBRAND, J. G. (1976). Acetylcholine and its metabolic enzymes in developing antennae of the moth, Manduca sexta. Dev. Biol. 52:105-120.
51. SANES, J. R., PRESCOTT, D. J., and HILDEBRAND, J. G. (1977). Cholinergic neurochemical development of normal and deafferented antennal lobes in the brain of the moth, Manduca sexta. Brain Res. 119:389-402.
52. 2 (FMRFamide). Proc. Natl. Acad. Sci. USA 85: 1993-1997.
53. SCHOTZINGER, R. J. and LANDIS, S. C. (1990). Acquisition of cholinergic and peptidergic properties by sympathetic innervation of rat sweat glands requires interactions with normal targets. Neuron 5:91-100.
54. SCHWARTZ, L. M. and TRUMAN, J. W. (1983). Hormonal control of rates of metamorphic development in the tobacco hornworm, Manduca sexta. Dev. Biol. 99:103-114.
55. SHAFER, R. (1973). Acetylcholine: fast axoplasmic transport in insect chemoreceptor fibers. Science 180: 315-317.
56. SHANKLAND, D. L., ROSE, J. A., and DONNIGER, C. (1971). The cholinergic nature of the cereal nerve-giant fiber system in the sixth abdominal ganglion of the American cockroach, Periplaneta americana. (L.) J. Neurobiol. 2:247-262.
57. STEVENS, R. F. and LANDIS, S. C. (1987). Developmental interactions between sweat glands and the sympathetic neurons which innervate them: effects of delayed innervation on neurotransmitter plasticity and gland maturation. Dev. Biol. 130:703-720.
58. TAKAMI, K., KAWAI, Y., UCHIDA, S., TOHYAMA, M., SHIOTANI, Y., YOSHIDA, H., EMSON, P. C., GIRGIS, S., HILLYARD, C. J., and MACINTRYRE, I. (1985). Effect of calcitonin gene-related peptide on contraction of striated muscle in the mouse. Neurosci. Lett. 60:227-230.
59. TAYLOR, H. M. and TRUMAN, J. W. (1974). Metamorphosis of the abdominal ganglia of the tobacco hornworm, Manduca sexta. J. Comp. Physiol. 90:367-388.
60. TRUMAN, J. W. (1992). Developmental neuroethology of insect metamorphosis. J. Neurobiol. 23:1404-1422.
61. TRUMAN, J. W. and LEVINE, R. B. (1983). Cellular events in the nervous system during metamorphosis in the moth, Manduca sexta. In: Current Methods in Cellular Neurobiology, vol 1. J. Barker, Ed. John Wiley & Sons, New York, pp. 16-47.
62. TUBLITZ, N. J. and LOI, P. K. (1993). Hormonal control of transmitter plasticity in insect peptidergic neurons: II. Steroid control of the up-regulation of bursicon expression. J. Exp. Biol. 181:195-212.
63. TUBLITZ, N. J. and SYLWESTER, A. W. (1990). Postembryonic alteration of transmitter phenotype in individually identified peptidergic neurons. J. Neurosci. 10: 161-168.
64. TUBLITZ, N. J. and TRUMAN, J. W. (1985). Identification of neurons containing cardioacceleratory peptides (CAPs) in the ventral nerve cord of the tobacco hawkmoth, Manduca sexta. J. Exp. Biol. 116:395-410.
65. WALL, J. B. and TAGHERT, P. H. (1991). The timing of initial neuropeptide expression by an identified insect neuron does not depend on interactions with its normal peripheral target. J. Neurobiol. 22:935-956.
66. WATSON, A. W. D. and BURROWS, M. (1981). Input and output synapses on identified motoneurons of a locust revealed by the intracellular injection of horseradish peroxidase. Cell Tissue Res. 215:325-332.
67. WITTEN, J. L. and TRUMAN, J. W. (1990). Stage-specific expression of FMRFamide-like immunoreactivity in motoneurons of the tobacco hornworm, Manduca sexta, is mediated by steroid hormones. Soc. Neurosci. Abstr 16:633.
68. WITTEN, J. L. and TRUMAN, J. W. (1991). The regulation of transmitter expression in postembryonic lineages in the moth Manduca sexta. I: Transmitter identification and developmental acquisition of expression. J. Neurosci. 11:1980-1989.
69. WITTEN, J. L., KINGAN, T., SHABONOWITZ, J., and HUNT, D. F. (1993). Isolation and sequencing of two new members of the Manduca sexta FLRFamide family of peptides. Soc. Neurosci. Abstr. 19:1274.
70. ZITNAN, D., SEHNAL, F., MIZOGUCHI, A., ISHIZAKI, H., NAGASAWA, H., and SUZUKI, A. (1990). Developmental changes in the bombyxin- and insulin-like immunoreactive neurosecretory system in the wax moth, Galleria mellonella. Dev. Growth Differ. 32: 637-645.