The sup-pf-2 mutations of Chlamydomonas alter the activity of the outer dynein arms by modification of the γ-dynein heavy chain

Journal of Cell Biology

Volumn 135, Issue 6 II, 1996, Pages 1853-1865

  Rupp, Gerald ^a   O'Toole, Eileen ^b   Gardner, Lynne C ^a   Mitchell, Beth F ^c   Porter, Mary E ^a,d  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c LE MOYNE COLLEGE   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DYNEIN ADENOSINE TRIPHOSPHATASE;

ALLELE; ARTICLE; AXONEME; CHLAMYDOMONAS; ENZYME ACTIVITY; FLAGELLUM; GENE MUTATION; GENETIC LINKAGE; MICROTUBULE; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL;

ALLELES; ANIMALS; CELL MOVEMENT; CHLAMYDOMONAS; CHROMATOGRAPHY, ION EXCHANGE; DNA, PROTOZOAN; DYNEIN ATPASE; FLAGELLA; GENETIC COMPLEMENTATION TEST; IMAGE PROCESSING, COMPUTER-ASSISTED; ISOMERISM; MICROSCOPY, ELECTRON; MUTATION; PROTEIN STRUCTURE, TERTIARY;

EID: 0030463112     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.6.1853     Document Type: Article

References (63)

1. Bradford, M. 1976. A rapid and sensitive method for quantitation of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
2. Brokaw, C.J. 1971. Bend propagation by a sliding filament model for flagella. J. Exp. Biol. 55:289-304.
3. Brokaw, C.J., and R. Kamiya. 1987. Bonding 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. Brokaw, C.J., and D.J.L. Luck. 1985. Bending patterns of Chlamydomonas flagella. III. A radial spoke head deficient mutant and a central pair deficient mutant. Cell Motil. 5:195-208.
5. Brokaw, C.J., D.J.L. Luck, and B. Huang. 1982. Analysis of the movement of Chlamydomonas flagella: the function of the radial-spoke system is revealed by comparison of wild-type and mutant flagella. J. Cell Biol. 92:722-732.
6. Ebersold, W.T. 1967. Chlamydomonas reinhardtii: Heterozygous diploid strains. Science (Wash. DC). 157:446-449.
7. Fox, L.A., and W.S. Sale. 1987. Direction of force generated by the inner row of dynein arms on flagellar microlubules. J. Cell Biol. 105:1781-1787.
8. Gardner, L.C., E. OToole, C.A. Perrone, T. Giddings, and M.E. Porter. 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.
9. Gibbons, I.R. 1995. Dynein family of motor proteins: present status and future questions. Cell Motil. Cytoskeleton. 32:136-144.
10. Goodenough, U.W., B. Gebhart, V. Mermall, D.R. Mitehell, and J.E. Heuser. 1987. High-pressure liquid chromatography fractionation of Chlamydomonas dynein extracts and characterization of inner-arm dynein subunits. J. Mol. Biol. 194:481-494.
11. Habermacher, G., and W.S. Sale. 1995. Regulation of dynein-driven microtubule sliding by an axonemal kinase and phosphatase in Chlamydomonas flagella. Cell Motil. Cytoskeleton. 32:106-109.
12. Habermacher, G., and W.S. Sale. 1996. Regulation of flagellar dynein by an axonemal type-1 phosphatase in Chlamydomonas. J. Cell Sci. 109:1899-1907.
13. Holmes, J.A., and S.K. Dutcher. 1989. Cellular asymmetry in Chlamydomonas reinhardtii. J. Cell Sci. 94:273-285.
14. Hoops, H.J., and G.B. Wilman. 1983. Outer doublet heterogeneity reveals structural polarity related to beat direction in Chlamydomonas flagella. J. Cell Biol. 97:902-908.
15. Howard, D.R., G. Habermacher, D.B. Glass, E.F. Smith, and W.S. Sale. 1994. Regulation of Chlamydomonas flagellar dynein by an axonemal protein kinase. J. Cell Biol. 127:1683-1692.
16. Huang, B., G. Piperno, and D.J.L. Luck. 1979. Paralyzed flagellar mutants of Chlamydomonas reinhardtii defective for axonemal doublet microtubule arms. J. Biol. Chem. 254:3091-3099.
17. Huang, B., Z. Ramanis, and D.J.L. Luck. 1982. Suppressor mutations in Chlamydomonas reveal a regulatory mechanism for flagellar function. Cell. 28:115-125.
18. Kagami, O., and R. Kamiya. 1990. Strikingly low ATPase activities in flagellar axonemes of a Chlamydomonas mutant missing outer dynein arms. Eur. J. Biochem. 187:441-446.
19. Kagami, O., and R. Kamiya. 1992. Translocation and rotation of microlubules caused by multiple species of Chlamydomonas inner-arm dynein. J. Cell Sci. 103:653-664.
20. Kamiya, R. 1982. Extrusion and rotation of the central-pair microtubules in detergent-treated Chlamydomonas flagella. Cell Motil. 1 (Suppl.):169-173.
21. Kamiya, R. 1988. Mutations at twelve independent loci result in absence of outer dynein arms in Chlamydomonas reinhardtii. J. Cell Biol. 107:2253-2258.
22. Kamiya, R., E. Kurimoto, and E. Muto. 1991. Two types of Chlamydomonas flagellar mutants missing different components of inner-arm dynein. J. Cell Biol. 112:441-447.
23. King, S.J., W.B. Inwood, E.T. O'Toole, J. Power, and S.K. Dutcher. 1994. The bop2-1 mutation reveals radial asymmetry in the inner dynein arm region of Chlamydomonas reinhardii. J. Cell Biol. 126:1255-1266.
24. Kinoshita, S., T. Miki-Noumura, and C.K. Omoto. 1995. Regulatory role of nucleotides in axonemal function. Cell Motil. Cytoskeleton. 32:46-54.
25. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.). 227:680-685.
26. Levine, R.P., and W.T. Ebersold. 1960. The genetics and cytology of Chlamydomonas Annu. Rev. Microbiol. 14:197-216.
27. Lindemann, C.B. 1994a. A "geometric clutch" hypothesis to explain oscillations of the axoneme of cilia and flagella. J. Theor. Biol. 168:175-189.
28. Lindemann, C. B. 1994b. A model of flagellar and ciliary functioning which uses the forces transverse to the axoneme as the regulator of dynein activation. Cell Motil. Cytoskeleton. 29:141-154.
29. Luck, D.J.L., G. Piperno, Z. Ramanis, and B. Huang. 1977. Flagellar mutants of Chlamydomonas: studies of radial spoke-defective strains by dikaryon and revertant analysis. Proc. Natl. Acad. Sci. USA. 74:3456-3460.
30. Mastronarde, D.N., E.T. O'Toole, K.L. McDonald, J.R. McIntosh, and M.E. Porter. 1992. Arrangement of inner dynein arms in wild-type and mutant flagella of Chlamydomonas. J. Cell Biol. 118:1145-1162.
31. Minoura, I. and R. Kamiya. 1995. Strikingly different propulsive forces generated by different dynein-defieient mutants in viscous media. Cell Motil. Cytoskeleton. 31:130-139.
32. Mitchell, D.R. 1994. Cell and molecular biology of flagellar dyneins. Int. Rev. Cytol. 155:141-180.
33. Mitchell, D.R., and Y. Rang. 1991. Identification of oda6 as a Chlamydomonas dynein mutant by rescue with the wild-type gene. J. Cell Biol. 113:835-842.
34. Mitchell, D.R., and J.L. Rosenbaum. 1985. A motile Chlamydomonas flagellar mutant that lacks outer dynein arms. J. Cell Biol. 100:1228-1234.
35. Omoto, C.K., and C. Rung. 1979. The pair of central tubules rotates during ciliary beat in Paramecium. Nature (Lond.). 279:532-534.
36. Omoto, C.K., and G.B. Witman. 1981. Functionally significant central pair rotation in a primitive eukaryotic flagellum. Nature (Lond.). 290:708-710.
37. Omoto, C.K., T. Yagi, E. Kurimoto, and R. Kamiya. 1996. Ability of paralyzed flagella mutants of Chlamydomonas to move. Cell Motil. Cytoskeleton. 33:88-94.
38. Pfister, K.K., and G.B. Witman. 1984. Subfractionation of Chlamydomonas 18S dynein into two unique subunits containing ATPase activity. J. Biol. Chem. 259:12072-12080.
39. Piperno, G., and D.J.L. Luck. 1979. Axonemal adenosine triphosphatases from flagella of Chlamydomonas reinhardtii. Purification of two dyneins. J. Biol. Chem. 254:3084-3090.
40. Piperno, G., and Z. Ramanis. 1991. The proximal portion of Chlamydomonas flagella contains a distinct set of inner dynein arms. J. Cell Biol. 112:701-709.
41. Piperno, G., Z. Ramanis, E.F. Smith, and W.S. Sale. 1990. Three distinct inner dynein arms in Chlamydomonas flagella: molecular composition and location in the axoneme. J. Cell Biol. 110:379-389.
42. Piperno, G., R. Mead, and W. Shestak. 1992. The inner dynein arms 12 interact with a "dynein regulatory complex" in Chlamydomonas flagella. J. Cell Biol. 118:1455-1463.
43. Piperno, G., K. Mead, M. LeDizet, and A. Moscatelli. 1994. Mutations in the "dynein regulatory complex" alter the ATP-insensitive binding sites for inner arm dyneins in Chlamydomonas axonemes. J. Cell Biol. 125:1109-1117.
44. Porter, M.E. 1996. Axonemal dyneins: assembly, organization, and regulation. Curr. Opin. Cell Biol. 8:10-17.
45. Porter, M.E., J. Power, and S.R. Dutcher. 1992. Extragenic suppressors of paralyzed flagellar mutations in Chlamydomonas reinhardtii identify loci that alter the inner dynein arms. J. Cell Biol. 118:1163-1176.
46. Porter, M.E., J.A. Knott, L.C. Gardner, D.K. Mitchell, and S.K. Dutcher. 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.
47. Sager, R., and S. Granick. 1953. Nutritional studies in Chlamydomonas reinhardtii. Ann. NY Acad. Sci. 56:831-838.
48. Sakakibara, H., D.R. Mitchell, and R. Kamiya. 1991. A Chlamydomonas outer arm dynein mutant missing the α heavy chain. J. Cell Biol. 113:615-622.
49. Sakakibara, H., S. Takada, S.M. King, G.B. Wilman, and R. Kamiya. 1993. A Chlamydomonas outer arm dynein mutant with a truncated β heavy chain. J. Cell Biol. 122:653-661.
50. Sale, W.S., and P. Satir. 1977. The direction of active sliding of microtubules in Tetrahymena cilia, Proc. Natl. Acad Sci. USA. 74:2045-2049.
51. Segal, R.A., B. Huang, Z. Ramanis, and D.J.L. Luck. 1984. Mulant strains of Chlamydomonas reinhardtii that move backwards only. J. Cell Biol. 98:2026-2034.
52. Smith, E.F., and W.S. Sale. 1992a. Regulation of dynein-driven microtubule sliding by the radial spokes in flagella. Science (Wash. DC). 257:1557-1559.
53. Smith, E.F., and W.S. Sale. 1992b. Structural and functional reconstitution of inner dynein arms in Chlamydomonas flagellar axonemes. J. Cell Biol. 117:573-581.
54. Smith, E.F., and W.S. Sale. 1994. Mechanisms of flagellar movement: functional interactions between dynein arms and the radial spoke-central apparatus complex. In Microtubules. J.A. Hyams and C.W. Lloyd, editors. Wiley-Liss, New York, 381-392.
55. Takada, S., and R. Kamiya. 1994. Functional reconstitution Chlamydomonas outer dynein arms from α-β and γ subunits: requirement of a third factor. J. Cell Biol. 126:737-745.
56. Warner, F.D., and P. Satir. 1974. The structural basis of ciliary bend formation. Radial spoke positional changes accompanying microtubule sliding. J. Cell Biol. 63:35-63.
57. Waxman, L., and A.L. Goldberg. 1982. Protease La from Escherichia coli hydrolyzes ATP and proteins in a linked fashion. Proc. Natl. Acad. Sci. USA. 79:4883-4887.
58. Wilkerson, C.G., S.M. King, and G.B. Wilman. 1994. Molecular analysis of the γ heavy chain of Chlamydomonas flagellar outer arm dynein. J. Cell Sci. 107:497-506.
59. Witman, G.B. 1986. Isolation of Chlamydomonas flagella and flagcllar ax-onemes. Methods Enzymol. 134:280-290.
60. Witman, G., K. Carlson, J. Berliner, and J. Rosenbaum. 1972. Chlamydomonas flagella: I. Isolation and electrophoretic analysis of microtubules, matrix, membranes, and masligonemes. J. Cell Biol. 54:507-539.
61. Witman, G.B., J. Plummer, and G. Sander. 1978. Chlamydomonas flagellar mutants lacking radial spokes and central tubules. Structure, composition, and function of specific axonemal components. J. Cell Biol. 76:729-747.
62. Witman, G.B., C.G. Wilkerson, and S.M. King. 1994. The biochemistry, genetics, and molecular biology of flagellar dyncin. In Microtubules. J.S. Hyams and C.W. Lloyd, editors. Wiley-Liss, New York. 229-250.
63. Wray, W., T. Boulikas, V.P. Wray, and R. Hancock. 1981. Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118:197-203.