Advertisement

Molecular Neurobiology

, Volume 6, Issue 2–3, pp 137–155 | Cite as

Molecular motors in axonal transport

Cellular and molecular biology of kinesin
  • Janet L. Cyr
  • Scott T. Brady
Article

Abstract

Neurons require a large amount of intracellular transport. Cytoplasmic polypeptides and membrane-bounded organelles move from the perikaryon, down the length of the axon, and to the synaptic terminals. This movement occurs at distinct rates and is termed axonal transport. Axonal transport is divided into the slow transport of cytoplasmic proteins including glycolytic enzymes and cytoskeletal structures and the fast transport of membrane-bounded organelles along linear arrays of microtubules. The polypeptide compositions of the rate classes of axonal transport have been well characterized, but the underlying molecular mechanisms of this movement are less clear. Progress has been particularly slow toward understanding force-generation in slow transport, but recent developments have provided insight into the molecular motors involved in fast axonal transport. Recent advances in the cellular and molecular biology of one fast axonal transport motor, kinesin, have provided a clearer understanding of organelle movement along microtubules. The availability of cellular and molecular probes for kinesin and other putative axonal transport motors have led to a reevaluation of our understanding of intracellular motility.

Index Entries

Axonal transport molecular motors kinesin cytoplasmic dynein membrane-bounded organelles microtubules organelle transport 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen R. D., Allen N. S., and Travis J. L. (1981) Video-enhanced contrast, differential interference contrast (AVEC-DIC) microscopy: A new method capable of analyzing microtubule-related motility in the reticulopodial network ofAllogromia laticollaris, Cell Motility 1, 291–302.PubMedCrossRefGoogle Scholar
  2. Allen R. D., Weiss D. G., Hayden, J. H., Brown D. T., Fujiwake H., and Simpson M. (1985) Gliding movement of and bidirectional transport along single native microtubules from squid axoplasm: evidence for an active role of microtubules in cytoplasmic transport.J. Cell Biol. 100, 1736–1752.PubMedCrossRefGoogle Scholar
  3. Bamburg J. R., Bray D., and Chapman K. (1986) Assembly of microtubules at the tip of growing axons.Nature 321, 778–790.CrossRefGoogle Scholar
  4. Black M. M. and Lasek R. J. (1979) Axonal transport of actin: Slow Component b is the principal source of actin for the axon.Brain Res. 171, 401–413.PubMedCrossRefGoogle Scholar
  5. Black M. M. and Lasek R. J. (1980) Slow components of axonal transport: two cytoskeletal networks.J. Cell Biol. 86, 616–623.PubMedCrossRefGoogle Scholar
  6. Bloom G. S. (1992) Motor proteins for cytoplasmic microtubules.Curr. Opinion in Cell Biology 4, 1–8.CrossRefGoogle Scholar
  7. Bloom G. S., Wagner M. C., Pfister K. K., and Brady S. T. (1988) Native structure and physical properties of bovine brain kinesin and identification of the ATP-binding subunit polypeptide.Biochemistry 27, 3409–3416.PubMedCrossRefGoogle Scholar
  8. Bloom G. S., Wagner M. C., Pfister K. K., Leopold P. L., and Brady S. T. (1989) Involvement of microtubules and kinesin in the fast axonal transport of membrane-bounded organelles, inDynein and Microtubules Dynamics, Warner F. D. and McIntosh J. R., eds., Alan R. Liss, New York, pp. 321–333.Google Scholar
  9. Brady S. T. (1985a) A novel brain ATPase with properties expected for fast axonal transport.Nature 317, 73–75.PubMedCrossRefGoogle Scholar
  10. Brady S. T. (1985b) Axonal transport methods and applications, inGeneral Neurochemical Techniques, Boulton A.A. and Baker G. B., eds., Humana, Totowa, NJ, pp. 419–476.Google Scholar
  11. Brady S. T. (1988) Cytotypic specializations of the neuronal cytoskeleton and cytomatrix: Implications for neuronal growth and regeneration, inCellular and Molecular Aspects of Neural Development and Regeneration, Haber B., Gorio A., de Vellis J., and Perez-Polo, J. R., eds., Springer-Verlag, New York, pp. 311–322.Google Scholar
  12. Brady S. T. (1991) Molecular motors in the nervous system.Neuron 7, 1–20.CrossRefGoogle Scholar
  13. Brady S. T. (1992) Axonal dynamics and regeneration, inNeural Regeneration, Gorio A., eds., Raven, New York, in press.Google Scholar
  14. Brady S. T. and Lasek R. J. (1981) Nerve-specific enolase and creatine phosphokinase in axonal transport: soluble proteins and the axoplasmic matrix.Cell 23, 515–523.PubMedCrossRefGoogle Scholar
  15. Brady S. T. and Lasek R. J. (1982a) Axonal transport: a cell-biological method for studying proteins that associate with the cytoskeleton.Methods Cell Biol. 25, 365–398.PubMedCrossRefGoogle Scholar
  16. Brady S. T. and Lasek R. J. (1982b) The slow components of axonal transport: movements, compositions and organization, inAxoplasmic Transport, Weiss D. G., ed., Springer-Verlag, Berlin, pp. 206–213.Google Scholar
  17. Brady S. T., Lasek R. J., and Allen R. D. (1982) Fast axonal transport in extruded axoplasm from squid giant axon.Science 218, 1129–1131.PubMedCrossRefGoogle Scholar
  18. Brady S. T., Lasek R. J., and Allen R. D. (1985) Video microscopy of fast axonal transport in extruded axoplasm: a new model for study of molecular mechanisms.Cell Motility 5, 81–101.PubMedCrossRefGoogle Scholar
  19. Brady S. T., Lasek R. J., Allen R. D., Yin H. L., and Stossel T. P. (1984) Gelsolin inhibition of fast axonal transport indicates a requirement for actin microfilaments.Nature 310, 56–58.PubMedCrossRefGoogle Scholar
  20. Brady S. T., Tytell M., Heriot K., and Lasek R. J. (1981) Axonal transport of calmodulin: a physiological approach to identification of long-term associations between proteins.J. Cell Biol. 89, 607–614.PubMedCrossRefGoogle Scholar
  21. Breuer A. C., Allen R. D., and Lewis R. J. (1981) Rapid transport in neurites of “submicroscopic” structures: analysis by the new AVEC-DIC microscopy method.Neurology 31, 118a.Google Scholar
  22. Burdwood W. O. (1964) Rapid particle movement in neurons.J. Cell Biol. 27, 115a.Google Scholar
  23. Buster D., Lohka M., and Scholey J. M. (1990) Phosphorylation of sea urchin kinesin.J. Cell Biol. 111, 418a.Google Scholar
  24. Chen M. S., Obar R. B., Schroeder C. C., Austin T. W., Poodry C. A., Wadsworth S. C., and Vallee R. B. (1991) Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis.Nature 351, 583–586.PubMedCrossRefGoogle Scholar
  25. Cleveland D. W. and Hoffman P. N. (1991) Slow axonal transport models come full circle: Evidence that microtubule sliding mediates axonal elongation and tubulin transport.Cell 67, 453–456.PubMedCrossRefGoogle Scholar
  26. Cohn S. A., Inglod A. L., and Choley J. M. (1987) Correlation between the ATPase and microtubule translocating activities of sea urchin kinesin.Nature 328, 160–163.PubMedCrossRefGoogle Scholar
  27. Cohn S. A., Ingold A. L., and Scholey J. M. (1989) Quantitative analysis of sea urchin egg kinesin-driven microtubule motility.J. Biol. Chem. 264, 4290–4297.PubMedGoogle Scholar
  28. Cyr J. L., Pfister K. K., Bloom G. S., Slaughter C. A., and Brady S. T. (1991) Molecular genetics of kinesin light chains: generation of multiple isoforms by alternative splicing.Proc. Natl. Acad. Sci. USA 88, 10,114–10,118.CrossRefGoogle Scholar
  29. Douglas M. G., McCammon M. T., and Vassarotti A. (1986) Targeting proteins into mitochondria.Microbiological Reviews 50, 166–178.PubMedGoogle Scholar
  30. Elluru R. G., Pfister K. K., Bloom G. S., and Brady S. T. (1991) Phosphorylation of kinesin in the rat optic nerve/tract.J. Cell Biol. 115, 389a.Google Scholar
  31. Erickson P. F. and Moore B. W. (1980) Investigation of the axonal transport of three acid soluble proteins (14-3-2, 14-3-3, and S-100) in the rabbit visual system.J. Neurochem. 35, 232–241.PubMedCrossRefGoogle Scholar
  32. Garner J. A. and Lasek R. J. (1981) Clathrin is axonally transported as part of slow component b: the microfilament complex.J. Cell Biol. 88, 172–178.PubMedCrossRefGoogle Scholar
  33. Garner J. A. and Lasek R. J. (1982) Cohesive axonal transport of the slow component b complex of polypeptides.J. Neurosci. 2, 1824–1835.PubMedGoogle Scholar
  34. Gibbons L. R., Gibbons B. H., Mocz G., and Asai D. J. (1991) Multiple nucleotide binding sites in the sequence of dynein β heavy chain.Nature 352, 640–642.PubMedCrossRefGoogle Scholar
  35. Gilbert D. L., Adelman W. J., and Arnold J. M. eds. (1990)Squid as Experimental Animals. Plenum, New York.Google Scholar
  36. Gilbert S. P. and Sloboda R. D. (1986) Identification of a MAP2-like ATP-binding protein associated with axoplasmic vesicles that translocates on isolated microtubules.J. Cell Biol. 103, 947–956.PubMedCrossRefGoogle Scholar
  37. Grafstein B. and Forman D. S. (1980) Intracellular transport in neurons.Physiol. Rev. 60, 1167–1283.PubMedGoogle Scholar
  38. Hammerschlag R. and Brady S. T. (1989) Axonal transport and the neuronal cytoskeleton, inBasic Neurochemistry: Molecular, Cellular, and Medical Aspects, Siegel G. J., eds., Raven, New York, pp. 457–477.Google Scholar
  39. Hammerschlag R. and Stone G. C. (1982) Membrane delivery by fast axonal transport.Trends Neurosci. 5, 12–15.CrossRefGoogle Scholar
  40. Hayden J. H. and Allen R. D. (1984) Detection of single microtubules in living cells: particle transport can occur in both directions along the same microtubule.J. Cell Biol. 99, 1785–1793.PubMedCrossRefGoogle Scholar
  41. Hiller W. K. (1989) A glossary of laboratory techniques used in kinesin research and a discussion of the role of technical understanding in creating illustrations. M. S. thesis. University of Texas Southwestern Medical Center, Dallas, TX.Google Scholar
  42. Hirokawa N. (1982) The crosslinker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by quick-freeze, freeze fracture, deep-etching method.J. Cell Biol. 94, 129–142.PubMedCrossRefGoogle Scholar
  43. Hirokawa N., Pfister K. K., Yorifuji H., Wagner M. C., Brady S. T., and Bloom G. S. (1989) Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration.Cell 56, 867–878.PubMedCrossRefGoogle Scholar
  44. Hoffman P. N. and Lasek R. J. (1975) The slow component of axonal transport.J. Cell Biol. 66, 351–366.PubMedCrossRefGoogle Scholar
  45. Hollenbeck P. J. (1991) Kinesin heavy & light chains are phosphorylated in vivo in neurons.J. Cell Biol. 115, 390a.Google Scholar
  46. Holzbaur E. L. F., Hammarback J. A., Paschal B. M., Kravit N. G., Pfister K. K., and Vallee R. B. (1991) Homology of a 150K Cytoplasmic Dynein-associated Polypeptide with theDrosophila GeneGlued.Nature 351, 579–583.PubMedCrossRefGoogle Scholar
  47. Howard J., Hudspeth A. J., and Vale R. D. (1989) Movement of microtubules by single kinesin molecules.Nature 342, 154–158.PubMedCrossRefGoogle Scholar
  48. Karlsson J.-O. and Sjostrand J. (1971) Transport of microtubule protein in axons of retinal ganglion cells.J. Neurochem. 18, 2209–2216.PubMedCrossRefGoogle Scholar
  49. Keith C. H. (1987) Slow transport of tubulin in the neurites of differentiated PC12 cells.Science 235, 337–339.PubMedCrossRefGoogle Scholar
  50. Kosik K. S., Orecchio L. D., Schnapp B., Inouye H., and Neve R. L. (1990) The primary structure and analysis of the squid kinesin heavy chain.J. Biol. Chem. 265, 3278–3283.PubMedGoogle Scholar
  51. Kuczmarski E. R. and Rosenbaum J. L. (1979) Chick brain actin and myosin isolation and characterization.J. Cell Biol. 80, 341–355.PubMedCrossRefGoogle Scholar
  52. Kuznetsov S. A. and Gelfand V. I. (1986) Bovine brain kinesin is a microtubule-activated ATPase.Proc Natl. Acad. Sci. USA 83, 8530–8534.PubMedCrossRefGoogle Scholar
  53. Kuznetsov S. A., Vaisberg E. A., Rothwell S. W., Murphy D. B., and Gelfand V. I. (1989) Isolation of a 45-kDa fragment from the kinesin heavy chain with enhanced ATPase and microtubule-binding activities.J. Biol. Chem. 264, 589–595.PubMedGoogle Scholar
  54. Kuznetsov S. A., Vaisberg E. A., Shanina N. A., Magretova N. N., Chernyak V. Y., and Gelfand V. I. (1988) The quaternary structure of bovine brain kinesin.EMBO J. 7, 353–356.PubMedGoogle Scholar
  55. Lasek R. J. and Brady S. T. (1982) The structural hypothesis of axonal transport: two classes of moving elements, inAxoplasmic Transport, Weiss D. G., ed., Springer-Verlag, Berlin, pp. 397–405.Google Scholar
  56. Lasek R. J. and Brady S. T. (1985) Attachment of transported vesicles to microtubules in axoplasm is facilitated by AMP-PNP.Nature 316, 645–647.PubMedCrossRefGoogle Scholar
  57. Leopold P. L., McDowall A. W., Pfister K. K., Bloom G. S., and Brady S. T. (1992) Association of kinesin with characterized membrane-bounded organelles.Cell Motility Cytoske. in press.Google Scholar
  58. Levine J. and Willard M. (1981) Fodrin: axonally transported polypeptides associated with the internal periphery of many cells.J. Cell Biol. 90, 631–643.PubMedCrossRefGoogle Scholar
  59. McQuarrie I., Brady S., and Lasek R. (1980) Polypeptide composition and kinetics of SCa and SCb in sciatic nerve motor axons and optic axons of rat, in Soc.Neurosci. Abstr., p. 501.Google Scholar
  60. Miller R. H. and Lasek R. J. (1985) Cross-bridges mediate anterograde and retrograde vesicle transport along microtubules in squid axoplasm.J. Cell Biol. 101, 2181–2193.PubMedCrossRefGoogle Scholar
  61. Morris J. and Lasek R. J. (1982) Stable polymers of the axonal cytoskeleton: the axoplasmic ghost.J. Cell Biol. 92, 192–198.PubMedCrossRefGoogle Scholar
  62. Murofushi H., Ikai A., Okuhara K., Kotani S., Aizawa H., Kumakura K., and Sakai H. (1988) Purification and characterization of kinesin from bovine adrenal medulla.J. Biol. Chem. 263, 12,744–12,750.Google Scholar
  63. Murphy D. B., McNiven M. A., Wallis K. T., Kutznetsov S. A., and Gelfand V. I. (1989) The phosphorylation of kinesin does not affect its ATPase and translocating activities.J. Cell Biol. 109, 80a.CrossRefGoogle Scholar
  64. Nixon R. A. and Logvinenko K. B. (1986) Multiple fates of newly synthesized neurofilaments: Evidence for a stationary neurofilament network distributed nonuniformly along axons of retinal ganglion cells.J. Cell Biol. 102, 647–659.PubMedCrossRefGoogle Scholar
  65. Obar R. A., Collins C. A., Hammerback J. A., Shpetner H. S., and Vallee R. B. (1990) Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins.Nature 347, 256–261.PubMedCrossRefGoogle Scholar
  66. Oblinger M., Brady S., and McQuarrie I. (1982) Comparative compositional analysis of slowly transported axonal proteins in peripheral and central mammalian neurons.Soc. Neurosci. Abstr., p. 826.Google Scholar
  67. Ogawa K. (1991) Four ATP-binding sites in the midregion of the β heavy chain of dynein.Nature 352, 643–645.PubMedCrossRefGoogle Scholar
  68. O'Shea E. K., Klemm J. D., Kim P. S., and Abler T. (1991) X-ray structure of the GNC4 leucine zipper, a two-stranded, parallel coiled coil.Science 254, 539–544.PubMedCrossRefGoogle Scholar
  69. Paschal B. M. and Vallee R. B. (1987) Retrograde transport by the microtubule-associated protein MAP 1C.Nature 330, 181–183.PubMedCrossRefGoogle Scholar
  70. Penningroth S. M., Rose P. M., and Peterson D. D. (1987) Evidence that the 116kDa component of kinesin binds and hydrolyzes ATP.FEBS Lett. 222, 204–210.PubMedCrossRefGoogle Scholar
  71. Pfister K. K., Wagner M. C., Stenoien D. L., Brady S. T., and Bloom G. S. (1989) Monoclonal antibodies to kinesin heavy and light chains stain vesicle-like structures, but not microtubules, in cultured cells.J. Cell Biol. 108, 1453–1463.PubMedCrossRefGoogle Scholar
  72. Porter M. E., Scholey J. M., Stemple D. L., Vigers G. P. A., Vale R. D., Sheetz M. P., and McIntosh J. R. (1987) Characterization of the microtubule movement produced by sea urchin egg kinesin.J. Biol. Chem. 262, 2794–2802.PubMedGoogle Scholar
  73. Reinsch S. S., Mitchinson T. J., and Kirschner M. (1991) Microtubule polymer assembly and transport during axonal elongation.J. Cell Biol. 115, 365–379.PubMedCrossRefGoogle Scholar
  74. Sabry J. H., O'Connor T. P., Evans L., Toroian-Raymond A., Kirschner M., and Bentley D. (1991) Microtubule behavior during guidance of pioneer neuron growth cones in situ.J. Cell Biol. 115, 381–395.PubMedCrossRefGoogle Scholar
  75. Saxton W. M., Porter M. E., Cohn S. A., Scholey J. M., Raff E. C., and McIntosh J. R. (1988)Drosophila kinesin: characterization of microtubule motility and ATPase.Proc. Natl. Acad. Sci. USA 85, 1109–1113.PubMedCrossRefGoogle Scholar
  76. Schliwa M. (1984) Mechanisms of intracellular organelle transport.Cell Muscle Motil. 5, 1–81.PubMedCrossRefGoogle Scholar
  77. Schnapp B. J. and Reese T. M. (1989) Dynein is the motor for retrograde axonal transport of organelles.Proc Natl. Acad. Sci. USA 86, 1548–1552.PubMedCrossRefGoogle Scholar
  78. Schnapp B. J., Vale R. D., Sheetz M. P., and Reese T. S. (1985) Single microtubules from squid axoplasm support bidirectional movement of organelles.Cell 40, 455–462.PubMedCrossRefGoogle Scholar
  79. Scholey J. M., Heuser J., Yang J. T., and Goldstein L. S. B. (1989) Identification of globular mechanochemical heads of kinesin.Nature 338, 355–357.PubMedCrossRefGoogle Scholar
  80. Schroer T. A., Steuer E. R., and Sheetz M. P. (1989) Cytoplasmic dynein is a minus end-directed motor for membranous organelles.Cell 56, 937–946.PubMedCrossRefGoogle Scholar
  81. Shpetner H. S. and Vallee R. B. (1989) Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules.Cell 59, 421–432.PubMedCrossRefGoogle Scholar
  82. Shpetner H. S., Paschal B. M., and Vallee R. B. (1988) Characterization of the microtubule-activated ATPase of brain cytoplasmic dynein (MAP 1C).J. Cell Biol. 107, 1001–1009.PubMedCrossRefGoogle Scholar
  83. Smith R. S. and Kendal W. S. (1984) The recovery of organelle transport and microtubule integrity in myelinated axons that are frozen and thawed.Can. J. Physiol. Pharmacol. 63, 292–297.Google Scholar
  84. Tanaka E. and Kirschner M. (1991) Microtubule behavior in the growth cones of living neurons during axonal elongation.J. Cell Biol. 115, 345–363.PubMedCrossRefGoogle Scholar
  85. Tytell M., Black M. M., Garner J. A., and Lasek R. J. (1981) Axonal transport: each major rate component reflects the movement of distinct macromolecular complexes.Science 214, 179–181.PubMedCrossRefGoogle Scholar
  86. Tytell M., Brady S. T., and Lasek R. (1984) Axonal transport of a subclass of τ proteins: evidence for the regional differentiation of microtubules in neurons.Proc Natl. Acad. Sci. USA 77, 3042–3046.CrossRefGoogle Scholar
  87. Vale R. D., Reese T. S., and Sheetz M. P. (1985a) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility.Cell 42, 39–50.PubMedCrossRefGoogle Scholar
  88. Vale R. D., Schnapp B. J., Mitchison T., Steuer E., Reese T. S., and Sheetz M. P. (1985b) Different axoplasmic proteins generate movement in opposite direction along microtubules in vivo.Cell 43, 623–632.PubMedCrossRefGoogle Scholar
  89. Vallee R. B. and Bloom G. S. (1991) Mechanisms of fast and slow axonal transport.Ann. Rev. Neurosci. 14, 59–92.PubMedCrossRefGoogle Scholar
  90. Vallee R. B., Sheptner H. S., and Paschal B. M. (1989) The role of dynein in retrograde transport.Trends Neurosci. 12, 66–70.PubMedCrossRefGoogle Scholar
  91. van der Bliek A. M. and Meyerowitz E. M. (1991) Dynamin-like protein encoded by the Drosophilashibire gene associated with vesicular traffic.Nature 351, 411–414.PubMedCrossRefGoogle Scholar
  92. Wagner M. C., Pfister K. K., Bloom G. S., and Brady S. T. (1989) Copurification of kinesin polypeptides with microtubule-stimulated Mg-ATPase activity and kinetic analysis of enzymatic properties.Cell Motil. Cytoskel. 12, 195–215.CrossRefGoogle Scholar
  93. Weisenberg R. C., Flynn J., Gao B. C., and Awodi S. (1988) Microtubule gelation-contraction in vitro and its relationship to component a of slow axonal transport.Cell Motil. Cytoskel. 10, 331–340.CrossRefGoogle Scholar
  94. Willard M. (1977) The identification of two intraaxonally transported polypeptides resembling myosin in some respects in the rabbit visual system.J. Cell Biol. 75, 1–11.PubMedCrossRefGoogle Scholar
  95. Willard M., Cowan W. M., and Vagelos P. R. (1974) The polypeptide composition of intraaxonally transported proteins: evidence for four transport velocities.Proc Natl. Acad. Sci. USA 71, 2183–2187.PubMedCrossRefGoogle Scholar
  96. Willard M., Wiseman M., Levine J., and Skene P. (1979) Axonal transport of actin in rabbit retinal ganglion cells.J. Cell Biol. 81, 581–591.PubMedCrossRefGoogle Scholar
  97. Wright B. D., Henson J. H., Wedaman K. P., Willy P. J., Morand J. N., and Scholey J. M. (1991) Subcellular localization and sequence of sea urchin kinesin heavy chain: evidence for its association with membranes in the mitotic apparatus and interphase cytoplasm.J. Cell Biol. 113, 817–833.PubMedCrossRefGoogle Scholar
  98. Yang J. T., Laymon R. A., and Goldstein L. S. B. (1989) A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses.Cell 56, 879–889.PubMedCrossRefGoogle Scholar
  99. Yang J. T., Saxton W. M., and Goldstein L. S. B. (1988) Isolation and characterization of the gene encoding the heavy chain ofDrosophila kinesin.Proc. Natl. Acad. Sci. USA 85, 1864–1868.PubMedCrossRefGoogle Scholar
  100. Yang J. T., Saxton W. M., Stewart R. J., Raff E. C., and Goldstein L. S. B. (1990) Evidence that the head of kinesin is sufficient for force generation and motility in vitro.Science 249, 42–47.PubMedCrossRefGoogle Scholar
  101. Yeh E., Driscoll R., Coletrera M., Olins A., and Bloom K. (1991) A dynamin-like protein encoded by yeast sporulation gene SPO15.Nature 349, 713–715.PubMedCrossRefGoogle Scholar

Copyright information

© The Humana Press, Inc 1992

Authors and Affiliations

  • Janet L. Cyr
    • 1
  • Scott T. Brady
    • 1
  1. 1.Department of Cell Biology and NeuroscienceUniversity of Texas Southwestern Medical CenterDallas

Personalised recommendations