Disruption of genes encoding predicted inner arm dynein heavy chains causes motility phenotypes in tetrahymena

Cell Motility and the Cytoskeleton

Volumn 59, Issue 3, 2004, Pages 201-214

  Liu, Siming ^a   Hard, Robert ^b   Rankin, Scott ^a   Hennessey, Todd ^b   Pennock, David G ^a  

^a MIAMI UNIVERSITY   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Axoneme; Cell motility; Cilia

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; MUTANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL MOTILITY; CILIARY MOTILITY; CONTROLLED STUDY; GENE DISRUPTION; GENE MUTATION; NONHUMAN; NORTHERN BLOTTING; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; TETRAHYMENA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL MOVEMENT; CILIA; DYNEIN ATPASE; GENE TARGETING; PHENOTYPE; PROTEIN ISOFORMS; PROTOZOAN PROTEINS; TETRAHYMENA THERMOPHILA;

HYLOBATIDAE; TETRAHYMENA;

EID: 7244234170     PISSN: 08861544     EISSN: None     Source Type: Journal    
DOI: 10.1002/cm.20034     Document Type: Article

References (92)

1. Andrews KL, Nettesheim P, Asai DJ, Ostrowski LE. 1996. Identification of seven rat axonemal dynein heavy chain genes: expression during ciliated cell differentiation. Mol Biol Cell 7:71-79.
2. Angus SP, Edelmann RE, Pennock DG. 2001. Targeted gene knockout of inner arm 1 in Tetrahymena thermophila. Eur J Cell Biol 80:486-497.
3. Asai DJ. 1995. Multi-dynein hypothesis. Cell Motil Cytoskeleton 32:129-132.
4. Asai DJ, Koonce MP. 2001. The dynein heavy chain: structure, mechanics and evolution. Trends Cell Biol 11:196-202.
5. Asai DJ, Wilkes DE. 2004. The dynein heavy chain family. J Eukaryot Microbiol 51:23-29.
6. Asai DJ, Beckwith SM, Kandl KA, Keating HH, Tjandra H, Forney JD. 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.
7. Beck E, Ludwig G, Auerswald EA, Reiss B, Schaller H. 1982. Nucleotide sequence and exact localization of the neomycin phosphotransferase gene from transposon Tn5. Gene 19:327-336.
8. Brokaw CJ, 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.
9. Fox LA, Sale WS. 1987. Direction of force generated by the inner row of dynein arms on flagellar microtubules. J Cell Biol 105:1781-1787.
10. Gaertig J, Gorovsky MA. 1992. Efficient mass transformation of Tetrahymena thermophila by electroporation of conjugants. Proc Natl Acad Sci USA 89:9196-9200.
11. Gaertig J, Gorovsky MA. 1995. DNA-mediated transformation in Tetrahymena. Methods Cell Biol 47:559-569.
12. Gaertig J, Gu L, Hai B, Gorovsky MA. 1994. High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res 22:5391-5398.
13. Gardner LC, O'Toole E, Perrone CA, Giddings T, Porter ME. 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.
14. Gee M, Vallee R. 1998. The role of the dynein stalk in cytoplasmic and flagellar motility. Eur Biophys J 27:466-473.
15. Gee MA, Heuser JE, Vallee RB. 1997. An extended microtubule-binding structure within the dynein motor domain. Nature 390:636-639.
16. Gibbons BH, Asai DJ, Tang WJ, Hays TS, Gibbons IR. 1994. Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins. Mol Biol Cell 5:57-70.
17. Gibbons IR. 1995. Dynein family of motor proteins: present status and future questions. Cell Motil Cytoskeleton 32:136-144.
18. Gibbons IR, Gibbons BH, Mocz G, Asai DJ. 1991. Multiple nucleotide-binding sites in the sequence of dynein beta heavy chain. Nature 352:640-643.
19. Gibbons IR, Lee-Eiford A, Mocz G, Phillipson CA, Tang WJ, Gibbons BH. 1987. Photosensitized cleavage of dynein heavy chains. Cleavage at the "V1 site" by irradiation at 365 nm in the presence of ATP and vanadate. J Biol Chem 262:2780-2786.
20. Gibson TM, Asai DJ. 2000. Isolation and characterization of 22S outer arm dynein from Tetrahymena cilia. Methods Cell Biol 62:433-440.
21. Goodenough U, Heuser J. 1984. Structural comparison of purified dynein proteins with in situ dynein arms. J Mol Biol 180:1083-1118.
22. Goodenough UW, Heuser JE. 1982. Substructure of the outer dynein arm. J Cell Biol 95:798-815.
23. Goodenough UW, Heuser JE. 1985. Substructure of inner dynein arms, radial spokes, and the central pair/projection complex of cilia and flagella. J Cell Biol 100:2008-2118.
24. Goodenough UW, Heuser JE. 1989. Structure of the soluble and in situ ciliary dyneins visualized by quick-freeze deep-etch microscopy. In: Warner FD, Satir P, Gibbons IR, editors. Cell movement, vol. 1. New York, NY: Alan R. Liss. p 121-140.
25. Goodenough UW, Gebhart B, Mermall V, Mitchell DR, Heuser JE. 1987. High-pressure liquid chromatography fractionation of Chlamydomonas dynein extracts and characterization of inner-arm dynein subunits. J Mol Biol 194:481-494.
26. Haddad A, Turkewitz AP. 1997. Analysis of exocytosis mutants indicates close coupling between regulated secretion and transcription activation in Tetrahymena. Proc Natl Acad Sci USA 94:10675-10680.
27. Hennessey TM, Kim DY, Oberski DJ, Hard R, Rankin SA, Pennock DG. 2002. Inner arm dynein 1 is essential for Ca++-dependent ciliary reversals in Tetrahymena thermophila. Cell Motil Cytoskeleton 53:281-288.
28. Johnson KA, Wall JS. 1983. Structure and molecular weight of the dynein ATPase. J Cell Biol 96:669-678.
29. Kagami O, Kamiya R. 1992. Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner-arm dynein. J Cell Sci 103:653-664.
30. Kamiya R. 1988. Mutations at twelve independent loci result in absence of outer dynein arms in Chylamydomonas reinhardtii. J Cell Biol 107:2253-2258.
31. Kamiya R. 2002. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int Rev Cytol 219:115-155.
32. Kamiya R, Okamoto M. 1985. A mutant of Chlamydomonas reinhardtii that lacks the flagellar outer dynein arm but can swim. J Cell Sci 74:181-191.
33. Kamiya R, Kurimoto E, Muto E. 1991. Two types of Chlamydomonas flagellar mutants missing different components of inner-arm dynein. J Cell Biol 112:441-447.
34. Karki S, Holzbaur EL. 1995. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J Biol Chem 270:28806-28811.
35. Karki S, Holzbaur EL. 1999. Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr Opin Cell Biol 11:45-53.
36. Karrer KM. 2000. Tetrahymena genetics: two nuclei are better than one. Methods Cell Biol 62:127-186.
37. Kato T, Kagami O, Yagi T, 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.
38. King SM. 2000. AAA domains and organization of the dynein motor unit. J Cell Sci 113:2521-2526.
39. King SM, Witman GB. 1990. Localization of an intermediate chain of outer arm dynein by immunoelectron microscopy. J Biol Chem 265:19807-19811.
40. King SM, Wilkerson CG, Witman GB. 1991. The Mr 78,000 intermediate chain of Chlamydomonas outer arm dynein interacts with alpha-tubulin in situ. J Biol Chem 266:8401-8407.
41. Koonce MP. 1997. Identification of a microtubule-binding domain in a cytoplasmic dynein heavy chain. J Biol Chem 272:19714-19718.
42. Lee S, Wisniewski JC, Dentier WL, Asai DJ. 1999. Gene knockouts reveal separate functions for two cytoplasmic dyneins in Tetrahymena thermophila. Mol Biol Cell 10:771-784.
43. Maiti AK, Mattel MG, Jorissen M, Volz A, Zeigler A, Bouvagnet P. 2000. Identification, tissue specific expression, and chromosomal localisation of several human dynein heavy chain genes. Eur J Hum Genet 8:923-932.
44. Marchese-Ragona SP, Wall JS, Johnson KA. 1988. Structure and mass analysis of 14S dynein obtained from Tetrahymena cilia. J Cell Biol 106:127-132.
45. Mastronarde DN, O'Toole ET, McDonald KL, McIntosh JR, Porter ME. 1992. Arrangement of inner dynein arms in wild-type and mutant flagella of Chlamydomonas. J Cell Biol 118:1145-1162.
46. Milisav I. 1998. Dynein and dynein-related genes. Cell Motil Cytoskeleton 39:261-272.
47. Mitchell DR. 2000. Chlamydomonas flagella. J Phycol 36:261-273.
48. Mitchell DR, Rosenbaum JL. 1985. A motile Chlamydomonas flagellar mutant that lacks outer dynein arms. J Cell Biol 100:1228-1234.
49. Mobberley PS, Sullivan JL, Angus SP, Kong X, Pennock DG. 1999. New axonemal dynein heavy chains from Tetrahymena thermophila. J Eukaryot Microbiol 46:147-154.
50. Mocz G, Gibbons IR. 1993. ATP-insensitive interaction of the amino-terminal region of the beta heavy chain of dynein with microtubules. Biochemistry 32:3456-3460.
51. Mocz G, Gibbons IR. 2001. Model for the motor component of dynein heavy chain based on homology to the AAA family of oligomeric ATPases. Structure (Camb) 9:93-103.
52. Muto E, Kamiya R, 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.
53. Muto E, Edamatsu M, Hirono M, Kamiya R. 1994. Immunological detection of actin in the 14S ciliary dynein of Tetrahymena. FEBS Lett 343:173-177.
54. Myster SH, Knott JA, O'Toole E, Porter ME. 1997. The Chlamydomonas Dhc1 gene encodes a dynein heavy chain subunit required for assembly of the II inner arm complex. Mol Biol Cell 8:607-620.
55. Myster SH, Knott JA, Wysocki KM, O'Toole E, Porter ME. 1999. Domains in the 1alpha dynein heavy chain required for inner arm assembly and flagellar motility in Chlamydomonas. J Cell Biol 146:801-818.
56. Neesen J, Koehler MR, Kirschner R, Steinlein C, Kreutzberger J, Engel W, Schmid M. 1997. Identification of dynein heavy chain genes expressed in human and mouse testis: chromosomal localization of an axonemal dynein gene. Gene 200:193-202.
57. Neesen J, Kirschner R, Ochs M, Schmiedl A, Habermann B, Mueller C, Holstein AF, Nuesslein T, Adham I, Engel W. 2001. Disruption of an inner arm dynein heavy chain gene results in asthenozoospermia and reduced ciliary beat frequency. Hum Mol Genet 10:1117-1128.
58. Neuwald AF, Aravind L, Spouge JL, Koonin EV. 1999. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27-43.
59. Ogawa K. 1991. Four ATP-binding sites in the midregion of the beta heavy chain of dynein. Nature 352:643-645.
60. Ogawa K, Mohri H. 1996. A dynein motor superfamily. Cell Struct Funct 21:343-349.
61. Paschal BM, Vallee RB. 1987. Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330:181-183.
62. Paschal BM, King SM, Moss AG, Collins CA, Vallee RB, Witman GB. 1987. Isolated flagellar outer arm dynein translocates brain microtubules in vitro. Nature 330:672-674.
63. Pennock DG, Thatcher T, Gorovsky MA. 1988. A temperature-sensitive mutation affecting cilia regeneration, nuclear development, and the cell cycle of Tetrahymena thermophila is rescued by cytoplasmic exchange. Mol Cell Biol 8:2681-2689.
64. Perrone CA, Myster SH, Bower R, O'Toole ET, Porter ME. 2000. Insights into the structural organization of the II inner arm dynein from a domain analysis of the 1beta dynein heavy chain. Mol Biol Cell 11:2297-2313.
65. Pfister KK, Witman GB. 1984. Subfractionation of Chlamydomonas 18 S dynein into two unique subunits containing ATPase activity. J Biol Chem 259:12072-12080.
66. Pfister KK, Fay RB, Witman GB. 1982. Purification and polypeptide composition of dynein ATPases from Chlamydomonas flagella. Cell Motil 2:525-547.
67. Piperno G, Luck DJ. 1979. Axonemal adenosine triphosphatases from flagella of Chlamydomonas reinhardtii. Purification of two dyneins. J Biol Chem 254:3084-3090.
68. Piperno G, Ramanis Z. 1991. The proximal portion of Chlamydomonas flagella contains a distinct set of inner dynein arms. J Cell Biol 112:701-709.
69. Piperno G, Ramanis Z, Smith EF, Sale WS. 1990. Three distinct inner dynein arms in Chlamydomonas flagella: molecular composition and location in the axoneme. J Cell Biol 110:379-389.
70. Porter ME, Power J, Dutcher SK. 1992. Extragenic suppressors of paralyzed flagellar mutations in Chlamydomonas reinhardtii identify loci that alter the inner dynein arms. J Cell Biol 118:1163-1176.
71. Porter ME, Knott JA, Myster SH, Farlow SJ. 1996. The dynein gene family in Chlamydomonas reinhardtii. Genetics 144:569-585.
72. Porter ME, Bower R, Knott JA, Byrd P, Dentier W. 1999. Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol Biol Cell 10:693-712.
73. Rasmusson K, Serr M, Gepner J, Gibbons I, Hays TS. 1994. A family of dynein genes in Drosophila melanogaster. Mol Biol Cell 5:45-55.
74. Sakakibara H, Mitchell DR, Kamiya R. 1991. A Chlamydomonas outer arm dynein mutant missing the alpha heavy chain. J Cell Biol 113:615-622.
75. Sakakibara H, Takada S, King SM, Witman GB, Kamiya R. 1993. A Chlamydomonas outer arm dynein mutant with a truncated beta heavy chain. J Cell Biol 122:653-661.
76. Sakato M, King SM. 2004. Design and regulation of the AAA+ microtubule motor dynein. J Struct Biol 146:58-71.
77. Sale WS, Satir P. 1977. Direction of active sliding of microtubules in Tetrahymena cilia. Proc Natl Acad Sci USA 74:2045-2049.
78. Sale WS, Goodenough UW, Heuser JE. 1985. The substructure of isolated and in situ outer dynein arms of sea urchin sperm flagella. J Cell Biol 101:1400-1412.
79. Sambrook J, Russell DW. 2001. Molecular laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
80. Smith EF, Sale WS. 1991. Microtubule binding and translocation by inner dynein arm subtype II. Cell Motil Cytoskeleton 18:258-268.
81. Steffen W, Hodgkinson JL, Wiche G. 1996. Immunogold localisation of the intermediate chain within the protein complex of cytoplasmic dynein. J Struct Biol 117:227-235.
82. Tanaka Y, Zhang Z, Hirokawa N. 1995. Identification and molecular evolution of new dynein-like protein sequences in rat brain. J Cell Sci 108:1883-1893.
83. Taylor HC, Satir P, Holwill ME. 1999. Assessment of inner dynein arm structure and possible function in ciliary and flagellar axonemes. Cell Motil Cytoskeleton 43:167-177.
84. Vale RD, Toyoshima YY. 1988. Rotation and translocation of microtubules in vitro induced by dyneins from Tetrahymena cilia. Cell 52:459-469.
85. Vale RD, Soll DR, Gibbons IR. 1989. One-dimensional diffusion of microtubules bound to flagellar dynein. Cell 59:915-925.
86. Vallee RB, Wall JS, Paschal BM, Shpetner HS. 1988. Microtubule-associated protein 1C from brain is a two-headed cytosolic dynein. Nature 332:561-563.
87. Vaughan KT, Mikami A, Paschal BM, Holzbaur EL, Hughes SM, Echeverri CJ, Moore KJ, Gilbert DJ, Copeland NG, Jenkins NA, Vallee RB. 1996. Multiple mouse chromosomal loci for dynein-based motility. Genomics 36:29-38.
88. Wang Z, Khan S, Sheetz MP. 1995. Single cytoplasmic dynein molecule movements: characterization and comparison with kinesin. Biophys J 69:2011-2023.
89. Witman GB, Johnson KA, Pfister KK, Wall JS. 1983. Fine structure and molecular weight of the outer arm dyneins of Chlamydomonas. J Submicrosc Cytol 15:193-197.
90. Witman GB, Wilkerson CG, King SM. 1994. The biochemistry, genetics and molecular biology of flagellar dynein. In: Hyams JS, Lloyd CW, editors. New York, NY: Wiley-Liss. p 229-249.
91. Woolley DM. 1997. Studies on the eel sperm flagellum. I. The structure of the inner dynein arm complex. J Cell Sci 110:85-94.
92. Xu W, Royalty MP, Zimmerman JR, Angus SP, Pennock DG. 1999. The dynein heavy chain gene family in Tetrahymena thermophila. J Eukaryot Microbiol 46:606-611.