Acute morphogenic and chemotropic effects of neurotrophins on cultured embryonic xenopus spinal neurons

Journal of Neuroscience

Volumn 17, Issue 20, 1997, Pages 7860-7871

  Ming, Guo Il ^a,b   Lohof, Ann M ^a,c   Zheng, James Q ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Actin; Chemotropism; Growth cone; Lamellipodium; Neurotrophic factors; Turning

Indexed keywords

BRAIN DERIVED GROWTH FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; GROWTH CONE; LAMELLIPODIUM; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SPINAL CORD NERVE CELL; XENOPUS;

EID: 0030772343     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-20-07860.1997     Document Type: Article

References (83)

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. Bailey CH, Chen M (1988) Long-term sensitization in Aplysia increases the number of presynaptic contacts onto the identified gill motor neuron L7. Proc Natl Acad Sci USA 85:9356-9359.
3. Bailey CH, Kandel ER (1993) Structural changes accompanying memory storage. Annu Rev Physiol 55:397-426.
4. Barbacid M (1994) The Trk family of neurotrophin receptors. J Neurobiol 25:1386-1403.
5. Barbacid M (1995) Neurotrophic factors and their receptors. Curr Opin Cell Biol 7:148-155.
6. Barde YA (1989) Trophic factors and neuronal survival. Neuron 2:1525-1534.
7. Barde YA (1990) The nerve growth factor family. Prog Growth Factor Res 2:237-248.
8. Barker SA, Caldwell KK, Hall A, Martincz AM, Pfeifer JR, Oliver JM, Wilson BS (1995) Wortmannin blocks lipid and protein kinase activities associated with PI 3-kinase and inhibits a subset of responses induced by Fc epsilon R1 cross-linking. Mol Biol Cell 6:1145-1158.
9. Berninger B, Poo MM (1996) Fast actions of neurotrophic factors. Curr Opin Neurobiol 6:324-330.
10. Boulton TG, Nye SH, Robbins DJ, Ip NY, Radzicjewska E, Morgenbesser SD, DePinho RA, Panayotatos N, Cobb MH, Yancopoulos GD (1991) ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65:663-675.
11. Bray D, White JG (1988) Cortical flow in animal cells. Science 239:883-888.
12. Chao MV (1992) Neurotrophin receptors: a window into neuronal differentiation. Neuron 9:583-593.
13. Cohen-Cory S, Fraser SE (1995) Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378:192-196.
14. Connolly JL, Seeley PJ, Greene LA (1985) Regulation of growth cone morphology by nerve growth factor: a comparative study by scanning electron microscopy. J Neurosci Res 13:183-198.
15. Connolly JL, Seeley PJ, Greene LA (1987) Rapid regulation of neuronal growth cone shape and surface morphology by nerve growth factor. Neurochem Res 12:861-868.
16. Davies AM (1994) The role of neurotrophins in the developing nervous system. J Neurobiol 25:1334-1348.
17. Davies AM, Bandtlow C, Heumann R, Korsching S, Rohrer H, Thoenen H (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353-358.
18. Dechant G, Rodriguez-Tebar A, Barde YA (1994) Neurotrophin receptors. Prog Neurobiol 42:347-352.
19. Desmond NL, Levy WB (1986) Changes in the postsynaptic density with long-term potentiation in the dentate gyrus. J Comp Neurol 253:476-482.
20. Ernfors P, Bengzon J, Kokaia Z, Persson H, Lindvall O (1991) Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7:165-176.
21. Funakoshi H, Frisen J, Barbany G, Timmusk T, Zachrisson O, Verge VM, Persson H (1993) Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123:455-465.
22. Glanzman DL, Kandel ER, Schacher S (1990) Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249:799-802.
23. Greene LA, Kaplan DR (1995) Early events in neurotrophin signalling via Trk and p75 receptors. Curr Opin Neurobiol 5:579-587.
24. Griffin CG, Letourneau PC (1980) Rapid retraction of neurites by sensory neurons in response to increased concentrations of nerve growth factor. J Cell Biol 86:156-161.
25. Gundersen RW, Barrett JN (1980) Characterization of the turning response of dorsal root neurites toward nerve growth factor. J Cell Biol 87:546-554.
26. Halegoua S (1987) Changes in the phosphorylation and distribution of vinculin during nerve growth factor induced neurite outgrowth. Dev Biol 121:97-104.
27. Hallböök F, Ibanez CF, Persson H (1991) Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6:845-858.
28. Hallböök F, Ibanez CF, Ebendal T, Persson H (1993) Cellular localization of brain-derived neurotrophic factor and neurotrophin-3 mRNA expression in the early chicken embryo. Eur J Neurosci 5:1-14.
29. Henderson CE, Camu W, Mettling C, Gouin A, Poulsen K, Karihaloo M, Rullamas J, Evans T, McMahon SB, Armanini MP, Berkemeier L, Phillips HS, Rosenthal A (1993) Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363:266-270.
30. Heumann R (1994) Neurotrophin signalling. Curr Opin Neurobiol 4:668-679.
31. Hyman C, Hofer M, Barde YA, Juhasz M, Yancopoulos GD, Squinto SP, Lindsay RM (1991) BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350:230-232.
32. Ip NY, Yancopoulos GD (1995) Neurotrophic factors and their receptors. Prog Brain Res 105:189-195.
33. Isackson PJ, Huntsman MM, Murray KD, Gall CM (1991) BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron 6:937-948.
34. Kaplan DR, Stephens RM (1994) Neurotrophin signal transduction by the Trk receptor. J Neurobiol 25:1404-1417.
35. Kater SB, Mills LR (1991) Regulation of growth cone behavior by calcium. J Neurosci 11:891-899.
36. Kennedy TE, Tessier-Lavigne M (1995) Guidance and induction of branch formation in developing axons by target-derived diffusible factors. Curr Opin Neurobiol 5:83-90.
37. Klein R (1994) Role of neurotrophins in mouse neuronal development. FASEB J 8:738-744.
38. Knusel B, Hefti F (1992) K-252 compounds: modulators of neurotrophin signal transduction. J Neurochem 59:1987-1996.
39. Kotani K, Hara K, Kotani K, Yonezawa K, Kasuga M (1995) Phosphoinositide 3-kinase as an upstream regulator of the small GTP-binding protein Rac in the insulin signaling of membrane ruffling. Biochem Biophys Res Commun 208:985-990.
40. Kuffler DP (1994) Promoting and directing axon outgrowth. Mol Neurobiol 9:233-243.
41. Letourneau PC (1978) Chemotactic response of nerve fiber clongation to nerve growth factor. Dev Biol 66:183-196.
42. Lewin GR, Barde YA (1996) Physiology of the neurotrophins. Annu Rev Neurosci 19:289-317.
43. Lo DC (1995) Neurotrophic factors and synaptic plasticity. Neuron 15:979-981.
44. Lohof AM, Quillan M, Dan Y, Poo MM (1992) Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. J Neurosci 12:1253-1261.
45. Lohof AM, Ip NY, Poo MM (1993) Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363:350-353.
46. Lu B, Yokoyama M, Dreyfus CF, Black IB (1991) Depolarizing stimuli regulate nerve growth factor gene expression in cultured hippocampal neurons. Proc Natl Acad Sci USA 88:6289-6292.
47. Lumsden AC, Davies AM (1983) Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor. Nature 306:786-788.
48. Lundborg G, Dahlin L, Danielsen N, Zhao Q (1994) Trophism, tropism, and specificity in nerve regeneration. J Reconstr Microsurg 10:345-354.
49. Maisonpierre PC, Belluscio L, Friedman B, Alderson RF, Wiegand SJ, Furth ME, Lindsay RM, Yancopoulos GD (1990) NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5:501-509.
50. Mason CA, Wang LC (1997) Growth cone form is behavior-specific and, consequently, position-specific along the retinal axon pathway. J Neurosci 17:1086-1100.
51. McAllister AK, Lo DC, Katz LC (1995) Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15:791-803.
52. McAllister AK, Katz LC, Lo DC (1996) Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17:1057-1064.
53. McTigue M, Cremins J, Halegoua S (1985) Nerve growth factor and other agents mediate phosphorylation and activation of tyrosine hydroxylase. A convergence of multiple kinase activities. J Biol Chem 260:9047-9056.
54. Menesini-Chen MG, Chen JS, Levi-Montalcini R (1978) Sympathetic nerve fibers ingrowth in the central nervous system of neonatal rodent upon intraccrebral NGF injections. Arch Ital Biol 116:53-84.
55. Nieuwkoop PD, Faber J (1967) Normal table of Xenopus laevis. Amsterdam: Elsevier.
56. Obermeier A, Lammers R, Wiesmuller K H, Jung G, Schlessinger J, Ullrich A (1993) Identification of Trk binding sites for SHC and phosphatidylinositol 3′-kinase and formation of a multimeric signaling complex. J Biol Chem 268:22963-22966.
57. Obermeier A, Bradshaw RA, Seedorf K, Choidas A, Schlessinger J, Ullrich A (1994) Neuronal differentiation signals are controlled by nerve growth factor receptor/Trk binding sites for SHC and PLC gamma. EMBO J 13:1585-1590.
58. Ohmichi M, Decker SJ, Saltiel AR (1992) Activation of phosphatidylinositol-3 kinase by nerve growth factor involves indirect coupling of the trk proto-oncogene with src homology 2 domains. Neuron 9:769-777.
59. Parker PJ (1995) Intracellular signalling. PI 3-kinase puts GTP on the Rac. Curr Biol 5:577-579.
60. Patterson SL, Grover LM, Schwartzkroin PA, Bothwell M (1992) Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9:1081-1088.
61. Ruit KG, Elliott JL, Osborne PA, Van Q, Snider WD (1992) Selective dependence of mammalian dorsal root ganglion neurons on nerve growth factor during embryonic development. Neuron 8:573-587.
62. Sato M, Lopez-Mascaraque L, Heffner CD, O'Leary DD (1994) Action of a diffusible target-derived chemoattractant on cortical axon branch induction and directed growth. Neuron 13:791-803.
63. Schnell L, Schneider R, Kolbeck R, Barde YA, Schwab ME (1994) Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367:170-173.
64. Seeley PJ, Greene LA (1983) Short-latency local actions of nerve growth factor at the growth cone. Proc Natl Acad Sci USA 80:2789-2793.
65. Segal RA, Greenberg ME (1996) Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 19:463-389.
66. Segal RA, Takahashi H, McKay RD (1992) Changes in neurotrophin responsiveness during the development of cerebellar granule neurons. Neuron 9:1041-1052.
67. Small JV, Rinnerthaler G, Hinssen H (1982) Organization of actin meshworks in cultured cells: the leading edge. Cold Spring Harb Symp Quant Biol 46:599-611.
68. Smith SJ (1988) Neuronal cytomechanics: the actin-based motility of growth cones. Science 242:708-715.
69. Snider WD (1994) Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77:627-638.
70. Snider WD, Johnson Jr EM (1989) Neurotrophic molecules. Ann Neurol 26:489-506.
71. Song H-j, Ming G-I, Poo MM (1997) cAMP-induced switching in turning direction of nerve growth cones. Nature 338:275-279.
72. Spitzer NC, Lamborghini JE (1976) The development of the action potential mechanism of amphibian neurons isolated in culture. Proc Natl Acad Sci USA 73:1641-1645.
73. Stoop R, Poo MM (1996) Synaptic modulation by neurotrophic factors differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J Neurosci 16:3256-3264.
74. Tabti N, Poo MM (1990) Culturing spinal cord neurons and muscle cells from Xenopus embryos. In: Culturing nerve cells (Banker G, Goslin K, eds). pp 137-154. Cambridge, MA: Massachusetts Institute of Technology.
75. Tanaka E, Sabry J (1995) Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-176.
76. Tapley P, Lamballe F, Barbacid M (1992) K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7:371-381.
77. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133.
78. Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270:593-598.
79. Vetter ML, Martin-Zanca D, Parada LF, Bishop JM, Kaplan DR (1991) Nerve growth factor rapidly stimulates tyrosine phosphorylation of phospholipasc C-gamma 1 by a kinase activity associated with the product of the trk protooncogene. Proc Natl Acad Sci USA 88:5650-5654.
80. Wennstrom S, Hawkins P, Cooke F, Hara K, Yonezawa K, Kasuga M, Jackson T, Claesson-Welsh L, Stephens L (1994) Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr Biol 4:385-393.
81. Zhang L, Schmidt RE, Yan O, Snider WD (1994) NGF and NT-3 have differing effects on the growth of dorsal root axons in developing mammalian spinal cord. J Neurosci 14:5187-5201.
82. Zheng JQ, Felder M, Connor JA, Poo MM (1994) Turning of nerve growth cones induced by neurotransmitters. Nature 368:140-144.
83. Zheng JQ, Wan JJ, Poo MM (1996) Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16:1140-1149.