Axon guidance by growth cones and branches: Common cytoskeletal and signaling mechanisms

Neuroscientist

Volumn 9, Issue 5, 2003, Pages 343-353

  Dent, Erik W ^a,b   Tang, Fangjun ^a   Kalil, Katherine ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Axon branching; Calcium; Cortical development; Cytoskeleton; Growth cone

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM ION; F ACTIN; NIFEDIPINE;

ACTIN FILAMENT; CENTRAL NERVOUS SYSTEM; CYTOSKELETON; GROWTH CONE; MICROTUBULE; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INJURY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CALCIUM SIGNALING; CYTOSKELETON; GROWTH CONES; HUMANS;

EID: 0141676512     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858403252683     Document Type: Review

References (60)

1. Bagnard D, Lohrum M, Uziel D, Puschel AW, Bolz J. 1998. Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development 125:5043-53.
2. Bagri A, Marin O, Plump AS, Mak J, Pleasure SJ, Rubenstein JL, and others. 2002. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain, Neuron 33:233-48.
3. Bashaw GJ, Kidd T, Murray D, Pawson T, Goodman CS. 2000. Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101:703-15.
4. Bear JE, Krause M, Gertler FB. 2001. Regulating cellular actin assembly. Curr Opin Cell Biol 13:158-66.
5. Bear JE, Loureiro JJ, Libova I, Fassler R, Wehland J, Gertler FB. 2000. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101:717-28.
6. Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser, and others. 2002. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109:509-21.
7. Bentley D, O'Connor TP. 1994. Cytoskeletal events in growth cone steering. Curr Opin Neurobiol 4:43-8.
8. Brose K, Tessier-Lavigne M. 2000. Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr Opin Neurobiol 10:95-102.
9. Buck K, Zheng JQ. 2002. Growth cone turning by direct local modification of microtubule dynamics. J Neurosci 22:9358-67.
10. Dent EW, Barnes AM, Tang F, Kalil K. Netrin-1 and Semaphorin 3A promote or inhibit cortical axon branching respectively by reorganization of the cytoskeleton. Forthcoming
11. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K. 1999. Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J Neurosci 19:8894-908.
12. Dent EW, Kalil K. 2001. Axon branching requires interactions between dynamic microtubules and actin filaments. J Neurosci 21:9757-69.
13. Dickson B. 2002. Molecular mechanisms of axon guidance. Science 298:1959-64.
14. Fan J, Mansfield SG, Redmond T, Gordon-Weeks PR, Raper JA. 1993. The organization of F-actin and microtubules in growth cones exposed to a brain-derived collapsing factor. J Cell Biol 121:867-78.
15. Fournier AE, Nakamura F, Kawamoto S, Goshima Y, Kalb RG, Strittmatter SM. 2000. Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J Cell Biol 149:411-22.
16. Fritsche J, Reber BF, Schindelholz B, Bandtlow CE. 1999. Differential cytoskeletal changes during growth cone collapse in response to hSema III and thrombin. Mol Cell Neurosci 14:398-418.
17. Gomez TM, Snow DM, Letourneau PC. 1995. Characterization of spontaneous calcium transients in nerve growth cones and their effect on growth cone migration. Neuron 14:1233-46.
18. Gomez TM, Spitzer NC. 1999. In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature 397:350-5.
19. Gu X, Spitzer NC. 1995. Distinct aspects of neuronal differentiation encoded by frequency of spontaneous Ca2+ transients. Nature 375:784-7.
20. Halloran MC, Kalil K. 1994. Dynamic behaviors of growth cones extending in the corpus callosum of living cortical brain slices observed with video microscopy. J Neurosci 14:2161-77.
21. Hong K, Nishiyama M, Henley J, Tessier-Lavigne M, Poo M. 2000. Calcium signalling in the guidance of nerve growth by netrin-1. Nature 403:93-8.
22. Kalil K, Szebenyi G, Dent EW. 2000. Common mechanisms underlying growth cone guidance and axon branching. J Neurobiol 44:145-58.
23. Kidd T, Bland KS, Goodman CS. 1999. Slit is the midline repellent for the robo receptor in Drosophila. Cell 96:785-94.
24. Komuro H, Rakic P. 1996. Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 17:275-85.
25. Lanier LM, Gates MA, Witke W, Menzies AS, Wehman AM, Macklis JD, and others. 1999. Mena is required for neurulation and commissure formation. Neuron 22:313-25.
26. Lanier LM, Gertler FB. 2000. From Ab1 to actin: Ab1 tyrosine kinase and associated proteins in growth cone motility. Curr Opin Neurobiol 10:80-7.
27. Lankford KL, Letourneau PC. 1989. Evidence that calcium may control neurite outgrowth by regulating the stability of actin filaments. J Cell Biol 109:1229-43.
28. Lin CH, Forscher P. 1993. Cytoskeletal remodeling during growth cone-target interactions. J Cell Biol 121:1369-83.
29. Lin CH, Thompson CA, Forscher P. 1994. Cytoskeletal reorganization underlying growth cone motility. Curr Opin Neurobiol 4:640-7.
30. Liu BP, Strittmatter SM. 2001. Semaphorin-mediated axonal guidance via Rho-related G proteins. Curr Opin Cell Biol 13:619-26.
31. Lohmann C, Myhr KL, Wong RO. 2002. Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 418:177-81.
32. Luo L. 2002. Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu Rev Cell Dev Biol 18:601-35.
33. Mao BQ, Hamzei-sichani F, Aranov D, Froemke RC, Yuste R. 2001. Dynamics of spontaneous activity in neortical slices. Neuron 32:883-98.
34. Mason C, Erskine L. 2000. Growth cone form, behavior, and interactions in vivo: retinal axon pathfinding as a model. J Neurobiol 44:260-70.
35. Ming G, Henley J, Tessier-Lavigne M, Song H, Poo M. 2001. Electrical activity modulates growth cone guidance by diffusible factors. Neuron 29:441-52.
36. 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 123:935-48.
37. O'Leary DD, Bicknese AR, De Carlos JA, Heffner CD, Koester SE, Kutka, and others. 1990. Target selection by cortical axons: alternative mechanisms to establish axonal connections in the developing brain. Cold Spring Harb Symp Quant Biol 55:453-68.
38. Pantaloni D, Le Clainche C, Carlier ME 2001. Mechanism of actin-based motility. Science 292:1502-6.
39. Plump AS, Erskine L, Sabatier C, Brose K, Epstein CJ, Goodman CS, and others. 2002. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33:219-32.
40. Polleux F, Giger RJ, Ginty DD, Kolodkin AL, Ghosh A. 1998. Patterning of cortical efferent projections by semaphorin-neuropilin interactions. Science 282:1904-6.
41. Redmond L, Kashani AH, Ghosh A. 2002. Calcium regulation of dendritic growth via CaM kinase IV and CREB- mediated transcription. Neuron 34:999-1010.
42. Renfranz PJ, Beckerle MC. 2002. Doing (F/L)PPPPs: EVH1 domains and their proline-rich partners in cell polarity and migration. Curr Opin Cell Biol 14:88-103.
43. Rochlin MW, Dailey ME, Bridgman PC. 1999. Polymerizing microtubules activate site-directed F-actin assembly in nerve growth cones. Mol Biol Cell 10:2309-27.
44. Roos J, Hummel T, Ng N, Klambt C, Davis GW. 2000. Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26:371-82.
45. 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 115:381-95.
46. Salmon WC, Adams MC, Waterman-Storr CM. 2002. Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells. J Cell Biol 158:31-37.
47. Schaefer AW, Kabir N, Forscher P. 2002. Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J Cell Biol 158:139-52.
48. Shitaka Y, Matsuki N, Saito H, Katsuki H. 1996. Basic fibroblast growth factor increases functional L-type Ca2+ channels in fetal rat hippocampal neurons: implications for neurite morphogenesis in vitro. J Neurosci 16:6476-89.
49. Shu T, Richards LJ. 2001. Cortical axon guidance by the glial wedge during the development of the corpus callosum. J Neurosci 21:2749-58.
50. Song H, Poo M. 2001. The cell biology of neuronal navigation. Nat Cell Biol 3:E81-8.
51. Szebenyi G, Callaway JL, Dent EW, Kalil K. 1998. Interstitial branches develop from active regions of the axon demarcated by the primary growth cone during pausing behaviors. J Neurosci 18:7930-40.
52. Szebenyi G, Dent EW, Callaway JL, Seys C, Lueth H, Kalil K. 2001. Fibroblast growth factor-2 promotes axon branching of cortical neurons by influencing morphology and behavior of the primary growth cone. J Neurosci 21:3932-41.
53. Tanaka E, Sabry J. 1995. Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-6.
54. Tanaka EM, Kirschner MW. 1991. Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol 115:345-63.
55. Tang F, Dent EW, Kalil K. 2003. Spontaneous calcium transients in developing cortical neurons regulate axon outgrowth. J Neuroscience 23:927-36.
56. Wang KH, Brose K, Arnott D, Kidd T, Goodman CS, Henzel W, and others. 1999. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96:771-84.
57. Yuste R, Peinado A, Katz LC. 1992. Neuronal domains in developing neocortex. Science 257:665-69.
58. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, and others. 2001. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci U S A 98:11024-31.
59. Wills Z, Marr L, Zinn K, Goodman CS, Van Vactor D. 1999. Profilin and the Ab1 tyrosine kinase are required for motor axon outgrowth in the Drosophila embryo. Neuron 22:291-9.
60. Zhou FQ, Waterman-Storer CM, Cohan CS. 2002. Focal loss of actin bundles causes microtubule redistribution and growth cone turning. J Cell Biol 157:839-49.