Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches

Journal of Neuroscience

Volumn 19, Issue 20, 1999, Pages 8894-8908

  Dent, Erik W ^a   Callaway, John L ^a   Szebenyi, Györgyi ^a,b   Baas, Peter W ^a   Kalil, Katherine ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Axon outgrowth; Cortical development; Cortical neuronal culture; Growth cone; Interstitial axon branch; Microtubule; Time lapse fluorescent microscopy

Indexed keywords

ANIMAL CELL; ARTICLE; CELL INVASION; CELL MATURATION; CELL MOTION; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GROWTH CONE; MICROTUBULE; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; PRIORITY JOURNAL;

EID: 0033570357     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-20-08894.1999     Document Type: Article

References (67)

1. Ahmad FJ, Echeverri CJ, Vallee RB, Baas PW (1998) Cytoplasmic dynein and dynactin are required for microtubule transport into the axon. J Cell Biol 140:391-402.
2. Ahmad FJ, Yu W, McNally FJ, Baas PW (1999) An essential role for katanin in severing microtubules in the neuron. J Cell Biol 145:305-315.
3. Baas PW (1997) Microtubules and axonal growth. Curr Opin Cell Biol 9:29-36.
4. Baas PW (1999) Microtubules and neuronal polarity: lessons from mitosis. Neuron 22:23-31.
5. Baas PW, Ahmad FJ (1992) The plus ends of stable microtubules are the exclusive nucleating structures for MTs in the axon. J Cell Biol 116:1231-1241.
6. Baas PW, Brown A (1997) Slow axonal transport: the polymer transport model. Trends Cell Biol 7:380-384.
7. Bastmeyer M, O'Leary DD (1996) Dynamics of target recognition by interstitial axon branching along developing cortical axons. J Neurosci 16:1450-1459.
8. Belmont LD, Hyman AA, Sawin KE, Mitchison TJ (1990) Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62:579-589.
9. Brewer GJ, Cotman CW (1989) Survival and growth of hippocampal neurons in defined medium at low density: advantages of a sandwich culture technique or low oxygen. Brain Res 494:65-74.
10. Chang S, Rodionov VI, Borisy GG, Popov SV (1998) Transport and turnover of microtubules in frog neurons depend on the pattern of axonal growth. J Neurosci 18:821-829.
11. de Lima AD, Merten MD, Voigt T (1997) Neuritic differentiation and synaptogenesis in serum-free neuronal cultures of the rat cerebral cortex. J Comp Neurol 382:230-246.
12. Desai A, Mitchison TJ (1997) Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 13:83-117.
13. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
14. Ferhat L, Cook C, Chauviere M, Harper M, Kress M, Lyons GE, Baas PW (1998) Expression of the mitotic motor protein Eg5 in postmitotic neurons: implications for neuronal development. J Neurosci 18:7822-7835.
15. Funakoshi T, Takeda S, Hirokawa N (1996) Active transport of photoactivated tubulin molecules in growing axons revealed by a new electron microscopic analysis. J Cell Biol 133:1347-1353.
16. Gallo G, Letourneau PC (1998) Localized sources of neurotrophins initiate axon collateral sprouting. J Neurosci 18:5403-5414.
17. Gallo G, Letourneau PC (1999) Different contributions of microtubule dynamics and transport to the growth of axons and collateral sprouts. J Neurosci 19:3860-3873.
18. Goslin K, Banker G (1991) Rat hippocampal neurons in low-density culture. In: Culturing nerve cells (Banker G, Goslin K, eds), pp 251-281. Cambridge, MA: MIT.
19. 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 14:2161-2177.
20. Hartman JJ, Mahr J, McNally K, Okawa K, Iwamatsu A, Thomas S, Cheesman S, Heuser J, Vale RD, McNally FJ (1998) Katanin, a microtubule-severing protein, is a novel AAA ATPase that targets to the centrosome using a WD40-containing subunit. Cell 93:277-287.
21. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382:420-425.
22. Heidemann SR, Landers JM, Hamborg MA (1981) Polarity orientation of axonal microtubules. J Cell Biol 91:661-665.
23. Hirokawa N, Terada S, Funakoshi T, Takeda S (1997) Slow axonal transport: the subunit model of transport. Trends Cell Biol 7:383-388.
24. Hyman A, Drechsel D, Kellogg D, Salser S, Sawin K, Steffen P, Wordeman L, Mitchison T (1991) Preparation of modified tuhulins. Methods Enzymol 196:478-485.
25. Inoué S (1986) Video Microscopy: the fundamentals. New York: Plenum.
26. Inoué S, Spring K (1997) Video microscopy: the fundamentals, Ed 2. New York: Plenum.
27. Keating TJ, Peloquin JG, Rodionov VI, Momcilovic D, Borisy GG (1997) Microtubule release from the centrosome. Proc Natl Acad Sei USA 94:5078-5083.
28. Kriegstein AR, Dichter MA (1983) Morphological classification of rat cortical neurons in cell culture. J Neurosci 3:1634-1647.
29. Kuang RZ, Kalil K (1994) Development of specificity in corticospinal connections by axon collaterals branching selectively into appropriate spinal targets. J Comp Neurol 344:270-282.
30. Lankford KL, Klein WL (1990) Ultrastructure of individual neurons isolated from avian retina: occurrence of microtubule loops in dendritcs. Brain Res Dev Brain Res 51:217-224.
31. Letourneau PC (1996) The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev Neurobiol 4:111-123.
32. Lin CH, Forscher P (1993) Cytoskeletal remodeling during growth cone-target interactions. J Cell Biol 121:1369-1383.
33. McNally FJ, Thomas S (1998) Katanin is responsible for the M-phase microtubule-severing activity in Xenopus eggs. Mol Biol Cell 9:1847-1861.
34. McNally FJ, Vale RD (1993) Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75:419-429.
35. McQuarrie IG, Brady ST, Lasek RJ (1986) Diversity in the axonal transport of structural proteins: major differences between optic and spinal axons in the rat. J Neurosci 6:1593-1605.
36. Mikhailov AV, Gundersen GO (1995) Centripetal transport of microtubules in motile cells. Cell Motil Cytoskeleton 32:173-186.
37. Okabe S, Hirokawa N (1992) Differential behavior of photoactivated microtubules in growing axons of mouse and frog neurons. J Cell Biol 117:105-120.
38. Okabe S, Hirokawa N (1993) Do photobleached fluorescent microtubules move?: re-evaluation of fluorescence laser photobleaching both in vitro and in growing Xenopus axon. J Cell Biol 120:1177-1186.
39. O'Leary DD, 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.
40. O'Leary DD, Bicknese AR, De Carlos JA, Heffner CD, Koester SE, Kutka LJ, Terashima T (1990) Target selection by cortical axons: alternative mechanisms to establish axonal connections in the developing brain. Cold Spring Harb Symp Quant Biol 55:453-468.
41. Rodionov VI, Borisy GG (1997) Microtubule treadmilling in vivo. Science 275:215-218.
42. Russ JC (1995) The image processing handbook, Ed 2. Boca Raton, FL: CRC.
43. Sabry J, 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.
44. Sabry J, O'Connor TP, Kirschner M (1995) Axonal transport of tubulin in Til pioneer neurons in situ. Neuron 14:1247-1256.
45. Salmon ED, Shaw SL, Waterman-Storer CM, Maddox PS, Yeh E, Bloom K (1998) A high resolution multimode digital microscope system. In: Video microscopy (Sluder G, Wolf DE, eds), pp 186-214. San Diego: Academic.
46. Slaughter T, Wang J, Black MM (1997) Microtubule transport from the cell body into the axons of growing neurons. J Neurosci 17:5807-5819.
47. Suter DM, Errante LD, Belotserkovsky V, Forscher P (1998) The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J Cell Biol 141:227-240.
48. Szebcnyi 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 18:7930-7940.
49. Takeda S, Funakoshi T, Hirokawa N (1995) Tubulin dynamics in neuronal axons of living zebrafish embryos. Neuron 14:1257-1264.
50. Tanaka EM, Kirschner MW (1991) Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol 115:345-363.
51. Tanaka E, Sabry J (1995) Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-176.
52. Tanaka E, Ho T, Kirschner MW (1995) The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol 128:139-155.
53. Tcrasaki M, Schmidek A, Galbraith JA, Gallant PE, Reese TS (1995) Transport of cytoskeletal elements in the squid giant axon. Proc Natl Acad Sei USA 92:11500-11503.
54. Tsui HT, Lankford KL, Ris H, Klein WL (1984) Novel organization of microtubules in cultured central nervous system neurons: formation of hairpin loops at ends of maturing neurites. J Neurosci 4:3002-3013.
55. Vorobjev IA, Svitkina TM, Borisy GG (1997) Cytoplasmic assembly of microtubules in cultured cells. J Cell Sei 110:2635-2645.
56. Waterman-StorcrCM, Salmon ED (1997) Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J Cell Biol 139:417-434.
57. Waterman-Storer CM, Salmon ED (1998) How microtubules get fluorescent speckles. Biophys J 75:2059-2069.
58. Waterman-Storer CM, Sanger JW, Sanger JM (1993) Dynamics of organelles in the mitotic spindles of living cells: membrane and microtubule interactions. Cell Motil Cytoskeleton 26:19-39.
59. Weiss DG, Maiie W (1993) Principles, practice, and applications of video-enhanced contrast microscopy. In: Electronic light microscopy: techniques in modern biomedical microscopy (Shotton W, ed), pp 106-136. New York: Wiley Liss.
60. White LA, Baas PW, Heidemann SR (1987) Microtubule stability in severed axons. J Neurocytol 16:775-784.
61. Willard M, Simon C (1983) Modulations of neurofilament axonal transport during the development of rabbit retinal ganglion cells. Cell 35:551-559.
62. Yamamoto N, Higashi S, Toyama K (1997) Stop and branch behaviors of geniculocortical axons: a time-lapse study in organotypic cocultures. J Neurosci 17:3653-3663.
63. Yu W, Baas PW (1994) Changes in microtubule number and length during axon differentiation. J Neurosci 14:2818-2829.
64. Yu W, Ahmad FJ, Baas PW (1994) Microtubule fragmentation and partitioning in the axon during collateral branch formation. J Neurosci 14:5872-5884.
65. Yu W, Schwei MJ, Baas PW (1996) Microtubule transport and assembly during axon growth. J Cell Biol 133:151-157.
66. Yvon A-MC, Wadsworth P (1997) Non-centrosomal microtubule formation and measurement of minus end dynamics in A498 cells. J Cell Sci 110:2391-2401.
67. 2+ induce the dedifferentiation of axonal segments into growth cones. J Neurosci 17:3568-3579.