Gene knockouts reveal separate functions for two cytoplasmic dyneins in Tetrahymena thermophila

Molecular Biology of the Cell

Volumn 10, Issue 3, 1999, Pages 771-784

  Lee, Seungwon ^a   Wisniewski, Julie C ^a   Dentler, William L ^b   Asai, David J ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE;

AMINO ACID SEQUENCE; ARTICLE; CELL REGENERATION; CELL SHAPE; CELL SIZE; CHROMOSOME SEGREGATION; ENZYME ACTIVITY; GENE DISRUPTION; GENE ISOLATION; GENETIC ANALYSIS; KNOCKOUT GENE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; TETRAHYMENA THERMOPHILA;

PROTOZOA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 0032963084     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.3.771     Document Type: Article

References (69)

1. Allen, S.L., Altschuler, M.A., Bruns, P.J., Cohen, J., Doerder, F.P., Gaertig, J., Gorovsky, M., Orias, E., and Turkewitz, A. (1998). Proposed genetic nomenclature rules for Tetrahymena thermophila, Paramecium primaurelia and Paramecium tetraurelia. Genetics 149, 459-462.
2. Aniento, F., Emans, N., Griffiths, G., and Gruenberg, J. (1993). Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123, 1373-1387.
3. Asai, D.J. (1996). Functional and molecular diversity of dynein heavy chains. Semin. Cell Dev. Biol. 7, 311-320.
4. Asai, D.J., and Brokaw, C.J. (1993). Dynein heavy chain isoforms and axonemal motility. Trends Cell Biol. 3, 398-402.
5. Asai, D.J., Brokaw, C.J., Harmon, R.C., and Wilson, L. (1982). Monoclonal antibodies to tubulin and their effects on the movement of reactivated sea urchin spermatozoa. Cell Motil. 1, 175-180.
6. Asai, D.J., and Criswell, P.S. (1995). Identification of new dynein heavy chain genes by RNA-directed PCR. Methods Cell Biol. 47, 579-585.
7. Batz, W., and Wunderlich, F. (1976). Structural transformation of the phagosomal membrane in Tetrahymena cells endocytosing latex beads. Arch. Microbiol. 109, 215-220.
8. Brokaw, C.J. (1994). Control of flagellar bending: a new agenda based on dynein diversity. Cell Motil. Cytoskeleton 28, 199-204.
9. Bruns, P.J., Brussard, T.B., and Merriam, E.V. (1983). Nullisomic Tetrahymena. II. A set of nullisomics define the germinal chromosomes. Genetics 104, 257-270.
10. Cassidy-Hanley, D., Bowen, J., Lee, J.H., Cole, E., VerPlank, L.A., Gaertig, J., Gorovsky, M.A., and Bruns, P.J. (1997). Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 146, 135-147.
11. Chilcoat, N.D., Melia, S.M., Haddad, A., and Turkewitz, A.P. (1996). Granule lattice protein 1 (Grl1p), an acidic, calcium-binding protein in Tetrahymena thermophila dense-core secretory granules, influences granule size, shape, content organization, and release but not protein sorting or condensation. J. Cell Biol. 135, 1775-1787.
12. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
13. Cleveland, D.W., and Hoffman, P.N. (1991). Slow axonal transport models come full circle: evidence that microtubule sliding mediates axon elongation and tubulin transport. Cell 67, 453-456.
14. Cole, D.G., and Scholey, J.M. (1995). Structural variations among the kinesins. Trends Cell Biol. 5, 259-262.
15. Cole, E.S., and Stuart, K.R. (1999). Nuclear and cytoskeletal fluorescence microscopy techniques. In: Methods in Cell Biology: Tetrahymena thermophila, ed. D.J. Asai and J.D. Forney, San Diego: Academic Press (in press).
16. Corthesy-Theulaz, I., Pauloin, A., and Pfeffer, S.R. (1992). Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J. Cell Biol. 118, 1333-1345.
17. Criswell, P.S., and Asai, D.J. (1998). Evidence for four cytoplasmic dynein heavy chain isoforms in rat testis. Mol. Biol. Cell 9, 237-247.
18. Criswell, P.S., Ostrowski, L.E., and Asai, D.J. (1996). A novel cytoplasmic dynein heavy chain: expression of DHC1b in mammalian ciliated epithelial cells. J. Cell Sci. 109, 1891-1898.
19. Dillman, J.F., III, Dabney, L.P., and Pfister, K.K. (1996). Cytoplasmic dynein is associated with slow axonal transport. Proc. Natl. Acad. Sci. USA 93, 141-144.
20. Echeverri, C.J., Paschal, B.M., Vaughan, K.T., and Vallee, R.B. (1996). Molecular characterization of the 50-kDa subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J. Cell Biol. 132, 617-633.
21. Eshel, D., Urrestarazu, L.A., Vissers, S., Jauniaux, J.-C, van Vliet-Reedijk, J.C., Planta, R.J., and Gibbons, I.R. (1993). Cytoplasmic dynein is required for normal nuclear segregation in yeast. Proc. Natl. Acad. Sci. USA 90, 11172-11176.
22. Fath, K.R., Trimbur, G.M., and Burgess, D.R. (1994). Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J. Cell Biol. 126, 661-675.
23. Frankel, J. (1999). Cell biology of Tetrahymena thermophila. In: Methods in Cell Biology: Tetrahymena thermophila, ed. D.J. Asai and J.D. Forney, San Diego: Academic Press (in press).
24. Gaertig, J., and Gorovsky, M. (1992). Efficient mass transformation of Tetrahymena thermophila by electroporation of conjugants. Proc. Natl. Acad. Sci. USA 89, 9196-9200.
25. Gepner, J., Li, M.-g., Ludmann, S., Kortas, C., Boylan, K., Iyadurai, S.J.P., McGrail, M., and Hays, T.S. (1996). Cytoplasmic dynein function is essential in Drosophila melanogaster. Genetics 142, 865-878.
26. Gibbons, B.H., Asai, D.J., Tang, W.-J.Y., Hays, T.S., and Gibbons, I.R. (1994). Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins. Mol. Biol. Cell 5, 57-70.
27. Gibbons, I.R. (1995). Dynein family of motor proteins: present status and future questions. Cell Motil. Cytoskeleton 32, 136-144.
28. Gibbons, I.R., Asai, D.J., Tang, W.-J.Y., and Gibbons, B.H. (1992). A cytoplasmic dynein heavy chain in sea urchin embryos. Biol. Cell 76, 303-309.
29. Harada, A., Takei, Y., Kanai, Y., Tanaka, Y., Nonaka, S., and Hirokawa, N. (1998). Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J. Cell Biol. 141, 51-59.
30. Haremaki, T., Sugai, T., and Takahashi, M. (1996). Involvement of active cellular mechanisms on the disorganization of oral apparatus in amicronucleate cells in Tetrahymena thermophila. Cell Struct. Funct. 21, 73-80.
31. Holleran, E.A., Tokito, M.K., Karki, S., and Holzbaur, E.L.F. (1996). Centractin (ARP1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles. J. Cell Biol. 135, 1815-1829.
32. Inoue, S., Turgeon, B.G., Yoder, O.C., and Aist, J.R. (1998). Role of fungal dynein in hyphal growth, microtubule organization, spindle pole body motility and nuclear migration. J. Cell Sci. 111, 1555-1566.
33. Jaeckel-Williams, R. (1978). Nuclear divisions with reduced numbers of microtubules in Tetrahymena. J. Cell Sci. 34, 303-319.
34. Koonce, M.P., and Samso, M. (1996). Overexpression of dynein's globular head causes a collapse of the interphase microtubule network in Dictyostelium. Mol. Biol. Cell 7, 935-948.
35. Kurz, S., and Tiedtke, A. (1993). The Golgi apparatus of Tetrahymena thermophila. J. Euk. Microbiol. 40, 10-13.
36. LaFountain, J.R., Jr., and Davidson, L.A. (1979). An analysis of spindle ultrastructure during prometaphase and metaphase of micronuclear division in Tetrahymena. Chromosoma 75, 293-308.
37. LaFountain, J.R., Jr., and Davidson, L.A. (1980). An analysis of spindle ultrastructure during anaphase of micronuclear division in Tetrahymena. Cell Motil. 1, 41-61.
38. Lee, S.-w., Wisniewski, J.C., Forney, J.D., and Asai, D.J. (1997). Gene knockouts demonstrate that cytoplasmic dyneins 1A and 1B perform separate functions in Tetrahymena. Mol. Biol. Cell 8, 160a.
39. Li, Y.-Y., Yen, E., Hays, T., and Bloom, K. (1993). Disruption of mitotic spindle orientation in a yeast dynein mutant. Proc. Natl. Acad. Sci. USA 90, 10096-10100.
40. Lu, M.J., Dadd, C.A., Mizzen, C.A., Perry, C.A., McLachlan, D.R., Annunziato, A.T., and Allis, C.D. (1994). Generation and characterization of novel antibodies highly selective for phosphorylated linker histone H1 in Tetrahymena and HeLa cells. Chromosoma 103, 111-121.
41. Lye, R.J., Wilson, R.K., and Waterston, R.H. (1995). Genomic structure of a cytoplasmic dynein heavy chain gene from the nematode Caenorhabditis elegans. Cell Motil. Cytoskeleton 32, 26-36.
42. Mastronarde, D.N., O'Toole, E.T., McDonald, K.L., McIntosh, J.R., and Porter, M.E. (1992). Arrangement of inner dynein arms in wild-type and mutant flagella of Chlamydomonas. J. Cell Biol. 118, 1145-1152.
43. Muresan, V., Godek, C.P., Reese, T.S., and Schnapp, B.J. (1996). Plus-end motors override minus-end motors during transport of squid axon vesicles on microtubules. J. Cell Biol. 135, 383-397.
44. Nanney, D.L., and Simon, E.M. (1999). Laboratory and evolutionary history of Tetrahymena thermophila. In: Methods in Cell Biology: Tetrahymena thermophila, ed. D.J. Asai and J.D. Forney, San Diego: Academic Press (in press).
45. Oda, H., Stockert, R.J., Collins, C., Wang, H., Novikoff, P.M., Satir, P., and Wolkoff, A.W. (1995). Interaction of the microtubule cytoskeleton with endocytic vesicles and cytoplasmic dynein in cultured rat hepatocytes. J. Biol. Chem. 270, 15242-15249.
46. Pazour, G.J., Dickert, B.L., and Witman, G.B. (1999). The DHC1B (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J. Cell Biol. (in press).
47. Pfarr, C.M., Coue, M., Grissom, P.M., Hays, T.S., Porter, M.E., and McIntosh, J.R. (1990). Cytoplasmic dynein is localized to kinetochores during mitosis. Nature 345, 263-265.
48. Piperno, G. (1990). Functional diversity of dyneins. Cell Motil. Cytoskeleton 17, 147-149.
49. Piperno, G., and Ramanis, Z. (1991). The proximal portion of Chlamydomonas flagella contains a distinct set of inner dynein arms. J. Cell Biol. 112, 701-709.
50. Plamann, M., Minke, P.F., Tinsley, J.H., and Bruno, K.S. (1994). Cytoplasmic dynein and actin-related protein arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127, 139-149.
51. Porter, M.E., Bower, R., Knott, J.A., Byrd, P., and Dentier, W.L. (1999). Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol. Biol. Cell 10, 693-712.
52. Rasmussen, L., and Orias, E. (1975). Tetrahymena: growth without phagocytosis. Science 190, 464-465.
53. Rieder, C.L., and Alexander, S.P. (1990). Kinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells. J. Cell Biol. 111, 81-95.
54. Rosenbaum, J.L., and Carlson, K. (1969). Cilia regeneration in Tetrahymena and its inhibitions by colchicine. J. Cell Biol. 40, 415-425.
55. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
56. Saunders, W.S., Koshland, D., Eshel, D., Gibbons, I.R., and Hoyt, M.A. (1995). Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. J. Cell Biol. 128, 617-624.
57. 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.
58. Shaw, S.L., Yen, E., Maddox, P., Salmon, E.D., and Bloom, K. (1997). Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud. J. Cell Biol. 139, 985-994.
59. Sonneborn, T.M. (1974). Tetrahymena pyriformis. In: Handbook of Genetics: Plants, Plant Viruses and Protists, ed. R.C. King, New York: Plenum Press, 433-467.
60. Steuer, E.R., Wordeman, L., Schroer, T.A., and Sheetz, M.P. (1990). Localization of cytoplasmic dynein to mitotic spindles and kinetochores. Nature 345, 266-268.
61. Supp, D.M., Witte, D.P., Potter, S.S., and Brueckner, M. (1997). Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice. Nature 389, 963-966.
62. Tanaka, Y., Zhang, Z., and Hirokawa, N. (1995). Identification and molecular evolution of new dynein-like protein sequences in rat brain. J. Cell Sci. 108, 1883-1893.
63. Tuxhorn, J., Daise, T., and Dentier, W.L. (1998). Regulation of flagellar length in Chlamydomonas. Cell Motil. Cytoskeleton 40, 133-146.
64. Vaisberg, E.A., Grissom, P.M., and McIntosh, J.R. (1996). Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles. J. Cell Biol. 133, 831-842.
65. Vaisberg, E.A., Koonce, M.P., and McIntosh, J.R. (1993). Cytoplasmic dynein plays a role in mammalian mitotic spindle formation. J. Cell Biol. 123, 849-858.
66. Vale, R.D., and Fletterick, R.J. (1997). The design plan of kinesin motors. Annu. Rev. Cell Dev. Biol. 13, 745-777.
67. Verde, F., Berrez, J.-M., Antony, C., and Karsenti, E. (1991). Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J. Cell Biol. 112, 1177-1187.
68. Wilson, R., et al. (1994). 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368, 32-38.
69. Xiang, X., Beckwith, S.M., and Morris, N.R. (1994). Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 91, 2100-2104.