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. 1994 Aug 1;126(3):661–675. doi: 10.1083/jcb.126.3.661

Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells

PMCID: PMC2120148  PMID: 8045931

Abstract

Microtubules (MT) are required for the efficient transport of membranes from the trans-Golgi and for transcytosis of vesicles from the basolateral membrane to the apical cytoplasm in polarized epithelia. MTs in these cells are primarily oriented with their plus ends basally near the Golgi and their minus-ends in the apical cytoplasm. Here we report that isolated Golgi and Golgi-enriched membranes from intestinal epithelial cells possess the actin based motor myosin-I, the MT minus- end-directed motor cytoplasmic dynein and its in vitro motility activator dynactin (p150/Glued). The Golgi can be separated into stacks, possessing features of the Golgi cisternae, and small membranes enriched in the trans-Golgi network marker TGN 38/41. Whereas myosin-I is present on all membranes in the Golgi fraction, dynein is present only on the small membrane fraction. Dynein, like myosin-I, is associated with membranes as a cytoplasmic peripheral membrane protein. Dynein and myosin-I coassociate with membranes that bind to MTs and cross-link actin filaments and MTs in a nucleotide-dependent manner. We propose that cytoplasmic dynein moves Golgi membranes along MTs to the cell cortex where myosin-I provides local delivery through the actin- rich cytoskeleton to the apical membrane.

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Selected References

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  1. Achler C., Filmer D., Merte C., Drenckhahn D. Role of microtubules in polarized delivery of apical membrane proteins to the brush border of the intestinal epithelium. J Cell Biol. 1989 Jul;109(1):179–189. doi: 10.1083/jcb.109.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allan V. J., Kreis T. E. A microtubule-binding protein associated with membranes of the Golgi apparatus. J Cell Biol. 1986 Dec;103(6 Pt 1):2229–2239. doi: 10.1083/jcb.103.6.2229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aniento F., Emans N., Griffiths G., Gruenberg J. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J Cell Biol. 1993 Dec;123(6 Pt 1):1373–1387. doi: 10.1083/jcb.123.6.1373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aoki D., Appert H. E., Johnson D., Wong S. S., Fukuda M. N. Analysis of the substrate binding sites of human galactosyltransferase by protein engineering. EMBO J. 1990 Oct;9(10):3171–3178. doi: 10.1002/j.1460-2075.1990.tb07515.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bacallao R., Antony C., Dotti C., Karsenti E., Stelzer E. H., Simons K. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J Cell Biol. 1989 Dec;109(6 Pt 1):2817–2832. doi: 10.1083/jcb.109.6.2817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bearer E. L., DeGiorgis J. A., Bodner R. A., Kao A. W., Reese T. S. Evidence for myosin motors on organelles in squid axoplasm. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11252–11256. doi: 10.1073/pnas.90.23.11252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bennett G., Carlet E., Wild G., Parsons S. Influence of colchicine and vinblastine on the intracellular migration of secretory and membrane glycoproteins: III. Inhibition of intracellular migration of membrane glycoproteins in rat intestinal columnar cells and hepatocytes as visualized by light and electron-microscope radioautography after 3H-fucose injection. Am J Anat. 1984 Aug;170(4):545–566. doi: 10.1002/aja.1001700404. [DOI] [PubMed] [Google Scholar]
  8. Bloom G. S., Brashear T. A. A novel 58-kDa protein associates with the Golgi apparatus and microtubules. J Biol Chem. 1989 Sep 25;264(27):16083–16092. [PubMed] [Google Scholar]
  9. Bloom G. S. Motor proteins for cytoplasmic microtubules. Curr Opin Cell Biol. 1992 Feb;4(1):66–73. doi: 10.1016/0955-0674(92)90060-p. [DOI] [PubMed] [Google Scholar]
  10. Bomsel M., Parton R., Kuznetsov S. A., Schroer T. A., Gruenberg J. Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell. 1990 Aug 24;62(4):719–731. doi: 10.1016/0092-8674(90)90117-w. [DOI] [PubMed] [Google Scholar]
  11. Breitfeld P. P., McKinnon W. C., Mostov K. E. Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells. J Cell Biol. 1990 Dec;111(6 Pt 1):2365–2373. doi: 10.1083/jcb.111.6.2365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Burgess D. R., Prum B. E. Reevaluation of brush border motility: calcium induces core filament solution and microvillar vesiculation. J Cell Biol. 1982 Jul;94(1):97–107. doi: 10.1083/jcb.94.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cheney R. E., Mooseker M. S. Unconventional myosins. Curr Opin Cell Biol. 1992 Feb;4(1):27–35. doi: 10.1016/0955-0674(92)90055-h. [DOI] [PubMed] [Google Scholar]
  14. Coffe G., Raymond M. N. Association between microtubules and Golgi vesicles isolated from rat parotid glands. Biol Cell. 1990;70(3):143–152. doi: 10.1016/0248-4900(90)90371-9. [DOI] [PubMed] [Google Scholar]
  15. Collins K., Sellers J. R., Matsudaira P. Calmodulin dissociation regulates brush border myosin I (110-kD-calmodulin) mechanochemical activity in vitro. J Cell Biol. 1990 Apr;110(4):1137–1147. doi: 10.1083/jcb.110.4.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Conzelman K. A., Mooseker M. S. The 110-kD protein-calmodulin complex of the intestinal microvillus is an actin-activated MgATPase. J Cell Biol. 1987 Jul;105(1):313–324. doi: 10.1083/jcb.105.1.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Cooper M. S., Cornell-Bell A. H., Chernjavsky A., Dani J. W., Smith S. J. Tubulovesicular processes emerge from trans-Golgi cisternae, extend along microtubules, and interlink adjacent trans-golgi elements into a reticulum. Cell. 1990 Apr 6;61(1):135–145. doi: 10.1016/0092-8674(90)90221-y. [DOI] [PubMed] [Google Scholar]
  18. Corthésy-Theulaz I., Pauloin A., Pfeffer S. R. Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J Cell Biol. 1992 Sep;118(6):1333–1345. doi: 10.1083/jcb.118.6.1333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Drenckhahn D., Dermietzel R. Organization of the actin filament cytoskeleton in the intestinal brush border: a quantitative and qualitative immunoelectron microscope study. J Cell Biol. 1988 Sep;107(3):1037–1048. doi: 10.1083/jcb.107.3.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Euteneuer U., Koonce M. P., Pfister K. K., Schliwa M. An ATPase with properties expected for the organelle motor of the giant amoeba, Reticulomyxa. Nature. 1988 Mar 10;332(6160):176–178. doi: 10.1038/332176a0. [DOI] [PubMed] [Google Scholar]
  21. Fath K. R., Burgess D. R. Golgi-derived vesicles from developing epithelial cells bind actin filaments and possess myosin-I as a cytoplasmically oriented peripheral membrane protein. J Cell Biol. 1993 Jan;120(1):117–127. doi: 10.1083/jcb.120.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fath K. R., Burgess D. R. Membrane motility mediated by unconventional myosin. Curr Opin Cell Biol. 1994 Feb;6(1):131–135. doi: 10.1016/0955-0674(94)90126-0. [DOI] [PubMed] [Google Scholar]
  23. Fath K. R., Mamajiwalla S. N., Burgess D. R. The cytoskeleton in development of epithelial cell polarity. J Cell Sci Suppl. 1993;17:65–73. doi: 10.1242/jcs.1993.supplement_17.10. [DOI] [PubMed] [Google Scholar]
  24. Fath K. R., Obenauf S. D., Burgess D. R. Cytoskeletal protein and mRNA accumulation during brush border formation in adult chicken enterocytes. Development. 1990 Jun;109(2):449–459. doi: 10.1242/dev.109.2.449. [DOI] [PubMed] [Google Scholar]
  25. Fujiki Y., Hubbard A. L., Fowler S., Lazarow P. B. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol. 1982 Apr;93(1):97–102. doi: 10.1083/jcb.93.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gibbons I. R., Lee-Eiford A., Mocz G., Phillipson C. A., Tang W. J., Gibbons B. H. Photosensitized cleavage of dynein heavy chains. Cleavage at the "V1 site" by irradiation at 365 nm in the presence of ATP and vanadate. J Biol Chem. 1987 Feb 25;262(6):2780–2786. [PubMed] [Google Scholar]
  27. Gilbert T., Le Bivic A., Quaroni A., Rodriguez-Boulan E. Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J Cell Biol. 1991 Apr;113(2):275–288. doi: 10.1083/jcb.113.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gill S. R., Schroer T. A., Szilak I., Steuer E. R., Sheetz M. P., Cleveland D. W. Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J Cell Biol. 1991 Dec;115(6):1639–1650. doi: 10.1083/jcb.115.6.1639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Goltz J. S., Wolkoff A. W., Novikoff P. M., Stockert R. J., Satir P. A role for microtubules in sorting endocytic vesicles in rat hepatocytes. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7026–7030. doi: 10.1073/pnas.89.15.7026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hirokawa N., Sato-Yoshitake R., Yoshida T., Kawashima T. Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J Cell Biol. 1990 Sep;111(3):1027–1037. doi: 10.1083/jcb.111.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Holzbaur E. L., Hammarback J. A., Paschal B. M., Kravit N. G., Pfister K. K., Vallee R. B. Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued. Nature. 1991 Jun 13;351(6327):579–583. doi: 10.1038/351579a0. [DOI] [PubMed] [Google Scholar]
  32. Howard J., Hudspeth A. J., Vale R. D. Movement of microtubules by single kinesin molecules. Nature. 1989 Nov 9;342(6246):154–158. doi: 10.1038/342154a0. [DOI] [PubMed] [Google Scholar]
  33. Hugon J. S., Bennett G., Pothier P., Ngoma Z. Loss of microtubules and alteration of glycoprotein migration in organ cultures of mouse intestine exposed to nocodazole or colchicine. Cell Tissue Res. 1987 Jun;248(3):653–662. doi: 10.1007/BF00216496. [DOI] [PubMed] [Google Scholar]
  34. Hunziker W., Mâle P., Mellman I. Differential microtubule requirements for transcytosis in MDCK cells. EMBO J. 1990 Nov;9(11):3515–3525. doi: 10.1002/j.1460-2075.1990.tb07560.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ingold A. L., Cohn S. A., Scholey J. M. Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains. J Cell Biol. 1988 Dec;107(6 Pt 2):2657–2667. doi: 10.1083/jcb.107.6.2657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Johnston G. C., Prendergast J. A., Singer R. A. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J Cell Biol. 1991 May;113(3):539–551. doi: 10.1083/jcb.113.3.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Jones S. M., Crosby J. R., Salamero J., Howell K. E. A cytosolic complex of p62 and rab6 associates with TGN38/41 and is involved in budding of exocytic vesicles from the trans-Golgi network. J Cell Biol. 1993 Aug;122(4):775–788. doi: 10.1083/jcb.122.4.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Joshi H. C. Gamma-tubulin: the hub of cellular microtubule assemblies. Bioessays. 1993 Oct;15(10):637–643. doi: 10.1002/bies.950151002. [DOI] [PubMed] [Google Scholar]
  39. Kuznetsov S. A., Langford G. M., Weiss D. G. Actin-dependent organelle movement in squid axoplasm. Nature. 1992 Apr 23;356(6371):722–725. doi: 10.1038/356722a0. [DOI] [PubMed] [Google Scholar]
  40. Lacey M. L., Haimo L. T. Cytoplasmic dynein is a vesicle protein. J Biol Chem. 1992 Mar 5;267(7):4793–4798. [PubMed] [Google Scholar]
  41. Leopold P. L., McDowall A. W., Pfister K. K., Bloom G. S., Brady S. T. Association of kinesin with characterized membrane-bounded organelles. Cell Motil Cytoskeleton. 1992;23(1):19–33. doi: 10.1002/cm.970230104. [DOI] [PubMed] [Google Scholar]
  42. Lillie S. H., Brown S. S. Suppression of a myosin defect by a kinesin-related gene. Nature. 1992 Mar 26;356(6367):358–361. doi: 10.1038/356358a0. [DOI] [PubMed] [Google Scholar]
  43. Lin S. X., Collins C. A. Immunolocalization of cytoplasmic dynein to lysosomes in cultured cells. J Cell Sci. 1992 Jan;101(Pt 1):125–137. doi: 10.1242/jcs.101.1.125. [DOI] [PubMed] [Google Scholar]
  44. Lippincott-Schwartz J. Bidirectional membrane traffic between the endoplasmic reticulum and Golgi apparatus. Trends Cell Biol. 1993 Mar;3(3):81–88. doi: 10.1016/0962-8924(93)90078-f. [DOI] [PubMed] [Google Scholar]
  45. Louvard D., Kedinger M., Hauri H. P. The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures. Annu Rev Cell Biol. 1992;8:157–195. doi: 10.1146/annurev.cb.08.110192.001105. [DOI] [PubMed] [Google Scholar]
  46. Louvard D. The function of the major cytoskeletal components of the brush border. Curr Opin Cell Biol. 1989 Feb;1(1):51–57. doi: 10.1016/s0955-0674(89)80036-5. [DOI] [PubMed] [Google Scholar]
  47. Luby-Phelps K., Castle P. E., Taylor D. L., Lanni F. Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4910–4913. doi: 10.1073/pnas.84.14.4910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Luzio J. P., Brake B., Banting G., Howell K. E., Braghetta P., Stanley K. K. Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38). Biochem J. 1990 Aug 15;270(1):97–102. doi: 10.1042/bj2700097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Matsudaira P. T., Burgess D. R. Identification and organization of the components in the isolated microvillus cytoskeleton. J Cell Biol. 1979 Dec;83(3):667–673. doi: 10.1083/jcb.83.3.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Matsudaira P. T., Burgess D. R. Organization of the cross-filaments in intestinal microvilli. J Cell Biol. 1982 Mar;92(3):657–664. doi: 10.1083/jcb.92.3.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Matsudaira P. T., Burgess D. R. SDS microslab linear gradient polyacrylamide gel electrophoresis. Anal Biochem. 1978 Jul 1;87(2):386–396. doi: 10.1016/0003-2697(78)90688-7. [DOI] [PubMed] [Google Scholar]
  52. Mays R. W., Beck K. A., Nelson W. J. Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery. Curr Opin Cell Biol. 1994 Feb;6(1):16–24. doi: 10.1016/0955-0674(94)90111-2. [DOI] [PubMed] [Google Scholar]
  53. Mooseker M. S. Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border. Annu Rev Cell Biol. 1985;1:209–241. doi: 10.1146/annurev.cb.01.110185.001233. [DOI] [PubMed] [Google Scholar]
  54. Olmsted J. B. Affinity purification of antibodies from diazotized paper blots of heterogeneous protein samples. J Biol Chem. 1981 Dec 10;256(23):11955–11957. [PubMed] [Google Scholar]
  55. Parczyk K., Haase W., Kondor-Koch C. Microtubules are involved in the secretion of proteins at the apical cell surface of the polarized epithelial cell, Madin-Darby canine kidney. J Biol Chem. 1989 Oct 5;264(28):16837–16846. [PubMed] [Google Scholar]
  56. Paschal B. M., Shpetner H. S., Vallee R. B. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J Cell Biol. 1987 Sep;105(3):1273–1282. doi: 10.1083/jcb.105.3.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pierre P., Scheel J., Rickard J. E., Kreis T. E. CLIP-170 links endocytic vesicles to microtubules. Cell. 1992 Sep 18;70(6):887–900. doi: 10.1016/0092-8674(92)90240-d. [DOI] [PubMed] [Google Scholar]
  58. Pollard T. D., Doberstein S. K., Zot H. G. Myosin-I. Annu Rev Physiol. 1991;53:653–681. doi: 10.1146/annurev.ph.53.030191.003253. [DOI] [PubMed] [Google Scholar]
  59. Provance D. W., Jr, McDowall A., Marko M., Luby-Phelps K. Cytoarchitecture of size-excluding compartments in living cells. J Cell Sci. 1993 Oct;106(Pt 2):565–577. doi: 10.1242/jcs.106.2.565. [DOI] [PubMed] [Google Scholar]
  60. Rizzolo L. J., Joshi H. C. Apical orientation of the microtubule organizing center and associated gamma-tubulin during the polarization of the retinal pigment epithelium in vivo. Dev Biol. 1993 May;157(1):147–156. doi: 10.1006/dbio.1993.1119. [DOI] [PubMed] [Google Scholar]
  61. Roth J., Lentze M. J., Berger E. G. Immunocytochemical demonstration of ecto-galactosyltransferase in absorptive intestinal cells. J Cell Biol. 1985 Jan;100(1):118–125. doi: 10.1083/jcb.100.1.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Sandoz D., Lainé M. C., Nicolas G. Distribution of microtubules within the intestinal terminal web as revealed by quick-freezing and cryosubstitution. Eur J Cell Biol. 1986 Jan;39(2):481–484. [PubMed] [Google Scholar]
  63. Scheel J., Kreis T. E. Motor protein independent binding of endocytic carrier vesicles to microtubules in vitro. J Biol Chem. 1991 Sep 25;266(27):18141–18148. [PubMed] [Google Scholar]
  64. Schnapp B. J., Reese T. S. Dynein is the motor for retrograde axonal transport of organelles. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1548–1552. doi: 10.1073/pnas.86.5.1548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Schroer T. A., Sheetz M. P. Functions of microtubule-based motors. Annu Rev Physiol. 1991;53:629–652. doi: 10.1146/annurev.ph.53.030191.003213. [DOI] [PubMed] [Google Scholar]
  66. Schroer T. A., Steuer E. R., Sheetz M. P. Cytoplasmic dynein is a minus end-directed motor for membranous organelles. Cell. 1989 Mar 24;56(6):937–946. doi: 10.1016/0092-8674(89)90627-2. [DOI] [PubMed] [Google Scholar]
  67. Shibayama T., Carboni J. M., Mooseker M. S. Assembly of the intestinal brush border: appearance and redistribution of microvillar core proteins in developing chick enterocytes. J Cell Biol. 1987 Jul;105(1):335–344. doi: 10.1083/jcb.105.1.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Skoufias D. A., Cole D. G., Wedaman K. P., Scholey J. M. The carboxyl-terminal domain of kinesin heavy chain is important for membrane binding. J Biol Chem. 1994 Jan 14;269(2):1477–1485. [PubMed] [Google Scholar]
  69. Skoufias D. A., Scholey J. M. Cytoplasmic microtubule-based motor proteins. Curr Opin Cell Biol. 1993 Feb;5(1):95–104. doi: 10.1016/s0955-0674(05)80014-6. [DOI] [PubMed] [Google Scholar]
  70. Steuer E. R., Wordeman L., Schroer T. A., Sheetz M. P. Localization of cytoplasmic dynein to mitotic spindles and kinetochores. Nature. 1990 May 17;345(6272):266–268. doi: 10.1038/345266a0. [DOI] [PubMed] [Google Scholar]
  71. Swanson J. A., Locke A., Ansel P., Hollenbeck P. J. Radial movement of lysosomes along microtubules in permeabilized macrophages. J Cell Sci. 1992 Sep;103(Pt 1):201–209. doi: 10.1242/jcs.103.1.201. [DOI] [PubMed] [Google Scholar]
  72. Tartakoff A. M., Vassalli P. Lectin-binding sites as markers of Golgi subcompartments: proximal-to-distal maturation of oligosaccharides. J Cell Biol. 1983 Oct;97(4):1243–1248. doi: 10.1083/jcb.97.4.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Titus M. A. Myosins. Curr Opin Cell Biol. 1993 Feb;5(1):77–81. doi: 10.1016/s0955-0674(05)80011-0. [DOI] [PubMed] [Google Scholar]
  74. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Toyoshima I., Yu H., Steuer E. R., Sheetz M. P. Kinectin, a major kinesin-binding protein on ER. J Cell Biol. 1992 Sep;118(5):1121–1131. doi: 10.1083/jcb.118.5.1121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Van der Sluijs P., Bennett M. K., Antony C., Simons K., Kreis T. E. Binding of exocytic vesicles from MDCK cells to microtubules in vitro. J Cell Sci. 1990 Apr;95(Pt 4):545–553. doi: 10.1242/jcs.95.4.545. [DOI] [PubMed] [Google Scholar]
  77. Velasco A., Hendricks L., Moremen K. W., Tulsiani D. R., Touster O., Farquhar M. G. Cell type-dependent variations in the subcellular distribution of alpha-mannosidase I and II. J Cell Biol. 1993 Jul;122(1):39–51. doi: 10.1083/jcb.122.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Walker R. A., Salmon E. D., Endow S. A. The Drosophila claret segregation protein is a minus-end directed motor molecule. Nature. 1990 Oct 25;347(6295):780–782. doi: 10.1038/347780a0. [DOI] [PubMed] [Google Scholar]
  79. Walsh C. Synthesis and assembly of the cytoskeleton of Naegleria gruberi flagellates. J Cell Biol. 1984 Feb;98(2):449–456. doi: 10.1083/jcb.98.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Weiser M. M., Neumeier M. M., Quaroni A., Kirsch K. Synthesis of plasmalemmal glycoproteins in intestinal epithelial cells. Separation of Golgi membranes from villus and crypt cell surface membranes; glycosyltransferase activity of surface membrane. J Cell Biol. 1978 Jun;77(3):722–734. doi: 10.1083/jcb.77.3.722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Yu H., Toyoshima I., Steuer E. R., Sheetz M. P. Kinesin and cytoplasmic dynein binding to brain microsomes. J Biol Chem. 1992 Oct 5;267(28):20457–20464. [PubMed] [Google Scholar]

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