Microtubule Transport in the Axon: Re-thinking a Potential Role for the Actin Cytoskeleton

The Neuroscientist

Volumn 12, Issue 2, 2006, Pages 107-118

  Myers, Kenneth A ^a   he, Yan ^a   Hasaka, Thomas P ^a   Baas, Peter W ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Actin; Axon; Axonal retraction; Dynein; Growth cone; Microtubule transport; Microtubules; Molecular motor

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; MOLECULAR MOTOR;

ANIMAL; BIOLOGICAL MODEL; CELL DIFFERENTIATION; GROWTH CONE; HUMAN; METABOLISM; MICROFILAMENT; MICROTUBULE; NERVE FIBER; NERVE FIBER TRANSPORT; PHYSIOLOGY; REVIEW; ULTRASTRUCTURE;

ANIMALS; AXONAL TRANSPORT; AXONS; CELL DIFFERENTIATION; DYNEIN ATPASE; GROWTH CONES; HUMANS; MICROFILAMENTS; MICROTUBULES; MODELS, BIOLOGICAL; MOLECULAR MOTOR PROTEINS;

EID: 33646671227     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858405283428     Document Type: Review

References (54)

1. Ahmad FJ, Baas PW. 1995. Microtubule released from the neuronal centrosome are transported into the axon. J Cell Sci 108: 2761–2769.
2. Ahmad FJ, Echeverri CJ, Vallee RB, Baas PW. 1998. Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J Cell Biol 140: 246–256.
3. Ahmad FJ, Hughey J. Wittmann T, Hyman A, Greaser M, Baas PW. 2000. Motor proteins regulate force interactions between microtubules and microfilaments in the axon. Nat Cell Biol 2: 276–280.
4. Baas PW. 1999. Microtubules and neuronal polarity: lessons from mitosis. Neuron 22: 23–31.
5. Baas PW, Ahmad FJ. 2001. Force generation by cytoskeletal motor proteins as a regulator of axonal elongation and retraction. Trends Cell Biol 11: 244–249.
6. Baas PW, Buster DW. 2004. Slow axonal transport and the genesis of neuronal morphology. J Neurobiol 58: 3–17.
7. Baas PW, Karabay A. Qiang L. 2005. Microtubules cut and run. Trends Cell Biol. In press.
8. Brito DA, Strauss J. Magidson V, Tikhonenko I, Khodjakov A, Koonce MP. 2005. Pushing forces drive the comet-like motility of microtubule arrays in Dictyostelium. Mol Biol Cell 16: 3334–3340.
9. Brunner D. 2002. How to grab a microtubule on the move [Review]. Dev Cell 3: 2–4.
10. Burnstein M. Lichtman JW. 1999. Axonal atrophy: the retraction reaction. Curr Opin Neurobiol 9: 364–370.
11. Chuang JZ, Yeh TY, Bollati F. Conde C, Canavosio F, Caceres A, and others. 2005. The dynein light chain Tctex-1 has a dynein-independent role in actin remodeling during neurite outgrowth. Dev Cell 9: 75–86.
12. D'Addario M, Arora PD, Ellen RP, McCulloch CA. 2003. Regulation of tension-induced mechanotranscriptional signals by the microtubule network in fibroblasts. J Biol Chem 278: 53090–53097.
13. Dehmelt L. Halpain S. 2004. Actin and microtubules in neurite initiation: are MAPs the missing link [Review]? J Neurobiol 58: 18–33.
14. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K. 1999. Reorganization and movement of microtubules in growth cones and developing interstitial branches. J Neurosci 9: 8894–8904.
15. Dent EW, Kalil K. 2001. Axon branching requires interactions between dynamic microtubules and actin filaments. J Neurosci 21: 9757–9769.
16. Dent EW, Tang F. Kalil K. 2003. Axon guidance by growth cones and branches: common cytoskeletal and signaling mechanisms [Review]. Neuroscientist 9: 343–353.
17. Dillman JF 3rd, Dabney LP, Karki S. Paschal BM, Holzbauer EL, Pfister KK. 1996. Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J Neurosci 16: 6742–6752.
18. Dillman JF 3rd, Dabney LP, Pfister KK. 1996. Cytoplasmic dynein is associated with slow axonal transport. Proc Natl Acad Sci U S A 93: 141–144.
19. Dujardin DL, Barnhart LE, Stehman SA, Gomes ER, Gunderston GG, Vallee RB. 2003. A role for cytoplasmic dynein and LIS1 in directed cell movement. J Cell Biol 163: 1205–1211.
20. Gallo G. Yee HF Jr, Letourneau PC. 2002. Actin turnover is required to prevent axon retraction by endogenous actomyosin contractility. J Cell Biol 158: 1219–1228.
21. Gordon-Weeks PR. 2004. Microtubules and growth cone function [Review]. J Neurobiol 58: 70–83.
22. Gupton SL, Salmon WC, Waterman-Storer CM. 2002. Converging populations of f-actin promote breakage of associated microtubules to spatially regulate microtubule turnover in migrating cells. Curr Biol 12: 1891–1899.
23. Hasaka TP, Myers KA, Baas PW. 2004. Role of actin filaments in the axonal transport of microtubules. J Neurosci 24: 11291–11301.
24. He Y. Frances F, Myers KA, Black M, Baas PW. 2005. Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments. J Cell Biol 168: 697–703.
25. He Y. Yu W, Baas PW. 2002. Microtubule reconfiguration during axonal retraction induced by nitric oxide. J Neurosci 22: 5982–5991.
26. Heidemann SR, Landers JM, Hamborg MA. 1981. Polarity orientation of axonal microtubules. J Cell Biol 91: 661–665.
27. Henriquez JP, Cross D. Vial C, Maccioni RB. 1995. Subpopulations of tau interact with microtubules and actin filaments in various cell types. Cell Biochem Funct 13: 239–250.
28. Houseweart MK, Cleveland DW. 1999. Cytoskeletal linkers: new MAPs for old destinations [Review]. Curr Biol 9: R864–6.
29. Kodama A. Lechler T, Fuchs E. 2004. Coordinating cytoskeletal tracks to polarize cellular movements [Review]. J Cell Biol 167: 203–207.
30. Lee H. Van Vactor D. 2003. Neurons take shape [Review]. Curr Biol 13: R152–61.
31. Lee JS, Gotlieb AI. 2002. Microtubule-actin interactions may regulate endothelial integrity and repair [Review]. Cardiovasc Pathol 11: 135–140.
32. Letourneau PC. 1996. The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev Neurobiol 4: 111–123.
33. Lin CH, Forscher P. 1993. Cytoskeletal remodeling during growth cone-target interactions. J Cell Biol 121: 1369–1383.
34. Lin CM, Chen HJ, Leung CL, Parry DA, Liem RK. 2005. Microtubule actin crosslinking factor 1b: a novel plakin that localizes to the Golgi complex. J Cell Sci 118: 3727–3738.
35. Ma Y. Shakiryanova D, Vardya I, Popov SV. 2004. Quantitative analysis of microtubule transport in growing nerve processes. Curr Biol 14: 725–730.
36. Marrari Y. Clarke EJ, Rouviere C, Houliston E. 2003. Analysis of microtubule movement on isolated Xenopus egg cortices provides evidence that the cortical rotation involves dynein as well as kinesin related proteins and is regulated by local microtubule polymerization. Dev Biol 257: 55–70.
37. Noritake J. Watanabe T, Sato K, Wang S, Kaibuchi K. 2005. IQGAP1: a key regulator of adhesion and migration. J Cell Sci 118: 2085–2092.
38. Pfister KK. 1999. Cytoplasmic dynein and microtubule transport in the axon: the actin connection. Mol Neurobiol 20: 81–91.
39. Rochlin MW, Dailey ME, Bridgman PC. 1999. Polymerizing microtubules activate site-directed F-actin assembly in nerve growth cones. Mol Biol Cell 10: 2309–2327.
40. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P. Bement WM, Waterman-Storer CM. 2003. Conserved microtubule-actin interactionsin cell movement and morphogenesis [Review]. Nat Cell Biol 5: 599–609.
41. Roger B. Al-Bassam J, Dehmelt L, Milligan RA, Halpain S. 2004. MAP2c, but not tau, binds and bundles F-actin via its microtubule binding domain. Curr Biol 14: 363–371.
42. Ryan XP, Alldritt J, Svenningsson P, Allen PB, Wu GY, Nairn AC, and others. 2005. The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47: 85–100.
43. Salmon WC, Adams MC, Waterman-Storer CM. 2002. Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells. J Cell Biol 158: 31–37.
44. Sammak PJ, Borisy GG. 1988. Direct observation of microtubule dynamics in living cells. Nature 332: 724–726.
45. 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: 139–152.
46. Schmit AC, Lambert AM. 1988. Plant actin filament and microtubule interactions during anaphase—telophase transition: effects of antagonist drugs. Biol Cell 64: 309–319.
47. Stepanova T, Slemmer J, Hoogenraad CC, Lansbergen G, Dortland B, De Zeeuw CI, and others. 2003. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J Neurosci 23: 2655–2664.
48. Suter DM, Schaefer AW, Forscher P. 2004. Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr Biol 14: 1194–1199.
49. Tanaka EM, Kirschner MW. 1991. Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol 115: 345–363.
50. Vallee RB, Bloom GS. 1991. Mechanisms for fast and slow axonal transport. Annu Rev Neurosci 14: 59–92.
51. Wang L. Brown A. 2002. Rapid movement of microtubules in axons. Curr Biol 12: 1496–1501.
52. Watanabe T. Noritake J, Kaibuchi K. 2005. Regulation of microtubules in cell migration. Trends Cell Biol 15: 76–83.
53. Yarm F. Sagot I, Pellman D. 2001. The social life of actin and microtubules: interaction versus cooperation [Review]. Curr Opin Microbiol 4: 696–702.
54. Zhou FQ, Cohan CS. 2004. How actin filaments and microtubules steer growth cones to their targets [Review]. J Neurobiol 58: 84–91.