Steroid hormones, dendritic remodeling and neuronal death: Insights from insect metamorphosis

Brain, Behavior and Evolution

Volumn 54, Issue 1, 1999, Pages 51-60

  Weeks, Janis C ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Apoptosis; Dendrite; Ecdysteroids; Manduca sexta; Metamorphosis; Motoneuron; Nervous system; Programmed cell death; Steroid hormone; Synapse

Indexed keywords

CASPASE; ECDYSTEROID; STEROID HORMONE;

APOPTOSIS; ARTICLE; BEHAVIOR; DENDRITE; ELECTROPHYSIOLOGY; LEPIDOPTERA; METAMORPHOSIS; MONOSYNAPTIC PATHWAY; MOTONEURON; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL;

ANIMALS; CELL DEATH; DENDRITES; ESTROGENS; FEMALE; INSECTS; MALE; MOTOR NEURONS; SYNAPSES; TESTOSTERONE;

AMPHIBIA; ANIMALIA; AVES; INSECTA; INVERTEBRATA; LEPIDOPTERA; MANDUCA; MANDUCA SEXTA; PRIMATES; REPTILIA; RODENTIA; VERTEBRATA;

EID: 0032859348     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000006611     Document Type: Article

References (53)

1. Baker, F.C., L.W. Tsai, C.C. Reuter, and D.A. Schooley (1987) In vivo fluctuation of JH, JH acid, ecdysteroid titer, and JH esterase activity during the development of fifth stadium Manduca sexta. Insect Biochem., 17: 989-996.
2. Bollenbacher, W., S.L. Smith, W. Goodman, and L.I. Gilbert (1981) Ecdysteroid titer during larval-pupal-adult development of the tobacco hornworm, Manduca sexta. Gen. Comp. Endocrin., 44: 302-306.
3. Bottjer, S.W., and A.P. Arnold (1997) Developmental plasticity in neural circuits for a learned behavior. Ann. Rev. Neurosci., 20: 459-481.
4. Breedlove, S.M. (1992) Sexual dimorphism in the vertebrate nervous system. J. Neurosci., 12: 4133-4142.
5. Breedlove, S.M. (1994) Sexual differentiation of the human nervous system. Ann. Rev. Psychol., 45: 389-418.
6. Burek, M.J., and R.W. Oppenheim (1996) Programmed cell death in the developing nervous system. Brain Pathol., 6: 427-446.
7. García-Segura, L.M., J.A. Chowen, A. Párducz, and F. Naftolin (1994) Gonadal hormones as promoters of structural synaptic plasticity: cellular mechanisms. Prog. Neurobiol., 44: 279-307.
8. Gilbert, L.I., J.R. Tata, and B.G. Atkinson (1996) Metamorphosis: postembryonic reprogramming of gene expression in amphibian and insect cells. Academic Press, New York.
9. Glanzman, D.L. (1994) Postsynaptic regulation of the development and long-term plasticity of Aplysia sensorimotor synapses in cell culture. J. Neurobiol., 25: 666-693.
10. Gray, J.R., and J.C. Weeks (1999) Anatomical correlates of a steroid-induced change in synaptic strength during development. Soc. Neurosci. Abstr., 25: in press.
11. Green, D.R., and J.C. Reed (1998) Mitochondria and apoptosis. Science, 281: 1309-1312.
12. Hoffman, K.L., and J.C. Weeks (1998a) Programmed cell death of an identified motoneuron in vitro: temporal requirements for steroid exposure and protein synthesis. J. Neurobiol., 35: 300-322.
13. Hoffman, K.L., and J.C. Weeks (1998b) A cellular pathway that involves caspases underlies the steroid-mediated programmed cell death of motoneurons. Soc. Neurosci. Abstr., 24: 1788.
14. Jacobs, G.A., and J.C. Weeks (1990) Postsynaptic changes at a sensory-to-motor synapse cause the developmental loss of a reflex behavior during insect metamorphosis. J. Neurosci., 10: 1341-1356.
15. Kawata, M. (1995) Roles of steroid hormones and their receptors in structural organization in the nervous system. Neurosci. Res., 24: 1-46.
16. Lawrence, P.A., and G. Morata (1994) Homeobox genes: their function in Drosophila segmentation and pattern formation. Cell, 78: 181-189.
17. Levine, R.B., and J.W. Truman (1985) Dendritic reorganization of abdominal motoneurons during metamorphosis of the moth, Manduca sexta. J. Neurosci., 5: 2424-2431.
18. Levine, R.B., D.B. Morton, and L.L. Restifo (1995) Remodeling of the insect nervous system. Curr. Opin. Neurobiol., 5: 28-35.
19. Lubischer, J.L., and J.C. Weeks (1996) Target muscles and sensory afferents do not influence steroid-regulated, segment-specific death of identified motoneurons in Manduca sexta. J. Neurobiol., 31: 449-460.
20. Lubischer, J.L., L.D. Verhegge, and J.C. Weeks (1999) Respecified larval proleg and body wall muscles circulate hemolymph in developing wings of Manduca sexta pupae. J. Exp. Biol., 202: 787-796.
21. Mangelsdorf, D.J., C. Thummel, M. Beato, P. Herrlich, G. Schütz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and R.M. Evans (1995) The nuclear receptor superfamily: the second decade. Cell. 83: 835-839.
22. Nijhout, H.F. (1994) Insect Hormones. Princeton University Press, New Jersey.
23. Peterson, B.A., and J.C. Weeks (1988) Somatotopic mapping of sensory neurons innervating mechanosensory hairs on the larval prolegs of Manduca sexta. J. Comp. Neurol., 275: 128-144.
24. Richards, G. (1997) The ecdysone regulatory cascades in Drosophila. Adv. Dev. Biol., 5: 81-135.
25. Riddiford, L.M., and J.W. Truman (1994) Hormone receptors and the orchestration of development during insect metamorphosis. In Perspectives in Comparative Endocrinology, National Research Council of Canada, pp. 389-394.
26. Sandstrom, D.J., and J.C. Weeks (1991) Reidentification of larval interneurons in the pupal stage of the tobacco hornworm, Manduca sexta. J. Comp. Neurol., 308: 311-327.
27. Sandstrom, D.J., and J.C. Weeks (1996) Novel dual innervation of a larval proleg muscle by two similar motoneurons in the tobacco hornworm, Manduca sexta. J. Exp. Biol., 199: 775-791.
28. Sandstrom, D.J., and J.C. Weeks (1998) Segment-specific retention of a larval neuromuscular system and its role in a new, rhythmic pupal motor pattern in Manduca sexta. J. Comp. Physiol. A, 183: 283-302.
29. Sapolsky, R.M. (1996) Why stress is bad for your brain. Science, 273: 749.
30. Schwartz, L.M., and J.W. Truman (1983) Hormonal control of rates of metamorphic development in the tobacco hornworm. Manduca sexta. Dev. Biol., 99: 103-114.
31. Steller, H., and M.E. Grether (1994) Programmed cell death on Drosophila. Neuron, 13: 1269-1274.
32. Streichert, L.C., and J.C. Weeks (1995) Decreased monosynaptic sensory input to an identified motoneuron is associated with steroid-mediated dendritic regression during metamorphosis in Manduca sexta. J. Neurosci., 15: 1484-1495.
33. Streichert, L.C., J.T. Pierce, J.A. Nelson, and J.C. Weeks (1997) Steroid hormones act directly to trigger segment-specific programmed cell death of identified motoneurons in vitro. Dev. Biol., 183: 95-107.
34. Susin, S.S., N. Zamzami, and G. Kroemer (1998) Mitochondria as regulators of apoptosis: doubt no more. Biochim. Biophys. Acta. 1366: 151-165.
35. Thornberry, N.A., and Y. Lazebnik (1998) Caspases: enemies within. Science, 281: 1312-1316.
36. Truman, J.W. (1996) Steroid receptors and nervous system metamorphosis in insects. Dev. Neurosci., 18: 87-101.
37. Weeks, J.C. (1987) Time course of hormonal independence for developmental events in neurons and other cell types during insect metamorphosis. Dev. Biol., 124: 163-176.
38. Weeks, J.C. (1999) Metamorphosis as midlife crisis: what to do with the leftover neurons? In The Biology of Early Influences (ed. by R.L. Hyson and F. Johnson), Plenum Publishing Corp., New York, in press.
39. Weeks, J.C., and S.K. Davidson (1994) Influence of interganglionic interactions on steroid-mediated dendritic reorganization and death of proleg motor neurons during metamorphosis in Manduca sexta. J. Neurobiol., 25: 535-554.
40. Weeks, J.C., and K. Ernst-Utzschneider (1989) Respecification of larval proleg motoneurons during metamorphosis of the tobacco hornworm, Manduca sexta: segmental dependence and hormonal regulation. J. Neurobiol., 20: 569-592.
41. Weeks, J.C., and G.A. Jacobs (1987) A reflex behavior mediated by monosynaptic connections between hair afferents and motoneurons in the larval tobacco hornworm. Manduca sexta. J. Comp. Physiol. A, 160: 315-329.
42. Weeks, J.C., and R.B. Levine (1995) Steroid hormone effects on neurons subserving behavior. Curr. Opin. Neurobiol., 5: 809-815.
43. Weeks, J.C., and B.S. McEwen (1997) Modulation of neural circuits by steroid hormones in rodent and insect model systems. In Neurons, Networks, and Motor Behavior (ed. by P.S.G. Stein, S. Grillner, A.I. Selverston, and D.G. Stuart), The MIT Press, Cambridge, Mass., pp. 195-207.
44. Weeks, J.C., and J.W. Truman (1984) Neural organization of peptide-activated ecdysis behaviors during the metamorphosis of Manduca sexta. II. Retention of the proleg motor pattern despite loss of the prolegs at pupation. J. Comp. Physiol. A, 155: 423-433.
45. Weeks, J.C., and J.W. Truman (1985) Independent steroid control of the fates of motoneurons and their muscles during insect metamorphosis. J. Neurosci., 5: 2290-2300.
46. Weeks, J.C., and J.W. Truman (1986) Hormonally mediated reprogramming of muscles and motoneurones during the larval-pupal transformation of the tobacco hornworm, Manduca sexta. J. Exp. Biol., 125: 1-13.
47. Weeks, J.C., S.K. Davidson, and B.H.G. Debu (1993) Effects of a protein synthesis inhibitor on the hormonally mediated regression and death of motoneurons in the tobacco hornworm, Manduca sexta. J. Neurobiol., 24: 125-140.
48. Weeks, J.C., G.A. Jacobs, J.T. Pierce, D.J. Sandstrom, L.C. Streichert, B.A. Trimmer, D.E. Wiel, and E.R. Wood (1997) Neural mechanisms of behavioral plasticity: metamorphosis and learning in Manduca sexta. Brain Behav. Evol., 50: suppl. 1, 69-80.
49. Weeks, J.C., W.M. Roberts, and D.L. Trimble (1992) Hormonal regulation and segmental specificity of motoneuron phenotype during metamorphosis of the tobacco hornworm, Manduca sexta. Dev. Biol., 149: 185-196.
50. Wiel, D.E., and J.C. Weeks (1996) Habituation and dishabituation of the proleg withdrawal reflex in larvae of the hawk moth. Manduca sexta. Behav. Neurosci., 5: 1133-1147.
51. Woolley, C.S., and B.S. McEwen (1993) Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol., 336: 293-306.
52. Woolley, C.S., N.G. Weiland, B.S. McEwen, and P.A. Schwartzkroin (1997) Estradiol increases the sensitivity of hippocampal CA 1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J. Neurosci., 17: 1848-1859.
53. Zee, M.C., and J.C. Weeks (1998) Developmental changes in the steroid hormone signal for segment-specific programmed cell death of motoneurons. Soc. Neurosci. Abstr., 24: 1788.