Effects of dynactin disruption and dynein depletion on axonal microtubules

Traffic

Volumn 7, Issue 5, 2006, Pages 524-537

  Ahmad, Fridoon J ^a,b   He, Yan ^a   Myers, Kenneth A ^a   Hasaka, Thomas P ^a   Francis, Franto ^c   Black, Mark M ^c   Baas, Peter W ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF THE PUNJAB   (Pakistan)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axon; Cytoplasmic dynein; Dynactin; EB3; Microtubule; Neurofilament; Neuron

Indexed keywords

CYTOPLASM PROTEIN; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; MICROTUBULE PROTEIN; PROTEIN P50; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FILOPODIUM; GENE OVEREXPRESSION; GENE SILENCING; GROWTH CONE; HEAVY CHAIN; MICROTUBULE; MICROTUBULE ASSEMBLY; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DEPLETION; RAT; THEORY; TRANSPORT KINETICS;

ANIMALS; AXONS; CELLS, CULTURED; DYNEIN ATPASE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; RATS;

EID: 33745807269     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2006.00403.x     Document Type: Article

References (40)

1. Schaefer AW, Kabir N, Forscher P. 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 2002; 158: 139-152.
2. Baas PW, Ahmad FJ. The plus ends of stable microtubules are the exclusive nucleating structures for microtubules in the axon. J Cell Biol 1992; 116: 1231-1241.
3. Yu W, Baas PW. Changes in microtubule number and length during axon differentiation. J Neurosci 1994; 14: 2818-2829.
4. Wang L, Brown A. Rapid movement of microtubules in axons. Curr Biol 2002; 12: 1496-1501.
5. Hasaka TP, Myers KA, Baas PW. Role of actin filaments in the axonal transport of microtubules. J Neurosci 2004; 24: 11291-11301.
6. He Y, Frances F, Myers KA, Yu W, Black MM, Baas PW. Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments. J Cell Biol 2005; 168: 697-703.
7. Echeverri CJ, Paschal BM, Vaughan KT, Vallee RB. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J Cell Biol 1996; 132: 617-633.
8. Ahmad FJ, Echeverri CJ, Vallee RB, Baas PW. Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J Cell Biol 1998; 140: 391-401.
9. Ma Y, Shakiryanova D, Vardya I, Popov SV. Quantitative analysis of microtubule transport in growing nerve processes. Curr Biol 2004; 14: 725-730.
10. Keating TJ, Peloquin JG, Rodionov VI, Momcilovic D, Borisy GG. Microtubule release from the centrosome. Proc Natl Acad Sci USA 1997; 94: 5078-5083.
11. Schroer TA. Dynactin. Annu Rev Cell Dev Biol 2004; 20: 759-779.
12. LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascano J, Tokito M, Van Winkle T, Howland DS, Holzbaur EL. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 2002; 34: 715-727.
13. Heerssen HM, Pazyra MF, Segal RA. Dynein motors transport activated Trks to promote survival of target-dependent neurons. Nat Neurosci 2004; 7: 596-604.
14. Vallee RB, Williams JC, Varma D, Barnhart LE. Dynein: An ancient motor protein involved in multiple modes of transport. J Neurobiol 2004; 58: 189-200.
15. Ho WC, Allan VJ, Van Meer G, Berger EG, Kreis TE. Reclustering of scattered Golgi elements along microtubules. Eur J Cell Biol 1989; 48: 250-263.
16. Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB. Overexpression of the dynamitin (P50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 1997; 139: 469-484.
17. Wang L, Ho CL, Sun D, Liem RKH, Brown A. Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat Cell Biol 2000; 2: 137-141.
18. Roy S, Coffee P, Smith G, Liem RKH, Brady ST, Black MM. Neurofilaments are transported rapidly but intermittently in axons: Implications for slow axonal transport. J Neurosci 2000; 20: 6849-6861.
19. Francis F, Roy S, Brady ST, Black MM. Transport of neurofilaments in growing axons requires microtubules but not actin filaments. J Neurosci Res 2005; 79: 442-450.
20. Helfand BT, Loomis P, Yoon M, Goldman RD. Rapid transport of neural intermediate filament protein. J Cell Sci 2003; 116: 2345-2359.
21. Stepanova T, Slemmer J, Hoogenraad CC, Lansbergen G, Dortland B, De Zeeuw CI, Grosveld F, van Cappellen G, Akhmanova A, Galjart N. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (End-Binding Protein 3-Green Fluorescent Protein). J Neurosci 2003; 23: 2655-2664.
22. Vaughan KT. Surfing, regulating and capturing: Are all microtubule-tip-tracking proteins created equal? Trends Cell Biol 2004; 14: 491-496.
23. Abal M, Piel M, Bouckson-Castaing V, Mogensen M, Sibarita JB, Bornens M. Microtubule release from the centrosome in migrating cells. J Cell Biol 2002; 159: 731-737.
24. Baas PW, White LA, Heidemann SR. Microtubule polarity reversal accompanies regrowth of amputated neurites. Proc Natl Acad Sci USA 1987; 84: 5272-5276.
25. Piehl M, Cassimeris L. Organization and dynamics of growing microtubule plus ends during early mitosis. Mol Biol Cell 2003; 14: 916-925.
26. Suter DM, Schaefer AW, Forscher P. Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr Biol 2004; 14: 1194-1199.
27. Lim SS, Edson KJ, Letourneau PC, Borisy GG. A test of microtubule translocation during neurite elongation. J Cell Biol 1990; 111: 123-130.
28. Hirokawa N, Terada S, Funakoshi T, Tekeda S. Slow axonal transport: The subunit transport model. Trends Cell Biol 1997; 7: 384-388.
29. Chang S, Svitkina TM, Borisy GG, Popov SV. Speckle microscopic evaluation of microtubule transport in growing nerve processes. Nat Cell Biol 1999; 7: 399-403.
30. Baas PW, Karabay A, Qiang L. Microtubules cut and run. Trends Cell Biol 2005; 15: 518-524.
31. Baas PW, Nadar CV, Myers KA. Axonal microtubule transport: The long and short of it. Traffic 2006 (in press).
32. Deacon SW, Serpinskaya AS, Vaughan PS, Lopez-Fanarraga M, Vernos I, Vaughan KT, Gelfand VI. Dynactin is required for bidirectional organelle transport. J Cell Biol 2003; 160: 297-301.
33. Gross SP. Dynactin: Coordinating motors with opposite inclinations. Curr Biol 2003; 13: R320-R322.
34. Carvalho P, Gupta ML, Hoyt MA, Pellman D. Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. Dev Cell 2004; 6: 815-829.
35. Ahmad FJ, Hughey J, Wittmann T, Hyman A, Greaser M, Baas PW. Motor proteins regulate force interactions between microtubules and microfilaments in the axon. Nat Cell Biol 2000; 2: 276-280.
36. Dent EW, Kalil K. Axon branching requires interactions between dynamic microtubules and actin filaments. J Neurosci 2001; 21: 9757-9769.
37. He Y, Baas PW. Growing and working with peripheral neurons. Methods Cell Biol 2003; 71: 17-35.
38. Karabay A, Yu W, Solowska JM, Baird DH, Baas PW. Axonal growth is sensitive to the levels of katanin, a protein that severs microtubules. J Neurosci 2004; 24: 5778-5788.
39. Baas PW, Ahmad FJ. The transport properties of axonal microtubules establish their polarity orientation. J Cell Biol 1993; 120: 1427-1437.
40. Brown A, Slaughter T, Black MM. Newly assembled microtubules are concentrated in the proximal and distal regions of growing axons. J Cell Biol 1992; 119: 867-882.