Katanin regulates dynamics of microtubules and biogenesis of motile cilia

Journal of Cell Biology

Volumn 178, Issue 6, 2007, Pages 1065-1079

  Sharma, Neeraj ^a   Bryant, Jessica ^a   Wloga, Dorota ^a   Donaldson, Rachel ^a   Davis, Richard C ^a,c   Jerka Dziadosz, Maria ^b   Gaertig, Jacek ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; CELL PROTEIN; GLUTAMINE; GLYCINE; KATANIN; POLYMER; PROTEIN SUBUNIT; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL MOTILITY; EUKARYOTIC FLAGELLUM; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; TETRAHYMENA;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CILIA; MICROTUBULES; MUTATION; PHYLOGENY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTOZOAN PROTEINS; TETRAHYMENA THERMOPHILA; TUBULIN;

TETRAHYMENA;

EID: 34548838592     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200704021     Document Type: Article

References (54)

1. Allen, R.D. 1969. The morphogenesis of basal bodies and accessory structures of the cortex of the ciliate protozoan Tetrahymena pyriformis. J. Cell Biol. 40:716-733.
2. Baas, P.W., A. Karabay, and L. Qiang. 2005. Microtubules cut and run. Trends Cell Biol. 15:518-524.
3. Beisson, J., and M. Jerka-Dziadosz. 1999. Polarities of the centriolar structure: morphogenetic consequences. Biol. Cell. 91:367-378.
4. Bichet, A., T. Desnos, S. Turner, O. Grandjean, and H. Hofte. 2001. BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J. 25:137-148.
5. Bonnet, C., D. Boucher, S. Lazereg, B. Pedrotti, K. Islam, P. Denoulet, and J.C. Larcher. 2001. Differential binding regulation of microtubule- associated proteins MAP1A, MAP1B, and MAP2 by tubulin polyglutamylation. J. Biol. Chem. 276:12839-12848.
6. Burk, D.H., B. Liu, R. Zhong, W.H. Morrison, and Z.H. Ye. 2001. A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell. 13:807-827.
7. Cassidy-Hanley, D., J. Bowen, J.H. Lee, E. Cole, L.A. VerPlank, J. Gaertig, M.A. Gorovsky, and P.J. Bruns. 1997. Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics. 146:135-147.
8. Dymek, E.E., P.A. Lefebvre, and E.F. Smith. 2004. PF15p is the Chlamydomonas homologue of the Katanin p80 subunit and is required for assembly of flagellar central microtubules. Eukaryot. Cell. 3:870-879.
9. Eddé, B., J. Rossier, J.-P. Le Caer, E. Desbruyeres, F. Gros, and P. Denoulet. 1990. Posttranslational glutamylation of α-tubulin. Science. 247:83-85.
10. Eisen, J.A., R.S. Coyne, M. Wu, D. Wu, M. Thiagarajan, J.R. Wortman, J.H. Badger, Q. Ren, P. Amedeo, K.M. Jones, et al. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4:e286.
11. Felsenstein, J. 1997. An alternating least squares approach to inferring phylogenies from pairwise distances. Syst. Biol. 46:101-111.
12. Fouquet, J.P., Y. Prigent, and M.L. Kann. 1996. Comparative immunogold analysis of tubulin isoforms in the mouse sperm flagellum: unique distribution of glutamylated tubulin. Mol. Reprod. Dev. 43:358-365.
13. Frankel, J., E.M. Nelsen, and L.M. Jenkins. 1981. Development of the ciliature of Tetrahymena thermophila. II. Spatial subdivision prior to cytokinesis. Dev. Biol. 88:39-54.
14. Gaertig, J., M.A. Cruz, J. Bowen, L. Gu, D.G. Pennock, and M.A. Gorovsky. 1995. Acetylation of lysine 40 in alpha-tubulin is not essential in Tetrahymena thermophila. J. Cell Biol. 129:1301-1310.
15. Galtier, N., M. Gouy, and C. Gautier. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12:543-548.
16. Hartman, J.J., and R.D. Vale. 1999. Microtubule disassembly by ATP-dependent oligomerization of the AAA enzyme katanin. Science. 286:782-785.
17. Hazan, J., N. Fonknechten, D. Mavel, C. Paternotte, D. Samson, F. Artiguenave, C.S. Davoine, C. Cruaud, A. Durr, P. Wincker, et al. 1999. Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia. Nat. Genet. 23:296-303.
18. Iftode, F., and A. Fleury-Aubusson. 2003. Structural inheritance in Paramecium: ultrastructural evidence for basal body and associated rootlets polarity transmission through binary fission. Biol. Cell. 95:39-51.
19. Janke, C., K. Rogowski, D. Wloga, C. Regnard, A.V. Kajava, J.-M. Strub, N. Temurak, J. van Dijk, D. Boucher, A. van Dorsselaer, et al. 2005. Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science. 308:1758-1762.
20. Kann, M.L., S. Soues, N. Levilliers, and J.P. Fouquet. 2003. Glutamylated tubulin: diversity of expression and distribution of isoforms. Cell Motil. Cytoskeleton. 55:14-25.
21. Lechtreck, K.-F., and S. Geimer. 2000. Distributon of polyglutamylated tubulin in the flagellar apparatus of green flagellates. Cell Motil. Cytoskeleton. 47:219-235.
22. Levilliers, N., A. Fleury, and A.M. Hill. 1995. Monoclonal and polyclonal antibodies detect a new type of post-translational modification of axonemal tubulin. J. Cell Sci. 108:3013-3028.
23. Lohret, T.A., F.J. McNally, and L. Quarmby. 1998. A role for katanin-mediated axonemal severing during Chlamydomonas defalgellation. Mol. Biol. Cell. 9:1195-1207.
24. Lu, C., M. Srayko, and P.E. Mains. 2004. The Caenorhabditis elegans microtubule-severing complex MEI-1/MEI-2 katanin interacts differently with two superficially redundant beta-tubulin isotypes. Mol. Biol. Cell. 15:142-150.
25. McNally, F.J., and R.D. Vale. 1993. Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell. 75:419-429.
26. McNally, F.J., and S. Thomas. 1998. Katanin is responsible for the M-phase microtubule-severing activity in Xenopus eggs. Mol. Biol. Cell. 9:1847-1861.
27. McNally, K., A. Audhya, K. Oegema, and F.J. McNally. 2006. Katanin controls mitotic and meiotic spindle length. J. Cell Biol. 175:881-891.
28. Multigner, L., I. Pignot-Paintrand, Y. Saoudi, D. Job, U. Plessmann, M. Rüdiger, and K. Weber. 1996. The A and B tubules of the outer doublets of sea urchin sperm axonemes are composed of different tubulin variants. Biochemistry. 35:10862-10871.
29. Orso, G., A. Martinuzzi, M.G. Rossetto, E. Sartori, M. Feany, and A. Daga. 2005. Disease-related phenotypes in a Drosophila model of hereditary spastic paraplegia are ameliorated by treatment with vinblastine. J. Clin. Invest. 115:3026-3034.
30. Peris, L., M. Thery, J. Faure, Y. Saoudi, L. Lafanechere, J.K. Chilton, P. Gordon-Weeks, N. Galjart, M. Bornens, L. Wordeman, et al. 2006. Tubulin tyrosination is a major factor affecting the recruitment of CAP-Gly proteins at microtubule plus ends. J. Cell Biol. 174:839-849.
31. Piperno, G., M. Ledizet, and X.J. Chang. 1987. Microtubules containing acetylated ?-tubulin in mammalian cells in culture. J. Cell Biol. 104:289-302.
32. Pitelka, D.R. 1961. Fine structure and silver line and fibrillar systems of three tetrahyminid species. J. Protozool. 8:75-89.
33. Qiang, L., W. Yu, A. Andreadis, M. Luo, and P.W. Baas. 2006. Tau protects microtubules in the axon from severing by katanin. J. Neurosci. 26:3120-3129.
34. Quarmby, L.M. 2004. Cellular deflagellation. Int. Rev. Cytol. 233:47-91.
35. Redeker, V., N. Levilliers, J.-M. Schmitter, J.-P. Le Caer, J. Rossier, A. Adoutte, and M.-H. Bré. 1994. Polyglycylation of tubulin: a post-translational modification in axonemal microtubules. Science. 266:1688-1691.
36. Reed, N.A., D. Cai, L. Blasius, G.T. Jih, E. Meyhofer, J. Gaertig, and K.J. Verhey. 2006. Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16:2166-2172.
37. Roll-Mecak, A., and R.D. Vale. 2005. The Drosophila homologue of the heredi tary spastic paraplegia protein, spastin, severs and disassembles microtubules. Curr. Biol. 15:650-655.
38. Rudiger, A.H., M. Rudiger, J. Wehland, and K. Weber. 1999. Monoclonal antibody ID5: epitope characterization and minimal requirements for the recognition of polyglutamylated alpha- and beta-tubulin. Eur. J. Cell Biol. 78:15-20.
39. Scholey, J.M. 2003. Intraflagellar transport. Annu. Rev. Cell Dev. Biol. 19:423-443.
40. Shang, Y., X. Song, J. Bowen, R. Corstanje, Y. Gao, J. Gaertig, and M.A. Gorovsky. 2002. A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc. Natl. Acad. Sci. USA. 99:3734-3739.
41. Sherwood, N.T., Q. Sun, M. Xue, B. Zhang, and K. Zinn. 2004. Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol. 2:e429.
42. Srayko, M., D.W. Buster, O.A. Bazirgan, F.J. McNally, and P.E. Mains. 2000. MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes Dev. 14:1072-1084.
43. Srayko, M., E.T. O'toole E, A.A. Hyman, and T. Müller-Reichert. 2006. Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr Biol. 16:1944-1949.
44. Stargell, L.A., D.P. Heruth, J. Gaertig, and M.A. Gorovsky. 1992. Drugs affecting microtubule dynamics increase ?-tubulin mRNA accumulation via transcription in Tetrahymena thermophila. Mol. Cell. Biol. 12:1443-1450.
45. Tarrade, A., C. Fassier, S. Courageot, D. Charvin, J. Vitte, L. Peris, A. Thorel, E. Mouisel, N. Fonknechten, N. Roblot, et al. 2006. A mutation of spastin is responsible for swellings and impairment of transport in a region of axon characterized by changes in microtubule composition. Hum. Mol. Genet. 15:3544-3558.
46. Terada, S., M. Kinjo, and N. Hirokawa. 2000. Oligomeric tubulin in large transporting complex is transported via kinesin in squid giant axons. Cell. 103:141-155.
47. Thazhath, R., C. Liu, and J. Gaertig. 2002. Polyglycylation domain of beta-tubulin maintains axonemal architecture and affects cytokinesis in Tetrahymena. Nat. Cell Biol. 4:256-259.
48. Thazhath, R., M. Jerka-Dziadosz, J. Duan, D. Wloga, M.A. Gorovsky, J. Frankel, and J. Gaertig. 2004. Cell context-specific effects of the beta-tubulin glycylation domain on assembly and size of microtubular organelles. Mol. Biol. Cell. 15:4136-4147.
49. Trotta, N., G. Orso, M.G. Rossetto, A. Daga, and K. Broadie. 2004. The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr. Biol. 14:1135-1147.
50. Ueno, H., K. Gonda, T. Takeda, and O. Numata. 2003. Identification of elongation factor-1alpha as a Ca2+/calmodulin-binding protein in Tetrahymena cilia. Cell Motil. Cytoskeleton. 55:51-60.
51. White, S.R., K.J. Evans, J. Lary, J.L. Cole, and B. Lauring. 2007. Recognition of C-terminal amino acids in tubulin by pore loops in Spastin is important for microtubule severing. J. Cell Biol. 176:995-1005.
52. Wloga, D., A. Camba, K. Rogowski, G. Manning, M. Jerka-Dziadosz, and J. Gaertig. 2006. Members of the Nima-related kinase family promote disassembly of cilia by multiple mechanisms. Mol. Biol. Cell. 17:2799-2810.
53. Xia, L., B. Hai, Y. Gao, D. Burnette, R. Thazhath, J. Duan, M.-H. Bré, N. Levilliers, M.A. Gorovsky, and J. Gaertig. 2000. Polyglycylation of tubulin is essential and affects cell motility and division in Tetrahymena thermophila. J. Cell Biol. 149:1097-1106.
54. Zhang, D., G.C. Rogers, D.W. Buster, and D.J. Sharp. 2007. Three microtubule severing enzymes contribute to the "Pacman-flux" machinery that moves chromosomes. J. Cell Biol. 177:231-242.