Posttranslational modification of brain tubulins from the Antarctic fish Notothenia coriiceps: Reduced C-terminal glutamylation correlates with efficient microtubule assembly at low temperature

Biochemistry

Volumn 43, Issue 38, 2004, Pages 12265-12274

  Redeker, Virginie ^c,d   Frankfurter, Anthony ^b   Parker, Sandra K ^a   Rossier, Jean ^c   Detrich III, H William ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c Brain Plasticity Unit   (France)

^d LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DEGRADATION; PROTEINS;

BRAIN TUBULINS; MICROTUBULE ASSEMBLY;

BRAIN;

TUBULIN;

ALPHA CHAIN; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ANTARCTICA; ARTICLE; BRAIN TISSUE; FISH; LOW TEMPERATURE; MICROTUBULE ASSEMBLY; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PROCESSING;

AGING; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; ANTARCTIC REGIONS; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLD; DNA, COMPLEMENTARY; GLUTAMINE; MICROTUBULES; MOLECULAR SEQUENCE DATA; PERCIFORMES; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; RATS; SEQUENCE ALIGNMENT; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUBULIN;

ANIMALIA; MAMMALIA; NOTOTHENIA; NOTOTHENIA CORIICEPS; TREMATOMUS BERNACCHII;

EID: 4644267074     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049070z     Document Type: Article

References (39)

1. Detrich, H. W., III, Parker, S. K., Williams, R. C., Jr., Nogales, E., and Downing, K. H. (2000) Cold adaptation of microtubule assembly and dynamics. Structural interpretation of primary sequence changes present in the alpha- and beta-tubulins of Antarctic fishes, J. Biol. Chem. 275, 37038-37047.
2. Williams, R. C., Jr., Correia, J. J., and DeVries, A. L. (1985) Formation of microtubules at low temperature by tubulin from Antarctic fish, Biochemistry 24, 2790-2798.
3. Detrich, H. W., III, Johnson, K. A., and Marchese-Ragona, S. P. (1989) Polymerization of Antarctic fish tubulins at low temperatures: energetic aspects, Biochemistry 28, 10085-10093.
4. Detrich, H. W., III, Fitzgerald, T. J., Dinsmore, J. H., and Marchese-Ragona, S. P. (1992) Brain and egg tubulins from Antarctic fishes are functionally and structurally distinct, J. Biol. Chem. 267, 18766-18775.
5. Himes, R. H. and Detrich, H. W., III (1989) Dynamics of Antarctic fish microtubules at low temperatures, Biochemistry 28, 5089-5095.
6. Billger, M., Wallin, M., Williams, R. C., Jr., and Detrich, H. W., III (1994) Dynamic instability of microtubules from cold-living fishes, Cell Motil. Cytoskeleton 28, 327-332.
7. Paluh, J. L., Killilea, A. N., Detrich, H. W., III, and Downing, K. H. (2004) Meiosis-specific failure of cell cycle progression in fission yeast by mutation of a conserved beta-tubulin residue, Mol. Biol. Cell 15, 1160-1171.
8. Detrich, H. W., III, Prasad, V., and Luduena, R. F. (1987) Cold-stable microtubules from Antarctic fishes contain unique alpha tubulins, J. Biol. Chem. 262, 8360-8366.
9. Detrich, H. W., III, and Parker, S. P. (1993) Divergent neural beta tubulin from the Antarctic fish Notothenia coriiceps neglecta: potential sequence contributions to cold adaptation of microtubule assembly, Cell Motil. Cytoskeleton 24, 156-166.
10. Detrich, H. W., III, and Overton, S. A. (1986) Heterogeneity and structure of brain tubulins from cold-adapted Antarctic fishes. Comparison to brain tubulins from a temperate fish and a mammal, J. Biol. Chem. 261, 10922-10930.
11. Edde, B., Rossier, J., Le Caer, J. P., Desbruyeres, E., Gros, F., and Denoulet, P. (1990) Posttranslational glutamylation of alpha-tubulin, Science 247, 83-85.
12. Alexander, J. E., Hunt, D. F., Lee, M K., Shabanowitz, J., Michel, H., Berlin, S. C., MacDonald, T. L., Sundberg, R. J., Rebhun, L. I., and Frankfurter, A. (1991) Characterization of posttranslational modifications in neuron-specific class III beta-tubulin by mass spectrometry, Proc. Natl. Acad. Sci. U.S.A. 88, 4685-4689.
13. Redeker, V., Melki, R., Prome, D., Le Caer, J. P., and Rossier, J. (1992) Structural characterization of the fibrillar form of the yeast Saccharomyces cerevisiae prion Ure2p, FEBS Lett. 313, 185-192.
14. Redeker, V., Rossier, J., and Frankfurter, A. (1998) Posttranslational modifications of the C-terminus of alpha-tubulin in adult rat brain: alpha 4 is glutamylated at two residues, Biochemistry 37, 14838-14844.
15. Redeker, V., Rusconi, F., Mary, J., Prome, D., and Rossier, J. (1996) Structure of the C-terminal tail of alpha-tubulin: increase of heterogeneity from newborn to adult, J. Neurochem. 67, 2104-2114.
16. Redeker, V., Frankfurter, A., and Detrich, H. W., III. (1998) Posttranslational glutamylation of brain tubulins from Antarctic fish Notothenia coriiceps, Mol. Biol. Cell 9, 150a.
17. Parker, S. K., and Detrich, H. W., III (1998) Evolution, organization, and expression of alpha-tubulin genes in the Antarctic fish Notothenia coriiceps. Adaptive expansion of a gene family by recent gene duplication, inversion, and divergence, J. Biol. Chem. 273, 34358-34369.
18. Lacey, E., and Snowdon, K. L. (1990) Isolation of mammalian brain tubulin by amino-activated gel chromatography, J. Chromatogr. 525, 71-84.
19. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
20. Kuriyama, R., Levin, A., Nelson, D., Madl, J., Frankfurter, A., and Kimble, M. (1995) Monoclonal anti-dipeptide antibodies cross-react with detyrosinated and glutamylated forms of tubulins, Cell Motil. Cytoskeleton 30, 171-182.
21. Wallin, M. and Eiliger, M. (1997) Coassembly of bovine and cod microtubule proteins: the ratio of the different tubulins within hybrid microtubules determines the ability to assemble at low temperatures, MAPs dependency and effects of Ca2+, Cell Motil. Cytoskeleton 38, 297-307.
22. Mandelkow, E.-M., Mandelkow, E., and Milligan, R. A. (1991) Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study, J. Cell Biol 114, 977-991.
23. Tran, P. T., Joshi, P., and Salmon, E. D. (1997) How tubulin subunits are lost from the shortening ends of microtubules, J. Struct. Biol. 118, 107-118.
24. Serrano, L., de la Torre, J., Maccioni, R. B., and Avila, J. (1984) Involvement of the carboxyl-terminal domain of tubulin in the regulation of its assembly, Proc. Natl. Acad. Sci. U.S.A. 81, 5989-5993.
25. Bhattacharyya, B., Sackett, D. L., and Wolff, J. (1985) Tubulin, hybrid dimers, and tubulin S. Stepwise charge reduction and polymerization, J. Biol. Chem. 260, 10208-10216.
26. Sackett, D. L., Bhattacharyya, B., and Wolff, J. (1985) Tubulin subunit carboxyl termini determine polymerization efficiency, J. Biol. Chem. 260, 43-45.
27. Detrich, H. W., III, and Overton, S. A. (1988) Antarctic fish tubulins: heterogeneity, structure, amino acid compositions and charge, Comp. Biochem. Physiol. 90B, 593-600.
28. Detrich, H. W., III (1997) Microtubule assembly in cold-adapted organisms: functional properties and structural adaptations of tubulins from Antarctic fishes, Comp. Biochem. Physiol. 118A, 501-513.
29. Klotz, A., Rutberg, M., Denoulet, P., and Wallin, M. (1999) Polyglutamylation of Atlantic cod tubulin: immunochemical localization and possible role in pigment granule transport, Cell Motil. Cytoskeleton 44, 263-273.
30. Breitling, F., and Little, M. (1986) Carboxy-terminal regions on the surface of tubulin and microtubules. Epitope locations of YOL1/34, DM1A and DM1B, J Mol. Biol. 189, 367-370.
31. Nogales, E., Whittaker, M., Milligan, R. A., and Downing, K. H. (1999) High-resolution model of the microtubule, Cell 96, 79-88.
32. Eastman, J. T. (1997) Phyletic divergence and specialization for pelagic life in the Antarctic nototheniid fish Pleuragramma antarcticum, Comp. Biochem. Physiol. 118A, 1095-1101.
33. Rosenbaum, J. (2000) Cytoskeleton: functions for tubulin modifications at last, Curr. Biol. 10, R801-R803.
34. Boucher, D., Larcher, J. C., Gros, F., and Denoulet, P. (1994) Polyglutamylation of tubulin as a progressive regulator of in vitro interactions between the microtubule-associated protein Tau and tubulin, Biochemistry 33, 12471-12477.
35. Gagnon, C., White, D., Cosson, J., Huitorel, P., Edde, B., Desbruyeres, E., Paturle-Lafanechere, L., Multigner, L., Job, D., and Cibert, C. (1996) The polyglutamylated lateral chain of alpha-tubulin plays a key role in flagellar motility, J. Cell Sci. 109, 1545-1553.
36. Larcher, J. C., Boucher, D., Lazereg, S., Gros, F., and Denoulet, P. (1996) Interaction of kinesin motor domains with alpha- and beta-tubulin subunits at a tau-independent binding site. Regulation by polyglutamylation, J. Biol. Chem. 271, 22117-22124.
37. Bonnet, C., Boucher, D., Lazereg, S., Pedrotti, B., Islam, K., Denoulet, P., and Larcher, J. C. (2001) Differential binding regulation of microtubule-associated proteins MAP1A, MAP1B, and MAP2 by tubulin polyglutamylation, J. Biol. Chem. 276, 12839-12848.
38. Detrich, H. W., III, Neighbors, B. W., Sloboda, R. D., and Williams, R. C., Jr. (1990) Microtubule-associated proteins from Antarctic fishes, Cell Motil. Cytoskeleton 17, 174-186.
39. Modig, C., Rutberg, M., Detrich, H. W., III, Billger, M., Stromberg, E., and Wallin, M. (1997) MAP 0, a 400-kDa microtubule-associated protein unique to teleost fish, Cell Motil. Cytoskeleton 38, 258-269.