Dynein light chain family in Tetrahymena thermophila

Cell Motility and the Cytoskeleton

Volumn 64, Issue 2, 2007, Pages 82-96

  Wilkes, David E ^a   Rajagopalan, Vidyalakshmi ^b   Chan, Clarence W C ^a   Kniazeva, Ekaterina ^a   Wiedeman, Alice E ^a   Asai, David J ^a  

^a HARVEY MUDD COLLEGE   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

ATPase; Axoneme; Cilia; Motor protein

Indexed keywords

CELL PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; DYNEIN LIGHT CHAIN 2; DYNEIN LIGHT CHAIN 4; DYNEIN LIGHT CHAIN 5; DYNEIN LIGHT CHAIN 6; DYNEIN LIGHT CHAIN 7; DYNEIN LIGHT CHAIN 8; ISOPROTEIN; MOLECULAR MOTOR; PROTEIN P28; PROTEIN TCTEX1; PROTOZOAL PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHLAMYDOMONAS; CILIARY MOTILITY; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENOME ANALYSIS; HUMAN; LIGHT CHAIN; MICROTUBULE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEOMICS; PROTOZOAL GENETICS; QUANTITATIVE ASSAY; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TETRAHYMENA THERMOPHILA; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; CILIA; CONSENSUS SEQUENCE; DYNEIN ATPASE; GENE EXPRESSION REGULATION; GENOME, PROTOZOAN; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN ISOFORMS; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TETRAHYMENA THERMOPHILA; UP-REGULATION;

CHLAMYDOMONAS; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 33846208299     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20165     Document Type: Article

References (86)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389-3402.
2. Asai DJ, Koonce MP. 2001. The dynein heavy chain: Structure, mechanics and evolution. Trends Cell Biol 11:196-202.
3. Asai DJ, Wilkes DE. 2004. The dynein heavy chain family. J Eukaryot Microbiol 51:23-29.
4. Barkalow K, Hamasaki T, Satir P. 1994. Regulation of 22S dynein by a 29-kD light chain. J Cell Biol 126:727-735.
5. Benashski SE, Harrison A, Patel-King RS, King SM. 1997. Dimerization of the highly conserved light chain shared by dynein and myosin V. J Biol Chem 272:20929-20935.
6. Benashski SE, Patel-King RS, King SM. 1999. Light chain 1 from the Chlamydomonas outer dynein arm is a leucine-rich repeat protein associated with the motor domain of the γ heavy chain. Biochemistry 38:7253-7264.
7. Bowman AB, Patel-King RS, Benashski SE, McCaffery JM, Goldstein LSB, King SM. 1999. Drosophila roadblock and Chlamydomonas LC7: A conserved family of dynein-associated proteins involved in axonal transport, flagellar motility, and mitosis. J Cell Biol 146:165-179.
8. Bruns PJ, Cassidy-Hanley D. 2000. Biolistic transformation of macro- and micronuclei. Methods Cell Biol 62:501-512.
9. Burgess SA, Walker ML, Sakakibara H, Knight PJ, Oiwa K. 2003. Dynein structure and power stroke. Nature 421:715-718.
10. Calzone FJ, Oorovsky MA. 1982. Cilia regeneration in Tetrahymena. A simple reproducible method for producing large numbers of regenerating cells. Exp Cell Res 140:471-476.
11. Chilcote TJ, Johnson KA. 1990. Phosphorylation of Tetrahymena 22S dynein. J Biol Chem 265:17257-17266.
12. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294-5299.
13. Christensen ST, Guerra C, Wada Y, Valentin T, Angeletti RH, Satir P, Hamasaki T. 2001. A regulatory light chain of ciliary outer arm dynein in Tetrahymena thermophila. J Biol Chem 276:20048-20054.
14. Collins K, Gorovsky MA. 2006. Tetrahymena thermophila. Curr Biol 15:R317-R318.
15. DiBella LM, Sakato M, Patel-King RS, Pazour GJ, King SM. 2004a. The LC7 light chains of Chlamydomonas flagellar dyneins interact with components required for both motor assembly and regulation. Mol Biol Cell 15:4633-4646.
16. DiBella LM, Smith EF, Patel-King RS, Wakabayashi K-I, King SM. 2004b. A novel Tctex2-related light chain is required for stability of inner dynein arm I1 and motor function in the Chlamydomonas flagellum. J Biol Chem 279:21666-21676.
17. DiBella LM, Gorbatyuk O, Sakato M, Wakabayashi K-I, Patel-King RS, Pazour GJ, Witman GB, King SM. 2005. Differential light chain assembly influences outer arm dynein motor function. Mol Biol Cell 16:5661-5674.
18. Dick T, Ray K, Salz HK, Chia W. 1996. Cytoplasmic dynein (ddlc1) mutations cause morphogenetic defects and apoptotic cell death in Drosophila melanogaster. Mol Cell Biol 16:1966-1977.
19. Eck RV, Dayhoff MO. 1966. Atlas of Protein Sequence and Structure. Silver springs, MD: National Biomedical Research Foundation.
20. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M, Wortman JR, Badger JH, Ren Q, Amedeo P, Jones KM, Tallon LJ, Delcher AL, Salzberg SL, Silva JC, Haas BJ, Majoros WH, Farzad M, Carlton JM, Smith RK Jr, Garg J, Pearlman RE, Karrer KM, Sun L, Manning G, Eide NC, Turkewitz AP, Asai DJ, Wilkes DE, Wang DE, Wang Y, Cai H, Collins K, Stewart BA, Lee SR, Wilamowska K, Weinberg Z, Ruzzo WL, Wloga D, Gaertig J, Frankel J, Tsao CC, Gorovsky MA, Keeling PJ, Waller RF, Patron NJ, Cherry M, Stover NA, Krieger CJ, del Toro C, Ryder HF, Williamson SC, Barbeau RA, Hamilton EP, Orias E. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4:e286.
21. Espindola FS, Suter DM, Partata LBE, Cao T, Wolenski JS, Cheney RE, King SM, Mooseker MS. 2000. The light chain composition of chicken brain myosin-Va: Calmodulin, myosin-II essential light chains, and 8-kDa dynein light chain/PIN. Cell Motil Cytoskeleton 47:269-281.
22. Gaertig J. 2000. Molecular mechanism of microtubular organelle assembly in Tetrahymena. J Eukaryot Microbiol 47:185-190.
23. Gaertig J, Fleury A. 1992. Spatio-temporal reorganization of intracytoplasmic microtubules is associated with nuclear selection and differentiation during the developmental process in Tetrahymena thermophila. Protoplasma 167:74-87.
24. Gibbons BH, Asai DJ, Tang WJY, Hays TS, Gibbons IR. 1994. Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins. Mol Biol Cell 5:57-70.
25. Gibbons IR, Lee-Eiford A, Mocz G, Phillipson CA, Tang WY, 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.
26. Gingras D, White D, Garin J, Multigner L, Job D, Cosson J, Huitore P, Zingg H, Dumas F, Gagnon C. 1996. Purification, cloning, and sequence analysis of a Mr=30,000 protein from sea urchin axonemes that is important for sperm motility. J Biol Chem 271:12807-12813.
27. Goodenough UW. 1983. Motile detergent-extracted cells of Tetrahymena and Chlamydomonas. J Cell Biol 96:1610-1621.
28. Goodenough UW, Heuser J. 1984. Structural comparison of purified dynein proteins with in situ dynein arms. J Mol Biol 180:1083-1118.
29. Hai B, Gaertig J, Gorovsky MA. 2000. Knockout heterokaryons enable facile mutagenic analysis of essential genes in Tetrahymena. Methods Cell Biol 62:513-531.
30. Hamasaki T, Barkalow K, Richmond J, Satir P. 1991. cAMP-stimulated phosphorylation of an axonemal polypedtide that co-purifies with the 22S dynein arm regulates microtubule translocation velocity and swimming speed in Paramecium. Proc Natl Acad Sci USA 88:7918-7922.
31. Harrison A, Olds-Clarke P, King SM. 1998. Identification of the t complex-encoded cytoplasmic dynein light chain Tctex1 in inner arm I1 supports the involvement of flagellar dyneins in meiotic drive. J Cell Biol 140:1137-1147.
32. Harrison A, Sakato M, Tedford HW, Benashski SE, Patel-King RS, King SM. 2002. Redox-based control of the γ heavy chain ATPase from Chlamydomonas outer arm dynein. Cell Motil Cytoskeleton 52:131-143.
33. Inaba K, Morisawa S, Morisawa M. 1998. Proteasomes regulate the motility of salmonid fish sperm through modulation of cAMP-dependent phosphorylation of an outer arm dynein light chain. J Cell Sci 111:1105-1115.
34. Jaffery SR, Snyder SH. 1996. PIN: An associated protein inhibitor of neuronal nitric oxide synthase. Science 274:774-777.
35. Jiang J, Yu L, Huang X, Chen X, Li D, Zhang Y, Tang L, Zhao S. 2001. Identification of two novel human dynein light chain genes. DNLC2A and DNLC2B, and their expression changes in hepatocellular carcinoma tissues from 68 Chinese patients. Gene 281:103-113.
36. Kagami O, Gotoh M, Makino Y, Mohri H, Kamiya R, Ogawa K. 1998. A dynein light chain of sea urchin sperm flagella is a homolog of mouse Tctex1, which is encoded by a gene of the t complex sterility locus. Gene 211:383-386.
37. Kai N, Mishina M, Yagi T. 1997. Molecular cloning of Fyn-associated molecules in the mouse central nervous system. J Neurosci Res 48:407-424.
38. Kamiya R. 2002. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int Rev Cytol 219:115-155.
39. Karrer KM. 2000. Tetrahymena genetics: Two nuclei are better than one. Methods Cell Biol 62:127-186.
40. Kastury K, Taylor WE, Shen R, Arver S, Gutierrez M, Fisher CE, Coucke PJ, Van Hauwe P, Van Camp G, Bhasin S. 1997. Complementary deoxyribonucleic acid cloning and characterization of a putative human axonemal dynein light chain gene. J Clin Endocrinol Metab 82:3047-3053.
41. King SM. 2000. The dynein microtubule motor. Biochim Biophys Acta 1496:60-75.
42. King SM, Patel-King RS. 1995a. The Mr=8,000 and 11,000 outer arm dynein light chains from Chlamydomonas flagella have cytoplasmic homologues. J Biol Chem 270:11445-11452.
43. 2+- binding light chain within Chlamydomonas outer arm dynein. J Cell Sci 108:3757-3764.
44. King SM, Barbarese E, Dillman JF III, PatelhyphenKing RS, Carson JH, Pfister KK. 1996a. Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved Mr 8,000 light chain. J Biol Chem 271:19358-19366.
45. King SM, Dillman JF III, Benashski SE, Lye RJ, Patel-King RS, Pfister KK. 1996b. The mouse t-complex-encoded protein Tctex-1 is a light chain of brain cytoplasmic dynein. J Biol Chem 271:32281-32287.
46. King SM, Barbarese E, Dillman JF III, Benashski SE, Do KT, Patel-King RS, Pfister KK. 1998. Cytoplasmic dynein contains a family of differentially expressed light chains. Biochemistry 37:15033-15041.
47. Koonce MP. 1997. Identification of a microtubule-binding domain in a cytoplasmic dynein heavy chain. J Biol Chem 242:19714-19718.
48. Koonce MP, Samso M. 2004. Of rings and levers: The dynein motor comes of age. Trends Cell Biol 14:612-619.
49. Koonce MP, Tikhonenko I. 2000. Functional elements within the dynein microtubule-binding domain. Mol Biol Cell 11:523-529.
50. Kumar S, Tamura K, Jakobsen IB, Nei M. 2001. MEGA2: Molecular Evolutionary Genetics Analysis software. Tempe, AZ: Arizona State University.
51. LeDizet M, Piperno O. 1995. The light chain p28 associates with a subset of inner dynein arm heavy chains in Chlamydomonas axonemes. Mol Biol Cell 6:697-711.
52. Lee SW, Wisniewski JC, Dentler WL, Asai DJ. 1999. Gene knockouts reveal separate functions for two cytoplasmic dyneins in Tetrahymena thermophila. Mol Biol Cell 10:771-784.
53. Lincoln LM, Gibson TM, Lee SW, Forney JD, Asai DJ. 1998. The characterization and targeted disruption of the dynein β heavy chain in Tetrahymena thermophila. Mol Biol Cell 9(Suppl):899.
54. Lindemann CB, Goltz JS. 1988. Calcium regulation of flagellar curvature and swimming pattern in Triton X-100- extracted rat sperm. Cell Motil Cytoskeleton 10:420-431.
55. Liu B, Xiang X, Lee Y-RJ. 2003. The requirement of the LC8 dynein light chain for nuclear migration and septum positioning is temperature dependent in Aspergillus nidulans. Mol Microbiol 47:291-301.
56. 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 9:93-103.
57. Mou T, Krass JR, Fung ET, Swope SL. 1998. Identification of a dynein molecular motor component in Torpedo electroplax; binding and phosphorylation of Tctex-1 by Fyn. FEBS Lett 435:275-281.
58. Naisbitt S, Valtschanoff J, Allison DW, Sala C, Kim E, Craig AM, Weinberg RJ, Sheng M. 2000. Interaction of the postsynaptic density-95/guanylate kinase domain- associated protein complex with a light chain of myosin-V and dynein. J Neurosci 20:4524-4534.
59. Navarro-Lerida I, Moreno MM, Roncal F, Gavilanes F, Albar JP, Rodriguez-Crespo I. 2004. Proteomic identification of brain proteins that interact with dynein light chain LC8. Proteomics 4:339-346.
60. Nikulina K, Patel-King RS, Takebe S, Pfister KK, King SM. 2004. The roadblock light chains are ubiquitous components of cytoplasmic dynein that form homo- and heterodimers. Cell Motil Cytoskeleton 57:233-245.
61. Nishiura M, Kon T, Shiroguchi K, Ohkura R, Shima T, Toyoshima YY, Sutoh K. 2004. A single-headed recombinant fragment of Dictyostelium cytoplasmic dynein can drive robust sliding of microtubules. J Biol Chem 279:22799-22802.
62. Ogawa K, Takai H, Ogiwara A, Yokota E, Shimizu T, Inaba K, Mohri H. 1996. Is outer arm dynein intermediate chain 1 multifunctional? Mol Biol Cell 7:1895-1907.
63. Patel-King RS, Benashski SE, Harrison A, King SM. 1996. Two functional thioredoxins containing redox-sensitive vicinal dithiols from the Chlamydomonas outer dynein arm. J Biol Chem 271:6283-6291.
64. Patel-King RS, Benashski SE, Harrison A, King SM. 1997. A Chlamydomonas homologue of the putative murine t complex distorter Tctex-2 is an outer arm dynein light chain. J Cell Biol 137:1081-1090.
65. Pazour GJ, Witman GB. 2000. Forward and reverse genetic analysis of microtubule motors in Chlamydomonas. Methods 22:285-298.
66. Pazour GJ, Wilkerson CG, Witman GB. 1998. A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT). J Cell Biol 141:979-992.
67. Pazour GJ, Koutoulis A, Benashski SE, Dickert BL, Sheng H, Patel-King RS, King SM, Witman GB. 1999. LC2, the Chlamydomonas homologue of the t complex-encoded protein Tctex2, is essential for outer dynein arm assembly. Mol Biol Cell 10:3507-3520.
68. Pazour GJ, Agrin N, Laszyk J, Witman GB. 2005. Proteomic analysis of a eukaryotic cilium. J Cell Biol 170:103-113.
69. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT- PCR. Nucleic Acids Res 29:e45.
70. Pfister KK, Fay RB, Witman GB. 1982. Purification and polypeptide composition of dynein ATPases from Chlamydomonas flagella. Cell Motil 2:525-547.
71. Porter ME. 1996. Axonemal dyneins: Assembly, organization, and regulation. Curr Opin Cell Biol 8:10-17.
72. Rompolas P, Patel-King RS, Gorbatyuk O, Wakabayashi K, Pazour GJ, King SM. 2005. Identification of a third member of the LC8 family of dynein light chains in Chlamydomonas flagella. Mol Biol Cell 16(Suppl):263a.
73. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
74. Sakato M, King SM. 2003. Calcium regulates ATP-sensitive microtubule binding by Chlamydomonas outer arm dynein. J Biol Chem 278:43571-43579.
75. Sakato M, King SM. 2004. Design and regulation of the AAA+ microtubule motor dynein. J Struct Biol 146:58-71.
76. Shang Y, Song X, Bowen J, Corstanje R, Gao Y, Gaertig J, Gorovsky MA. 2002. A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and over-expression of homologous and heterologous genes in Tetrahymena thermophila. Proc Natl Acad Sci USA 99:3734-3739.
77. Smith JC, Northey JGB, Garg J, Pearlman RE, Siu KWM. 2005. Robust method for proteome analysis by MS/MS using an entire translated genome: Demonstration on the ciliome of Tetrahymena thermophila. J Proteome Res 4:909-919.
78. Sokal RR, Michener CD. 1958. A statistical method for evaluating systematic relationships. Univ Kansas Sci Bull 28:1409-1438.
79. Tai AW, Chuang J-Z, Bode C, Wolfrum U, Sung C-H. 1999. Rhodopsin's carboxy- terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1. Cell 97:877-887.
80. Tai AW, Cuang J-Z, Sung C-H. 2001. Cytoplasmic dynein regulation by subunit heterogeneity and its role in apical transport. J Cell Biol 153:1499-1509.
81. Toba S, Gibson TM, Shiroguchi K, Toyoshima YY, Asai DJ. 2004. Properties of the full- length heavy chains of Tetrahymena ciliary outer arm dynein separated by urea treatment. Cell Motil Cytoskeleton 58:30-38.
82. Vale RD. 2003. The molecular motor toolbox for intracellular transport. Cell 112:467-480.
83. Wilson MJ, Salata MW, Susalka SJ, Pfister KK. 2001. Light chains of mammalian cytoplasmic dynein: Identification and characterization of a family of LC8 light chains. Cell Motil Cytoskeleton 49:229-240.
84. Wu H, King SM. 2003. Backbone dynamics of dynein light chains. Cell Motil Cytoskeleton 54:267-273.
85. Wu H, Blackledge M, Maciejewski MW, Mullen GP, King SM. 2003. Relaxation-based structure refinement and backbone molecular dynamics of the dynein motor domain-associated light chain. Biochemistry 42:57-71.
86. Yang P, Diener DR, Rosenbaum JL, Sale WS. 2001. Localization of calmodulin and dynein light chain LC8 in flagellar radial spokes. J Cell Biol 153:1315-1325.