The Biochemistry of Microtubules

A Review
  • Timothy W. McKeithan
  • Joel L. Rosenbaum


The whole of the complex field of microtubule structure and function is far too broad to cover in this brief review. The intention has been to give a brief overview of the field and to place emphasis on a few areas of recent significant progress. In particular, the related topics of microtubule “treadmilling,” polarity of assembly, and role of nucleotide hydrolysis have been addressed at some length, as has the topic of tubulin heterogeneity. For a more detailed discussion, several recent books can be recommended. Microtubules (Roberts and Hyams, eds., 1979) contains excellent reviews on the major areas of microtubule structure, chemistry, mechanisms of assembly, and functions. Microtubules and Microtubule Inhibitors (De Brabander and De Mey, eds., 1980) contains briefer articles on many topics of current interest. In Microtubules (1978), P. Dustin has authored a remarkably comprehensive review which is especially strong in providing historical perspective, to which this present review is heavily indebted. Also to be recommended is the more recent book Biological Functions of Microtubules and Related Structures (Sakai et al.,1982).


Microtubule Assembly Tubulin Polymerization Tubulin Dimer Cytoplasmic Microtubule Microtubule Protein 


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  1. Allen, C., and Borisy, G. G., 1974, Structural polarity and directional growth of microtubules of Chlamydomonas flagella, J. Mol. Biol. 90: 381–402.PubMedGoogle Scholar
  2. Amara, S. G., Jonas, V., Rosenfeld, M. G., Ong, E. S., and Evans, R. M., 1982, Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products, Nature (London) 298: 240–244.Google Scholar
  3. Amos, L. A., 1977, Arrangement of high molecular weight associated proteins on purified mammalian brain microtubules, J . Cell Biol. 72: 642–654.PubMedGoogle Scholar
  4. Amos, L. A., 1979, Structure of microtubules, in: Microtubules ( K. Roberts and J. S. Hyams), pp. 1–64, Academic Press, London.Google Scholar
  5. Amos, L. A., and Baker, T. S., 1979, The three-dimensional structure of tubulin protofilaments, Nature (London) 279: 607–612.Google Scholar
  6. Amos, L. A., and Klug, A., 1974, Arrangement of subunits in flagellar microtubules, J. Cell Sci. 14: 523–549.PubMedGoogle Scholar
  7. Andre, J., and Thiery, J. P., 1963, Mise en evidence d’une sous-structure fibrillaire dans les filaments axonematique des flagelles, J. Microscopie 2: 71–80.Google Scholar
  8. Arai, T., and Kaziro, Y., 1976, Effect of guanine nucleotides on the assembly of brain micro-tubules: Ability of guanylyl imidophosphate to replace GTP in promoting the polymerization of microtubules in vitro, Biochem. Biophys. Res. Commun. 69: 369–376.PubMedGoogle Scholar
  9. Arce, C. A., Rodriguez, J. A., Barra, H. S., and Caputto, R. 1975, Incorporation of L-tyrosine, Lphenylalanine, and L-3,4-dihydroxyphenylalanine as single units into rat brain tubulin, Eur. J . Biochem. 59: 145–149.PubMedGoogle Scholar
  10. Argarana, 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 alpha subunit of tubulin, Arch. Biochem. Biophys. 180: 264–268.Google Scholar
  11. Baker, T. S., and Amos, L. A., 1978, Structure of the tubulin chimer in zinc-induced sheets, J. Mol. Biol. 123: 89–106.PubMedGoogle Scholar
  12. Ballowitz, E., 1888, Untersuchungen uber die structur der spermatozoen zuggleich ein beitrag zur lehre vom feineren bau der contraktilen elemente. Arch. Mikroskop. Anat. 32: 401–473.Google Scholar
  13. Barnicot, N. A., 1966, A note on the structure of spindle fibers, J. Cell Sci. 1: 217–222.Google Scholar
  14. Barra, H. S., Arce, C. A. A., Rodriguez, J. A., and Caputto, R., 1974, Some common properties of the protein that incorporates tyrosine as a single unit and the microtubule proteins, Biochem. Biophys. Res. Commun. 60: 1384–1390.PubMedGoogle Scholar
  15. Behnke, O., and Forer, A., 1967, Evidence for four classes of microtubules in individual cells, J. Cell Sci. 2: 169–192.PubMedGoogle Scholar
  16. Ben-Zeev, A., Farmer, S. R., and Penman, S., 1979, Mechanisms of regulated tubulin synthesis in cultured mammalian cells, Cell 17: 319–325.Google Scholar
  17. Bergen, L. G., and Borisy, G. G., 1980, Head-to-tail polymerization of microtubules in vitro: Electron microscope analysis of seeded assembly, J. Cell Biol. 84: 141–150.PubMedGoogle Scholar
  18. Bergen, L. G., Kuriyama, R., and Borisy, G. G., 1980, Polarity of microtubules nucleated by centrosomes and chromosomes of Chinese hamster ovary cells in vitro, J. Cell Biol. 84: 151–159.PubMedPubMedCentralGoogle Scholar
  19. Berkowitz, S. A., Katagiri, J., Binder, H. K., and Williams, R. C., Jr., 1977, Separation and characterization of microtubule proteins from calf brain, Biochemistry 16: 5610–5617.PubMedGoogle Scholar
  20. Bershadsky, A. D., and Gelfand, V. I., 1981, ATP-dependent regulation of cytoplasmic micro-tubule disassembly, Proc. Natl. Acad. Sci. USA 78: 3610–3613.PubMedPubMedCentralGoogle Scholar
  21. Bibring, T., Baxandall, J., Denslow, S., and Walker, B., 1976, Heterogeneity of the alpha subunit of tubulin and the variability of tubulin within a single organism, J. Cell Biol. 69: 301–312.PubMedGoogle Scholar
  22. Binder, L. I., and Rosenbaum, J. L., 1973, Directionality of assembly of chick brain tubulin onto sea urchin flagellar microtubules, Biol. Bull. (Woods Hole) 145: 425.Google Scholar
  23. Binder, L. I., and Rosenbaum, J. L., 1978, The in vitro assembly of flagellar outer doublet tubulin, J. Cell Biol. 79: 500–515.PubMedGoogle Scholar
  24. Binder, L. I., Dentier, W. L., and Rosenbaum, J. L., 1975, Assembly of chick brain tubulin onto flagellar axonemes of Chlamydomonas and sea urchin sperm, Proc. Natl. Acad. Sci. USA 72: 1122–1126.PubMedPubMedCentralGoogle Scholar
  25. Bloodgood, R. A., 1974, Resorption of organdies containing microtubules, Cytobios 9: 143–161.Google Scholar
  26. Bonne, D., and Pantoloni, D., 1982, Mechanism of tubulin assembly: Guanosine tripho tehydrolysis decreases the rate of microtubule depolymerization, Biochemistry 21: 1075–1081.PubMedGoogle Scholar
  27. Borisy, G. G., and Olmsted, J. B., 1972, Nucleated assembly of microtubules in porcine brain extracts, Science 177: 1196–1197.Google Scholar
  28. Borisy, G. G., and Taylor, E. W., 1967a, The mechanism of action of colchicine. Binding of colchicine-3-H to cellular protein,./. Cell Biol. 34: 525–533.Google Scholar
  29. Borisy, G. G., and Taylor, E. W., 1967b, The mechanism of action of colchicine. Colchicine binding to sea urchin egg and the mitotic apparatus, J. Cell Biol. 34: 535–548.PubMedPubMedCentralGoogle Scholar
  30. Brown, D. L., and Rogers, K. A., 1978, Hydrostatic pressure-induced internalization of flagellar axonemes, disassembly, and reutilization during flagellar regeneration in Polytomella, Exp. Cell Res. 117: 313–324.PubMedGoogle Scholar
  31. Brown, D. L., Massalski, A., and Patenaude, R., 1976, Organization of the flagellar apparatus and associated cytoplasmic microtubules in the quadriflagellate alga Polytomella agilis, J. Cell Biol. 69: 106–125.PubMedGoogle Scholar
  32. Brunke, K. J., Collis, P. S., and Weeks, D. P., 1982a, Post-translational modification of tubulin dependent on organelle assembly, Nature (London) 297: 516–518.Google Scholar
  33. Brunke, K. J., Young, E. E., Buchbinder, B. U., and Weeks, D. P., 19826, Coordinate regulation of the four tubulin genes of Chlamydomonas reinhardi, Nucleic Acids Res. 71:749–767.Google Scholar
  34. Bryan, J., 1976, A quantitative analysis of microtubule elongation, J. Cell Biol. 10: 1295–1310.Google Scholar
  35. Bryan, J., and Wilson, L., 1971, Are cytoplasmic microtubules heteropolymers? Proc. Natl. Acad. Sci. USA 68: 1762–1766.PubMedPubMedCentralGoogle Scholar
  36. Bucher, P., 1939, Zur kenntnis der mitose. VI. Der einfluss von colchicin und trypaflavin auf den wachstumsrhthmus und auf die zellteilung in fibrocyten-kulturen, Z. Zellforsch. 29: 283–322.Google Scholar
  37. Bulinski, J. C., and Borisy, G. G., 1979, Self-assembly of microtubules in extracts of cultured HeLa cells and the identification of HeLa microtubule-associated proteins, Proc. Natl. Acad. Sci. USA 76: 293–297.PubMedPubMedCentralGoogle Scholar
  38. Burchill, B. R., Oliver, J. M., Pearson, C. B., Leinbach, E. D., and Berlin, R. D., 1978, Microtubule dynamics and glutathione metabolism in phagocytizing human polymorphonuclear leukocytes, J. Cell Biol. 76: 439–447.PubMedPubMedCentralGoogle Scholar
  39. Burns, R. G., and Starling, D., 1974, The in vitro assembly of tubulins from sea-urchin eggs and rat brain: Use of heterologous seeds, J. Cell Sci. 14: 411–419.PubMedGoogle Scholar
  40. Burton, P. R., and Fernandez, H. L., 1973, Delineation by lanthanum staining of filamentous elements associated with the surfaces of axonal microtubules, J. Cell Sci. 12: 567–583.PubMedGoogle Scholar
  41. Burton, P. R., and Himes, R. H., 1978, Electron microscope studies of pH effects on assembly of tubulin free of associated proteins, J. Cell Biol. 77: 120–133.Google Scholar
  42. Burton, B. R., and Hinkley, R. E., 1974, Further electron microscopic characterization of ax-oplasmic microtubules of the ventral cord of the crayfish, J. Submicrosc. Cytol. 6: 311–326.Google Scholar
  43. Burton, P. R., and Paige, J. L., 1981, Polarity of axoplasmic microtubules in the olfactory nerve of the frog, Proc. Natl. Acad. Sci. USA 78: 3269–3273.PubMedPubMedCentralGoogle Scholar
  44. Burton, P. R., Hinkley, R. E., and Pierson, G. B., 1975, Tannic acid-stained microtubules with 12, 13, and 15 protofilaments, J. Cell Biol. 65: 227–233.PubMedPubMedCentralGoogle Scholar
  45. Caplow, M., Langford, G. M., and Zeeberg, B., 1982, Concerning the efficiency of the treadmilling phenomenon with microtubules, J. Biol. Chem. 257: 15012–15021.PubMedGoogle Scholar
  46. Cartier, M. F., 1982, Guanosine-5-triphosphate hydrolysis and tubulin polymerization, Mol. Cell Biochem. 47: 97–113.Google Scholar
  47. Cartier, M. F., 1983, Kinetic evidence for a conformation change of tubulin preceding micro-tubule assembly, J. Biol. Chem. 258: 2315–2420.Google Scholar
  48. Cartier, M. F., and Pantaloni, D., 1978, Kinetic analysis of cooperativity in tubulin polymerization in the presence of guanosine di-or triphosphate nucleotides, Biochemistry 17: 1908–1915.Google Scholar
  49. Cartier, M. F., and Pantaloni, D., 1981, Kinetic analysis of guanosine triphosphate hydrolysis associated with tubulin polymerization, Biochemistry 20: 1918–1924.Google Scholar
  50. Carlier, M. F., and Pantaloni, D., 1982, Assembly of microtubule protein: role of guanosine di-and triphospate nucleotides, Biochem. 21: 1215–1224.Google Scholar
  51. Chalfie, M., and Thomson, J. N., 1982, Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans, J. Cell Biol. 93: 15–23.PubMedGoogle Scholar
  52. Cleveland, D. W., Lopata, M. A., MacDonald, R. J., Cowan, N.J., Rutter, W.J., and Kirschner, M. W., 1980, Number and evolutionary conservation of a and ß tubulin and cytoplasmic ß and y actin genes using specific cloned cDNA probes, Cell 20: 95–105.PubMedGoogle Scholar
  53. Cleveland, D. W., Lopata, M. A., Sherline, P., and Kirschner, M. W., 1981, Unpolymerized tubulin modulates the level of tubulin mRNAs, Cell 25: 537–546.PubMedGoogle Scholar
  54. Connolly, J. A., Kalnins, V. I., Cleveland, D. W., and Kirschner, M. W., 1977, Immunofluorescent staining of cytoplasmic and spindle microtubules in mouse fibroblasts with antibody to tau protein, Proc. Natl. Acad. Sci. USA 74: 2437–2440.PubMedPubMedCentralGoogle Scholar
  55. Connolly, J. A., Kalnins, V. I., Cleveland, D. W., and Kirschner, M. W., 1978, Intracellular localization of the high molecular weight microtubule accessory protein by indirect immunofluorescence, J. Cell Biol. 76: 8781–786.Google Scholar
  56. Cote, R. H., and Borisy, G. G., 1981, Head-to-tail polymerization of microtubules in vitro,/ Mol. Biol. 150: 577–602.Google Scholar
  57. Dales, S., 1972, Concerning the universality of a microtubule antigen in animal cells, J. Cell Biol. 52: 748–754.PubMedPubMedCentralGoogle Scholar
  58. David-Pfeuty, T., Laport, J., and Pantaloni, D., 1978, GTPase activity at ends of microtubules, Nature (London) 272: 282–284.Google Scholar
  59. Davidse, L. C., 1975, Antimitotic activity of methyl benzimidazol-2-ylcarbamate in fungi and its binding to cellular protein, in: Microtubules and Microtubule Inhibitors ( M. Borgers and M. De Brabander), pp. 483–495, ASP Biological and Medical Press, New York.Google Scholar
  60. Deanin, G. G., Preston, S. F., and Gordon, M. W., 1981, Carboxyl terminal tryosine metabolism of alpha tubulin and changes in cell shape: Chinese hamster ovary cells, Biochem. Biophys. Res. Commun. 100: 1642–1650.PubMedGoogle Scholar
  61. De Brabander, M., 1982, A model for the microtubule organizing activity of the centrosomes and kinetochores in mammalian cells, Cell Biol. Int. Rep. 6: 901–915.PubMedGoogle Scholar
  62. De Brabander, M., and De Mey, J. (eds.), 1980, Microtubules and Microtubule Inhibitors, Elsevier/North Holland Biomedical Press, Amsterdam.Google Scholar
  63. De Brabander, M., Geuens, G., Nuydens, R., Willebrords, R., and De Mey, J., 1980, The micro-tubule nucleating and organizing activity of kinetochores and centrosomes in living PTK-2 cells, in: Microtubules and Microtubule Inhibitors ( M. De Brabander and J. De Mey), pp. 255–270, Elsevier/North Holland Biomedical Press, Amsterdam.Google Scholar
  64. Dentier, W. L., Granett, S., Witman, G. B., and Rosenbaum, J. L., 1974, Directionality of brain microtubule assembly in vitro, Proc. Natl. Acad. Sci. USA 71: 1710–1714.Google Scholar
  65. Dentier, 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.Google Scholar
  66. Detrich, H. W., and Williams, R. C., 1978, Reversible dissociation of the aß dimer of tubulin from bovine brain, Biochemistry 17: 3900–3907.PubMedGoogle Scholar
  67. Detrich, H. W., Williams, R. C., and Wilson, L., 1982, Effect of colchicine binding on the reversible dissociation of the tubulin dimer, Biochemistry 21: 2392–2400.PubMedGoogle Scholar
  68. Dustin, P., 1978, Microtubules, Springer-Verlag, Berlin.Google Scholar
  69. Eipper, B. A., 1974a, Rat brain tubulin and protein kinase activity,’ J. Biol. Chem. 249: 1398–1406.PubMedGoogle Scholar
  70. Eipper, B. A., 1974b, Properties of rat brain tubulin, J. Biol. Chem. 249: 1407–1416.PubMedGoogle Scholar
  71. Engelbroghs, Y., and Van Houtte, A., 1981, Temperature jump relaxation study of microtubule elongation in the presence of GTP/GDP mixtures, Biophys. Chem. 14: 195–202.Google Scholar
  72. Erickson, H. P., 1974, Microtubule surface lattice and subunit structure and observations on reassembly, J. Cell Biol. 60: 153–167.PubMedPubMedCentralGoogle Scholar
  73. Erickson, H. P., and Pantaloni, D., 1980, Nucleation of microtubule assembly—a simple model based on thermodynamics, in: Microtubules and Microtubule Inhibitors ( M. De Brabander and J. De Mey), pp. 119–132, Elsevier/North Holland Biomedical Press, Amsterdam.Google Scholar
  74. Erickson, H. P., and Voter, W. A., 1976, Polycation-induced assembly of purified tubulin, Proc. Natl. Acad. Sci. USA 73: 2813–2817.PubMedPubMedCentralGoogle Scholar
  75. Euteneuer, U., and McIntosh, J. R., 1981, Polarity of some motility-related microtubules, Proc. Natl. Acad. Sci. USA 78: 372–376.PubMedPubMedCentralGoogle Scholar
  76. Euteneuer, U., Jackson, W. T., and McIntosh, J. R., 1982, Polarity of spindle microtubules in Haemanthus endosperm, J. Cell Biol. 94: 644–653.PubMedGoogle Scholar
  77. Euteneuer, U., Ris, H., and Borisy, G. G., 1983. Polarity of kinetochore microtubules in Chinese hamster ovary cells after recovery from a colcemid block, J. Cell Biol. 97: 202–208.PubMedGoogle Scholar
  78. Fawcett, D. W., and Porter, K. R., 1954, A study of the fine structure of ciliated epithelia, J.Morphol. 94: 221–228.Google Scholar
  79. Frigon, R. P., and Timasheff, S. H., 1975a, Magnesium-induced self-association of calf brain tubulin. I. Stoichiometry, Biochemistry 14: 4559–4566.PubMedGoogle Scholar
  80. Frigon, R. P., and Timasheff, S. H., 1975b, Magnesium-induced self-association of calf brain tubulin. II. Thermodynamics, Biochemistry 14: 4567–4573.PubMedGoogle Scholar
  81. Frigon, R. P., Valenzuela, M. S., and Timasheff, S. N., 1974, Structure of a magnesium-induced polymer of calf brain microtubule protein, Arch. Biochem. Biophys. 165: 442–443.PubMedGoogle Scholar
  82. Fulton, C., 1977, Cell differentiation in Naegleria gruberi, Annu. Rev. Microbiol. 31: 597–629.PubMedGoogle Scholar
  83. Fulton, C., and Kowit, J. D., 1975, Programmed synthesis of flagellar tubulin during cell differ-entiation in Naegleria, Ann. N. Y. Acad. Sci. 253: 318–332.PubMedGoogle Scholar
  84. Fulton, C., and Simpson, P. A., 1976, Selective synthesis and utilization of flagellar tubulin. The multitubulin hypothesis, in: Cell Motility ( Fulton, C., and Simpson, P. A.), pp. 987–1005, Cold Spring Laboratory.Google Scholar
  85. Fulton, C., Kane, R. E., and Stephens, R. E., 1971, Serological similarity of flagella and mitotic microtubules, J. Cell Biol. 50: 762–773.PubMedPubMedCentralGoogle Scholar
  86. Gall, J. G., 1965, Fine structure of microtubules (Abstr.) J. Cell Biol. 27: 32a.Google Scholar
  87. Gozes, I., and Sweadner, K J, 1981, Multiple brain tubulin forms are expressed by a single neuron, Nature 294: 477–480.PubMedGoogle Scholar
  88. Grigg, G. W., and Hodge, A. J., 1949, Electron microscopic studies of spermatozoa. I. The morphology of the spermatozoan of the common domestic fowl (Gallas domesticus), Austr. J. Sci. Res. Ser. B. Biol. Sci. 2: 271–286.Google Scholar
  89. Grimstone, A. V., and Klug, A., 1966, Observations on the substructure of flagellar fibers, J. Cell Sci. 1: 351–362.Google Scholar
  90. Guttman, S. D., and Gorovsky, M. A., 1979, Cilia regeneration in starved Tetrahymena: An inducible system for studying gene expression and organelle biosynthesis, Cell 17: 307–317.PubMedGoogle Scholar
  91. Haimo, L. T., and Telzer, B. R., 1981, Dynein-microtubule interactions: ATP-sensitive dynein binding and the structural polarity of mitotic microtubules, Cold Spring Harbor Symp. Quant. Biol. 46: 207–217.Google Scholar
  92. Haimo, L. T., Telzer, B. R., and Rosenbaum, J. L., 1979, Dynein binds to and crossbridges cytoplasmic microtubules, Proc. Natl. Acad. Sci. USA 76: 5759–5763.PubMedPubMedCentralGoogle Scholar
  93. Hallack, M. E., Rodriguez, J. A., Barra, H. S., and Caputto, R., 1977, Release of tyrosine from tyrosinated tubulin. Some common factors that affect this process and the assembly of tubulin, FEBS Lett. 73: 147–150.Google Scholar
  94. Hamel, E., del Campo, A. A., and Lin, C. M., 1983, Microtubule assembly with the guanosine 5’-diphosphate analogue 2’,3’-dideoxyguanosine 5’-diphosphate, Biochem. 22: 3664–3671.Google Scholar
  95. Harris, P., 1962, Some structural and functional aspects of the mitotic apparatus in sea urchin embryos, J. Cell Biol. 14: 475–488.PubMedPubMedCentralGoogle Scholar
  96. Heidemann, S. R., and McIntosh, J. R., 1980, Visualization of the structural polarity of micro-tubules, Nature (London) 286: 517–519.Google Scholar
  97. Heidemann, S. R., Zieve, G. G., and McIntosh, J. R., 1980, Evidence for microtubule addition to the distal end of mitotic structures in vitro, J. Cell Biol. 87: 152–159.PubMedGoogle Scholar
  98. Herzog, W., and Weber, K., 1977, In vitro assembly of pure tubulin into microtubules in the absence of microtubule-associated proteins and glycerol, Proc. Natl. Acad. Sci. USA 74: 1860–1864.Google Scholar
  99. Herzog, W., and Weber, K., 1978, Microtubule formation by pure brain tubulin in vitro: The influence of dextran and poly(ethylene glycol), Eur. J. Biochem. 91: 249–254.PubMedGoogle Scholar
  100. Heuser, J. E., and Kirschner, M. W., 1980, Filament organization revealed in platinum replicas of freeze-dried cytoskeletons, J. Cell Biol. 86: 212–234.PubMedGoogle Scholar
  101. Himes, R. H., Kersey, R. N., Ruscha, M., and Houston, L. L., 1976, Cytochalasin A inhibits the in vitro polymerization of brain tubulin and muscle actin, Biochem. Biophys. Res. Commun. 68: 1362–1370.PubMedGoogle Scholar
  102. Himes, R. H., Burton, P. R., and Gaito, J. M., 1977, Dimethyl sulfoxide-induced self-assembly of tubulin lacking associated proteins, J. Biol. Chem. 252: 6222–6228.PubMedGoogle Scholar
  103. Hyams, J. S., and Borisy, G. G., 1978, Nucleation of microtubules in vitro by isolated spindle pole bodies of the yeast Saccharomyces cerevisiae, J. Cell Biol. 78: 401–414.PubMedGoogle Scholar
  104. Inoue, S., 1952, The effect of colchicine on the microscopic and submicroscopic structure of the mitotic spindle, Exp. Cell Res. Suppl. 2: 305–318.Google Scholar
  105. Ishikawa, H., Bischoff, R., and Holtzer, H., 1969, The formation of arrowhead complexes with heavy meromyosin in a variety of cell types, J. Cell Biol. 43: 312–328.PubMedPubMedCentralGoogle Scholar
  106. Jacobs, M., 1975, Tubulin nucleotide reactions and their role in microtubule assembly and dissociation, Ann. N.Y. Acad. Sci. 253: 562–572.PubMedGoogle Scholar
  107. Jacobs, M., 1979, Tubulin and nucleotides, in: Microtubules ( K. Roberts and J. S. Hyams), pp. 255–277, Academic Press, London.Google Scholar
  108. Jacobs, M., and Huitorel, P., 1979, Tubulin-associated nucleoside diphosphokinase, Eur. J. Biochem. 99: 613–622.PubMedGoogle Scholar
  109. Jacobs, M., Smith, H., and Taylor, E. W., 1974, Tubulin-nucleotide binding and enzymic activity, J. Mol. Biol. 89: 455–468.PubMedGoogle Scholar
  110. Jakus, M. A., and Hall, C. E., 1946, Electron microscope observations of the trichocysts and cilia of Paramecium, Biol. Bull. (Woods Hole) 91: 141–144.Google Scholar
  111. Jameson, L., and Caplow, M., 1981, Modification of microtubule steady-state dynamics by phosphorylation of the microtubule-associated proteins, Proc. Natl. Acad. Sci. USA 78: 3413–3417.PubMedPubMedCentralGoogle Scholar
  112. Jameson, L., Frey, T., Zeeberg, B., Dalldorf, F., and Caplow, M., 1980, Inhibition of microtubule assembly by phosphorylation of microtubule-associated proteins, Biochemistry 19: 2472–2479.PubMedGoogle Scholar
  113. Job, D., Rauch, C. T., Fischer, E. H., and Margolis, R. L., 1982, Recycling of cold-stable micro-tubules: Evidence that cold stability is due to substoichiometric polymer blocks, Biochemistry 21: 509–515.PubMedGoogle Scholar
  114. Johnson, K. A., and Borisy, G. G., 1977, Kinetic analysis of microtubule self-assembly in vitro, J. Mol. Biol. 117: 1–31.PubMedGoogle Scholar
  115. Jolly, J., 1920, Hematies des tylopodes, C. R. Soc. Biol. 93: 125–127.Google Scholar
  116. Jolly, J., 1923, Traite Technique Hematologie, Maloine et Fils, Paris.Google Scholar
  117. Joseph, M. K., Fernstrom, M. A., and Soloff, M. S., 1982, Switching of ß-to a-tubulin phosphorylation in uterine smooth muscle of parturient rats, J. Biol. Chem. 257: 11728–11733.PubMedGoogle Scholar
  118. Kakuichi, S., and Sobue, K., 1981, Cat+- and calmodulin-dependent flip-flop mechanism in microtubule assembly-disassembly, FEBS Lett. 132: 141–143.Google Scholar
  119. Kalfayan, L., and Wensink, P. C., 1982, Developmental regulation of Drosophila a-tubulin genes, Cell 29: 91–98.PubMedGoogle Scholar
  120. Kalfayan, L., Lowenberg, J., and Wensick, P. C., 1981, Drosophila a-tubulin genes and their transcription patterns, Cold Spring Harbor Symp. Quant. Biol. 46: 183–190.Google Scholar
  121. Karr, T. L., Prodrasky, A. E., and Purich, D. L., 1979, Participation of guanine nucleotides in nucleation and elongation steps of microtubule assembly, Proc. Natl. Acad. Sci. USA 76: 5475–5479.PubMedPubMedCentralGoogle Scholar
  122. Kemphues, K. J., Raff, R. A., Kaufman, T. C., and Raff, E. C, 1979, Mutation in a structural gene for a beta-tubulin specific to testis in Drosophila melanogaster, Proc. Natl. Acad. Sci. USA 76: 3991–3995.PubMedPubMedCentralGoogle Scholar
  123. Kemphues, K. J., Raff, E. C., Raff, R. A., and Kaufman, T. C., 1980, Mutation in a testis-specific beta-tubulin in Drosophila: Analysis of its effects on meiosis and map location, Cell 21: 445–451.PubMedGoogle Scholar
  124. Kemphues, K. J., Kaufman, T. C., Raff, R. A., and Raff, E. C., 1982. The testis-specific 6-tubulin in Drosophila melanogaster has multiple functions in spermatogenesis, Cell 31: 655–670.PubMedGoogle Scholar
  125. Kim, H., Binder, L. I., and Rosenbaum, J. L., 1979, The periodic association of MAP2 with brain microtubules in vitro, J. Cell Biol. 80: 266–276.PubMedGoogle Scholar
  126. Kirkpatrick, J. B., Hyams, L., Thomas, V. L., and Howley, P. M., 1970, Purification of intact microtubules from brain, J. Cell Biol. 47: 389–394.Google Scholar
  127. Kirschner, M. W., 1980, Implication of treadmilling for the stability and polarity of actin and tubulin polymers in vivo, J. Cell Biol. 86: 330–334.PubMedGoogle Scholar
  128. Kirschner, M. W., Honig, L. S., and Williams, R. C., 1975, Quantitative electron microscopy of microtubule assembly in vitro, J . Mol. Biol. 99: 263–276.PubMedGoogle Scholar
  129. Kobayashi, Y., 1982. Stable microtubules in starfish sperm flagellum: their structure and heterogeneity of tubulin, J. Biochem. (Tokyo) 92: 1305–1318.Google Scholar
  130. Kobayashi, T., and Flavin, M., 1978, Tubulin-tyrosine ligase: Do invertebrates have it? J. Cell Biol. (Abstr.) 79: 285a.Google Scholar
  131. Kowit, J. D., and Fulton, C., 1974a, Programmed synthesis of tubulin for the flagella that develop during cell differentiation in Naugleria gruberi, Proc. Natl. Acad. Sci. USA 71: 2877–2881.PubMedPubMedCentralGoogle Scholar
  132. Kowit, J. D., and Fulton, C., 1974b, Purification and properties of flagellar outer doublet tubulin from Naegleria gruberi and a radioimmune assay for tubulin, J. Biol. Chem. 249: 3638–3646.PubMedGoogle Scholar
  133. Krauhs, E., Little, M., Kempf, T., Hofer-Warbinek, R., Ade, W., and Pontingl, H., 1981, Com-plete amino acid sequence of (3-tubulin from porcine brain, Proc. Natl. Acad. Sci. USA 78: 4156–4160.PubMedPubMedCentralGoogle Scholar
  134. Kumar, N., and Flavin, M., 1981, Preferential action of a brain detyrosinolating carboxypeptidase on polymerized tubulin, J. Biol. Chem. 256: 7678–7686.PubMedGoogle Scholar
  135. Kuriyama, R., 1976, In vitro polymerization of flagellar and ciliary outer fiber tubulin into micro-tubules, J. Biochem. (Tokyo) 80: 153–165.Google Scholar
  136. Kuriyama, R., and Sakai, H., 1974, Role of tubulin -SH groups in polymerization to microtubules. Functional -SH groups in tubulin for polymerization, J. Biochem. (Tokyo) 76: 651–654.Google Scholar
  137. Lai, E. Y., Walsh, C., Wardell, D., and Fulton, C., 1979, Programmed appearance of translatable flagellar tubulin mRNA during cell differentiation in Naegleria, Cell 17: 867–878.PubMedGoogle Scholar
  138. Langford, G. E., 1980, Arrangement of subunits in microtubules with 14 protofilaments, J. Cell Biol. 87: 521–526.Google Scholar
  139. Ledbetter, M. C., and Porter, K. R., 1963, A microtubule in plant fine structure, J. Cell Biol. 19: 239–250.PubMedPubMedCentralGoogle Scholar
  140. Ledbetter, M. C., and Porter, K. R., 1964, The morphology of microtubules of plant cells, Science 144: 872–874.PubMedGoogle Scholar
  141. Lee, M. G.-S., Lewis, S. A., Wilde, C. D., and Cowan, N. J., 1983, Evolutionary history of a multigene family: an expressed human fl-tubulin gene and three processed pseudogenes, Cell 33: 477–487.PubMedGoogle Scholar
  142. Lee, S.-H., Kristofferson, D., and Purich, D. L., 1982, Microtubule interactions with GDP provide evidence that assembly-disassembly properties depend on the method of brain microtubulle protein isolation, Biochem. Biophys. Res. Commun. 105: 1605–1610.PubMedGoogle Scholar
  143. Lee, Y. C., and Wolff, J., 1982, Two opposing effects of calmodulin on microtubule assembly depend on the presence of microtubule-associated proteins, J . Biol. Chem. 257: 6306–6310.PubMedGoogle Scholar
  144. Lefebvre, P. A., Nordstrom, S. A., Moulder, J. E., and Rosenbaum, J. L., 1978, Flagellar elongation and shortening in Chlamydomonas. IV. Effects of flagellar detachment, regeneration, and resorption on the induction of flagellar protein synthesis, J. Cell Biol. 78: 8–27.PubMedGoogle Scholar
  145. Lefebvre, P. A., Silflow, C. D., Wieben, E. D., and Rosenbaum, J. L., 1980, Increased levels of mRNAs for tubulin and other flagellar proteins after amputation or shortening of Chlamyodomonas flagella, Cell 20: 469–477.PubMedGoogle Scholar
  146. Hernault, S. W., and Rosenbaum, J. L., 1983, Chlamydomonas a-tubulin is posttranslationally modified in the flagella during flagellar assembly, J. Cell Biol. 97: 258–263.PubMedGoogle Scholar
  147. Linck, R. W., and Amos, L. A., 1974, The hands of helical lattices in flagellar doublet micro-tubules, J. Cell Sci. 14: 551–559.PubMedGoogle Scholar
  148. Linck, R. W., and Langevin, G. L., 1981, Reassembly of flagellar B (aß) tubulin into singlet microtubules. Consequences for cytoplasmic microtubule structure and assembly, J. Cell Biol. 89: 323–337.Google Scholar
  149. Lockwood, A. H., 1978, Tubulin assembly protein: Immunochemicai and irnmunofluorescent studies on its function and distribution in microtubules and cultured cells, Cell 13: 613–628.PubMedGoogle Scholar
  150. Lockwood, A., Penningroth, S. M., and Kirschner, M. W., 1975, Function of GTP in microtubule formation, Fed. Proc. (Abstr.) 34: 540.Google Scholar
  151. Ludford, R. J., 1936, The action of toxic substances upon the division of normal and malignant cells in vitro and in vivo, Arch. Exp. Zellforsch. 18: 411–441.Google Scholar
  152. Luduena, R. F., Shooter, E. M., and Wilson, L., 1977, Structure of the tubulin dimer, J. Biol. Chem. 252: 7006–7114.PubMedGoogle Scholar
  153. Maccioni, R. B., and Seeds, N. W., 1982, Residual nucleotide and tubulin’s ability to polymerize with nucleotide analogues, J. Biol. Chem. 257: 3334–3338.PubMedGoogle Scholar
  154. Maki, R., Roeder, W., Traunecker, A., Sidman, C., Wabl, M., Raschke, W., and Tonegawa, S., 1981, The role of DNA rearrangement and alternative RNA processing in the expression of immunoglobulin delta genes, Cell 24: 353–365.PubMedGoogle Scholar
  155. Mandelkow, E.-M., and Mandelkow, E., 1979, Junctions between microtubule walls, J. Mol. Biol. 129: 135–148.PubMedGoogle Scholar
  156. Mandelkow, E., Mandelkow, E.-M., and Bordas, J., 1983, Structure of tubulin rings studied by x-ray scattering using synchrotron radiation, J. Mol. Biol. 167: 179–196.PubMedGoogle Scholar
  157. Mandelkow, E., Thomas, J., and Cohen, C., 1977, Microtubule structure at low resolution by x-ray diffraction, Proc. Natl. Acad. Sci. USA 74: 3370–3374.PubMedPubMedCentralGoogle Scholar
  158. Manton, I., and Clarke, B., 1952, An electron microscope study of spermatozoid of Sphagnum, J. Exp. Bot. 3: 265–275.Google Scholar
  159. Marcaud, L., and Hayes, D., 1979, RNA synthesis in starved deciliated Tetrahymena pyriformis, Eur. J. Biochem. 98: 267–273.Google Scholar
  160. Marcum, J. M., and Borisy, G. G., 1978, Characterization of microtubule protein oligomers by analytical ultracentrifugation, J. Biol. Chem. 253: 2825–2833.PubMedGoogle Scholar
  161. Marcum, J. M., Dedman, J. R., Brinkley, B. R., and Means, A. R., 1978, Control of microtubule assembly-disassembly by calcium-dependent regulator protein, Proc. Natl. Acad. Sci. USA 75: 3771–3775.PubMedPubMedCentralGoogle Scholar
  162. Margolis, R. L., 1981, Role of GTP hydrolysis in microtubule treadmilling and assembly, Proc. Natl. Acad. Sci. USA 78: 1586–1590.PubMedPubMedCentralGoogle Scholar
  163. Margolis, R. L., and Wilson, L., 1978, Opposite end assembly and disassembly of microtubules at steady state in vitro, Cell 13: 1–8.PubMedGoogle Scholar
  164. Margolis, R. L., and Wilson, L., 1979, Regulation of the microtubule steady state in vitro by ATP, Cell 18: 673–679.PubMedGoogle Scholar
  165. Marie, J., Simon, M.-P., Dreyfus, J.-C., and Kahn, A., 1981, One gene, but two messenger RNAs encode liver L and red cell pyruvate kinase subunits, Nature (London) 292: 70–72.Google Scholar
  166. Matus, A., Bernhardt, R., and Hugh-Jones, T., 1981, High-molecular weight microtubule-associ-ated proteins are preferentially associated with dendritic microtubules in brain, Proc. Natl. Acad. Sci. USA 78: 3010–3014.PubMedPubMedCentralGoogle Scholar
  167. McEwen, B., and Edelstein, S. J., 1980, Evidence for a mixed lattice in microtubules reassembled in vitro, J. Mol. Biol. 139: 123–145.Google Scholar
  168. McGill, M., and Brinkley, B. R., 1975, Human chromosomes and centrioles as nucleating sites for the in vitro assembly of microtubules from bovine brain tubulin, J. Cell Biol. 67: 189–199.PubMedGoogle Scholar
  169. McKeithan, T. W., and Rosenbaum, J. L., 1981, Multiple forms of tubulin in the cytoskeletal and flagellar microtubules of Polytomella, J. Cell Biol. 91: 352–360.PubMedPubMedCentralGoogle Scholar
  170. McKeithan, T. W., Lefebvre, P. A., Silflow, C. D., and Rosenbaum, J. L., 1979, Posttranslational modification of flagellar tubulin, J. Cell Biol. (Abstr.) 83: 338a.Google Scholar
  171. McKeithan, T., W., Lefebvre, P. A., Silflow, C. D., and Rosenbaum, J. L., 1983, Tubulin heterogeneity in Polytomella and Chlamydomonas. Evidence for a precursor of flagellar alpha tubulin, J. Cell Biol., 96: 1056–1063PubMedPubMedCentralGoogle Scholar
  172. Mellon, M., and Rebhun, L. I., 1976, Sulfhydryls and in vitro polymerization of tubulin, J. Cell Biol. 70: 226–238.PubMedGoogle Scholar
  173. Merlino, G. T., Chamberlin, J. P., and Kleinsmith, L. J., 1978, Effects of deciliation on tubulin messenger RNA activity in sea urchin embryos, J. Biol. Chem. 253: 7078–7085.PubMedGoogle Scholar
  174. Moore, K. W., Roger, J., Hunkapiller, T., Early, P., Nottemburg, C., Weissman, I., Bazin, H., Wall, R., and Hood, L. E., 1981, Expression of IgD may use both DNA rearrangement and RNA splicing mechanisms, Proc. Natl. Acad. Sci. USA 78: 1800–1804.PubMedPubMedCentralGoogle Scholar
  175. Morris, N. R., Lai, M. H., and Oakley, C. E., 1979, Identification of a gene for a-tubulin in Aspergillus nidulans, Cell 16: 437–442.Google Scholar
  176. Murphy, D. B., and Borisy, G. G., 1975, Association of high molecular weight proteins with microtubules and their role in microtubule assembly in vitro, Proc. Natl. Acad. Sci. USA 72: 2696–2700.PubMedPubMedCentralGoogle Scholar
  177. Murphy, D. B., Johnson, K. A., and Borisy, G. G., 1977, Role of tubulin-associated proteins in microtubule nucleation and elongation, J. Mol. Biol. 117: 33–52.PubMedGoogle Scholar
  178. Nagano, T., and Suzuki, F., 1975, Microtubules with 15 subunits in cockroach epidermal cells, J. Cell Biol. 64: 242–245.PubMedPubMedCentralGoogle Scholar
  179. Nath, J., and Flavin, M., 1978, A structural difference between cytoplasmic and membrane-bound tubulin of brain, FEBS Lett. 95: 335–338.PubMedGoogle Scholar
  180. 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 syndromes, J. Cell Biol. 95: 519–526.PubMedGoogle Scholar
  181. Nath, J., Whitlock, J., and Flavin, M., 1978, Tyrosylation of tubulin in synchronized HeLa cells, J. Cell Biol. (Abstr.) 79: 294a.Google Scholar
  182. Nishida, E., and Sakai, H., 1977, Calcium-sensitivity of the microtubule reassembly system. Difference between crude brain extract and purified microtubule proteins, J. Biochem. (Tokyo) 82: 303–306.Google Scholar
  183. Oakley, B. R., and Morris, N. R., 1981, A beta-tubulin mutation in Aspergillus nidulans that blocks microtubule function without blocking assembly, Cell 24: 837–845.PubMedGoogle Scholar
  184. Oliver, J. M., Albertini, D. F., and Berlin, R. D., 1976, Effects of glutathione-oxidizing agents on microtubule assembly and microtubule-dependent surface properties of human neutrophils, J. Cell Biol. 71: 921–932.PubMedGoogle Scholar
  185. Olmsted, J. B., and Borisy, G. G., 1975, Ionic and nucleotide requirements for microtubule polymerization in vitro, Biochemistry 14: 2996–3005.PubMedGoogle Scholar
  186. Olmsted, J. B., Carlson, K., Klebe, R., Ruddle, F., and Rosenbaum, J., 1970, Isolation of micro-tubule protein from cultured mouse neuroblastoma cells, Proc. Natl. Acad. Sci. USA 65: 129–136.PubMedPubMedCentralGoogle Scholar
  187. Olmsted, J. B., Marcum, J. M., Johnson, K. A., Allen, C., and Borisy, G. G. 1974, Microtubule assembly: Some possible regulatory mechanisms, J. Supramol. Struct. 2: 429–450.PubMedGoogle Scholar
  188. Oosawa, F., and Asakura, S., 1975, Thermodynamics of the Polymerization of Protein Academic Press, London.Google Scholar
  189. Pantaloni, D., Carlier, M.-F., Simon, C., and Batelier, G., 1981, Mechanism of tubulin assembly: Role of rings in the nucleation process and of associated proteins in the stabilization of microtubules, Biochemistry 20: 3709–4716.Google Scholar
  190. Papaconstantinou, E., and Pantaloni, D., 1982, Mechanism of tubulin assembly: Evidence for GTP hydrolysis on microtubule precursors, Biol. Cell (Abstr.) 45: 257.Google Scholar
  191. Pease, D. C., 1963, The ultrastructure of flagellar fibrils, J. Cell Biol. 18: 313–326.PubMedPubMedCentralGoogle Scholar
  192. Penningroth, S. M., Cleveland, D. W., Kirschner, M. W., 1976, In vitro studies of the regulation of microtubule assembly, in: Cell Motilit (R. Goldman, T. Pollard, J. Rosenbaum Houtte), pp. 1233–1258, Cold Spring Harbor Laboratory.Google Scholar
  193. Pepper, D. A., and Brinkley, B. R., 1979, Microtubule initiation at kinetochores and centrosomes in lysed mitotic cells, J. Cell Biol. 82: 585–591.PubMedGoogle Scholar
  194. Perlman, D., and Halvorson, H. 0., 1981, Distinct repressible mRNAs for cytoplasmic and secreted yeast invertase are encoded by a single gene, Cell 25: 526–536.Google Scholar
  195. Pernice, B., 1889, Sulla cariocinesi delle cellule epiteliali e dellendotelio dei vasi della mucosa dello stomaco e dellintestino, nelle studio della gastroenterite sperimentale (nellavvelenamento per colchico), Sicilia Med. 1: 265–279.Google Scholar
  196. Pickett-Heaps, J. D., 1969, The evolution of the mitotic apparatus: An attempt at comparative ultrastructural cytology in dividing plant cells, Cytobios 1: 257–280.Google Scholar
  197. Pierson, G. B., Burton, P. R., and Himes, R. H., 1978, Alterations in number of protofilaments in microtubules assembled in vitro, J. Cell Biol. 76: 223–228.PubMedGoogle Scholar
  198. Piperno, G., and Luck, D. J., 1976, Phosphorylation of axonemal proteins in Chlamydomonas reinhardtii, J. Biol. Chem. 251: 2161–2167.PubMedGoogle Scholar
  199. Piperno, G., and Luck, D. J., 1977, Microtubule proteins of Chlamydomonas reinhardtii. An immunochemical study based on the use of an antibody specific for the 3-tubulin subunit, J. Biol. Chem. 252: 383–391.PubMedGoogle Scholar
  200. Piras, R., and Piras, M. M., 1975, Changes in microtubule phosphorylation during cell cycle of HeLa cells, Proc. Natl. Acad. Sci. USA 72: 1161–1165.PubMedPubMedCentralGoogle Scholar
  201. Ponstingl, H., Krauhs, E., Little, M., and Kempf, T., 1981, Complete amino acid sequence of atubulin from porcine brain, Proc. Natl. Acad. Sci. USA 78: 2757–2761.PubMedPubMedCentralGoogle Scholar
  202. Purich, D. L., Terry, B. J., MacNeal, R. K., and Karr, T. L., 1982, Characterization of tubulin and microtubule-associated protein interactions with guanine nucleotides and their non-hydrolyzable analogues, Methods Enzym. 85: 416–433.Google Scholar
  203. Ranvier, L., 1875, Recherches sur les elements du sang, Arch. Physiol. 2: 1–15.Google Scholar
  204. Raybin, D., and Flavin, M., 1975, An enzyme tyrosylating a-tubulin and its role in microtubule assembly, Biochem. Biophys. Res. Commun. 65: 1088–1095.PubMedGoogle Scholar
  205. Raybin, D., and Flavin, M., 1977, Modification of tubulin by tyrosylation in cells and extracts and its effect on assembly in vitro, J. Cell Biol. 73: 492–504.PubMedGoogle Scholar
  206. Rebhun, L. I., Miller, M., Schnaitman, T. C., Nath, J., and Mellon, M., 1976, Cyclic nucleotides, thioldisulfide status of proteins, and cellular control processes, J. Supramol. Struct. 5: 199–219.PubMedGoogle Scholar
  207. Rebhun, L. I., Jemiolo, D., Keller, T., Burgess, W., and Kretsinger, R., 1980, Calcium, calmodulin, and control of assembly of brain and spindle microtubules, in: Microtubules and Micro-tubule Inhibitors ( M. De Brabander and J. De Mey), pp. 243–252, Elsevier/North Holland Biomedical Press, Amsterdam.Google Scholar
  208. Roberts, K., and Hyams, J. S. (eds.), 1979, Microtubules, Academic Press, London.Google Scholar
  209. Rodnan, G. P., and Benedek, T. G., 1970, The early history of antirheumatic drugs, Arth. Rheum. 13: 145–165.Google Scholar
  210. Rodriguez, J. A., and Borisy, G. G., 1977, Developmental studies on the tyrosination of chick brain tubulin, J. Cell Biol. (Abstr.) 75: 296a.Google Scholar
  211. Rogers, J., Early, P., Carter, C., Calame, K., Bond, M., Hood, L., and Wall, R., 1980, Two mRNAs with different 3’ ends encode membrane-bound and secreted forms of immunoglobulin µ chain, Cell 20: 303–312.PubMedGoogle Scholar
  212. Rosenbaum, J. L., and Child, F. M., 1967, Flagellar regeneration in protozoan flagellates, J. Cell Biol. 34: 345–364.PubMedPubMedCentralGoogle Scholar
  213. Roth, L. E., and Daniels, E. W., 1962, Electron microscope studies of mitosis in amebae. II. The giant ameba Pelomyxa carolinensis, J. Cell Biol. 12: 57–78.PubMedPubMedCentralGoogle Scholar
  214. Sabatini, D. D., Bensch, K., and Barrnett, R. J., 1963, Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation, J. Cell Biol. 17: 19–58.PubMedPubMedCentralGoogle Scholar
  215. Safer, D., 1973, Comparison of ciliary and flagellar microtubule subunits, J. Cell Biol. (Abstr.) 59: 299a.Google Scholar
  216. Sakai, H., Mohri, H., and Borisy, G. G., 1982, Biological Functions of Microtubules and Related Structures, Academic Press, Tokyo.Google Scholar
  217. Sandoval, I. V., and Weber, K., 1981, Different tubulin polymers are produced by microtubuleassociated proteins MAP2 and tau in the presence of guanosine (a,(3 methylene)triphosphate, J. Biol. Chem. 255: 8952–8954.Google Scholar
  218. Sandoval, I. V., MacDonald, E., Jameson, L. J., and Cuatrecasas, P., 1977, Role of nucleotide in tubulin polymerization: Effect of guanylyl methylenediphosphonate, Proc. Natl. Acad. Sci. USA 74: 4881–4885.PubMedPubMedCentralGoogle Scholar
  219. Sandoval, I. V., Jameson, J. L., Niedel, J., MacDonald, E., and Cuatrecasas, P., 1978, Role of nucleotides in tubulin polymerization. Effect of guanosine methylene diphosphonate, Proc. Natl. Acad. Sci. USA 75: 3178–3182.PubMedPubMedCentralGoogle Scholar
  220. Schliwa, M., 1980, Pharmacological evidence for an involvement of calmodulin in calcium-induced microtubule disassembly in lysed tissue culture cells, in: Microtubules and Microtubule Inhibitors ( M. De Brabander and J. De Mey), pp. 57–70, Elsevier/North Holland Biomedical Press, Amsterdam.Google Scholar
  221. Schliwa, M., Euteneuer, U., Bulinski, J. C., and Izant, J. G., 1981, Calcium lability of cytoplasmic microtubules and its modulation by microtubule-associated proteins, Proc. Natl. Acad. Sci. USA 78: 1037–1041.PubMedPubMedCentralGoogle Scholar
  222. Schmitt, F. O., Hall, C. E., and Jakus, M. A., 1943, The ultrastructure of protoplasmic fibrils, Biol. Symp. 10: 261–276.Google Scholar
  223. Sheele, R. B., and Borisy, G. G., 1979, In vitro assembly of microtubules, in: Microtubules ( K. Roberts and J. S. Hyams), pp. 175–254, Academic Press, London.Google Scholar
  224. Sheele, R. B., Bergen, L. G., and Borisy, G. G., 1982, Control of the structural fidelity of microtubules by initiation sites, J. Mol. Biol. 154: 485–500.Google Scholar
  225. Sheir-Neiss, G., Lai, M. H., and Morris, N. R., 1978, Identification of a gene for l3-tubulin in Aspergillus nidulans, Cell 15: 638–647.Google Scholar
  226. Shelanski, M. L., and Taylor, E. W., 1967, Isolation of a protein subunit from microtubules, j. Cell Biol. 34: 549–554.PubMedPubMedCentralGoogle Scholar
  227. Shelanski, M. L., and Taylor, E. W., 1968, Properties of the protein subunit of central pair and outer-doublet microtubules of sea urchin flagella, J. Cell Biol. 38: 304–315.PubMedPubMedCentralGoogle Scholar
  228. Shriver, K., and Byers, B., 1977, Yeast microtubules: Constituent proteins and their synthesis, J. Cell Biol. (Abstr.) 75: 297a.Google Scholar
  229. Silflow, C. D., and Rosenbaum, J. L., 1981, Multiple alpha-and beta-tubulin genes in Chlamyodomonas and regulation of tubulin mRNA levels after deflagellation, Cell 24: 81–88.PubMedGoogle Scholar
  230. Silflow, C. D., Lefebvre, P. A., McKeithan, T. W., Schloss, J. A., Keller, L. R., and Rosenbaum, J. L., 1981, Expression of flagellar protein genes during flagellar regeneration in Chlamydomonas, Cold Spring Harbor Symp. Quant. Biol. 45: 157–169.Google Scholar
  231. Slautterback, D. B., 1961, A fine tubular component of secretory cells, Am. Soc. Cell Biol. (Abstr.) 199.Google Scholar
  232. Slautterback, D. B., 1963, Cytoplasmic microtubules. I. Hydra, J. Cell Biol. 18:367–388. Sloboda, R. D., and Rosenbaum, J. L., 1977, Decoration of intact, smooth-walled microtubules with microtubule-associated proteins, J. Cell Biol. (Abstr.) 76: 286a.Google Scholar
  233. Sloboda, R. D., Dentier, W. L., Bloodgood, R. A., Telzer, B., Granett, S., and Rosenbaum, J. L., 1976, Microtubule-associated proteins (MAPs) and the assembly of microtubules in vitro, in: Cell Motility ( R. Goldman, T. Pollard, and J. Rosenbaum), pp. 987–1005, Cold Spring Harbor Laboratory, New York.Google Scholar
  234. Sloboda, R. D., Rudolph, S. A., Rosenbaum, J. L., and Greengard, P., 1975, Cyclic AMP-dependent endogenous phosphorylation of a microtubule-associated protein, Proc. Natl. Acad. Sci. USA 72: 177–181.PubMedPubMedCentralGoogle Scholar
  235. Smith, D. S., 1971, On the significance of cross-bridges between microtubules and synaptic vesicles, Phil Trans. R. Soc. Ser. B. Biol. Sci. 261: 395.Google Scholar
  236. Snell, W. J., Dentier, W. L., Haimo, L. T., Binder, L. I., and Rosenbaum, J. L., 1974, Assembly of chick brain tubulin onto isolated basal bodies of Chlamydomonas reinhardii, Science 185: 357–360.PubMedGoogle Scholar
  237. Sobue, K., Fujita, M., Muramoto, Y., and Kakuichi, S., 1981, The calmodulin-binding protein in microtubules is tau factor, FEBS Lett. 132: 137–143.PubMedGoogle Scholar
  238. Solomon, F., Gyson, R., Rentsch, M., and Monard, D., 1976, Purification of tubulin from neuroblastoma cells: Absence of covalently bound phosphate in tubulin from normal and morphologically differentiated cells, FEBS Lett. 63: 316–319.PubMedGoogle Scholar
  239. Stearns, M. E., and Brown, D. L., 1979, Purification of cytoplasmic tubulin and microtubule organizing center proteins functioning in microtubule initiation from the alga Polytomella, Proc. Natl. Acad. Sci. USA 76: 5745–5749.PubMedPubMedCentralGoogle Scholar
  240. Stearns, M. E., and Brown, D. L., 1981, Microtubule organizing centers (MTOCs) of the alga Polytomella exert spatial control over microtubule initiation in vivo and in vitro, J. Ultrastruct. Res. 77: 366–378.PubMedGoogle Scholar
  241. Stearns, M. E., Connolly, J. A., and Brown, D. L., 1976, Cytoplasmic microtubule organizing centers isolated from Polytomella agilis, Science 191: 188–191.PubMedGoogle Scholar
  242. Stephens, R. E., 1970, Thermal fractionation of outer doublet microtubules into A- and Btubulin, J. Mol. Biol. 47: 353–363.PubMedGoogle Scholar
  243. Stephens, R. E., 1975, Structural chemistry of the axoneme: Evidence for chemically and functionally unique tubulin dimers in outer fibers, in: Molecules and Cell Movement ( S. Inoue and R. E. Stephens), Raven Press, New York.Google Scholar
  244. Stephens, R. E., 1977, Differential protein synthesis and utilization during cilia formation in sea urchin embryos, Dev. Biol. 61: 311–329.PubMedGoogle Scholar
  245. Stephens, R. E., 1978, Primary structural differences among tubulin subunits from flagella, cilia, and the cytoplasm, Biochemistry 14: 2882–2891.Google Scholar
  246. Stephens, R. E., 1982, Equimolar heterodimers in microtubules, J. Cell Biol. 94: 263–270.PubMedGoogle Scholar
  247. Summers, K., and Kirschner, M. W., 1979, Characteristics of the polar assembly and disassembly of microtubules observed in vitro by dark-field light microscopy, J. Cell Biol. 83: 205–217.PubMedGoogle Scholar
  248. Taylor, E. W., 1965, The mechanism of colchicine inhibition of mitosis. I. Kinetics of inhibition and the binding of 3H-colchicine, J. Cell Biol. 25: 145–160.PubMedPubMedCentralGoogle Scholar
  249. Telzer, B. R., and Haimo, L. T., 1981, Decoration of spindle microtubules with dynein: Evidence for uniform polarity, J. Cell Biol. 89: 373–378.PubMedGoogle Scholar
  250. Telzer, B. R., Moses, M. J., and Rosenbaum, J. L., 1975, Assembly of microtubules onto kinetochores of isolated mitotic chromosomes of HeLa cells, Proc. Natl. Acad. Sci. USA 72: 4023–4027.PubMedPubMedCentralGoogle Scholar
  251. Thomashow, L. S., Milhausen, M., Rutter, W. J., and Agabian, N., 1983. Tubulin genes are tandemly linked and clustered in the genome of Trypanosoma brucei, Cell 32: 35–43.PubMedGoogle Scholar
  252. Thompson, W. C., Deanin, G. G., and Gordon, M. W., 1979, Intact microtubules are required for rapid turnover of carboxyl-terminal tyrosine of a-tubulin in cell cultures, Proc. Natl. Acad. Sci. USA 76: 1318–1322.PubMedPubMedCentralGoogle Scholar
  253. Tilney, L. G., 1971, Origin and continuity of microtubules, in: Origin and Continuity of Cell Organelles U. Reinert and H. Ursprung Houtte), pp. 222–260, Springer, Berlin.Google Scholar
  254. Tilney, L. G., Bryan, J., Bush, D. J., Fugiwara, K., Mooseker, M. S., Murphy, D. B., and Snyder, D. H., 1973, Microtubules: Evidence for 13 protofilaments, J. Cell Biol. 59: 267–275.PubMedPubMedCentralGoogle Scholar
  255. Tucker, J. B., Dunn, M., and Pattesson, J. B., 1975, Control of microtubule pattern during the development of a large organelle in the ciliate Nassula, Dev. Biol. 47: 439–453.PubMedGoogle Scholar
  256. 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 a and (3 tubulin mRNAs, Nature (London) 289: 650–655.Google Scholar
  257. Vallee, R., and Borisy, G. G., 1977, Removal of the projections from cytoplasmic microtubules in vitro by digestion with trypsin, J. Biol. Chem. 252: 377–382.PubMedGoogle Scholar
  258. Water, R. D., and Kleinsmith, L. J., 1976, Identification of a and ß tubulin in yeast, Biochem. Biophys. Res. Commun. 70: 704–708.PubMedGoogle Scholar
  259. Weatherbee, J. A., Sherline, P., Mascardo, R. N., Izart, J. G., Luftig, R. B., and Weihing, R. R., 1982, Microtubule-associated proteins of HeLa cells: Heat stability of the 200,000 mol wt HeLa MAPs and detection of the presence of MAP2 in HeLa cell extracts and cycled micro-tubules, J. Cell Biol. 92: 155–163.Google Scholar
  260. Weeks, D. P., and Collis, P. S., 1976, Induction of microtubule protein synthesis in Chlamydomonas reinhardii during flagellar regeneration, Cell 9: 15–27.PubMedGoogle Scholar
  261. Wegener, A., 1976, Head to tail polymerization of actin, J. Mol. Biol. 108: 139–150.Google Scholar
  262. 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.PubMedPubMedCentralGoogle Scholar
  263. Weisenberg, R. C., 1972, Microtubule formation in vitro in solutions containing low calcium concentration, Science 177: 1104–1105.PubMedGoogle Scholar
  264. Weisenberg, R. C., 1974, The role of ring aggregates and other structures in the assembly of microtubules, J. Supramol. Struct. 2: 451–465.PubMedGoogle Scholar
  265. Weisenberg, R. C., 1980a, A microtubule assembly model, in: Microtubules and Microtubule Inhibitors ( M. De Brabander and J. De Mey), pp. 161–172, Elsevier/North Holland Biomedical Press, Amsterdam.Google Scholar
  266. Weisenberg, R. C., 19806, Role of co-operative interactions, microtubule-associated proteins and guanosine triphosphate in microtubule assembly: A model, J. Mol. Biol. 139: 660–667.Google Scholar
  267. Weisenberg, R. C., Borisy, G. G., and Taylor, E. W., 1968, The colchicine binding protein of mammalian brain and its relationship to microtubules, Biochemistry 7: 4466–4479.PubMedGoogle Scholar
  268. Weisenberg, R. C., Deery, W. J., and Dickenson, P. J., 1976, Tubulin-nucleotide interaction during the polymerization and depolymerization of microtubules, Biochemistry 15: 4248–4254.PubMedGoogle Scholar
  269. Wilde, C. D., Crowther, C. E., Cripe, T. P., Lee, M. G.-S., and Cowan, N. J., 1982, Evidence that a human 13-tubulin gene is derived from its corresponding mRNA, Nature 292: 83–84.Google Scholar
  270. Witman, G. B., 1975, The site of in vivo assembly of flagellar microtubules, Ann. N.Y. Acad. Sci. 253: 178–191.PubMedGoogle Scholar
  271. Witt, P. L., Ris, H., and Borisy, G. G., 1980, Origin of kinetochore microtubules in Chinese hamster ovary cells, Chromosoma (Berlin) 81: 483–505.Google Scholar
  272. Wuerker, R. B., and Kirkpatrick, J. B., 1972, Neuronal microtubules, neurofilaments, and micro-filaments, Int. Rev. Cytol. 33: 45–75.PubMedGoogle Scholar
  273. Wuerker, R. B., and Palay, S. L., 1969, Neurofilaments and microtubules in anterior horn cells of the rat, Tissue Cell 1: 387–402.PubMedGoogle Scholar
  274. Yamada, K. M., Spooner, B. S., and Wessells, N. K., 1971, Ultrastructure and function of growth cones and axons of cultured nerve cells, J. Cell Biol. 49: 614–635.PubMedPubMedCentralGoogle Scholar
  275. Zabrecky, J. R., and Cole, R. D., 1982a, Binding of ATP to tubulin, Nature 296: 775–776.PubMedGoogle Scholar
  276. Zabrecky, J. R., and Cole, R. D., 1982b, Effect of ATP on the kinetics of microtubule assembly, J. Biol. Chem. 257: 4633–4638.PubMedGoogle Scholar
  277. Zackroff, V., and Weisenberg, R. C., 1978, Microtubule assembly competence of GDP-tubulin, J. Supramol. Struct. (Abstr.) 7: 327.Google Scholar
  278. Zackroff, R. V., Weisenberg, R. C., and Deery, W. J., 1980, Equilibrium and kinetic analysis of microtubule assembly in the presence of guanosine diphosphate, J. Mol. Biol. 139: 641–677.PubMedGoogle Scholar
  279. Zeeberg, B., and Caplow, M., 1981, An isoenergetic exchange mechanism which accounts for tubulin-GDP stabilization of microtubules, J. Biol. Chem. 256: 12051–12057.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Timothy W. McKeithan
    • 1
  • Joel L. Rosenbaum
    • 1
  1. 1.Department of BiologyYale UniversityNew HavenUSA

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