The Chlamydomonas Dhc1 gene encodes a dynein heavy chain subunit required for assembly of the I1 inner arm complex

Molecular Biology of the Cell

Volumn 8, Issue 4, 1997, Pages 607-620

  Myster, Steven H ^a   Knott, Julie A ^a   O'Toole, Eileen ^b   Porter, Mary E ^a,c  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c 4 135 Jackson Hall ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE;

ARTICLE; AXONEME; CHLAMYDOMONAS; FLAGELLUM; GENE INSERTION; GENE ISOLATION; GENE LOCUS; GENE SEQUENCE; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY;

CHLAMYDOMONAS;

EID: 0030956345     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.4.607     Document Type: Article

References (82)

1. Andrews, K.L., Nettesheim, P., Asai, D.J., and Ostrowski, L.E. (1996). Identification of seven rat axonemal dynein heavy chain genes: expression during ciliated cell differentiation. Mol. Biol. Cell 7, 71-79.
2. Asai, D.J., Beckwith, S.M., Kandl, K.A., Keating, H.H., Tjandra, H., and Forney, J.D. (1994). The dynein genes of Paramecium tetraurelia. Sequences adjacent to the catalytic P-loop identify cytoplasmic and axonemal heavy chain isoforms. J. Cell Sci. 107, 839-847.
3. Brokaw, C.J., and Kamiya, R. (1987). Bending patterns of Chlamydomonas flagella IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function. Cell Motil. Cytoskeleton 8, 68-75.
4. Chisholm, D. (1989). A convenient procedure for obtaining DNA from bacteriophage lambda. Biotechniques 7, 21-23.
5. 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.
6. Debuchy, R., Purton, S., and Rochaix, J.-D. (1989). The arginosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. EMBO J. 8, 2803-2809.
7. Dutcher, S.K. (1995). Genetic nomenclature guide. Trends Genet. 3 (suppl.), 16-18.
8. Ebersold, W.T. (1967). Chlamydomonas reinhardti: heterozygous diploid strains. Science 57, 446-449.
9. Eversole, R.A. (1956). Biochemical mutants of Chlamydomonas reinhardi. J. Bot. 43, 404-407.
10. Fernandez, E., Schnell, R., Ranum, L.P.W., Hussey, S.C., Silflow, C.D., and Lefebvre, P.A. (1989). Isolation and characterization of the nitrate reductase structural gene of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 86, 6449-6453.
11. Gardner, L.C., O'Toole, E., Perrone, C.A., Giddings, T., and Porter, M.E. (1994). Components of a "dynein regulatory complex" are located at the junction between the radial spokes and the dynein arms in Chlamydomonas flagella. J. Cell Biol. 127, 1311-1325.
12. Gibbons, I.R. (1995). Dynein family of motor proteins: present status and future questions. Cell Motil. Cytoskeleton 32, 136-144.
13. 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.
14. Goodenough, U.W., Gebhart, B., Mermall, V., Mitchell, D.R., and Heuser, J.E. (1987). High pressure liquid chromatography fractionation of Chlamydomonas dynein extracts and characterization of inner arm dynein subunits. J. Mol. Biol. 194, 481-494.
15. German, D.S., and Levine, R.P. (1965). Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 54, 1665-1669.
16. Gumpel, N.J., and Purton, S. (1994). Playing tag with Chlamydomonas. Trends Cell Biol. 4, 299-301.
17. Habermacher, G., and Sale, W.S. (1995). Regulation of dynein-driven microtubule sliding by an axonemal kinase and phosphatase in Chlamydomonas flagella. Cell Motil. Cytoskeleton 32, 106-109.
18. Habermacher, G., and Sale, W.S. (1997). Regulation of flagellar dynein by phosphorylation of a 138-kD inner arm dynein intermediate chain. J. Cell Biol. 136, 167-176.
19. Harris, E. (1989). The Chlamydomonas Sourcebook, San Diego, CA: Academic Press, 399-446.
20. Hastings, P.J., Levine, E.E., Cosbey, E., Hudock, M.O., Gillham, N.W., Surzycki, S.J., Loppes, R., and Levine, R.P. (1965). The linkage groups of Chlamydomonas reinhardi. Microb. Genet. Bull. B 23, 17-19.
21. Holmes, J.A., and Dutcher, S.K. (1989). Cellular asymmetry in Chlamydomonas reinhardtii. J. Cell Sci. 94, 273-285.
22. Holzbauer, E.L.F., and Vallee, R.B. (1994). Dyneins: molecular structure and cellular function. Annu. Rev. Cell Biol. 10, 339-372.
23. Howard, D.R., Habermacher, G., Glass, D.B., Smith, E.F., and Sale, W.S. (1994). Regulation of Chlamydomonas flagellar dynein by an axonemal protein kinase. J. Cell Biol. 127, 1683-1692.
24. James, S.W., Silflow, C.D., Thompson, M.D., Ranum, L.P.W., and Lefebvre, P.A. (1989). Extragenic suppression and synthetic lethality among Chlamydomonas reinhardtii mutants resistant to anti-microtubule drugs. Genetics 122, 567-577.
25. Jameson, B.A., and Wolf, H. (1988). The antigenic index: a novel algorithm, for predicting antigenic determinants. Comput. Appl. Biosci. 4, 181-186.
26. Kagami, O., and Kamiya, R. (1992). Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner-arm dynein. J. Cell Sci. 103, 653-664.
27. Kamiya, R., Kurimoto, E., and Muto, E. (1991). Two types of Chlamydomonas flagellar mutants missing different components of inner-arm dynein. J. Cell Biol. 112, 441-447.
28. Kato, T., Kagami, O., Yagi, T., and Kamiya, R. (1993). Isolation of two species of Chlamydomonas reinhardtii flagellar mutants, ida5 and ida6, that lack a newly identified heavy chain of the inner dynein arm. Cell Struct. Funct. 18, 371-377.
29. Kindle, K.L. (1990). High frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 87, 1228-1232.
30. King, S.J., and Dutcher, S.K. (1977). Phosphoregulation of an inner dynein arm complex in Chlamydomonas reinhardtii is altered in phototactic mutant strains. J. Cell Biol. 136, 177-191.
31. King, S.J., Inwood, W.B., O'Toole, E.T., Power, J., and Dutcher, S.K. (1994). The bop2-1 mutation reveals radial asymmetry in the inner dynein arm region of Chlamydomonas reinhardtii. J. Cell Biol. 126, 1255-1266.
32. King, S.M., Otter, T., Witman, G.B. (1986). Purification and characterization of Chlamydomonas flagellar dyneins. Methods Enzymol. 134, 291-306.
33. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
34. LeDizet, M., and Piperno, G. (1995a). ida4-1, ida4-2, and ida4-3 are intron splicing mutations affecting the locus encoding p28, a light chain of Chlamydomonas axonemal inner dynein arms. Mol. Biol. Cell 6, 713-723.
35. LeDizet, M., and Piperno, G. (1995b). The light chain p28 associates with a subset of inner dynein arm heavy chains in Chlamydomonas axonemes. Mol. Biol. Cell 6, 697-711.
36. Levine, R.P., and Ebersold, W.T. (1960). The genetics and cytology of Chlamydomonas. Annu. Rev. Microbiol. 14, 197-216.
37. Loppes, R. (1969). A new class of arginine-requiring mutants in Chlamydomonas reinhardi. Mol. Gen. Genet. 104, 172-177.
38. 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, 1145-1162.
39. McVittie, A. (1972a). Flagellar mutants of Chlamydomonas reinhardtii. J. Gen. Microbiol. 71, 525-540.
40. McVittie, A. (1972b). Genetic studies on flagellum mutants of Chlamydomonas reinhardtii. Genet. Res. Camb. 19, 157-164.
41. Mitchell, D.R. (1989). Molecular analysis of the alpha and beta dynein genes of Chlamydomonas reinhardtii. Cell Motil. Cytoskeleton 14, 435-445.
42. Mitchell, D.R. (1994). Cell and molecular biology of flagellar dyneins. Int. Rev. Cytol. 155, 141-175.
43. Mitchell, D.R., and Brown, K.S. (1994) Sequence analysis of the Chlamydomonas a and β dynein heavy chain genes. J. Cell Sci. 107, 635-644.
44. Mitchell, D.R., and Kang, Y. (1991). Identification of oda6 as a Chlamydomonas dynein mutant by rescue with the wild-type gene. J. Cell Biol. 113, 835-842.
45. Muto, E., Kamiya, R., and Tsukita, S. (1991). Double-rowed organization of inner dynein arms in Chlamydomonas flagella revealed by tilt series, thin-section electron microscopy. J. Cell Sci. 99, 57-66.
46. Nelson, J.A.E., Savereide, P.B., and Lefebvre, P.A. (1994). The CRY1 gene in Chlamydomonas reinhardtii: structure and use as a dominant selectable marker for nuclear transformation. Mol. Cell. Biol. 14, 4011-4019.
47. Olmsted, J.B. (1981). Affinity purification of antibodies from diazotized paper blots of heterogeneous protein samples. J. Biol. Chem. 256, 11955-11957.
48. Piperno, G. (1988). Isolation of a sixth dynein subunit adenosine triphosphatase. J. Cell Biol. 106, 133-140.
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. Piperno, G., Ramanis, Z., Smith, E.F., and Sale, W.S. (1990). Three distinct inner dynein arms in Chlamydomonas flagella: Molecular composition and location in the axoneme. J. Cell Biol. 110, 379-389.
51. Porter, M.E. (1996). Axonemal dyneins: assembly, organization, and regulation. Curr. Opin. Cell Biol. 8, 10-17.
52. Porter, M.E., and Johnson, K.A. (1983). Characterization of the ATP sensitive binding of Tetrahymena 30 S dynein to bovine brain microtubules. J. Biol. Chem. 258, 6575-6581.
53. Porter, M.E., Knott, J.A., Gardner, L.C., Mitchell, D.R., and Dutcher, S.K. (1994). Mutations in the SUP-PF-1 locus of Chlamydomonas reinhardtii identify a regulatory domain in the β-dynein heavy chain. J. Cell Biol. 126, 1495-1507.
54. Porter, M.E., Knott, J.A., Myster, S.H., and Farlow, S.J. (1996). The dynein gene family in Chlamydomonas reinhardtii. Genetics 144, 569-585.
55. Porter, M.E., Power, J., and Dutcher, S.K. (1992). Extragenic suppressors of paralyzed flagellar mutations in Chlamydomonas reinhardtii identify loci that alter the inner dynein arms. J. Cell Biol. 118, 1163-1176.
56. Rasmusson, K., Serr, M., Gepner, J., Gibbons, I., and Hays, T.S. (1994). A family of dynein genes in Drosophila melanogaster. Mol. Biol. Cell 5, 45-55.
57. Rupp, G.,O'Toole, E., Gardner, L.C., Mitchell, B.F., and Porter, M.E. (1996). The sup-pf-2 mutations of Chlamydomonas alter the activity of the outer dynein arms by modification of the γ-dynein heavy chain. J. Cell Biol. 135, 1853-1865.
58. Sager, R., and Granick, S. (1953). Nutritional studies in Chlamydomonas reinhardtii. Ann. N.Y. Acad. Sci. 56, 831-838.
59. Sakakibara, H., Mitchell, D.R., and Kamiya, R. (1991). A Chlamydomonas outer-arm dynein mutant missing the alpha heavy chain. J. Cell Biol. 113, 615-622.
60. Sakakibara, H., Takada, S., King, S.M., Witman, G.B., and Kamiya, R. (1993). A Chlamydomonas outer arm dynein mutant with a truncated beta heavy chain. J. Cell. Biol. 122, 653-661.
61. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
62. Savereide, P.B. (1991). The molecular basis of resistance to the protein synthesis inhibitor cryptopleurine in Chlamydomonas reinhardtii. Ph.D. Thesis. St. Paul, MN: University of Minnesota.
63. Schnell, R.A., and Lefebvre, P.A. (1993). Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging. Genetics 134, 737-747.
64. Silflow, C.D., Chisholm, R.L., Conner, T.W., and Ranum, L.P.W. (1985). The two alpha-tubulin genes of Chlamydomonas reinhardtii code for a slightly different protein. Mol. Cell. Biol. 5, 2389-2398.
65. Smith, E.F., and Lefebvre, P.A. (1996). PF16 encodes a protein with armadillo repeats and localizes to a single microtubule of the central apparatus in Chlamydomonas flagella. J. Cell Biol. 132, 359-370.
66. Smith, E.F., and Sale, W.S. (1991). Microtubule binding and translocation by inner dynein arm subtype I1. Cell Motil. Cytoskeleton 18, 258-268.
67. Smith, E.F., and Sale, W.S. (1992). Regulation of dynein-driven microtubule sliding by the radial spokes in flagella. Science 257, 1557-1559.
68. Sosa, P.M., Ortega, T., and Barea, J.L. (1978). Mutants from Chlamydomonas reinhardtii affected in their nitrate assimilation capability. Plant. Sci. Lett. 11, 51-58.
69. Takada, S., and Kamiya, R. (1994). Functional reconstitution of Chlamydomonas outer dynein arms from α-β and γ subunits: requirement of a third factor. J. Cell Biol. 131, 399-409.
70. Tarn, L.W., and Lefebvre, P.A. (1993). Cloning of flagellar genes in Chlamydomonas reinhardtii by DNA insertional mutagenesis. Genetics 135, 375-384.
71. 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.
72. 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.
73. Warr, J.R., McVittie, A., Randall, J.T., and Hopkins, J.M. (1966). Genetic control of flagellar structure in Chlamydomonas reinhardtii. Genet. Res. 7, 335-351.
74. r intermediate chain of Chlamydomonas outer arm dynein is a WD-repeat protein required for arm assembly. J. Cell Biol. 129, 169-178.
75. Wilkerson, C.G., King, S.M., and Witman, G.B. (1994). Molecular analysis of the γ heavy chain of Chlamydomonas flagellar outer arm dynein. J. Cell Sci. 107, 497-506.
76. Williams, B.D., Velleca, M.A., Curry, A.M., and Rosenbaum, J.L. (1989). Molecular cloning and sequence analysis of the Chlamydomonas gene coding for radial spoke protein 3: flagellar mutation pf-14 is an ochre allele. J. Cell Biol. 109, 235-245.
77. Witman, G.B. (1986). Isolation of Chlamydomonas flagella and flagellar axonemes. Methods Enzymol. 134, 280-290.
78. Witman, G.B., Carlson, K., Berliner, J., and Rosenbaum, J.L. (1972). Chlamydomonas flagella 1. Isolation and electrophoretic analysis of microtubules, membranes, matrix, and mastigonemes. J. Cell Biol. 54, 507-539.
79. Witman, G.B., Plummer, J., and Sander, G. (1978). Chlamydomonas flagellar mutants lacking radial spokes and central tubules. Structure and function of specific axonemal components. J. Cell Biol. 76, 729-747.
80. Witman, G.B., Wilkerson, C.G., and King, S.M. (1994). The biochemistry, genetics, and molecular biology of flagellar dynein. In: Microtubules, ed. J.S. Hyams, and C.W. Lloyd, New York: Wiley-Liss, 229-249.
81. Wray, W., Boulikas, T., Wray, V.P., and Hancock, R. (1981). Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118, 197-203.
82. Zhang, D. (1996). Regulation of nitrate assimilation in Chlamydomonas reinhardtii. Ph.D. Thesis. St. Paul, MN: University of Minnesota.