Focusing-in on microtubules

Current Opinion in Structural Biology

Volumn 10, Issue 2, 2000, Pages 236-241

  Amos, Linda A ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; MICROTUBULE ASSOCIATED PROTEIN; TUBULIN;

ELECTRON MICROSCOPY; MICROTUBULE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; REVIEW; X RAY CRYSTALLOGRAPHY;

EID: 0034113893     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(00)00070-1     Document Type: Review

References (59)

1. Desai A., Mitchison T.J. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol. 13:1997;83-117.
2. Nogales E., Wolf S., Downing K.H. Structure of the αβ tubulin dimer by electron crystallography. Nature. 391:1998;199-203.
3. Nogales E., Whittaker M., Milligan R.A., Downing K.H. High resolution model of the microtubule. Cell. 96:1999;79-88. This paper showed there is only one way that the atomic structure of tubulin [2] can be placed in a 3D map of microtubules obtained from electron cryo-microscopy data. The authors identified the 'M-loops' of tubulin, which mediate lateral interactions between protofilaments. The site equivalent to that occupied by paclitaxel in β-tubulin was shown to be filled by an extended S9-S10 loop in α-tubulin.
4. ••]: tubulin dimer coordinates from [2], together with those of kinesin [43,52], were docked into a map of microtubules decorated with kinesin motor domains (results summarised in Figure 1). Also, tightly bound kinesin was shown to produce a tilt in β-tubulin similar to that found previously [12] for the reverse motor, ncd.
5. Diaz J.F., Valpuesta J.M., Chacon P., Diakun G., Andreu J.M. Changes in microtubule protofilament number induced by taxol binding to an easily accessible site- internal microtubule dynamics. J Biol Chem. 273:1998;33803-33810. When paclitaxel was added to pre-assembled microtubules, there was a rapid change in protofilament number, showing that the drug has no problem in making its way to binding sites on the inside surface.
6. Chrétien D., Flyvbjerg H., Fuller S.D. Limited flexibility of the inter-protofilament bonds in microtubules assembled from pure tubulin. Eur Biophys J (with Biophys Lett). 27:1998;490-500.
7. Dias D.P., Milligan R.A. Motor protein decoration of microtubules grown in high salt conditions reveals the presence of mixed lattices. J Mol Biol. 287:1999;287-392.
8. Vandecandelaere A., Brune M., Webb M.R., Martin S.R., Bayley P.M. Phosphate release during microtubule assembly: what stabilizes growing microtubules? Biochemistry. 38:1999;8179-8188. Careful quantitation during microtubule assembly showed no evidence of a burst of phosphate (Pi) release during the growth phase. Nucleotide hydrolysis kept pace with tubulin-GTP addition, even during rapid growth, supporting earlier conclusions that extended caps of tubulin-GTP or tubulin-GDP-Pi do not occur in normal assembly.
9. Nogales E., Downing K.H., Amos L.A., Löwe J. Tubulin and FtsZ form a distinct family of GTPases. Nat Struct Biol. 5:1998;451-458.
10. Amos L.A., Löwe J. How does taxol stabilise microtubule structure? Chem Biol. 6:1999;R65-R69. A review of paclitaxel activity. As the binding of this drug to one side of the core helix of β-tubulin has an effect similar to the binding of unhydrolysed nucleotide to the other side, it was proposed that the core helix plays a key role in stabilising a tubulin conformation that favours the assembled state.
11. Desai A., Verma S., Mitchison T.J., Walczak C.E. Kin I kinesins are microtubule-destabilizing enzymes. Cell. 96:1999;69-78. The activities of a microtubule-depolymerising motor revealed some interesting properties of tubulin; when microtubules were assembled with paclitaxel, the products of depolymerisation were tubulin dimers, but in the presence of the nonhydrolysable GTP analogue GMP·CPP, the longitudinal protofilaments rolled up into spirals. This suggests that interdimer bonds are stabilised by unhydrolysed nucleotide, but not by paclitaxel.
12. Hirose K., Cross R.A., Amos L.A. Nucleotide-dependent structural changes in dimeric ncd molecules complexed to microtubules. J Mol Biol. 278:1998;389-400.
13. Endow S.A., Kang S.J., Satterwhite L.L., Rose M.D., Skeen V.P., Salmon E.D. Yeast KAR3 is a minus-end microtubule motor protein that destabilizes microtubules preferentially at the minus ends. EMBO J. 13:1994;2708-2713.
14. 2+-induced FtsZ sheets. EMBO J. 18:1999;2364-2371. The likelihood that filaments of FtsZ closely resemble tubulin protofilaments was confirmed by 3D image reconstruction from electron micrographs of 2D sheets. Docking the atomic coordinates of FtsZ into the map explained why the most homologous residues include a loop (T7) located on the opposite side of a subunit from the GTP-binding pocket; this loop is thought to trigger hydrolysis of the nucleotide in the next subunit.
15. RayChaudhuri D. ZipA is a MAP-tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J. 18:1999;2372-2383. Bacteria divide through constriction of a Z-ring containing the tubulin homologue FtsZ. In this paper, another cell division protein, ZipA, was shown to stabilise labile Z-rings in vivo and to interact with FtsZ in vitro. Parts of its sequence have some homology to tau and MAP2.
16. Kreis T., Vale R. Guidebook to the Cytoskeletal and Motor Proteins. 2:1999;Sambrook & Tooze at Oxford University Press, Oxford. The updated and expanded second edition includes excellent summaries of the properties of tubulin, microtubule-associated proteins and microtubule-associated motor proteins.
17. Brisch E., Ahrens D.P., Suprenant K.A. Phosphatase-sensitive regulators of microtubule assembly copurify with sea urchin egg microtubules. J Exp Zool. 283:1999;258-269.
18. Denarier E., Fourest-Lieuvin A., Bosc C., Pirollet F., Chapel A., Margolis R.L., Job D. Nonneuronal isoforms of STOP protein are responsible for microtubule cold stability in mammalian fibroblasts. Proc Natl Acad Sci USA. 95:1998;6055-6060.
19. Hartman J.J., Vale R.D. Microtubule disassembly by ATP-dependent oligomerization of the AAA enzyme katanin. Science. 286:1999;782-785. Katanin, an AAA ATPase, was shown, by fluorescence resonance energy transfer, to form ring-shaped oligomers that bind more strongly to microtubules and hydrolyse ATP more rapidly than monomeric katanin. The authors discuss ways in which katanin rings might induce microtubule severing.
20. Heil-Chapdelaine R.A., Adames N.R., Cooper J.A. Formin' the connection between microtubules and the cell cortex. J Cell Biol. 144:1999;809-811.
21. Howell B., Larsson N., Gullberg M., Cassimeris L. Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18 stathmin. Mol Biol Cell. 10:1999;105-118. At pH 6.8, the microtubule-associated protein stathmin slowed microtubulin elongation and increased catastrophes at both ends, consistent with high-affinity tubulin-sequestering activity; this was lost when stathmin's C terminus was truncated. At pH 7.5, stathmin merely promoted microtubule catastrophes, particularly at plus ends, by a mechanism requiring the N terminus.
22. Moreno F.J., Bagnat M., Lim F., Avila J. OP18/stathmin binds near the C-terminus of tubulin and facilitates GTP binding. Eur J Biochem. 262:1999;557-562. This study used proteolysis and cross-linking to localise the stathmin-binding site to a region close to the C terminus of α-tubulin. The site overlaps the longitudinal contact that α-tubulin makes in protofilaments and it was shown that binding of stathmin can modulate the binding of GTP to β-tubulin.
23. Wallon G., Rappsilber J., Mann M., Serrano L. Model for stathmin/OP18 binding to tubulin. EMBO J. 19:2000;213-222. This paper presents further details of the way that stathmin controls tubulin polymerisation. The intact molecule can bind to two tubulin dimers, whereas molecules lacking the N-terminal part sequester dimers by binding to α-tubulin helix 10 on the surface that contacts the next subunit in a protofilament.
24. Infante C., Ramos-Morales F., Fedriani C., Bornens M., Rios R.M. GMAP-210, a cis-Golgi network-associated protein, is a minus end microtubule-binding protein. J Cell Biol. 145:1999;83-98.
25. Karabay A., Walker R.A. The Ncd tail domain promotes microtubule assembly and stability. Biochem Biophys Res Commun. 258:1999;39-43.
26. Wickham L., Duchaîne T., Luo M., Nabi I., DesGroseillers L. Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol Cell Biol. 19:1999;2220-2230.
27. •].
28. •]) show that, when transfected into cells, the protein CLIP-170 localises to recently polymerised microtubule plus ends via its N-terminal domain. A chimera with the green fluorescent protein appears to move with the growing microtubule tips at speeds comparable to microtubule elongation in vivo. The authors propose that CLIP-170 specifically recognises the structure of newly polymerised tubulin.
29. Vaughan K.T., Tynan S.H., Faulkner N.E., Echeverri C.J., Vallee R.B. Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends. J Cell Sci. 112:1999;1437-1447. CLIP-170 and dynactin both mark growing microtubule (plus) ends and have similar binding motifs. These authors show that cytoplasmic dynein, a minus-end-directed microtubule motor, can also be localised there at low temperatures. They propose that plus ends provide loading sites at which cytoplasmic dynein can associate with cargo destined to be transported towards the microtubule minus ends.
30. Chau M.F., Radeke M.J., de Inés C., Barasoain I., Kohlstaedt L.A., Feinstein S.C. The microtubule-associated protein tau cross-links to two distinct sites on each alpha and beta tubulin monomer via separate domains. Biochemistry. 37:1998;17692-17703. Data presented here suggest that the binding and assembly inducing effects of the repeat regions and the proline-rich region of tau are not simply additive. Even within the repeat regions, different segments could interact with two distinct regions of tubulin. Adult tau (containing four repeats) cross-linked to the last 12 residues of tubulin via repeat 1 and/or the R1-R2 inter-repeat; a more internal site within the C-terminal one-third of α- and β-tubulin cross-linked to a subset of the other repeat units. A model is presented in which each tau molecule folds up to interact with only one or two tubulin monomers.
31. Loveland K.L., Herszfeld D., Chu B., Rames E., Christy E., Briggs L.J., Shakri R., de Kretser D.M., Jans D.A. Novel low molecular weight microtubule-associated protein-2 isoforms contain a functional nuclear localization sequence. J Biol Chem. 274:1999;19261-19268.
32. Tokuraku K., Katsuki M., Nakagawa H., Kotani S. A new model for microtubule-associated protein (MAP)-induced microtubule assembly- the Pro-rich region of MAP4 promotes nucleation of microtubule assembly in vitro. Eur J Biochem. 259:1999;158-166. Efficient nucleation of microtubules by microtubule-associated proteins, a more demanding step than growth, requires the proline-rich domain in addition to the repeat domain. Without it, microtubules appeared (by electron microscopy) to be wavy, possibly because they failed to close properly.
33. Tokuraku K., Katsuki M., Matui T., Kuroya T., Kotani S. Microtubule binding property of microtubule-associated protein 2 differs from that of microtubule-associated protein 4 and tau. Eur J Biochem. 264:1999;996-1001. Excess amounts of the microtubule-binding domain of tau completely released tau and MAP4 from microtubules, but released only about half of bound MAP2. MAP1 was partially released.
34. Trinczek B., Ebneth A., Mandelkow E-M., Mandelkow E. Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J Cell Sci. 112:1999;2355-2367. Tau transfected into non-neuronal cells did not alter the speed of moving vesicles, but it changed their frequency of attachment to and detachment from microtubules.
35. Felgner H., Frank R., Biernat J., Mandelkow E-M., Mandelkow E., Ludin B., Matus A., Schliwa M. Domains of neuronal microtubule-associated proteins and flexural rigidity of microtubules. J Cell Biol. 138:1997;1067-1075.
36. Goode B.L., Denis P.E., Panda D., Radeke M.J., Miller H.P., Wilson L., Feinstein S.C. Functional interactions between the proline-rich and repeat regions of tau enhance microtubule binding and assembly. Mol Biol Cell. 8:1997;353-365.
37. Ceska T.A., Edelstein S.J. Three-dimensional reconstruction of tubulin in zinc-induced sheets. II. Consequences of removal of microtubule associated proteins. J Mol Biol. 175:1984;349-370.
38. Panda D., Miller H.P., Wilson L. Rapid treadmilling of brain microtubules free of microtubule-associated proteins in vitro and its suppression by tau. Proc Natl Acad Sci USA. 96:1999;12459-12464. Conditions were found under which the dynamic instability of microtubules assembled from pure tubulin was suppressed, but rapid treadmilling still occurred. The addition of tau suppressed the treadmilling.
39. Hagiwara H., Yorifuji H., Satoyoshitake R., Hirokawa N. Competition between motor molecules (kinesin and cytoplasmic dynein) and fibrous microtubule-associated proteins in binding to microtubules. J Biol Chem. 269:1994;3581-3589.
40. Hirose K., Löwe J., Alonso M., Cross R.A., Amos L.A. Congruent docking of dimeric kinesin and ncd into 3-D electron cryo-microscopy maps of microtubule-motor·ADP complexes. Mol Biol Cell. 10:1999;2063-2074. Dimeric kinesin, in the same conformation as solved by X-ray crystallography, was docked into a map of microtubules decorated in the same nucleotide state as in the crystals. The result is somewhat different from some earlier reports [42] based on docking weakly binding kinesin/ncd conformations into maps showing motors in tightly bound states.
41. Sakowicz R., Berdelis M.S., Ray K., Blackburn C.L., Hopmann C., Faulkner D.J., Goldstein L.S. A marine natural product inhibitor of kinesin motors. Science. 280:1998;292-295. A compound isolated from a marine sponge was shown to inhibit kinesin activity by binding to its motor domain, in competition with microtubules.
42. Mandelkow E., Hoenger A. Structures of kinesin and kinesin-microtubule interactions. Curr Opin Cell Biol. 11:1999;34-44.
43. Kozielski F., Sack S., Marx A., Thormählen M., Schönbrunn E., Biou V., Thompson A., Mandelkow E.M., Mandelkow E. The crystal structure of dimeric kinesin and implications for microtubule-dependent motility. Cell. 91:1997;941-985.
44. Alonso M.C., Vanderkerckhove J., Cross R.A. Proteolytic mapping of kinesin/ncd-microtubule interface: nucleotide-dependent conformational changes in the loops L8 and L12. EMBO J. 17:1998;945-951.
45. Okada Y., Hirokawa N. A processive single-headed motor: kinesin superfamily protein KIF1A. Science. 283:1999;1152-1157. A motor domain construct of KIF1A, a single-headed kinesin superfamily protein, was shown to move along the microtubule for more than 1 μm before detaching. The movement along the microtubules was stochastic and fitted a biased Brownian movement model.
46. Iyadurai S., Lu M.G., Gilbert S.P., Hays T.S. Evidence for cooperative interactions between the two motor domains of cytoplasmic dynein. Curr Biol. 9:1999;771-774.
47. Sakakibara H., Kojima H., Sakai Y., Katayama E., Oiwa K. Inner-arm dynein c of Chlamydomonas flagella is a single-headed processive motor. Nature. 400:1999;586-590. This paper showed, using light microscopy, that beads carrying only one molecule of a single-headed axonemal dynein moved processively along microtubules in 8 nm steps, but slipped backwards under high loads.
48. Goldsmith M., Yarbrough L., van der Kooy D. Mechanics of motility: distinct dynein binding domains on alpha- and beta-tubulin. Biochem Cell Biol. 73:1995;665-671.
49. Audebert S., White D., Cosson J., Huitorel P., Edde B., Gagnon C. The carboxy-terminal sequence Asp427-Glu432 of beta-tubulin plays an important function in axonemal motility. Eur J Biochem. 261:1999;48-56. Monoclonal antibodies specific to particular tubulin isoforms were shown to be directed at the C termini. Their effect on demembranated sperm was to reduce the flagellar beat frequency.
50. Gee M., Vallee R. The role of the dynein stalk in cytoplasmic and flagellar motility. Eur Biophys J. 27:1998;466-473.
51. Hirose K., Amos W.B., Lockhart A., Cross R.A., Amos L.A. Three-dimensional cryo-electron microscopy of 16-protofilament microtubules: structure, polarity and interaction with motor protein. J Struct Biol. 118:1997;140-148.
52. Sack S., Müller J., Marx A., Thormählen M., Mandelkow E.M., Brady S.T., Mandelkow E. X-ray structure of motor and neck domains from rat brain kinesin. Biochemistry. 36:1997;16155-16165.
53. Jimenez M., Evangelio J., Aranda C., Lopez Brauet A., Andreu D., Rico M., Lagos R., Andreu J., Monasterio O. Helicity of alpha(404-451) and beta(394-445) tubulin C-terminal recombinant peptides. Protein Sci. 8:1999;788-799. Circular dichroism showed that peptides corresponding to the final approximately 50 residues of α- and β-tubulin had no defined structure in water, but formed α helices in trifluoroethanol. The helical segment of α(404-451) was the same as α-H12 in the α-tubulin crystal structure [2], but the helical segment in β(394-445) was longer than β-H12 of β-tubulin by at least nine residues.
54. ••].
55. ••]. Site-specific cross-linking confirmed that it can bind to both α- and β-tubulin in the weakly binding state.
56. Rice S., Lin A.W., Safer D., Hart C.L., Naber N., O'Carragher B., Cain S.M., Pechatnikova E., Wilson-Kubalek E.M., Whittaker M.et al. A structural change in the kinesin motor protein that drives motility. Nature. 402:1999;778-784. Using labels detectable by electron spin resonance, fluorescence resonance energy transfer and electron cryomicroscopy, this work revealed that the essential neck linker of monomeric kinesin is mobile in solution, irrespective of the nucleotide bound to the molecule. Surprisingly, the neck became immobilised only when kinesin is bound to microtubules (MTs) in the presence of ATP. The authors present a model that helps to explain the processive movement of dimeric kinesin. Their results show that binding of fresh ATP to a motor attached to a MT causes the neck linker to make a decisive move towards the MT plus end.
57. Cross R.A. Kinesin's dynamically dockable neck. Curr Biol. 10:2000;R124-R126.
58. Case R.B., Rice S., Hart C.L., Ly B., Vale R.D. Role of the kinesin neck linker and catalytic core in microtubule-based motility. Curr Biol. 10:2000;157-160.
59. Koonce M.P., Tikhonenko I. Functional elements within the dynein microtubule-binding domain. Mol Biol Cell. 11:2000;523-529. The authors put alanine in place of various residues in the microtubule (MT)-binding loop that extends from the globular 380 kDa monomeric head domain of Dictyostelium cytoplasmic dynein. Several substitutions caused loss of binding to MTs, others enhanced binding; some mutants even remained bound in the presence of ATP. The results reveal the complexity of this 'loop' and show that its activity is closely coupled in some way to the active site within the globular domain.