Filopodial adhesion does not predict growth cone steering events in vivo

Journal of Neuroscience

Volumn 19, Issue 7, 1999, Pages 2589-2600

  Isbister, Carolyn M ^a   O'Connor, Timothy P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adhesion; Filopodia; Growth cones; Guidance mechanisms; Motility; Neuronal development

Indexed keywords

ARTICLE; CELL ADHESION; CELL MOTILITY; EMBRYO; GROWTH CONE; GROWTH REGULATION; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; SECOND MESSENGER;

EID: 0033119116     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-07-02589.1999     Document Type: Article

References (65)

1. Anderson H, Tucker RP (1988) Pioneer neurones use basal lamina as a substratum for outgrowth in the embryonic grasshopper limb. Development 104:601-608.
2. Bentley D, Caudy M (1983) Pioneer axons lose directed growth after selective killing of guidepost cells. Nature 304:62-65.
3. Bentley D, O'Connor TP (1992) Guidance and steering of peripheral pioneer growth cones in grasshopper embryos. In: The nerve growth cone (Letourneau PC, Kater SB, Macagno ER, eds), pp 265-282. New York: Raven.
4. Bentley D, Toroian-Raymond A (1986) Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Nature 323:712-715.
5. Bentley D, Keshishian H, Shankland M, Toroian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper Schistocerca nitens. J Embyol Exp Morphol 54:47-74.
6. Brambilla R, Klein R (1995) Telling axons where to grow: a role for EPH receptor tyrosine kinases in guidance. Mol Cell Neurosci 6:487-492.
7. Calof AL, Lander AD (1991) Relationship between neuronal migration and cell-substratum adhesion: laminin and merosin promote olfactory neuronal migration but arc anti-adhesive. J Cell Biol 115:779-794.
8. Caudy M, Bentley D (1986a) Pioneer growth cone morphologies reveal proximal increases in substrate affinity within leg segments of grasshopper embryos. J Neurosci 6:364-379.
9. Caudy M, Bentley D (1986b) Pioneer growth cone steering along a series of neuronal and non-neuronal cues of different affinities. J Neurosci 6:1781-1795.
10. Chang HY, Takei K, Sydor AM, Born T, Rusnak F, Jay DG (1995) Asymmetric retraction of growth cone filopodia following focal inactivation of calcineurin. Nature 376:686-690.
11. Chien C-B, Rosenthal DE, Harris WA, Holt CE (1993) Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain. Neuron 11:237-251.
12. Condic ML, Bentley D (1989a) Removal of the basal lamina in vivo reveals growth cone-basal lamina adhesive interactions and axonal tension in grasshopper embryos. J Neurosci 9:2678-2686.
13. Condic ML, Bentley D (1989b) Pioneer growth cone adhesion in vivo to boundary cells and neurons after enzymatic removal of basal lamina in grasshopper embryos. J Neurosci 9:2687-2696.
14. Condic ML, Letourneau PC (1997) Ligand-induced changes in integrin expression regulate neuronal adhesion and neurite outgrowth. Nature 389:852-856.
15. Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473-1478.
16. Davenport RW, Dou P, Mills LR, Kater SB (1996) Distinct calcium signaling within neuronal growth cones and filopodia. J Neurobiol 31:1-15.
17. Desai CJ, Gindhart JR, Goldstein LSB, Zin K (1996) Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 84:599-604.
18. Dubreuil RR, MacVicar G, Dissanayake S, Liu C, Homer D, Hortsch M (1996) Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites. J Cell Biol 133:647-655.
19. Forscher P, Smith SJ (1988) Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol 107:1505-1516.
20. Gallo G, Lefcort FB, Letourneau PC (1997) The trkA receptor mediates growth cone turning toward a localized source of nerve growth factor. J Neurosci 17:5445-5454.
21. Gomez TM, Letourneau PC (1994) Filopodia initiate choices made by sensory neuron growth cones at laminin/fibronectin borders in vitro. J Neurosci 14:5959-5972.
22. Gomez TM, Snow DM, Letourneau PC (1995) Characterization of spontaneous calcium transients in nerve growth cones and their effect on growth cone migration. Neuron 14:1233-1246.
23. Gundersen RW (1987) Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. Dev Biol 121:423-431.
24. Gundersen RW (1988) Interference reflection microscopic study of dorsal root growth cones on different substrates: assessment of growth cone-substrate contacts. J Neurosci Res 21:298-306.
25. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509-514.
26. He Q, Dent EW, Meiri KF (1997) Modulation of actin filament behaviour by GAP-43 (neuromodulin) is dependent on the phosphorylation status of serine 41, the protein kinase C site. J Neurosci 17:3515-3524.
27. Heidemann SR, Lamoureux P, Buxbaum RE (1990) Growth cone behaviour and production of traction force. J Cell Biol 111:1949-1957.
28. Hortsch M, Wang Y-ME, Marikar Y, Bieber AJ (1995) The cytoplasmic domain of the Drosophila cell adhesion molecule neuroglian is not essential for its homophilic adhesive properties. J Biol Chem 270:18809-18817.
29. Jan LY, Jan YN (1982) Antibodies to horseradish peroxidase as specific neural markers in Drosophila and grasshopper embryos. Proc Natl Acad Sci USA 79:2700-2704.
30. Kater SB, Rehder V (1995) The sensory-motor role of growth cone filopodia. Curr Opin Neurobiol 5:68-74.
31. Kim Y-t, Wu C-f (1996) Reduced growth cone motility in cultured neurons from Drosophila memory mutants with a defective cAMP cascade. J Neurosci 16:5593-5602.
32. Kolodkin Al, Matthes DJ, O'Connor TP, Pate NH, Admon A, Bentley D, Goodman CS (1992) Fasciclin IV: sequence, expression and function during growth cone guidance in the grasshopper embryo. Neuron 9:831-845.
33. Kreft B, Berndoff D, Bottinger A, Finnemann S, Wedlich D, Hortsch M, Tauber R, Gebner R (1997) LI-cadherin-mediated cell-cell adhesion does not require cytoplasmic interactions. J Cell Biol 136:1109-1121.
34. Krueger NX, Van Vactor D, Wan HI, Gelbart WM, Goodman CS, Saito H (1996) The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84:611-622.
35. Kuhn TB, Schmidt MF, Kater SB (1995) Laminin and fibronectin guideposts signal sustained but opposite effects to passing growth cones. Neuron 14:275-285.
36. Kuhn TB, Wilcox CL, Bamburg JL (1997) RAC1, a small GTPase, alters F-actin organization in motor neuron growth cones regulating both extension and differentiation of neurites. Soc Neurosci Abstr 23:603.
37. Kuhn TB, Williams CV, Dou P, Kater SB (1998) Laminin directs growth cone navigation via two temporally and functionally distinct calcium signals. J Neurosci 18:184-194.
38. Lamoureux P, Zheng J, Buxbaum RE, Heidemann SR (1992) A cytomechanical investigation of neurite growth on different culture surfaces. J Cell Biol 118:655-661.
39. Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84:359-369.
40. Lemmon V, Burden S, Payne HR, Elmslie GJ, Hlavin ML (1992) Neurite growth on different substrates: permissive versus instructive influences and the role of adhesive strength. J Neurosci 12:818-826.
41. Letourneau PC (1975) Cell-to-substratum adhesion and guidance of axonal elongation. Dev Biol 44:92-101.
42. Letourneau PC, Shattuck TA, Ressler AH (1987) "Pull" and "push" in neurite elongation: observations on the effects of different concentrations of cytochalasin B and taxol. Cell Motil Cytoskeleton 8:193-209.
43. Lewis AK, Bridgman PC (1992) Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J Cell Biol 119:1219-1243.
44. Lin C-H, Forscher P (1995) Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron 14:763-771.
45. Lin C-H, Thompson CA, Forscher P (1994) Cytoskeletal reorganization underlying growth cone motility. Curr Opin Neurobiol 4:640-647.
46. Luo L, Jan LY, Jan Y-n (1997) Rho family small GTP-binding proteins in growth cone signalling. Curr Biol 7:81-86.
47. MacLean-Fletcher S, Pollard TD (1980) Mechanism of action of cytochalasin B on actin. Cell 20:329-341.
48. Marsh L, Letourneau PC (1984) Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J Cell Biol 99:2041-2047.
49. Mitchison TJ, Cramer LP (1996) Actin-based cell motility and cell locomotion. Cell 84:371-379.
50. Myers PZ, Bastiani MJ (1993) Growth cone dynamics during the migration of an identified commissural growth cone. J Neurosci 13:127-143.
51. 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 vivo. J Cell Biol 123:935-948.
52. O'Connor TP, Duerr JS, Bentley D (1990) Pioneer growth cone steering decisions mediated by single filopodial contacts in vivo. J Neurosci 10:3935-3946.
53. Regen CM, Horwitz AF (1992) Dynamics of b1 integrin-mediated adhesive contacts in motile fibroblasts. J Cell Biol 117:1321-1330.
54. Sabry JH, O'Connor TP, Evans L, Toroian-Raymond A, Kirschner M, Bentley D (1991) Microtubule behaviour during guidance of pioneer neuron growth cones in situ. J Cell Biol 115:381-395.
55. Saffell JL, Williams EJ, Mason IJ, Walsh FS, Doherty P (1997) Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs. Neuron 18:231-242.
56. Sampath P, Pollard TD (1991) Effects of cytochalasins, phalloidin, and pH on the elongation of actin filaments. Biochemistry 30:1972-1980.
57. Sanchez D, Ganfornina MD, Bastiani MJ (1995) Contributions of an orthopteran to the understanding of neuronal pathfinding. Immunol Cell Biol 73:565-574.
58. Schliwa M (1982) Action of cytochalasin D on cytoskeletal networks. J Cell Biol 92:79-91.
59. Schmidt CE, Horwitz AF, Lauffenburger DA, Sheetz MP (1993) Integrin-cytoskeletal interactions in migrating fibroblasts are dynamic, asymmetric, and regulated. J Cell Biol 123:977-991.
60. Shapiro L, Fannon AM, Kwong PD, Thompson A, Lehmann MS, Grubel G, Legrand JF, Als JJ, Colman DR, Hendrickson WA (1995) Structural basis of cell-cell adhesion by cadherins. Nature 374:327-337.
61. Song H-j, Ming G-l, Poo M-m (1997) cAMP-induced switching in turning direction of nerve growth cones. Nature 388:275-279.
62. Tsai A, Wong S, Isbister C, Kolodkin AL, O'Connor TP (1997) Characterization of grasshopper semaphorin II. Soc Neurosci Abstr 23:613.
63. Williams EJ, Doherty P, Turner G, Reid RA, Henperly JJ, Walsh FS (1992) Calcium influx into neurons can solely account for cell contact-dependent neurite outgrowth stimulated by transfected L1. J Cell Biol 119:883-892.
64. Wong JTW, Yu WTC, O'Connor TP (1997) Transmembrane grasshopper semaphorin I promotes axon outgrowth in vivo. Development 124:3597-3607.
65. Zheng JQ, Wan J-j, Poo M-m (1996) Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16:1140-1149.