Tubulin and microtubule structure

Current Opinion in Cell Biology

Volumn 10, Issue 1, 1998, Pages 16-22

  Downing, Kenneth H ^a   Nogales, Eva ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TUBULIN;

CELL ULTRASTRUCTURE; CRYOELECTRON MICROSCOPY; DEPOLYMERIZATION; MICROTUBULE; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW;

EID: 0032005075     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(98)80082-3     Document Type: Article

References (37)

1. Caplow M, Shanks J. Evidence that a single monolayer tubulin-GTP cap is both necessary and sufficient to stabilize microtubules. of special interest Mol Biol Cell. 7:1996;663-675 The minus ends of microtubules assembled from tubulin-GTP were transiently stabilized against dilution-induced disassembly by reaction with tubulin-GMPCPP. The minimum size of a tubulin-GMPCPP cap sufficient to prevent disassembly was estimated from the lifetime of the microtubules following dilution, and fromm the time required for the loss of a single tubulin-GMPCPP subunit from the microtubule end. The authors concluded that a microtubule capped with 13-14 tubulin-GMPCPP subunits switches to disassembly after only one dissociation event.
2. Tran PT, Walker RA, Salmon ED. A metastable intermediate state of microtubule dynamic instability that differs significantly between plus and minus ends. of special interest J Cell Biol. 138:1997;105-117 Microtubules were cut using a UV microbeam or severed with a glass microneedle while observed by dark field microscopy or video-enhanced differential interference contrast microscopy, respectively. The severed plus ends rapidly shortened, as expected by the lack of a GTP cap, but minus ends immediately resumed elongation. These results suggest the existence of a metastable kinetic intermediate in dynamic instability between the elongation and shortening rates.
3. Ludueña RF. The multiple forms of tubulin: different gene products and covalent modifications. of outstanding interest Int Rev Cytol. 178:1998;207-275 This is an extensive review of the functional significance of tubulin isotypes and the regulation of their expression, from protists to vertebrates. The review also covers all the known post-translational modifications on tubulin.
4. Wilson PG, Borisy GG. Evolution of the multi-tubulin hypothesis. Bioessays. 19:1997;451-454.
5. Raff EC, Fackenthal JD, Hutchens JA, Hoyle HD, Turner FR. Microtubule architecture specified by a β-tubulin isoform. of outstanding interest Science. 275:1997;70-74 In order to test whether orthologous β tubulins from different species are functionally equivalent, the moth Heliothis virescens β2 homologue was expressed in Drosophila testes. Co-expression of the moth and fly β isotypes resulted in the formation of accessory microtubules with the structural characteristics of those from the moth (e.g. higher protofilament number). These experiments demonstrate that the architecture of the microtubule cytoskeleton can be directed by a component β tubulin.
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9. Sosa H, Milligan RA. Three-dimensional structure of ncd-decorated microtubules obtained by a back-projection method. of outstanding interest J Mol Biol. 260:1996;743-755 Using cryoelectron microscopy and a back-projection method the authors obtained reconstructions of microtubules decorated with the motor domain of ncd. A view of the reconstructions along the microtubules axis from the minus end shows that the ncd motor domain tilts anticlockwise, while the tubulin subunits tilt clockwise.
10. Arnal I, Metoz F, DeBonis S, Wade RH. Three-dimensional structure of functional motor proteins on microtubules. of special interest Curr Biol. 6:1996;1265-1270 Three-dimensional maps of motor - microtubule complexes obtained by cryoelectron microscopy and helical reconstruction showed that the motors have one attached head and one unattached head per tubulin dimer. The unattached heads of kinesin and ncd had distinctly different conformations.
11. Hirose K, Lockhart A, Cross RA, Amos LA. Three-dimensional cryoelectron microscopy of dimeric kinesin and ncd motor domains on microtubules. of special interest Proc Natl Acad Sci USA. 93:1996;9539-9544 Naturally occurring 16-protofilament microtubules were decorated with dimeric kinesin and ncd motor domains and images were reconstructed by cryoelectron microscopy and helical methods. The reconstruction show that the attached heads of kinesin and ncd bind to tubulin in the same way, while the unattached heads point in opposite directions; the second kinesin head points towards the plus microtubule end, the second ncd head towards the minus end.
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18. Hoenger A, Milligan RA. Motor domains of kinesin and ncd interact with microtubule protofilaments with the same binding geometry. of special interest J Mol Biol. 265:1997;553-564 The structure and microtubule-binding properties of kinesin and ncd were compared using negative stain electron microscopy and tilt series of tubulin sheets decorated with the motor domains of those proteins. Both motors bind to the crest of the protofilament and make contact with both α and β tubulin. The geometry of attachment is very similar. The binding seemed to induce a conformational change in tubulin that the authors suggested could take an active role in motor directionality.
19. Hoenger A, Milligan RA. Polarity of 2-D and 3-D maps of tubulin sheets and motor-decorated sheets. J Mol Biol. 263:1996;114-119.
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24. De Pereda JM, Andreu JM. Mapping surface sequences of the tubulin dimer and taxol-induced microtubules with limited proteolysis. of special interest Biochemistry. 35:1996;14184-14202 Proteolysis studies of tubulin dimers and microtubules with 12 different proteases revealed 80 different points of nicking by proteolysis that were mapped to α and β tubulin sequences with the aid of site-directed antibodies. Although the majority of the sites remained accessible in microtubules, two sites in α and one in β became protected upon polymerization.
25. Nogales E, Wolf SG, Khan IA, Ludueña RF, Downing KH. Structure of tubulin at 6.5 Å and location of the taxol-binding site. Nature. 375:1995;424-427.
26. Nogales E, Wolf SG, Wolf SG, Downing KH. Visualizing the secondary structure of tubulin: Three-dimensional map at 4 Å J Struct Biol. 118:1997;119-127.
27. Nogales E, Wolf SG, Downing KH. Atomic model of the tubulin dimer. of outstanding interest Nature. 1997; This paper provides the first atomic model of tubulin. The model was fitted to a 3.7 Å density map obtained by electron crytallography of zinc-induced tubulin sheets, and includes a molecule of GTP bound to α tubulin and molecules of GDP and taxol bound to β tubulin. The model is related to previous biochemical and mutagenesis data that dealt with cysteine cross-linking linking, drug binding, and nucleotide binding, hydrolysis and exchangeability.
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29. Tran PT, Joshi P, Salmon ED. How tubulin subunits are lost from the shortening ends of microtubules. J Struct Biol. 118:1997;107-118.
30. Caplow M, Ruhlen RL, Shanks J. The free energy of hydrolysis of a microtubule-bound nucleotide triphosphate is near zero: all of the free energy for hydrolysis is stored in the microtubule lattice. J Cell Biol. 127:1994;779-788.
31. Vale RD, Coppin CM, Malik F, Kull FJ, Milligan RA. Tubulin GTP hydrolysis influences the structure, mechanical properties, and kinesin-driven transport of microtubules. J Biol Chem. 269:1994;23769-23775.
32. Hyman AA, Chrétien D, Arnal I, Wade RH. Structural changes accompanying GTP hydrolysis of microtubules: information from a slowly hydrolyzable analog guanylyl-(α,β)-methylenediphosphonate. J Cell Biol. 128:1995;117-125.
33. Severin FF, Sorger PK, Hyman AA. Kinetochores distinguish GTP from GDP forms of the microtubule lattice. of special interest Nature. 388:1997;888-891 The authors monitor the attachment of reconstituted kinetochores from yeast to microtubules containing regions made of tubulin-GDP and tubulin-GMPCPP. Kinetochores bound preferentially to GMPCPP regions. They also studied the binding of kinetochores to microtubules of known polarity made with tubulin-GMPCPP, and observed that kinetochores bind preferentially to the plus ends.
34. Hirose K, Fan J, Amos LA. Re-examination of the polarity of microtubules and sheets decorated with kinesin motor domain. J Mol Biol. 251:1995;329-333.
35. Wolf SG, Nogales E, Kikkawa M, Gratzinger D, Hirokawa N, Downing KH. Interpreting a medium-resolution model of tubulin: comparison of zinc-sheet and microtubule structure. J Mol Biol. 263:1996;485-501.
36. Mitchison TJ. Localization of an exchangeable GTP binding site at the plus end of microtubules. Science. 261:1993;1044-1047.
37. Fan J, Griffiths AD, Lockhart A, Cross RA, Amos LA. Microtubule minus ends can be labeled with a phage display antibody specific to α-tubulin. of outstanding interest J Mol Biol. 259:1996;325-330 The amino-terminal 100 residues of α tubulin were bacterially expressed, and a clone was selected from antibody-expressing phagemid particles that reacted with the expressed α tubulin amino terminus and native tubulin but not with expressed β tubulin amino terminus. Gold beads coated with the antibody were found to bind exclusively to minus ends of axonemes, indicating that α tubulin crowns the minus end of microtubules.