Centractin (ARP1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles

Journal of Cell Biology

Volumn 135, Issue 6 II, 1996, Pages 1815-1829

  Holleran, Elizabeth A ^a   Tokito, Mariko K ^a   Karki, Sher ^a   Holzbaur, Erika L F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BACULOVIRUS; CALCULATION; CELL FUSION; CELL INTERACTION; LIPID ANALYSIS; MEMBRANE CONDUCTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ACTINS; ANIMALS; BIOLOGICAL MARKERS; BIOLOGICAL TRANSPORT; CELL LINE; CHROMATOGRAPHY, AFFINITY; CYTOSKELETON; GENE EXPRESSION; GOLGI APPARATUS; MACROPODIDAE; MICROFILAMENTS; MICROTUBULE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR SEQUENCE DATA; POLYMERS; PRECIPITIN TESTS; RABBITS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTRIN; SUBCELLULAR FRACTIONS; TRANSFECTION;

EID: 0030479303     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.6.1815     Document Type: Article

References (89)

1. Allen, V.J., and T.E. Kreis. 1986. A microlubule-binding protein associated with membranes of the Golgi apparatus. J. Cell Biol. 103:2229-2239.
2. Aniento, F., N. Emans, G. Griffiths, and J. Gruenbery. 1993. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123:1373-1387.
3. Beck, K.A., J.A. Buchanan, V. Malhotra, and W.J. Nelson. 1994. Golgi spectrin: identification of an erythroid β-spectrin homolog associated with the Golgi complex. J. Cell Biol. 127:707-723.
4. Bennett, V. 1990. Spectrin-based membrane skeleton: a multipotential adapter between the plasma membrane and cytoplasm. Physiol. Rev. 70:1029-1065.
5. Bennett V., K. Gardner, and J.P. Steiner. 1988. Brain adducin: a protein kinase C substrate that may mediate site-directed assembly at the spectrin-actin junction. J. Biol. Chem. 263:5860-5869.
6. Black, J.D., S.T. Koury, R.B. Bankert, and E.A. Repasky. 1988. Heterogeneity in lymphocyte spectrin distribution: ultrastructure identification of a new spectrin-rich cytoplasmic structure. J. Cell Biol. 106:97-109.
7. Bloom, G.S., and T.A. Brashear. 1989. A novel 58 kDa-protein associates with the Golgi apparatus and microtubules. J. Biol. Chem. 264:16083-16092.
8. Bonder, E.M., and M.S. Mooseker. 1986. Cytochalasin B slows but does not prevent monomer addition at the barbed end of the actin filament. J. Cell Biol. 102:282-288.
9. Bruno, K.S., J.H. Tinsley, F.F. Minke, and M. Plamann. 1996. Genetic interactions among cytoplasmic dynein and nuclear distribution mutants of Neurospora crassa. Proc. Natl. Acad. Sci. USA. 93(10):4775-4780.
10. Cao, L.-G., D.J. Fishkind, and Y.-L. Wang. 1993. Localization and dynamics of non-filamentous actin in cultured cells. J. Cell Biol. 123:173-181.
11. Clark, S.W., and D.I. Meyer. 1992. Centractin is an actin homologue associated with the centrosome. Nature (Lond.). 359:246-250.
12. Clark, S.W., and D.I. Meyer. 1994. ACT3: a putative centractin homologue in S. cerevisiae is required for proper orientation of the mitotic spindle. J. Cell Biol. 127:129-138.
13. Clark, S.W., O. Staub, I.B. Clark, E.L.F. Holzbaur, B.M. Paschal, R.B. Vallee, and D.I. Meyer. 1994. β-Centractin: characterization and distribution of a new member of the centractin family of actin-related proteins. Mol. Biol. Cell. 5:1301-1310.
14. Collins, C.A., and R.B. Vallee. 1989. Preparation of microtubules from rat liver and testis: cytoplasmic dynein is a major microtubule-associated protein. Cell Motil. Cytoskeleton. 14:491-500.
15. Cooper, J.A. 1987. Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105:1473-1478.
16. Courthesy-Theulaz, I., A. Pauloin, and S.R. Pfeffer. 1992. Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J. Cell Biol. 118:1333-1345.
17. Dubreuil, R.R., T.J. Byers, A.L. Sillman, D. Bar-Zvi, L.S. Goldstein, and D. Branton. 1989. The complete sequence of Drosophila α-spectrin: conservation of structural domains between α-spectrins and α-actinin. J. Cell Biol. 109:2197-2205.
18. Echeverri, C.J., B.M. Paschal, K.T. Vaughan, and R.B. Vallee. 1996. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J. Cell Biol. 132:617-633.
19. Eschel, D., L.A. Urrestarazu, S. Visers, J.C. Jauniaux, J.C. van Vliet-Reedijk, R.J. Planta, and I.R. Gibbons. 1993. Cytoplasmic dynein is required for normal nuclear segregation in yeast. Proc. Natl. Acad. Sci. USA. 90:11172-11176.
20. Fach, B., S.F. Graham, and R. Keates. 1985. Association of fodrin with brain microtubules. Can. J. Biochem. Cell. Biol. 63:372-381.
21. Path, K.R., G.M. Trimbur, and D.R. Burgess. 1994. Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J. Cell Biol. 126:661-675.
22. Frankel, S., M.B. Heintzelman, S. Artavania-Tsakonas, and M.S. Mooseker. 1994. Identification of a divergent actin-related protein in Drosophila. J. Mol. Biol. 235:1351-1356.
23. Fyrberg, C., L. Ryan, M. Kenton, and E. Fyrberg. 1994. Genes encoding actin-related proteins of Drosophila melanogaster. J. Mol. Biol. 241:498-503.
24. Gardner, K., and V. Bennett. 1986. A new erythrocyte membrane-associated protein with calmodulin binding activity. Identification and purification. J. Biol. Chem. 261:1339-1348.
25. Gill, S.R., T.A. Schroer, I. Szilak, E.R. Steuer, M.P. Sheetz, and D.W. Cleveland. 1991. Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115:1639-1650.
26. Goodman, S.R., K.E. Krebs, C.F. Whitfield, B.M. Riederer, and I.S. Zagon. 1988. Spectrin and related molecules. CRC Critical Reviews in Biochemistry. 23:171-234.
27. Harata, M. A. Karwan, and U. Wintersberger. 1994. An essential gene of Saccharomyces cerevisiae coding for an actin-related protein. Proc. Natl. Acad. Sci. USA. 91:8258-8262.
28. Harris, A.S., J.P. Anderson, P.D. Yurchenco, L.A.D. Green, K.J. Ainger, and J.S. Morrow. 1986. Mechanisms of cytoskeletal regulation: functional and antigenic diversity in human erythrocyte and brain brain β spectrin. J. Cell Biochem. 30:51-70.
29. Hartwig, J. 1994. Spectrin superfamily. Protein Profiles. 1:711-714.
30. Hirokawa, N., R. Sato-Yoshitake, T. Yoshida, and T. Kawashima. 1990. Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J. Cell Biol. 111:1027-1037.
31. Holzbaur, E.L.F., and R.B.Vallee. 1994. Dyneins: molecular structure and cellular function. Annu. Rev. Cell Biol. 10:339-372.
32. Holzbaur, E.L.F., J.A. Hammerback, B.M. Paschal, N.G. Kravit, K.K. Pfister, and R.B. Vallee. 1991. Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued. Nature (Lond.). 351:579-583.
33. Joshi, R., and V. Bennett. 1990. Mapping the domain structure of human erythrocyle adducing. J. Biol. Chem. 265(22):13130-13136.
34. Kabsch, W., and K.C. Holmes. 1995. The actin fold. FASEB. (Fed. Am. Soc. Exp. Biochem.). 9:167-174.
35. Karki, S., and E.L.F. Holzbaur. 1995. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270:28806-28811.
36. Kelleher, J.F., S.J. Atkinson, and T.D. Pollard. 1995. Sequences, structural models and cellular localization of the actin-related proteins Arp2 and Arp3 from Acanthamoeba. J. Cell Biol. 131:385-397.
37. Lacey, M.L., and L.T. Haimo. 1992. Cytoplasmic dynein is a vesicle protein. J. Biol. Chem. 267:4793-4798.
38. Laemmli, U.K. 1970. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature (Lond.). 227:680-685.
39. Lazerides, E., and W.J. Nelson. 1983. Erythrocyte and brain forms of spectrin in cerebellum: distinct membrane-cytoskeletal domains in neurons. Science (Wash. DC). 220:1295-1296.
40. Lees-Miller, J.P., D.M. Helfman, and T.A. Schroer. 1992a. A vertebrate actin-related protein is a component of a multisubunit complex involved in microtubule-based vesicle motility. Nature (Lond.). 359:244-246.
41. Lees-Miller, J.P., G. Henry, and D.M. Helfman. 1992a. Identification of act2, an essential gene in the fission yeast Schizosaccharomyces pombe that encodes a protein related to actin. Proc. Natl. Acad. Sci. USA. 89:80-83.
42. Li, X., and V. Bennett. 1996. Identification of the spectrin subunit domains required for formation of spectrin/adducin/actin complexes. J. Biol. Chem. 271:15695-15702.
43. Li, Y.-Y., E. Yeh, T. Hays, and K. Bloom. 1993. Disruption of mitotic spindle orientation in a yeast dynein mutant. Proc. Natl. Acad. Sci. USA. 90:10096-10100.
44. Lin, S.X., and C.A. Collins. 1992. Immunolocalization of cytoplasmic dynein to lysosomes in cultured cells. J. Cell Sci. 101:125-137.
45. Lloyd, C., and P. Gunning. 1993. Noncoding regions of the γ-actin gene influence the impact of the gene on myoblast morphology. J. Cell Biol. 121:73-82.
46. Lloyd, C., G. Schevzov, and P. Gunning. 1992. Transfection of β- and γ-actin genes into myoblasts elicits different feedback regulatory response. J. Cell Biol. 117:787-797.
47. Lucocq, J.M., E.M. Berger, and G. Warren. 1989. Mitolic Golgi fragments in Hela cells and their role in the reassembly pathway. J. Cell Biol. 109:463-474.
48. Machesky, L.M., S.J. Atkinson, C. Ampe, J. Vanderkerckhove, and T.D. Pollard. 1994. Purification of a cortical complex containing two unconventional actins from Acanthamoeha by affinity chromatography on profilin-agarose. J. Cell Biol. 127:107-116.
49. Matsudaira, P. 1994. The fimbrin and α-actinin footprint on actin. J. Cell Biol. 126:285-287.
50. McGrail, M., J. Gepner, A. Silvanovich, S. Ludmann, M. Serr, T.S. Mayes. 1995. Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex. J. Cell Biol. 131:411-425.
51. Melki, R., I.E. Vainberg, R.L. Chow, and N.J. Cowan. 1993. Chaperonin-mediated folding of vertebrate actin-related protein and γ-tubulin. J. Cell Biol. 122:1301-1310.
52. Melloni, R.H., M.K. Tokito, and E.L.F. Holzbaur. 1995. Distribution of the mRNA encoding the 150 kD cytoplasmic dynein-associated polypeptide in rat brain. J. Comp. Neurol. 357:15-24.
53. Morrow, J. 1989. The spectrin membrane skeleton: emerging concepts. Curr. Opin. Cell Biol. 1:23-29.
54. Muhua, L., T. Karpova, and J.A. Cooper. 1994. A yeast actin-related protein homologous to that in vertebrate dynactin complex is important for spindle orientation and nuclear migration. Cell. 78:669-679.
55. Mullins, R.D., J.F. Kelleher, and T.D. Pollard. 1996. Actin' like actin? TICB. 6:208-212.
56. Mullins, R.D., W.P. Stafford, and T.D. Pollard. 1997. Structure, subunit topology and actin-hinding activity of the Arp2/3 complex from Acanthamoeba. J. Cell Biol. In press.
57. Paschal, B.M., H.S. Shpetner, and R.B. Vallee. 1991. Purification of brain cytoplasmic dynein and characterization. 1991. Methods Enzymol. 196:181-191.
58. Glued and a novel actin. J. Biol. Chem. 268:15318-15323.
59. Plamann, M., P.P. Minke, J.H. Tinsley, and K.S. Bruno. 1994. Cytoplasmic dynein and actin-rclated protein Arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127:139-149.
60. Robb, M.J., M.A. Wilson, and P.J. Vierula. 1995. A fungal actin-related protein involved in nuclear migration. Mol. Gen. Genet. 247:583-590.
61. Robinson. M.S., and T.E. Kreis. 1992. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell. 69:129-138.
62. Sahr, K.E., P. Laurila, L. Kotula, A.L. Scarpa, E. Coupal, T.L. Leto, A.J. Linnenbach, J.C. Winkelman, D.W. Speicher, V.T. Marchesi, et al. 1990. The complete cDNA and polypeptide sequence of human erythroid α spectrin. J. Biol. Chem. 265:4434-4443.
63. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. p.p. 16.30 and 16.32.
64. Saunders, W.S., D. Koshland, D. Eshel, I.R. Gibbons, and M.A. Hoyt. 1995. Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. J. Cell Biol. 128:617-624.
65. Schafer, D.A., S.R. Gill, J.A. Cooper, J.E. Heuser, and T.A. Schroer. 1994. Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin. J. Cell Biol. 126:403-412.
66. Schevzov, G., C. Lloyd, and P. Gunning. 1992. High level expression of transfected β- and γ-actin genes differentially impacts on myoblast cytoarchitecture. J. Cell Biol. 117:775-785.
67. Schnapp, B.J., and T.S. Reese. 1989. Dynein is the motor for retrograde axonal transport of organelles. Proc. Natl. Acad. Sci. USA. 86;1548-1552.
68. Schroer, T.A., E. Fyrberg, J. Cooper. R. Waterson, D. Helfman, T. Pollard, and D. Meyer. 1994. Actin-related protein nomenclature and classification. J. Cell Biol. 127:1777-1778.
69. Schwob, E., and R.P. Martin. 1992. New yeast actin-like gene required late in the cell cycle. Nature (Loud.). 355:179-182.
70. Sheterline, P., and J.C. Sparrow. 1994. Actin. Protein Profiles. 1:1-121.
71. Shu, H.-B., and H.C. Joshi. 1995. γ-Tubulin can both nucleate microtubule assembly and self-assemble into novel tubular structures in mammalian cells. J. Cell Biol. 130:1137-1147.
72. Steuer, E., L. Wordeman, T.A. Schroer, and M.P. Sheetz. 1989. Cytoplasmic dynein is a minus-end directed motor for membranous organelles. Cell. 56:937-946.
73. Sweeney, H.L., and E.L.F. Holzhaur. 1996. Mutational analysis of motor proteins. Annu. Rev. Physial. 58:751-792.
74. Glued, the largest subunit of the dynactin complex, is nonessential in Neurospora but required for nuclear distribution. Mol. Biol. Cell. 7:731-742.
75. Tokito, M.K., D.S. Howland, V.M.-Y. Lee, and E.L.F. Holzbaur. 1996. Functionally distinct isoforms of dynactin are expressed in human neurons. Mol. Biol. Cell. 7:1167-1180.
76. Glued. J. Cell Biol. 131:1507-1516.
77. Vaisberg, E.A., M.P. Koonce, and J.R. McIntosh. 1993. Cytoplasmic dynein plays a role in mammalian mitotic spindle formation. J. Cell Biol. 123:849-858.
78. Vallee, R.B., and M.P. Sheetz. 1996. Targeting of motor proteins. Science (Wash. DC). 271:1539-1544.
79. von-Arx, P., S. Bantle, T. Soldati, and J.-C. Perriard. 1995. Dominant negative effect of Cytoplasmic actin isoproteins on carfliomyocyte cyloarchitecture and function. J. Cell Biol. 131:1759-1773.
80. Waseem, A., and H.C. Palfrey. 1990. Identification and protein kinase C-dependent phosphorylation of α-adducin in human fibroblasts. J. Cell Sci. 96:93-98.
81. Wasenius, V.-M., M. Saraste, P. Salven, M. Eramaa, L. Holm, and V.-P. Lehto. 1989. Primary structure of brain α spectrin. J. Cell Biol. 108:79-93.
82. Glued binds directly to both the microtuhule and centractin. Proc. Natl. Acad. Sci. USA. 92:1634-1638.
83. Waters, J.C., R.W. Cole, and C.L. Rieder. 1993. The force-producing mechanism for centrosome separation during spindle formation in vertebrates is intrinsic to each aster. J. Cell Biol. 122:361-372.
84. Weber, V., M. Harata, H. Hauser, and U. Wintersberger. 1995. The actin-related protein Act3p of Saccharomyces cerevisiae is located in the nucleus. Mol. Biol. Cell. 6:1263-1270.
85. Winkelman, J.C., and B.C. Forget. 1993. Erythroid and non-erythroid spectrins. Blood. 81:3173-3185.
86. Xiang, X., S.M. Beckwith, and R.N. Morris. 1994. Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA. 91:2100-2104.
87. Yeh, E., R.V. Skibbens, J.W. Cheng, E.D. Salmon, and K.S. Bloom. 1995. Spindle dynamics and cell cycle regulation of dynein in the budding yeast Saccharomyces cerevisiae. J. Cell Biol. 130:687-700.
88. Yu, H., I. Toyoshima, E.R. Steuer, and M.P. Sheetz. 1992. Kinesin and cytoplasmic dynein binding to brain microsomes. J. Biol. Chem. 267:20457-20464.
89. Zagon, I.S., R. Higbee, B.M. Riederer, and S.R. Goodman. 1986. Spectrin subtypes in mammalian brain: an immunoelectron microscopic study. J. Neurosci. 6:2977-2986.