Regulation of flagellar dynein by phosphorylation of a 138-kD inner ann dynein intermediate chain

Journal of Cell Biology

Volumn 136, Issue 1, 1997, Pages 167-176

  Habermacher, Geoffrey ^a   Sale, Winfield S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; PHOSPHOPROTEIN; REGULATOR PROTEIN;

ARTICLE; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; DEPHOSPHORYLATION; FLAGELLUM; MICROTUBULE; MOVEMENT (PHYSIOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CHLAMYDOMONAS REINHARDTII; DYNEIN ATPASE; ENZYME INHIBITORS; FLAGELLA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROCYSTINS; MICROTUBULES; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDES, CYCLIC; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS;

EID: 0031022258     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.136.1.167     Document Type: Article

References (55)

1. Barkalow, K., T. Hamasaki, and P. Satir. 1994. Regulation of 22S dynein by a 29-kD light chain. J. Cell Biol. 126:727-735.
2. Bessen, M., R.B. Fay, and G.B. Witman. 1980. Calcium control of waveform on isolated flagellar axonemes of Chlamydomonas. J. Cell Biol. 86:446-455.
3. Blum, H., H. Beier, and B. Huang. 1987. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis. 8:93-97.
4. Brokaw, C.J. 1994. Control of flagellar bending: a new agenda based on dynein diversity. Cell Motil. Cytoskeleton, 28:199-204.
5. Brokaw, C.J., and R, Kamiya. 1987. Bending patterns on Chlamydomonas flagella. IV. Mutants with defects in inner and outer arms indicate differences in dynein arm function. Cell Motil. Cytoskeleton. 8:68-75.
6. 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.
7. Burgess, S.A., D.A. Carter, S.D. Dover, and D.M. Woolley. 1991. The inner dynein arm complex: compatible images from freeze-etch and thin section methods of microscopy, 7. Cell Sci. 100:319-328.
8. Chaudhry, P.S., S. Creagh, N. Yu, and C.J. Brokaw. 1995. Multiple protein kinase activities required for activation of sperm flagellar mutility. Cell Motil. Cytoskeleton. 32:65-79.
9. Curry, A.M., and J.L. Rosenbaum. 1993. Flagellar radial spoke: model molecular genetic system for studying organelle assembly. Cell Motil, Cytoskeleton. 24:224-232.
10. Dutcher, S.K. 1995. Flagellar assembly in two hundred and fifty easy-to-follow steps. Trends Genet. 11:398-404.
11. Gardner, L.C., E. O'Toole, 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.
12. Goodenough, U.W., and J.E. Heuser. 1984. Structural comparison of purified proteins with in situ dynein arms. J. Mol. Biol. 180:1083-1118.
13. Goodenough, U.W., B. Gebhart, V. Memall, D.R. Mitchell, and J.E. Heuser. 1987. HPLC fractionalion of Chlamydomonas dynein extracts and characterization of inner arm dynein subunits. J. Mol. Biol. 194:481-494.
14. Habermacher, G., and W.S. Sale. 1995. Regulation of dynein-driven microtubule; sliding by an axoncmal kinase and phosphatasc in Chlamydomonas flagella. Cell Motil. Cytoskeleton. 32:106-109.
15. 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.
16. Hanmaki, T., T.J. Murtaugh, B.H. Satir, and P. Satir. 1989. In vitro phosphorylation of Paramecium axonemes and permeabilizod cells. Cell Motil. Cytoskeleton. 12:1-11.
17. Hamasaki, T., K. Barkalow, J. Richmond, and P. Satir. 1991. cAMP-stimulated phosphorylation of an axonemal polypeptide that copurifies with the 22S dynein arm regulates microtuhule translocation velocity and swimming speed in Paramecium. Proc. Natl. Acad. Sci. USA. 88:7918-7922.
18. Hamasaki, T., M.E.J. Holwill, K. Barkalow, and P. Satir. 1995. Mechanochemical aspects of axonemal dynein activity studied by in vitro microtuhule translocation. Biophys. J. 69:2569-2579.
19. Hasegawa, E., H. Hayashi, S. Asakura, and R. Kamiya. 1987. Stimulation of in vitro motility of Chlamydomonas axonemes by inhibition of cAMP-dependent phosphorylation. Cell Motil. Cytoskeleton. 8:302-311.
20. Howard, D., 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.
21. Huang, B. 1986. Chlamydomonas reinhardtii; a model system for the genetic analysis of flagellar structure and motility. Int. Rev. Cytol. 99:181-215.
22. Huang, B., Z. Ramanis, and D.J.L. Luck. 1982. Suppressor mutations in Chlamvdomonas reveal a regulatory mechanism for flagellar function. Cell. 28:115-124.
23. Kagami, O., and R. Kamiya. 1992. Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner arm dynein. J. Cell Sci. 103:653-664.
24. Kamiya, R. 1995. Exploring the function of inner and outer dynein arms with Chlamydomonas mutants. Cell Motil. Cytoskeleton. 32:98-102.
25. 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.
26. Kato, T., O. Kagami, T. Yagi, and R. Kamiya. 1993. Isolation of two species of Chlamydomonas reinhardtii flagellar mutants, ida5 and ida6, that lack a newly identified heavy chain of inner dynein arm. Cell Struct. Funct. 18:371-377.
27. King, S.J., and S.K. Dutcher. 1997. Phosphoregulation of an inner dynein arm complex in Chlamvdomonas reinhardtii is altered in phototactic mutant strains. J. Cell Biol. 136:177-191.
28. King, S.J., W. Inwood, E. O'Toole, J. Power, and S.K. Dutcher. 1994. The bop2-1 mutation reveals radial asymmetry in the inner dynein arm region of Chlamydomonas reinhardtii. J. Cell Biol. 126:1255-1266.
29. 2+-binding light chain within Chlamydomonas outer arm dynein. J. Cell Sci. 108:3757-3764.
30. King, S.M., and G.B. Witman. 1990. Localization of an intermediate chain of outer arm dynein by immunoelectron microscopy. J. Biol. Chem. 265:19807-19811.
31. King, S.M., and G.B. Witman. 1994. Multiple sites of phosphorylation within the α-heavy chain of Chlamydomonas outer arm dynein. J. Biol. Chem. 269: 5452-5457.
32. r 78,000 intermediate chain of Chlamydomonas outer arm dynein interacts with α-tubulin in situ. J. Biol. Chem. 266:8401-8407.
33. r 8,000 light chain. J. Biol. Chem. 271:19358-19366.
34. Kurimoto, E., and R. Kamiya. 1991. Microtubule sliding in flagellar axonemes of Chlamydomonas mutants missing inner or outer arm dynein: valocity measurements on new types of mutants by an improved method. Cell mol. Cytoskeleton 19:275-281.
35. LeDizet, M., and G. Piperno. 1995. The light chain p28 associates with a subset of inner dynein arm heavy chains in Chlamydomonas axonemes. Mol. Biol. Cell. 6:697-711.
36. Mastronarde, D., E. OToole, K. McDonald, J.R. McIntosh, and M. Porter 1992. Arrangement on inner dynein arms in wild-type and mutant flagella of Chlamydomonas. J. Cell Biol. 118:1145-1162.
37. Muto, E., R. Kamiya, and S. Tsukita. 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.
38. Omoto, C.K., and C.J. Brokaw. 1985. Bending patterns of Chlamydomonas flagella. II. Calcium effects on reactivated Chlamydomonas flagella. Cell Moil. Cytoskeleton. 5:53-60.
39. Pfister, K.K., and G.B. Witman. 1984. Subfractionation of Chlamydomonas 188 dynein into two unique subunits containing ATPase activity. J. Biol. Chem. 259:12072-12080.
40. Piperno, G. 1995. Regulation of dynein activity within Chlamydomonaa flagella. Cell Motil. Cytoskeleton, 32:103-105.
41. Piperno, G., and Z. Ramanis. 1991. The proximal portion of the Chlamydomonos flagella contains a distinct set of inner dynein arms. J. Cell Biol. 112:701-709.
42. Piperno, G., Z. Ramanis, E.F. Smith, and W.S. Sale. 1990. Three distinct inaer dynein arms in Chlamydomonas flagella: molecular composition and location in the axoneme. J. Cell Biol. 110:379-389.
43. Piperno, G., K. Mead, and W. Shestak. 1992. The inner dynein arms 12 interact with a "dynein regulatory complex" in Chlamydomonas flagella. J. Cell Biol. 118:1455-1464.
44. 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.
45. Porter, M.E. 1996. Axonemal dyneins: assembly, organization, and regulation. Curr. Opin. Cell Biol. 8:10-17.
46. Porter, M.E., J. Power, and S.K. 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.
47. Sager, R., and S. Granick. 1953. Nutritional studies with Chlamydomonas reinhardtii, Ann. NY Acad. Sci. 56:831-838.
48. Smith, E.F., and W.S. Sale. 1991. Microtubule binding and translocation by inner dynein arm subtype I1. Cell Motil. Cytoskeleton. 18:258-268.
49. 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.
50. 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.
51. Smith, E.F., and W.S. Sale. 1994. Mechanism of flagellar movement and functional interactions between dynein arms and radial spoke/central pair apparatus complex. In Microtubules. J.S. Hyams and C.W. Lloyd, editors. Academic Press, New York. 491-496.
52. Tash, J.S., and G.E. Bracho. 1994. Regulation of sperm motilily: emerging evidence for major role of protein phosphatases. J. Androl 15:505-509.
53. Walzak, C.E., and D.L. Nelson. 1994. Regulation of dynein-driven motility in cilia and flagella. Cell Motil. Cytoskeleton. 27:101-107.
54. Witman, G.B. 1986. Isolation of Chlamydomonas flagella and flagellar axonemes. Methods Enzymol. 134:280-290.
55. Witman, G.B. 1992. Axonemal dyneins. Curr. Opin. Cell Biol. 4:74-79.