Steroid hormone enhancement of neurite outgrowth in identified insect motor neurons involves specific effects on growth cone form and function

Journal of Neurobiology

Volumn 38, Issue 1, 1999, Pages 27-45

  Matheson, Stephen F ^a,c   Levine, Richard B ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Cell culture; Cytoskeleton; Ecdysone; Growth cone; Insect; Metamorphosis; Morphometry; Neurite outgrowth; Steroid hormone

Indexed keywords

ECDYSTEROID; STEROID HORMONE;

ARTICLE; CYTOSKELETON; GROWTH CONE; GROWTH REGULATION; HORMONAL REGULATION; HORMONE ACTION; LEPIDOPTERA; METAMORPHOSIS; MOTONEURON; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELLS, CULTURED; ECDYSTEROIDS; GROWTH CONES; INSECT HORMONES; LARVA; MANDUCA; MOTOR NEURONS; NEURITES; PUPA; STEROIDS;

EID: 0032945454     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199901)38:1<27::AID-NEU3>3.0.CO;2-U     Document Type: Article

References (84)

1. Aletta JM, Greene LA 1988. Growth cone configuration and advance: a time-lapse study using video-enhanced differential interference contrast microscopy. J Neurosci 8:1425-1435.
2. Arnold AP, Gorski RA 1984. Gonadal steroid induction of structural sex differences in the central nervous system, Annu Rev Neurosci 7:413-442.
3. Banker G, Goslin K. 1991. Characterizing and studying neuronal cultures. In: Banker G, Goslin K, editors. Culturing Nerve Cells. Cambridge, MA: MIT Press, p 94-95.
4. Bastmeyer M, O'Leary DDM 1996. Dynamics of target recognition by interstitial axon branching along developing cortical axons. J Neurosci 16:1450-1459.
5. Bentley D, O'Connor TP 1994. Cytoskeletal events in growth cone steering. Curr Opin Neurobiol 4:43-48.
6. Bollenbacher WE, Smith SL, Goodman W, Gilbert LI. 1981. Ecdysteroid titer during larval-pupal-adult development of the tobacco hornworm, Manduca sexta. Gen Comp Endocrinol 44:302-306.
7. Brandt R, Léger J, Lee G. 1995. Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J Cell Biol 131:1327-1340.
8. Bray D. 1973. Branching patterns of individual sympathetic neurons in culture. J Cell Biol 56:702-712.
9. Breedlove SM. 1992. Sexual dimorphism in the vertebrate nervous system. J Neurosci 12:4133-4142.
10. Bridgman PC, Dailey ME. 1989. The organization of myosin and actin in rapid frozen nerve growth cones. J Cell Biol 108:95-109.
11. Brinton RD. 1993. 17β-Estradiol induction of filopodial growth in cultured hippocampal neurons within minutes of exposure. Mol Cell Neurosci 4:36-46.
12. Brugg B, Reddy D, Matus A. 1993. Attenuation of microtubule-associated protein 1B expression by antisense oligodeoxynucleotides inhibits initiation of neurite outgrowth. Neuroscience 52:489-496.
13. Brushart TM. 1993. Motor axons preferentially reinnervate motor pathways. J Neurosci 13:2730-2738.
14. Càceres A, Kosik KS. 1990. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343:461-463.
15. Cáceres A, Mautino J, Kosik KS. 1992. Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 9:607-618.
16. Cambiazo V, Gonzalez M, Maccioni RB. 1995. DMAP-85: a tau-like protein from Drosophila melanogaster larvae. J Neurochem 64:1288-1297.
17. Chamak B, Fellous A, Glowinski J, Prochiantz A. 1987. MAP2 expression and neuritic outgrowth and branching are coregulated through region-specific neuro-astroglial interactions. J Neurosci 7:3163-3170.
18. Condeelis J. 1993. Life at the leading edge: the formation of cell protrusions. Annu Rev Cell Biol 9:411-444.
19. Consoulas C, Kent KS, Levine RB. 1996. Remodeling of the peripheral processes and presynaptic terminals of leg motoneurons during metamorphosis of the hawk moth, Manduca sexta. J Comp Neurol 372:415-434.
20. Consoulas C, Levine RB. 1997. Accumulation and proliferation of adult leg muscle precursors in Manduca are dependent on innervation. J Neurobiol 32:531-553.
21. Dìaz H, Lorenzo A, Carrer HF, Càceres A. 1992. Time lapse study of neurite growth in hypothalamic dissociated neurons in culture: sex differences and estrogen effects. J Neurosci Res 33:266-281.
22. Dotti CG, Sullivan CA, Banker GA. 1988. The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
23. Egid K, Lnenicka GA. 1993. Regeneration from crayfish phasic and tonic motor axons in vitro. J Neurobiol 24: 1111-1120.
24. Esmaeli-Azad B, McCarty JH, Feinstein SC. 1994. Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J Cell Sci 107:869-879.
25. Ferhat L, Represa A, Bernard A, Ben-Ari Y, Khrestchatisky M. 1996. MAP2d promotes bundling and stabilization of both microtubules and microfilaments. J Cell Sci 109: 1095-1103.
26. Ferreira A, Càceres A. 1991. Estrogen-enhanced neurite growth: evidence for a selective induction of tau and stable microtubules. J Neurosci 11:392-400.
27. 2+-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity? Neuron 16:233-236.
28. Goedert M, Baur CP, Ahringer J, Jakes R, Hasegawa M, Spillantini MG, Smith MJ, Hill F. 1996. PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J Cell Sci 109:2661-2672.
29. Goldberg DJ, Burmeister DW 1986. Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J Cell Biol 103:1921-1931.
30. Goldstein LA, Sengelaub DR. 1994. Differential effects of dihydrotestosterone and estrogen on the development of motoneuron morphology in a sexually dimorphic rat spinal nucleus. J Neurobiol 25:878-892.
31. Gould E, Woolley CS, Frankfurt M, McEwen BS 1990. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10: 1286-1291.
32. Griffith LM, Pollard TD. 1982. The interaction of actin with microtubules and microtubule-associated proteins. J Biol Chem 257:9143-9151.
33. Grünewald B, Levine RB. 1998. Ecdysteroid control of ionic current development in Manduca sexta motoneurons. J Neurobiol 37:211-223.
34. Hanzel DK, Pickett SC. 1993. Labeling microtubules. In: CLSM applications manual. Sunnyvale, CA: Molecular Dynamics Corp.
35. Harris WA, Holt CE, Bonhoeffer F. 1987. Retinal axons with and without their somata growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. Development 101:123-133.
36. Hartwig JH, Bokoch GM, Carpenter CL, Janmey PA, Taylor LA, Toker A, Stossel TP 1995. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82:643-653.
37. Hayashi JH, Hildebrand JG. 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.
38. Hayashi JH, Levine RB. 1992. Calcium and potassium currents in leg motoneurons during postembryonic development in the hawkmoth Manduca sexta. J Exp Biol 171:15-42.
39. Innocenti GM. 1988. Loss of axonal projections in the development of the mammalian brain. In: Parnavelas JG, Stern CD, Stirling RV, editors. The making of the nervous system. New York: Oxford University Press. p 319-339.
40. Kater S, Mills L. 1991. Regulation of growth cone behavior by calcium. J Neurosci 11:891-899.
41. Kent KS. 1992. Influences on postembryonic dendritic changes in an identified leg motor neuron. Soc Neurosci Abstr 18:602.
42. Kent KS, Levine RB. 1993. Dendritic reorganization of an identified neuron during metamorphosis of the moth Manduca sexta: the influence of interactions with the periphery. J Neurobiol 24:1-22.
43. Kim Y-T, Wu C-F. 1987. Reversible blockage of neurite development and growth cone formation in neuronal cultures of a temperature-sensitive mutant of Drosophila. J Neurosci 7:3245-3255.
44. Koester SE, O'Leary DDM. 1992. Functional classes of cortical projection neurons develop dendritic distinctions by class-specific sculpting of an early common pattern. J Neurosci 12:1382-1393.
45. Kurz EM, Sengelaub DR, Arnold AP. 1991. Androgens regulate the dendritic length of mammalian motoneurons in adulthood. Science 232:395-398.
46. Letourneau PC. 1983. Differences in the organization of actin in the growth cones compared with the neurites of cultured neurons from chick embryos. J Cell Biol 97: 963-973.
47. Letourneau PC, Shattuck TA, Ressler AH. 1986. Branching of sensory and sympathetic neurites in vitro is inhibited by treatment with taxol. J Neurosci 6:1912-1917.
48. Levine RB, Fahrbach SE, Weeks JC. 1991. Steroid hormones and the reorganization of the nervous system during insect metamorphosis. Semin Neurosci 3:437-447.
49. Levine RB, Truman JW. 1985. Dendritic reorganization of abdominal motoneurons during metamorphosis of the moth, Manduca sexta. J Neurosci 5: 2424-2431.
50. Levine RB, Weeks JC. 1996. Cell culture approaches to understanding the actions of steroid hormones on the insect nervous system. Dev Neurosci 18:73-86.
51. Lin C-H, Forscher P. 1993. Cytoskeletal remodeling during growth cone-target interactions. J Cell Biol 121:1369-1383.
52. Lin C-H, Thompson CA, Forscher P. 1994. Cytoskeletal reorganization underlying growth cone motility. Curr Opin Neurobiol 4:640-647.
53. Mandelkow E, Mandelkow EM. 1995. Microtubules and microtubule-associated proteins. Curr Opin Cell Biol 7:72-81.
54. Mitchison T, Kirschner M. 1988. Cytoskeletal dynamics and nerve growth. Neuron 1:761-772.
55. Moraga DM, Nuñez P, Garrido J, Maccioni RB. 1993. A tau fragment containing a repetitive sequence induces bundling of actin filaments. J Neurochem 61:979-986.
56. Murphy DD, Segal M. 1996. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16:4059-4068.
57. Neely MD, Nicholls JG. 1995. Electrical activity, growth cone motility and the cytoskeleton. J Exp Biol 198:1433-1446.
58. O'Connor TP, Bentley D. 1993. Accumulation of actin in subsets of pioneer growth cone filopodia in response to neural and epithelial guidance cues in situ. J Cell Biol 123:935-948.
59. O'Connor TP, Duerr JS, Bentley D. 1990. Pioneer growth cone steering decisions mediated by single filopodial contacts in situ. J Neurosci 10:3935-3946.
60. O'Leary DDM, Terashima T. 1988. Cortical axons branch to multiple subcortical targets by interstitial axon budding: implications for target recognition and "waiting periods." Neuron 1:901-910.
61. Pedrotti B, Colombo R, Islam K. 1994. Microtubule associated protein MAP1A is an actin-binding and crosslinking protein. Cell Motil Cytoskel 29:110-116.
62. Prugh J, Della Croce K. Levine RB. 1992. Effects of the steroid hormone, 20-hydroxyecdysone, on the growth of neuntes by identified insect motoneurons in vitro. Dev Biol 154:331-347.
63. Rivas RJ, Burmeister DW, Goldberg DJ. 1992. Rapid effects of laminin on the growth cone. Neuron 8:107-115.
64. Sabry JH, O'Connor TP, Evans L, Toroian-Raymond A, Kirschner M, Bentley D. 1991. Microtubule behavior during guidance of pioneer neuron growth cones in situ. J Cell Biol 115:381-395.
65. Saffell JL, Walsh FS, Doherty P. 1992. Direct activation of second messenger pathways mimics cell adhesion molecule-dependent neunte outgrowth. J Cell Biol 118:663-670.
66. Sato M, Lopez-Mascaraque L, Heffner CD, O'Leary DDM. 1994. Action of a diffusible target-derived chemoattractant on cortical axon branch induction and directed growth. Neuron 13:791-803.
67. Simon DK, O'Leary DDM. 1992. Development of topographic order in the mammalian retinocollicular projection. J Neurosci 12:1212-1232.
68. Smith CL. 1994. Cytoskeletal movements and substrate interactions during initiation of neurite outgrowth by sympathetic neurons in vitro. J Neurosci 14:384-398.
69. Smith SJ. 1988. Neuronal cytomechanics: the actin-based motility of growth cones. Science 242:708-715.
70. Stewart J, Kolb B. 1994. Dendritic branching in cortical pyramidal cells in response to ovariectomy in adult female rats: suppression by neonatal exposure to testosterone. Brain Res 654:149-154.
71. Streichert LC, Pierce JT, Nelson JA, Weeks JC. 1997. Steroid hormones act directly to trigger segment-specific programmed cell death of identified motoneurons in vitro. Dev Biol 183:95-107.
72. Tanaka EM, Kirschner MW. 1991. Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol 115:345-363.
73. Tanaka EM, Kirschner MW. 1995. The role of microtubules in growth cone turning at substrate boundaries. J Cell Biol 128:127-137.
74. Tanaka E, Sabry J. 1995. Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-176.
75. Truman JW, Reiss SE. 1988. Hormonal regulation of the shape of identified motoneurons in the moth Manduca sexta. J Neurosci 8:765-775.
76. Weeks JC. 1987. Time course of hormonal independence for developmental events in neurons and other cell types during insect metamorphosis. Dev Biol 124:163-176.
77. Weeks JC, Ernst-Utzschneider K. 1989. Respecification of larval proleg motoneurons during metamorphosis of the tobacco hornworm, Manduca sexta: segmental dependence and hormonal regulation. J Neurobiol 20:569-592.
78. Weeks JC, Truman JW. 1985. Independent steroid control of the fates of motoneurons and their muscles during insect metamorphosis. J Neurosci 5:2290-2300.
79. Weeks JC, Truman JW. 1986. Steroid control of neuron and muscle development during the metamorphosis of an insect. J Neurobiol 17:249-267.
80. Wessells NK, Nuttall RP. 1978. Normal branching, induced branching, and steering of cultured parasympathetic motor neurons. Exp Cell Res 115:111-122.
81. Williams CV, Davenport RW, Dou P, Kater SB. 1995. Developmental regulation of plasticity along neurite shafts. J Neurobiol 27:127-140.
82. Williams EJ, Furness J, Walsh FS, Doherty P. 1994. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin. Neuron 13: 583-594.
83. Yu W, Ahmad FJ, Baas PW. 1994. Microtubule fragmentation and partitioning in the axon during collateral branch formation. J Neurosci 14:5872-5884.
84. Zou D-J, Cline HT. 1996. Expression of a constitutively active CaMKII in target tissue modifies presynaptic axon arbor growth. Neuron 16:529-539.