Molecular Neurobiology

, Volume 2, Issue 2, pp 133–153

Posttranslational tyrosination/detyrosination of tubulin

  • Héctor S. Barra
  • Carlos A. Arce
  • Carlos E. Argaraña
Article

Abstract

Tubulin can be posttranslationally modified at the carboxyl terminus of the α-subunit by the addition or release of a tyrosine residue. These reactions involve two enzymes, tubulin: tyrosine ligase and tubulin carboxypeptidase. The tyrosine incorporation reaction has been described mainly in nervous tissue but it has also been found in a great variety of tissues and different species. Molecular aspects of the reactions catalyzed by these enzymes are at present well known, especially the reaction carried out by the ligase. Several lines of evidence indicate that assembled tubulin is the preferred substrate of the carboxypeptidase, whereas nonassembled tubulin is preferred by the ligase. Apparently this posttranslational modification does not affect the capacity of tubulin to form microtubules but it generates microtubules with different degrees of tyrosination. Variation in the content of the carboxyterminal tyrosine of α-tubulin as well as changes in the activity of the ligase and the carboxypeptidase are manifested during development. Changes in the cellular microtubular network modify the turnover of the carboxyterminal tyrosine of α-tubulin. Different subsets of microtubules with different degrees of tyrosination have been detected in interphase cells and during the mitotic cycle. Data from biochemical, immunological, and genetic studies have been compiled in this review; these are presented, with pertinent comments, with the hope of facilitating the comprehension of this particular aspect of the microtubule field.

Index Entries

Tyrosination detyrosination tubulin microtubules tyrosination/detyrosination of tubulin posttranslational modification of tubulin carboxyl terminus of a-tubulin state of tyrosination of the carboxyl terminus of α-tubulin cytoskeleton 

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References

  1. Agrawal H. C., Davis J. M., and Himwich W. A. (1966) Postnatal changes in free amino acid pool of rat brain.J. Neurochem. 13, 607–615.PubMedGoogle Scholar
  2. Arce C. A., Barra H. S., Rodríguez J. A., and Caputto R. (1975a) Tentative identification of the amino acid that binds tyrosine as a single unit into a soluble brain protein.FEBS Lett. 50, 5–7.PubMedGoogle Scholar
  3. Arce C. A., Rodríquez J. A., Barra H. S., and Caputto R. (1975b) Incorporation ofl-tyrosine,l-Phenylalanine andl-3,4-dihydroxyphenylalanine as single units into rat brain tubulin.Eur. J. Biochem. 59, 145–149.PubMedGoogle Scholar
  4. Arce C. A., Hallak M. E., Rodríguez J. A., Barra H. S., Caputto R. (1978) Capability of tubulin and microtubules to incorporate and to release tyrosine and phenylalanine and the effect of the incorporation of these amino acids on tubulin assembly.J. Neurochem. 31, 205–210.PubMedGoogle Scholar
  5. Arce C. A. and Barra H. S. (1983) Association of tubulinyl-tyrosine carboxypeptidase with microtubules.FEBS Lett. 157, 75–78.PubMedGoogle Scholar
  6. Arce C. A. and Barra H. S. (1985) Release of C-terminal tyrosine from tubulin and microtubules at steady state.Biochem. J. 226, 311–317.PubMedGoogle Scholar
  7. Argaraña C. E., Arce C. A., Barra H. S., and Caputto R. (1977) In vivo incorporation of [14C]tyrosine into the C-terminal position of the α-subunit of tubulin.Arch. Biochem. Biophys. 180, 264–268.PubMedGoogle Scholar
  8. Argaraña C. E., Barra H. S., and Caputto R. (1978) 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.PubMedGoogle Scholar
  9. Argaraña C. E., Barra H. S., and Caputto R. (1980) Tubulinyl-tyrosine carboxypeptidase from chicken brain: properties and partial purification.J. Neurochem. 34, 114–118.PubMedGoogle Scholar
  10. Argaraña C. E., Barra H. S., and Caputto R. (1981) Inhibition of tubulinyl-tyrosine carboxypeptidase by brain soluble RNA and proteoglycan.J. Biol. Chem. 256, 827–830.PubMedGoogle Scholar
  11. Barra H. S., Uñates L. E., Sayavedra M., and Caputto R. (1972) Capacities for binding amino acids by tRNAs from rat brain and their changes during development.J. Neurochem. 19, 2289–2297.PubMedGoogle Scholar
  12. Barra H. S., Rodríguez J. A., Arce C. A., and Caputto R. (1973a) 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.PubMedGoogle Scholar
  13. Barra H. S., Arce C. A., Rodríguez J. A., and Caputto R. (1973b) Incorporation of phenylalanine as single unit into rat brain protein: Reciprocal inhibition by phenylalanine and tyrosine of their respective incorporations.J. Neurochem. 21, 1241–1251.PubMedGoogle Scholar
  14. Barra H. S., Arce C. A., Rodríguez J. A., and Caputto R. (1974) Some common properties of the protein that incorporates tyrosine as a single unit and the microtubule protein.Biochem. Biophys. Res. Commun. 60, 1384–1390.PubMedGoogle Scholar
  15. Barra H. S., Arce C. A., and Caputto R. (1980) Total tubulin and its amonoacylated and non-amino-acylated forms during development of rat brain.Eur. J. Biochem. 109, 439–446.PubMedGoogle Scholar
  16. Barra H. S., Argaraña Barra H. S., Argaraña C. E., and Caputto R. (1982) Enzymatic detyrosination of tubulin tyrosinated in rat brain slices and extracts.J. Neurochem. 38, 112–115.PubMedGoogle Scholar
  17. Barra H. S. and Argaraña C. E. (1982) Activation of tubulinyl-tyrosine carboxypeptidase by spermine, spermidine, and putrescine.Biochem. Biophys. Res. Commun. 108, 654–657.PubMedGoogle Scholar
  18. Barra H. S. and Arce C. A. (1983) State of tyrosination of soluble synaptosomal tubulin.Comun. Biolog. 1, 13–18.Google Scholar
  19. Barra H. S., Modesti N. M., and Arce C. A. (1987) Tyrosination-detyrosination of thec-terminus of α-tubulin in oocytes and embryos ofBufo arenarum.Comp. Biochem. Physiol. vol. 87B,1, 151–155.Google Scholar
  20. Bayer S. M. and McMurray W. C. (1967) The metabolism of amino acids in developing rat brain.J. Neurochem. 14, 695–706.PubMedGoogle Scholar
  21. Beltramo D. M., Carabelos A. C., Arce C. A., and Barra H. S. (1986) Effect of tubulin-interacting compounds and solution variables on the release ofc-terminal tyrosine from nonassembled tubulin.An. Asoc. Quim. Argent. 74 (6), 633–642.Google Scholar
  22. Beltramo D. M., Arce C. A., and Barra H. S. (1987a) Tyrosination of microtubules and nonassembled tubulin in brain slices.Eur. J. Biochem. 162, 137–141.PubMedGoogle Scholar
  23. Beltramo D. M., Arce C. A., and Barra H. S. (1987b) Tubulin but not microtubules is the substrate for tubulin:tyrosine ligase in mature avian erythrocytes.J. Biol. Chem. 262, 15673–15677.PubMedGoogle Scholar
  24. Bhattacharyya B. and Wolff J. (1975) Membrane bound tubulin in brain and thyroid tissue.J. Biol. Chem. 250, 7639–7646.PubMedGoogle Scholar
  25. Borisy G. G., Olmsted J. B., Marcum J. M., and Allen C. (1974) Microtubule assembly in vitro.Fed. Proc. 33, 167–174.PubMedGoogle Scholar
  26. Bré M. E., Kreis T. E., and Karsenti E. (1987) Control microtubule nucleation and stability in Madin-Darby canine kidney cells: The occurrence of non-centrosomal, stable detyrosinated microtubules.J. Cell Biol. 105, 1283–1296.PubMedGoogle Scholar
  27. Bulinski J. C., Rodríquez J. A., and Borisy G. G. (1981) Test of four possible mechanisms for the temporal control of spindle and cytoplasmic microtubule assembly in HeLa cells.J. Biol. Chem. 255, 1684–1688.Google Scholar
  28. Burgoyne R. D. and Norman K. M. (1986) Alpha-tubulin is not detyrosylated during axonal transport.Brain Res. 381, 113–120.PubMedGoogle Scholar
  29. Cambray-Deakin M. A. and Burgoyne R. D. (1987) Posttranslational modifications of α-tubulin: Acetylated and detyrosinated forms in axons of rat cerebellum.J. Cell Biol. 104, 1569–1574.PubMedGoogle Scholar
  30. Cumming R., Burgoyne R. D., and Lytton N. A. (1984) Immunocytochemical demonstration of α-tubulin modification during axonal maturation in the cerebellar cortex.J. Cell Biol. 98, 347–351.PubMedGoogle Scholar
  31. Deanin G. G. and Gordon M. W. (1976) The distribution of tyrosyltubulin ligase in brain and other tissues.Biochem. Biophys. Res. Commun. 71, 676–683.PubMedGoogle Scholar
  32. Deanin G. G., Thompson W. C., and Gordon M. W. (1977) Tyrosyltubulin ligase activity in brain, skeletal muscle and liver of the developing chick.Dev. Biol. 57, 230–233.PubMedGoogle Scholar
  33. Deanin G. G., Preston S. F., and Gordon M. W. (1981) Carboxyl terminal tyrosine metabolism of alpha tubulin and changes in cell shape: Chinese hamster ovary cells.Biochem. Biophys. Res. Commun. 100, 1642–1650.PubMedGoogle Scholar
  34. Deanin G. G., Preston S. F., and Gordon M. W. (1982) Nerve growth factor and the metabolism of the carboxyl terminal tyrosine of alpha tubulin.Develop. Neurosci. 5, 101–107.Google Scholar
  35. Dentler W. L., Granett S., and Rosenbaum J. L. (1975) Ultrastructural localization of the high molecular weight proteins associated with in vitro-assembled brain microtubules.J. Cell Biol. 65, 237–241.PubMedGoogle Scholar
  36. Eipper B. A. (1972) Rat brain microtubule protein: purification and determination of covalent bound phosphate and carbohydrate.Proc. Natl. Acad. Sci. USA 69, 2283–2287.PubMedGoogle Scholar
  37. Feit H. and Barondes S. H. (1970) Colchicine-binding activity in particulate fractions of mouse brain.J. Neurochem. 17, 1355–1364.PubMedGoogle Scholar
  38. Forrest G. L. and Klevecz R. R. (1978) Tyrosyltubulin ligase and colchicine binding activity in synchronized Chinese hamster cells.J. Cell Biol. 78, 441–450.PubMedGoogle Scholar
  39. Gabius H. J., Graupner G., and Cramer F. (1983) Activity patterns of aminoacyl-tRNA synthetases, tRNA methylases, arginyltransferases and tubulin:tyrosine ligase during development and aging ofCaenorhabditis elegans.Eur. J. Biochem. 131, 231–234.PubMedGoogle Scholar
  40. Gard D. L. and Kirschner M. W. (1985) A polymer-dependent increase in phosphorylation of β-tubulin accompanies differentiation of a mouse neuroblastoma cell line.J. Cell Biol. 100, 765–774.Google Scholar
  41. Geuens G., Gundersen G. G., Nuydens R., Cornelissen F., Bulinski J. C., and DeBrabander M. (1986) Ultrastructural colocalization of tyrosinated and detyrosinated α-tubulin in interphase and mitotic cells.J. Cell Biol. 103, 1883–1893.PubMedGoogle Scholar
  42. Gozes I. and Littauer U. Z. (1978) Tubulin microhetterogeneity increases with rat brain maturation.Nature 276, 411–413.PubMedGoogle Scholar
  43. Gundersen G. G., Kalnoski M. H., and Bulinski J. C. (1984) Distinct populations of microtubules: tyrosinated and non tyrosinated alpha tubulin are distributed differentlyin vivo.Cell 38, 779–789.PubMedGoogle Scholar
  44. Gundersen G. G. and Bulinski J. C. (1986a) Distribution of tyrosinated and non-tyrosinated α-tubulin during mitosis.J. Cell Biol. 102, 1118–1126.PubMedGoogle Scholar
  45. Gundersen G. G. and Bulinski J. C. (1986b) Microtubule arrays in differentiated cells contain elevated levels of a posttranslationally modified form of tubulin.Eur. J. Cell Biol. 42, 288–294.PubMedGoogle Scholar
  46. Gundersen G. G., Khawaja S., and Bulinski J. C. (1987) Postpolymerization detyrosination of α-tubulin: a mechanism for subcellular differentiation of microtubules.J. Cell Biol. 105, 251–264.PubMedGoogle Scholar
  47. Hallak M. E., Rodríguez J. A., Barra H. S., and Caputto R. (1977) Release of ryrosine from tyrosinatedtubulin. Some common factors that affect this process and the assembly of tubulin.FEBS Lett. 73, 147–150.PubMedGoogle Scholar
  48. Jacobs M. (1979) Tubulin and nucleotides,Microtubules, Roberts K. and Hyams J. S., eds., Academic Press, NY, pp. 255–277.Google Scholar
  49. Johnson J. C., Gold G. J., and Clouet D. H. (1973) An improved method for the assay ofDopa.Anal. Biochem. 54, 129–136.PubMedGoogle Scholar
  50. Kilmartin J. V., Wright B., and Milstein C. (1982) Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line.J. Cell Biol. 93, 576–582.PubMedGoogle Scholar
  51. Kobayashi T. and Flavin M. (1981) Tubulin tyrosylation in invertebrates.Comp. Biochem. Physiol. 69B, 387–392.Google Scholar
  52. Kobayashi T. and Matsumoto G. (1982) Cytoplasmic tubulin from squid nerve fully retains C-terminal tyrosine.J. Biochem. 92, 647–652.PubMedGoogle Scholar
  53. Kodowaki T., Fujita-Yamaguchi Y., Nishida E., Takaku F., Akiyama T., Kathuria S., Akanuma Y., and Kasuga M. (1985) Phosphorylation of tubulin and microtubules associated proteins by the purified insulin receptor kinase.J. Biol. Chem. 260, 4016–4020.Google Scholar
  54. Krämmer G., Singhofer-Wowra M., Seedorf K., Little M., and Schedl T. (1985) A plasmodial α-tubulin cDNA fromPhysarum polycephalum. Nucleotide sequence and comparative analysis.J. Mol. Biol. 183, 633–638.PubMedGoogle Scholar
  55. Kreis, T. E. (1987) Microtubules containing detyrosinated tubulin are less dynamic.EMBO J. 6, 2597–2606.PubMedGoogle Scholar
  56. Kumagai H. and Nishida E. (1980) The interaction between calcium-dependent regulator protein (calmodulin) and microtubule proteins. Further studies on the mechanism of microtubule assembly inhibition by calmodulin.Biomed. Res. 1, 223–229.Google Scholar
  57. Kumar N. and Flavin M. (1981) Preferential action of a brain detyrosinolating carboxypeptidase on polymerized tubulin.J. Biol. Chem. 256, 7678–7680.PubMedGoogle Scholar
  58. Kumar N. and Flavin M. (1982a) Modulation of some parameters of assembly of microtubules in vitro by tyrosination of tubulin.Eur. J. Biochem. 128, 215–222.PubMedGoogle Scholar
  59. Kumar N. and Flavin M. (1982b) A new tubulin-binding protein.Biochem. Biophys. Res. Commun. 106, 704–710.PubMedGoogle Scholar
  60. Lee J. C., Field D. J., George H. J., and Head J. (1986) Biochemical and chemical properties of tubulin subspecies,Dynamic Aspects of Microtubule Biology, Soifer D., ed.,Ann. NY Acad. Sci. 466, 111–128.PubMedGoogle Scholar
  61. Lewis S. A., Lee M. G. S., and Cowan N. J. (1985) Five mouse tubulin isotypes and their regulated expression during development.J. Cell Biol. 101, 852–861.PubMedGoogle Scholar
  62. L’Hernault S. W. and Rosenbaum J. L. (1985a) Reversal of the posttranslational modification onChlamydomonas flagellar α-tubulin occurs during flagellar resorption.J. Cell Biol. 100, 457–462.PubMedGoogle Scholar
  63. L’Hernault S. W. and Rosenbaum J. L. (1985b) Clamydomonas α-tubulin is posttranslationally modified by acetylation on the ε-amino group of a lysine.Biochemistry 24, 473–478.PubMedGoogle Scholar
  64. López R. A., Arce C. A., and Barra H. S. (1987) Acción de haparina sobre tubulina carboxipeptidasa. IVJornadas Científicas de la Sociedad de Biología de Córdoba. Carlos Paz (Pvcia. de Córdoba). Argentina.Google Scholar
  65. Lu R. C. and Elzinga M. (1978) The primary structure of tubulin. Sequences of the carboxyl terminus and seven other cyanogen bromide peptides from the α-chain.Biochem. Biophys. Acta. 537, 320–328.PubMedGoogle Scholar
  66. Marcum J. M., Dedman J. R., Brinkley B. R., and Means A. (1978) Control of microtubule assembly disassembly by calcium-dependent tregulator protein.Proc. Natl. Acad. Sci. USA 75, 3771–3775.PubMedGoogle Scholar
  67. Martensen T. M. (1982) Preparation of brain tyrosinotubulin carboxypeptidase.Meth. Cell Biol. 24, 265–269.Google Scholar
  68. Matsumoto G., Murofushi H. Endo S., Kobayashi T., and Sakai H. (1983) Tyrosinated tubulin is necessary for maintenance of membrane excitability in squid giant axon,Structure and Function in Excitable Cells, Chang D. C., Tasaki I., Adelman W. J., Jr., and Leuchtag H. R., eds., Plenum, 471–483.Google Scholar
  69. Modesti N. M., Argaraña C. E., Barra H. S., and Caputto R. (1984) Inhibition of brain tubulinyl-tyrosine carboxypeptidase by endogenous proteins.J. Neurosci. Research 12, 583–593.Google Scholar
  70. Modesti N. M. and Barra H. S. (1986) The interaction of myelin basic protein with tubulin and the inhibition of tubulin carboxypeptidase activity.Biochem. Biophys. Res. Commun. 136, 482–489.PubMedGoogle Scholar
  71. Monteiro M. J. and Cox R. A. (1987) Primary structure of an α-tubulin gene ofPhysarum polycephalum.J. Mol. Biol. 193, 427–438.PubMedGoogle Scholar
  72. Murofushi H. (1980) Purification and characterization of tubulin-tyrosine ligase from porcine brain.J. Biochem. 87, 979–984.PubMedGoogle Scholar
  73. Nath J. and Flavin M. (1979) Tubulin tyrosylationin vivo and changes accompanying differentiation of cultured neuroblastoma-glioma hybrid cells.J. Biol. Chem. 254, 11505–11510.PubMedGoogle Scholar
  74. Nath J., Flavin M., and Schiffmann E. (1981) Stimulation of tubulin tyrosinolation in rabbit leukocytes evoked by the chemoattractant formyl-methionylleucyl-phenylalanine.J. Cell Biol. 91, 232–239.PubMedGoogle Scholar
  75. Nath J., Flavin M., and Gallin J. I. (1982) Tubulin-tyrosinolation in human polymorphonuclear leukocytes: studies in normal subjects and in patients with the Chediak-Higashi syndrome.J. Cell Biol. 95, 519–526.PubMedGoogle Scholar
  76. Nath J. and Flavin M. (1984) Tubulin tyrosinolatedin vivo can be different from that tyrosinolatedin vitro.Biochem. Biophys. Acta. 803, 314–322.PubMedGoogle Scholar
  77. Nath J. and Gallin J. I. (1986) Ionic requirements and subcellular localization of tubulin tyrosinolation in human polymorphonuclear leukocytes.J. Immunol. 136, 628–635.PubMedGoogle Scholar
  78. Pierce T., Hanson R. K., Deanin G. G., Gordon M. W., and Levi A. (1978) Developmental and biochemical sudies on tubulin:tyrosine ligase,Maturation of Neurotransmission, Vernadakis A., Giacobini E., and Filogamo G., eds., Karger, Basil, Switzerland, pp. 142–151.Google Scholar
  79. Piperno G. and Fuller M. T. (1985) Monoclonal antibodies specific for an acetylated form of α-tubulin recognizes the antigen in cilia and flagella from a variety of organisms.J. Cell Biol. 101, 2085–2094.PubMedGoogle Scholar
  80. Ponsting I. H., Little M., Krauhs E., and Kempf T. (1979) Carboxy-terminal amino acid sequence of α-tubulin from porcine brain.Nature 282, 423–424.Google Scholar
  81. Pratt L. F., Okamura S., and Cleveland D. W. (1987) A divergent testis-specific α-tubulin isotype that does not contain a codedc-terminal tyrosine.Mol. Cell Biol. 7, 552–555.PubMedGoogle Scholar
  82. Preston S. F., Deanin G. G., Hanson R. D., and Gordon M. W. (1979) The phylogenetic distribution of tubulin:tyrosine ligase.J. Mol. Evol. 13, 233–244.PubMedGoogle Scholar
  83. Preston S. F., Deanin G. G., Hanson R. D., and Gordon M. W. (1981) Tubulin:tyrosine ligase in oocytes and embryos ofXenopus laevis.J. Develop. Biol. 81, 36–42.Google Scholar
  84. Raybin D. and Flavin M. (1975) An enzyme tyrosylating α-tubulin and its role in microtubule assembly.Biochem. Biophys. Res. Commun. 65, 1088–1095.PubMedGoogle Scholar
  85. Raybin D. and Flavin M. (1977a) Enzyme which specifically adds tyrosine to the α-chain of tubulin.Biochemistry 16, 2189–2194.PubMedGoogle Scholar
  86. Raybin D. and Flavin M. (1977b) Modification of tubulin by tyrosylation in cells and extracts and its effect on assemblyin vitro.J. Cell Biol. 73, 492–504.PubMedGoogle Scholar
  87. Roberts K. and Hyams J. (1979)Microtubules. Academic Press, NY, 1–595.Google Scholar
  88. Rodríguez J. A., Arce C. A., Barra H. S., and Caputto R. (1973) Release of tyrosine incorporated as single unit into rat brain protein.Biochem. Biophys. Res. Commun. 54, 335–340.PubMedGoogle Scholar
  89. Rodríguez J. A., Barra H. S., Arce C. A., and Hallak M. E., and Caputto R. (1975) The reciprocal exclusion byl-dopa (l-3,4-dihydroxyphenylalanine) andl tyrosine of their incorporations as single units into a soluble rat brain protein.Biochem. J. 149, 115–121.PubMedGoogle Scholar
  90. Rodríguez J. A. and Borisy G. G. (1978) Modification of thec-terminus of brain tubulin during development.Biochem. Biophys. Res. Commun. 83, 579–586.PubMedGoogle Scholar
  91. Rodríguez J. A. and Borisy G. G. (1979a) Tyrosination state of free tubulin subunits and tubulin disasembled from microtubules of rat brain tissue.Bichem. Biophys. Res. Commun. 89, 893–899.Google Scholar
  92. Rodríguez J. A. and Borisy G. G. (1979b) Experimental phenylketonuria: replacement of carboxyl terminal tyrosine by phenylalanine in infant rat brain tubulin.Science 206, 463–465.PubMedGoogle Scholar
  93. Rodríguez J. A. and Barra H. S. (1983) Tubulin and tubulin-colchicine complex bind to brain microsomal membranein vitro.Mol. Cell Biochem. 56, 49–53.PubMedGoogle Scholar
  94. Schroeder H. C., Wehland J., and Weber K. (1985) Purification of brain tubulin:tyrosine ligase by biochemical and immunological methods.J. Cell Biol. 100 276–281.Google Scholar
  95. Serrano L., De la Torre J., Maccioni R. B., and Avila J. (1984a) Involvement of the carboxyl-terminal domain of tubulin in the regulation of its assembly.Proc. Natl. Acad. Sci. USA,81, 5989–5993.PubMedGoogle Scholar
  96. Serrano L., Avila J., and Maccioni R. B. (1984b) Controlled proteolysis of tubulin by subtilisin: localization of the site for MAP 2 interaction.Biochemistry,23, 4675–4681.PubMedGoogle Scholar
  97. Sherwin T., Schneider A., Sasse R., Seebeck T., and Gull K. (1987) Distinct localization and cell cycle dependence of COOH terminal tyrosinated α-tubulin in the microtubules ofTrypanosoma brucei brucei.J. Cell Biol. 104, 439–446.PubMedGoogle Scholar
  98. Silflow C. D., Chisholm R. L., Conner T. W., and Ranum L. P. W. (1985) The two alpha-tubulin genes ofChlamydomonas reinhardtii code for slightly different proteins.Mol. Cell Biol. 5, 2389–2398.PubMedGoogle Scholar
  99. Soifer D. (1986) Dynamic Aspects of Microtubule Biology,Ann. NY Acad. Sci. 466.Google Scholar
  100. Solomon F. (1977) Binding sites for calcium on tubulin.Biochemistry 16, 358–363.PubMedGoogle Scholar
  101. Theurkauf W. E., Baun H., Bo J., and Wensink P. C. (1986) Tissue-specific and constitutive α-tubulin genes ofDrosophila melanogaster code for structurally distinct proteins.Proc. Natl. Acad. Sci. USA 83, 8477–8481.PubMedGoogle Scholar
  102. Thompson W. C. (1977) Posttranslational addition of tyrosine to alpha tubulin in vivo in intact brain and in myogenic cells in culture.FEBS Lett. 80, 9–13.PubMedGoogle Scholar
  103. Thompson W. C., Deanin G. G., and Gordon M. W. (1979) Intact microtubules are required for rapid turnover of carboxyl-terminal tyrosine of α-tubulin in cell cultures.Proc. Natl. Acad. Sci. USA 76, 1318–1322.PubMedGoogle Scholar
  104. Thompson W. C. (1982) The cyclic tyrosination/detyrosination of alpha tubulin,Methods in Cell Biology, vol. 24, part A, Wilson L., ed., Academic Press, NY, pp. 235–255.Google Scholar
  105. Valenzuela P., Quiroga M., Zaldivar J., Rutter W. J., Kirschner M. W., and Cleveland D. W. (1981) Nucleotide and corresponding amino acid sequences encoded by α and β tubulin mRNAs.Nature 289, 650–655.PubMedGoogle Scholar
  106. Villasante A., Wang D., Dobner P., Dolph P., Lewis S. A., and Cowan W. J. (1986) Six mouse α-tubulin mRNAs encode five distinct tubulin isotypes: testis-specific expression of two sister genes.Mol. Cell. Biol. 6, 2409–2419.PubMedGoogle Scholar
  107. Wandosell F., Serrano L., and Avila J. (1987) Phosphorylation of α-tubulin carboxyl-terminal tyrosine prevents its incorporation into microtubules.J. Biol. Chem. 262, 8268–8273.PubMedGoogle Scholar
  108. Wang D., Villasante A., Lewis S. A., and Cowan W. J. (1986) The mammalian tubulin repertoire, hematopoietic expression of a novel, heterologous β-tubulin isotype.J. Cell Biol. 103, 1903–1910.PubMedGoogle Scholar
  109. Webster D. R., Gundersen G. G., Bulinski J. C., and Borisy G. G. (1987) Assembly and turnover of detyrosinated tubulinin vivo.J. Cell Biol. 105, 265–276.PubMedGoogle Scholar
  110. Wehland J., Willingham M. C., and Sandoval I. V. (1983) A rat monoclonal antibody reacting specifically with the tyrosylated form of α-tubulin. I. Biochemical characterization, effects on microtubule polymerizationin vitro and microtubule polymerization and organizationin vivo.J. Cell Biol. 97, 1467–1475.PubMedGoogle Scholar
  111. Wehland J. and Willingham M. C. (1983) A rat monoclonal antibody reacting specifically with the tyrosylated form of a-tubulin. II. Effects on cell movement, organization of microtubules and intermediate filaments, and arrangements of Golgi elements.J. Cell Biol. 97, 1476–1490.PubMedGoogle Scholar
  112. Wehland J., Schroeder H. C., and Weber K. (1986) Contribution of microtubules to cellular physiology: microinjection of well-characterized monoclonal antibodies into cultured cells,Dynamic Aspects of Microtubule Biology Soifer D., ed.Ann. NY Acad. Sci. 466, 609–621.PubMedGoogle Scholar
  113. Wehland J. and Weber K. (1987a) Tubulin-tyrosine ligase has a binding site on β-tubulin: A two-domain structure of the enzyme.J. Cell Biol. 104, 1059–1067.PubMedGoogle Scholar
  114. Wehland J. and Weber K. (1987b) 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.PubMedGoogle Scholar
  115. Weingarten M. D., Lockwood A. H., Hwo S.-Y, and Kirschner, M. W. (1975) A protein factor essential for microtubule assembly.Proc. Natl. Acad. Sci. USA 72, 1858–1862.PubMedGoogle Scholar
  116. Yanagida M. (1987) Yeast tubulin genes.Microbiol. Sci. 4, 115–118.PubMedGoogle Scholar

Copyright information

© Humana Press Inc. 1988

Authors and Affiliations

  • Héctor S. Barra
    • 1
  • Carlos A. Arce
    • 1
  • Carlos E. Argaraña
    • 1
  1. 1.Centro de Investigaciones en Químíca Biológica de Córdoba, Facultad de Ciencias QuímicasUniversidad Nacional de CórdobaCórdobaArgentina

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