Key Points
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The carboxy-terminal tails of α- and β-tubulin are essential for microtubule function. They lie on the outer surface of the microtubule where they can influence the binding of associated proteins.
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With the exception of acetylation, the post-translational modifications of microtubules — that is, detyrosination/tyrosination, formation of Δ2-tubulin, polyglutamylation and polyglycylation — are all located in the carboxy-terminal tails.
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Acetylation of α-tubulin can be abolished without consequences in Tetrahymena, but it seems to have a function in cell motility. Two histone deacetylases, HDAC6 and SIRT2, have been shown to function as tubulin deacetylases.
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Genetic analysis of polyglycylation in Tetrahymena demonstrates its essential function in the organization of axonemes, cell motility and cytokinesis.
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Polyglutamylation can influence the binding of structural and motor microtubule-associated proteins (MAPs) to microtubules. Antibody-injection studies indicate an important role for polyglutamylation in centriole stability.
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The functional role of the tyrosination cycle of tubulin is still unclear; cells cultured with low activity of the tubulin tyrosine ligase (TTL) enzyme show no obvious defects. TTL-knockout mice, however, die early in development owing to an as-yet-uncharacterized defect.
Abstract
The αβ-tubulin heterodimer, the building block of microtubules, is subject to a large number of post-translational modifications, comparable in diversity to the intensively studied histone modifications. Although these unusual modifications are conserved throughout evolution, their functions have remained almost completely elusive. Recently, however, important advances in the understanding of how tubulin modifications regulate function and organization have been made.
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References
Luduena, R. F. Multiple forms of tubulin: different gene products and covalent modifications. Int. Rev. Cytol. 178, 207–275 (1998).
MacRae, T. H. Tubulin post-translational modifications — enzymes and their mechanisms of action. Eur. J. Biochem. 244, 265–278 (1997).
Nogales, E., Whittaker, M., Milligan, R. A. & Downing, K. H. High-resolution model of the microtubule. Cell 96, 79–88 (1999).
Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the αβ tubulin dimer by electron crystallography. Nature 391, 199–203 (1998).
Jimenez, M. A. et al. Helicity of α(404–451) and β(394–445) tubulin C-terminal recombinant peptides. Protein Sci. 8, 788–799 (1999).
Sullivan, K. F. & Cleveland, D. W. Identification of conserved isotype-defining variable region sequences for four vertebrate β tubulin polypeptide classes. Proc. Natl Acad. Sci. USA 83, 4327–4331 (1986).
Mejillano, M. R. & Himes, R. H. Assembly properties of tubulin after carboxyl group modification. J. Biol. Chem. 266, 657–664 (1991).
Mejillano, M. R., Tolo, E. T., Williams, R. C. Jr. & Himes, R. H. The conversion of tubulin carboxyl groups to amides has a stabilizing effect on microtubules. Biochemistry 31, 3478–3483 (1992).
Fackenthal, J. D., Turner, F. R. & Raff, E. C. Tissue-specific microtubule functions in Drosophila spermatogenesis require the β2-tubulin isotype-specific carboxy terminus. Dev. Biol. 158, 213–227 (1993).
Duan, J. & Gorovsky, M. A. Both carboxy-terminal tails of α- and β-tubulin are essential, but either one will suffice. Curr. Biol. 12, 313–316 (2002). Elegant genetic experiments identify essential functions for the tubulin carboxy-terminal tails in Tetrahymena.
Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41–45 (2000).
L'Hernault, S. W. & Rosenbaum, J. L. Chlamydomonas α-tubulin is posttranslationally modified by acetylation on the ε-amino group of a lysine. Biochemistry 24, 473–478 (1985).
LeDizet, M. & Piperno, G. Identification of an acetylation site of Chlamydomonas α-tubulin. Proc. Natl Acad. Sci. USA 84, 5720–5724 (1987).
Sasse, R. & Gull, K. Tubulin post-translational modifications and the construction of microtubular organelles in Trypanosoma brucei. J. Cell Sci. 90, 577–589 (1988).
Weber, K., Schneider, A., Westermann, S., Muller, N. & Plessmann, U. Posttranslational modifications of α- and β-tubulin in Giardia lamblia, an ancient eukaryote. FEBS Lett. 419, 87–91 (1997).
Schneider, A., Plessmann, U., Felleisen, R. & Weber, K. Posttranslational modifications of trichomonad tubulins; identification of multiple glutamylation sites. FEBS Lett. 429, 399–402 (1998).
Schneider, A., Plessmann, U. & Weber, K. Subpellicular and flagellar microtubules of Trypanosoma brucei are extensively glutamylated. J. Cell Sci. 110, 431–437 (1997).
Maruta, H., Greer, K. & Rosenbaum, J. L. The acetylation of α-tubulin and its relationship to the assembly and disassembly of microtubules. J. Cell Biol. 103, 571–579 (1986).
Hubbert, C. et al. HDAC6 is a microtubule-associated deacetylase. Nature 417, 455–458 (2002).
Matsuyama, A. et al. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21, 6820–6831 (2002).
Zhang, Y. et al. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J. 22, 1168–1179 (2003).
North, B. J., Marshall, B. L., Borra, M. T., Denu, J. M. & Verdin, E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol. Cell 11, 437–444 (2003). References 19–22 identify HDAC6 and SIRT2 as tubulin deacetylases and propose a role for tubulin acetylation in cell motility.
Kozminski, K. G., Diener, D. R. & Rosenbaum, J. L. High level expression of nonacetylatable α-tubulin in Chlamydomonas reinhardtii. Cell Motil. Cytoskeleton 25, 158–170 (1993).
Gaertig, J. et al. Acetylation of lysine 40 in α-tubulin is not essential in Tetrahymena thermophila. J. Cell Biol. 129, 1301–1310 (1995).
Haggarty, S. J., Koeller, K. M., Wong, J. C., Grozinger, C. M. & Schreiber, S. L. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl Acad. Sci. USA 100, 4389–4394 (2003).
Palazzo, A., Ackerman, B. & Gundersen, G. G. Cell biology: tubulin acetylation and cell motility. Nature 421, 230 (2003).
Redeker, V. et al. Polyglycylation of tubulin: a posttranslational modification in axonemal microtubules. Science 266, 1688–1691 (1994).
Rudiger, M., Plessmann, U., Rudiger, A. H. & Weber, K. β tubulin of bull sperm is polyglycylated. FEBS Lett. 364, 147–151 (1995).
Plessmann, U. & Weber, K. Mammalian sperm tubulin: an exceptionally large number of variants based on several posttranslational modifications. J. Protein Chem. 16, 385–390 (1997).
Mary, J., Redeker, V., Le Caer, J. P., Rossier, J. & Schmitter, J. M. Posttranslational modifications of axonemal tubulin. J. Protein Chem. 16, 403–407 (1997).
Bre, M. H., Redeker, V., Vinh, J., Rossier, J. & Levilliers, N. Tubulin polyglycylation: differential posttranslational modification of dynamic cytoplasmic and stable axonemal microtubules in paramecium. Mol. Biol. Cell 9, 2655–2665 (1998).
Weber, K., Schneider, A., Muller, N. & Plessmann, U. Polyglycylation of tubulin in the diplomonad Giardia lamblia, one of the oldest eukaryotes. FEBS Lett. 393, 27–30 (1996).
Xia, L. et al. Polyglycylation of tubulin is essential and affects cell motility and division in Tetrahymena thermophila. J. Cell Biol. 149, 1097–1106 (2000).
Thazhath, R., Liu, C. & Gaertig, J. Polyglycylation domain of β-tubulin maintains axonemal architecture and affects cytokinesis in Tetrahymena. Nature Cell Biol. 4, 256–259 (2002). References 33 and 34 provide a careful analysis of tubulin polyglycylation in Tetrahymena and identify its essential functions in cell motility and cytokinesis.
Edde, B. et al. Posttranslational glutamylation of α-tubulin. Science 247, 83–85 (1990).
Mary, J., Redeker, V., Le Caer, J. P., Prome, J. C. & Rossier, J. Class I and IVa β-tubulin isotypes expressed in adult mouse brain are glutamylated. FEBS Lett. 353, 89–94 (1994).
Rudiger, M., Plessman, U., Kloppel, K. D., Wehland, J. & Weber, K. Class II tubulin, the major brain β tubulin isotype is polyglutamylated on glutamic acid residue 435. FEBS Lett. 308, 101–105 (1992).
Alexander, J. et al. Characterization of posttranslational modifications in neuron-specific class III β-tubulin by mass spectrometry. Proc. Natl Acad. Sci. USA 88, 4685–4689 (1991).
Redeker, V., Rossier, J. & Frankfurter, A. Posttranslational modifications of the C-terminus of α-tubulin in adult rat brain: α4 is glutamylated at two residues. Biochemistry 37, 14838–14844 (1998).
Bre, M. H., de Nechaud, B., Wolff, A. & Fleury, A. Glutamylated tubulin probed in ciliates with the monoclonal antibody GT335. Cell Motil. Cytoskeleton 27, 337–349 (1994).
Lechtreck, K. F. & Geimer, S. Distribution of polyglutamylated tubulin in the flagellar apparatus of green flagellates. Cell Motil. Cytoskeleton 47, 219–235 (2000).
Bobinnec, Y. et al. Glutamylation of centriole and cytoplasmic tubulin in proliferating non-neuronal cells. Cell Motil. Cytoskeleton 39, 223–232 (1998).
Regnard, C. et al. Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 275, 15969–15976 (2000). Identifies the nucleosome assembly proteins NAP1 and NAP2 as substrates for polyglutamylation, indicating that this is a more general protein modification.
Regnard, C., Audebert, S., Desbruyeres Denoulet, P. & Edde, B. Tubulin polyglutamylase: partial purification and enzymatic properties. Biochemistry 37, 8395–8404 (1998).
Regnard, C. et al. Characterisation of PGs1, a subunit of a protein complex co-purifying with tubulin polyglutamylase. J. Cell Sci. 116, 4181–4190 (2003).
Regnard, C., Desbruyeres, E., Denoulet, P. & Edde, B. Tubulin polyglutamylase: isozymic variants and regulation during the cell cycle in HeLa cells. J. Cell Sci. 112, 4281–4289 (1999).
Westermann, S., Schneider, A., Horn, E. K. & Weber, K. Isolation of tubulin polyglutamylase from Crithidia; binding to microtubules and tubulin, and glutamylation of mammalian brain α- and β-tubulins. J. Cell Sci. 112, 2185–2193 (1999).
Westermann, S., Plessmann, U. & Weber, K. Synthetic peptides identify the minimal substrate requirements of tubulin polyglutamylase in side chain elongation. FEBS Lett. 459, 90–94 (1999).
Westermann, S. & Weber, K. Identification of CfNek, a novel member of the NIMA family of cell cycle regulators, as a polypeptide copurifying with tubulin polyglutamylation activity in Crithidia. J. Cell Sci. 115, 5003–5012 (2002). Identifies a kinase of the NIMA family as the first enzyme involved in tubulin polyglutamylation.
Liu, S. et al. A defect in a novel Nek-family kinase causes cystic kidney disease in the mouse and in zebrafish. Development 129, 5839–5846 (2002).
Pazour, G. J. & Rosenbaum, J. L. Intraflagellar transport and cilia-dependent diseases. Trends Cell Biol. 12, 551–555 (2002).
Manning, G., Whyte, D. B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912–1934 (2002).
Upadhya, P., Birkenmeier, E. H., Birkenmeier, C. S. & Barker, J. E. Mutations in a NIMA-related kinase gene, Nek1, cause pleiotropic effects including a progressive polycystic kidney disease in mice. Proc. Natl Acad. Sci. USA 97, 217–221 (2000).
Audebert, S. et al. Reversible polyglutamylation of α- and β-tubulin and microtubule dynamics in mouse brain neurons. Mol. Biol. Cell 4, 615–626 (1993).
Larcher, J. C., Boucher, D., Lazereg, S., Gros, F. & Denoulet, P. Interaction of kinesin motor domains with α- and β-tubulin subunits at a tau-independent binding site. Regulation by polyglutamylation. J. Biol. Chem. 271, 22117–22124 (1996).
Bonnet, C. et al. Differential binding regulation of microtubule-associated proteins MAP1A, MAP1B, and MAP2 by tubulin polyglutamylation. J. Biol. Chem. 276, 12839–12848 (2001).
Okada, Y. & Hirokawa, N. Mechanism of the single-headed processivity: diffusional anchoring between the K-loop of kinesin and the C terminus of tubulin. Proc. Natl Acad. Sci. USA 97, 640–645 (2000).
Thorn, K. S., Ubersax, J. A. & Vale, R. D. Engineering the processive run length of the kinesin motor. J. Cell Biol. 151, 1093–1100 (2000).
Gagnon, C. et al. The polyglutamylated lateral chain of α-tubulin plays a key role in flagellar motility. J. Cell Sci. 109, 1545–1553 (1996).
Million, K. et al. Polyglutamylation and polyglycylation of α- and β-tubulins during in vitro ciliated cell differentiation of human respiratory epithelial cells. J. Cell Sci. 112, 4357–4366 (1999).
Bobinnec, Y. et al. Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J. Cell Biol. 143, 1575–1589 (1998). Antibody-microinjection studies identify tubulin polyglutamylation as being essential for centriole stability and centrosome structure.
Bornens, M. Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25–34 (2002).
Argarana, C. E., Barra, H. S. & Caputto, R. Release of [14C]tyrosine from tubulinyl-[14C]tyrosine by brain extract. Separation of a carboxypeptidase from tubulin-tyrosine ligase. Mol. Cell. Biochem. 19, 17–21 (1978).
Barra, H. S., Rodriguez, J. A., Arce, C. A. & Caputto, R. A soluble preparation from rat brain that incorporates into its own proteins (14C)arginine by a ribonuclease-sensitive system and (14C)tyrosine by a ribonuclease-insensitive system. J. Neurochem. 20, 97–108 (1973).
Arce, C. A., Rodriguez, J. A., Barra, H. S. & Caputo, R. Incorporation of L-tyrosine, L-phenylalanine and L-3,4-dihydroxyphenylalanine as single units into rat brain tubulin. Eur. J. Biochem. 59, 145–149 (1975).
Argarana, C. E., Arce, C. A., Barra, H. S. & Caputto, R. In vivo incorporation of [14C]tyrosine into the C-terminal position of the α subunit of tubulin. Arch. Biochem. Biophys. 180, 264–268 (1977).
Paturle-Lafanechere, L. et al. Characterization of a major brain tubulin variant which cannot be tyrosinated. Biochemistry 30, 10523–10528 (1991).
Rudiger, M., Wehland, J. & Weber, K. The carboxy-terminal peptide of detyrosinated α tubulin provides a minimal system to study the substrate specificity of tubulin-tyrosine ligase. Eur. J. Biochem. 220, 309–320 (1994).
Banerjee, A. Coordination of posttranslational modifications of bovine brain α-tubulin. Polyglycylation of δ2 tubulin. J. Biol. Chem. 277, 46140–46144 (2002).
Multigner, L. et al. The A and B tubules of the outer doublets of sea urchin sperm axonemes are composed of different tubulin variants. Biochemistry 35, 10862–10871 (1996).
Johnson, K. A. The axonemal microtubules of the Chlamydomonas flagellum differ in tubulin isoform content. J. Cell Sci. 111, 313–320 (1998).
Bre, M. H. et al. Axonemal tubulin polyglycylation probed with two monoclonal antibodies: widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J. Cell Sci. 109, 727–738 (1996).
Huitorel, P. et al. Differential distribution of glutamylated tubulin isoforms along the sea urchin sperm axoneme. Mol. Reprod. Dev. 62, 139–148 (2002).
Murofushi, H. Purification and characterization of tubulin-tyrosine ligase from porcine brain. J. Biochem. 87, 979–984 (1980).
Ersfeld, K. et al. Characterization of the tubulin-tyrosine ligase. J. Cell Biol. 120, 725–732 (1993).
Galperin, M. Y. & Koonin, E. V. A diverse superfamily of enzymes with ATP-dependent carboxylate-amine/thiol ligase activity. Protein Sci. 6, 2639–2643 (1997).
Argarana, C. E., Barra, H. S. & Caputto, R. Tubulinyl-tyrosine carboxypeptidase from chicken brain: properties and partial purification. J. Neurochem. 34, 114–118 (1980).
Wehland, J. & Weber, K. Turnover of the carboxy-terminal tyrosine of α-tubulin and means of reaching elevated levels of detyrosination in living cells. J. Cell Sci. 88, 185–203 (1987).
Webster, D. R., Gundersen, G. G., Bulinski, J. C. & Borisy, G. G. Assembly and turnover of detyrosinated tubulin in vivo. J. Cell Biol. 105, 265–276 (1987).
Webster, D. R., Wehland, J., Weber, K. & Borisy, G. G. Detyrosination of α tubulin does not stabilize microtubules in vivo. J. Cell Biol. 111, 113–122 (1990).
Cook, T. A., Nagasaki, T. & Gundersen, G. G. Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J. Cell Biol. 141, 175–185 (1998).
Palazzo, A. F., Cook, T. A., Alberts, A. S. & Gundersen, G. G. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nature Cell Biol. 3, 723–729 (2001).
Infante, A. S., Stein, M. S., Zhai, Y., Borisy, G. G. & Gundersen, G. G. Detyrosinated (Glu) microtubules are stabilized by an ATP-sensitive plus-end cap. J. Cell Sci. 113, 3907–3919 (2000).
Gurland, G. & Gundersen, G. G. Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J. Cell Biol. 131, 1275–1290 (1995).
Liao, G. & Gundersen, G. G. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J. Biol. Chem. 273, 9797–9803 (1998).
Kreitzer, G., Liao, G. & Gundersen, G. G. Detyrosination of tubulin regulates the interaction of intermediate filaments with microtubules in vivo via a kinesin-dependent mechanism. Mol. Biol. Cell 10, 1105–1118 (1999).
Lafanechere, L. et al. Suppression of tubulin tyrosine ligase during tumor growth. J. Cell Sci. 111, 171–181 (1998).
Mialhe, A. et al. Tubulin detyrosination is a frequent occurrence in breast cancers of poor prognosis. Cancer Res. 61, 5024–5027 (2001).
Eiserich, J. P. et al. Microtubule dysfunction by posttranslational nitrotyrosination of α-tubulin: a nitric oxide-dependent mechanism of cellular injury. Proc. Natl Acad. Sci. USA 96, 6365–6370 (1999).
Kalisz, H. M., Erck, C., Plessmann, U. & Wehland, J. Incorporation of nitrotyrosine into α-tubulin by recombinant mammalian tubulin-tyrosine ligase. Biochim. Biophys. Acta 1481, 131–138 (2000).
Chang, W. et al. Alteration of the C-terminal amino acid of tubulin specifically inhibits myogenic differentiation. J. Biol. Chem. 277, 30690–30698 (2002).
Eipper, B. A. Properties of rat brain tubulin. J. Biol. Chem. 249, 1407–1416 (1974).
Gard, D. L. & Kirschner, M. W. A polymer-dependent increase in phosphorylation of β-tubulin accompanies differentiation of a mouse neuroblastoma cell line. J. Cell Biol. 100, 764–774 (1985).
Caron, J. M. Posttranslational modification of tubulin by palmitoylation: I. In vivo and cell-free studies. Mol. Biol. Cell 8, 621–636 (1997).
Ozols, J. & Caron, J. M. Posttranslational modification of tubulin by palmitoylation: II. Identification of sites of palmitoylation. Mol. Biol. Cell 8, 637–645 (1997).
Caron, J. M., Vega, L. R., Fleming, J., Bishop, R. & Solomon, F. Single site α-tubulin mutation affects astral microtubules and nuclear positioning during anaphase in Saccharomyces cerevisiae: possible role for palmitoylation of α-tubulin. Mol. Biol. Cell 12, 2672–2687 (2001).
Sisson, J. C., Ho, K. S., Suyama, K. & Scott, M. P. Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90, 235–245 (1997).
Nogales, E., Downing, K. H., Amos, L. A. & Lowe, J. Tubulin and FtsZ form a distinct family of GTPases. Nature Struct. Biol. 5, 451–458 (1998).
McKean, P. G., Vaughan, S. & Gull, K. The extended tubulin superfamily. J. Cell Sci. 114, 2723–2733 (2001).
Dupuis-Williams, P. et al. Functional role of ε-tubulin in the assembly of the centriolar microtubule scaffold. J. Cell Biol. 158, 1183–1193 (2002).
Vinh, J. et al. Structural characterization by tandem mass spectrometry of the posttranslational polyglycylation of tubulin. Biochemistry 38, 3133–3139 (1999).
Vinh, J., Loyaux, D., Redeker, V. & Rossier, J. Sequencing branched peptides with CID/PSD MALDI-TOF in the low–picomole range: application to the structural study of the posttranslational polyglycylation of tubulin. Anal. Chem. 69, 3979–3985 (1997).
Acknowledgements
The authors wish to thank G. Barnes and D. Drubin for critical reading of the manuscript. We thank E. Nogales, R. Thazhath and J. Gaertig for providing figures and J. Wehland, D. Job and B. Eddé for communicating results prior to publication. We apologize to all authors whose work could not be cited due to space limitations. S.W. is supported by a fellowship of the Deutsche Forschungsgemeinschaft (DFG).
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Glossary
- MITOTIC SPINDLE
-
A bipolar array of microtubules that functions to move the duplicated chromosomes during mitosis and meiosis.
- AXONEME
-
A bundle of microtubules and associated proteins that form the core of a flagellum or cilium.
- CILIA
-
Hair-like extensions of cells, which contain a microtubular axoneme. Beating movements of cilia are responsible for swimming.
- FLAGELLA
-
Long protrusions that contain a microtubular axoneme, the beating of which can drive a cell through liquid media. Note that bacterial flagella are constructed very differently from eukaryotic flagella.
- PROTISTS
-
Single-celled eukaryotic organisms that are either free living or parasitic.
- TETRAHYMENA THERMOPHILA
-
Unicellular ciliated eukaryote.
- CHLAMYDOMONAS REINHARDTII
-
Flagellated green algae that are often used as a model organism to study flagellar assembly and architecture.
- siRNA
-
Small interfering RNA that is used to specifically reduce protein expression by degradation of the corresponding messenger RNA.
- HETEROKARYONS
-
Multinucleate cells containing nuclei of more than one genotype.
- 9 + 2
-
The typical organization of microtubules within an axoneme, with 9 outer doublets and one pair of central microtubules.
- BASAL BODY
-
A short cylindrical array of microtubules that is found at the base of cilia and flagella. It is closely related, in structure, to a centriole.
- CENTRIOLES
-
Usually found in the centre of centrosomes in animal cells, the two centrioles contain triplet microtubules and are located orthogonally to each other. Centrioles are closely related to basal bodies.
- MIDBODY
-
The structure formed at the end of animal-cell cytokinesis, which tethers the cells and can persist for some time.
- HELA CELLS
-
A cultured human epithelial cell line derived from a cervical carcinoma.
- ISOELECTRIC FOCUSING
-
A method to separate proteins according to their isoelectric point; it is carried out by electrophoresis in a pH gradient.
- EDMAN DEGRADATION
-
A classical method of peptide sequencing by stepwise degradation and identification of the amino-terminal amino acid.
- TANDEM-MS
-
(or MS/MS). A variant of mass spectrometry that is used to sequence peptides and determine their structure.
- TRYPANOSOMES
-
Flagellate protozoans, ubiquitous parasites of insects, birds and mammals; some species are important human pathogens.
- CENTROSOME
-
The main microtubule-organizing centre of animal cells. It functions as a spindle pole during mitosis.
- POLYCYSTIC KIDNEY DISEASE
-
(PKD) A genetic disease that is characterized by the formation of multiple cysts in the kidney, which ultimately leads to loss of renal function and the need for dialysis or transplantation.
- KINESIN
-
A microtubular motor protein that generally moves towards the plus end of microtubules.
- DIPLOMONAD
-
A primitive single-celled organism with two nuclei and no mitochondria; includes the human intestinal parasite Giardia lamblia.
- B-TUBULES
-
Incomplete, 10-protofilament microtubules that comprise a part of the outer axoneme doublets.
- RHO-FAMILY GTPases
-
Ras-related small GTPases that mediate signal transduction to cause rearrangements of the actin- and microtubule-filament network.
- FORMINS
-
Rho-GTPase effector proteins that link signal-transduction pathways to actin assembly proteins.
- PLUS END
-
The end of a microtubule at which addition of tubulin dimers occurs most rapidly.
- INTERMEDIATE FILAMENTS
-
10-nm protein filaments that constitute one of the three main cytoskeletal filaments of eukaryotic cells.
- MYOBLAST
-
A specialized cell type that, by fusion with other myoblasts, forms myotubes that eventually differentiate into skeletal-muscle fibres.
- ASTRAL MICROTUBULES
-
A subset of microtubules within the mitotic spindle that are not attached to the kinetochore but extend from the centrosome to the cell cortex.
- BUD NECK
-
A constriction between the mother and daughter cell in the budding yeast Saccharomyces cerevisiae.
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Westermann, S., Weber, K. Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol 4, 938–948 (2003). https://doi.org/10.1038/nrm1260
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DOI: https://doi.org/10.1038/nrm1260
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