Twenty-five dyneins in Tetrahymena: A re-examination of the multidynein hypothesis

Cell Motility and the Cytoskeleton

Volumn 65, Issue 4, 2008, Pages 342-351

  Wilkes, David E ^a   Watson, Hadley E ^a   Mitchell, David R ^b   Asai, David J ^a  

^a HARVEY MUDD COLLEGE   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

AAA protein; Dynein; Phylogeny; Tetrahymena

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; PROTEIN DYH1; PROTEIN DYH2; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; AXONEME; CELL MOTILITY; CHROMALVEOLATA; COMPLEX FORMATION; CONTROLLED STUDY; EUKARYOTE; EXCAVATA; GENE FUNCTION; GENETIC VARIABILITY; GENOME; GREEN ALGA; METAZOON; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; TETRAHYMENA THERMOPHILA; UNINDEXED SEQUENCE; VIRIDIPLANTAE;

AMINO ACID SEQUENCE; ANIMALS; DYNEIN ATPASE; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENES, PROTOZOAN; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT; TETRAHYMENA THERMOPHILA;

CHROMALVEOLATA; EUKARYOTA; EXCAVATA; METAZOA; TETRAHYMENA; VIRIDIPLANTAE;

EID: 41449086954     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20264     Document Type: Article

References (52)

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. Andrews KK, 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.
3. Asai DJ. 1995. Multi-dynein hypothesis. Cell Motil Cytoskeleton 32:129-132.
4. Asai DJ, Brokaw CJ. 1993. Dynein heavy chain isoforms and axonemal motility. Trends Cell Biol 3:398-402.
5. Asai DJ, Criswell PS. 1995. Identification of new dynein heavy chain genes by RNA-directed PCR. Methods Cell Biol 47:579-585.
6. Asai DJ, Wilkes DE. 2004. The dynein heavy chain family. J Eukaryot Microbiol 51:23-29.
7. 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.
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. Burgess SA, Carter DA, Dover SD, Woolley DM. 1991. The inner arm complex: Compatible images from freeze-etch and thin section methods of microscopy. J Cell Sci 100:319-328.
10. Calzone FJ, Gorovsky MA. 1982. Cilia regeneration in Tetrahymena. A simple reproducible method for producing large numbers of regenerating cells. Exp Cell Res 140:471-476.
11. Cavalier-Smith T. 2002. The phagotropic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297-354.
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. Eck RV, Dayhoff MO. 1966. Atlas of Protein Sequence and Structure. Silver springs, MD: National Biomedical Research Foundation.
14. 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, Majores WH, Farzad M, Carlton JM, Smith RK Jr, Garg J, Pearlman RE, Karrer KM, Sun L, Manning G, Elde NC, Turkewitz AP, Asai DJ, Wilkes 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 JM, 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.
15. Fliegauf M, Olbrich H, Horvath J, Wildhaber JH, Zariwala MA, Kennedy M, Knowles MR, Orman H. 2005. Mislocalization of DNAH5 and DNAH9 in respiratory cells from patients with primary ciliary dyskinesia. Am J Respir Crit Care Med 171:1343-1349.
16. Gibbons BH, Asai DJ, Tang WJY, Hays TS, Gibbons IR. 1994. Phytogeny 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. 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 100:2008-2018.
19. Jekely G, Arendt D. 2006. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 28:191-198.
20. Kamiya R. 2002. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int Rev Cytol 219:115-155.
21. Koonce MP, Samsó M. 2004. Of rings and levers: The dynein motor comes of age. Trends Cell Biol 14:612-619.
22. Kumar S, Tamura K, Jakobsen IB, Nei M. 2001. MEGA2: Molecular Evolutionary Genetics Analysis software. Tempe, AZ: Arizona State University.
23. 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.
24. Lincoln LM, Gibson TM, Lee SW, Forney JD, Asai DJ. 1998. The characterization and targeted disruption of the dynein beta heavy chain in Tetrahymena thermophila. Mol Biol Cell 9(S): 899.
25. Mitchell DR. 2004. Speculations on the evolution of 9+2 organelles and the role of central pair microtubules. Biol Cell 96:691-696.
26. Mitchell DR. 2007. The evolution of eukaryotic cilia and flagella as motile and sensory organelles. Adv Exp Med Biol 607:130-140.
27. 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.
28. Morris RL, Hoffman MP, Obar RA, McCafferty SS, Gibbons IR, Leone AD, Cool J, Allgood EL, Musante AM, Judkins KM, Rossetti BJ, Rawson AP, Burgess DR. 2006. Analysis of cytoskeletal and motility proteins in the sea urchin genome assembly. Dev Biol 300:219-237.
29. 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.
30. Nicastro D, Schwartz C, Pierson J, Gaudette R, Porter ME, McIntosh JR. 2006. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313:944-948.
31. Ogawa K, Mohri H. 1996. A dynein motor superfamily. Cell Struct Funct 21:343-349.
32. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
33. Pfister KK, Shah PR, Hummerich H, Russ A, Cotton J, Annuar AA, King SM, Fisher EMC. 2006. Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet 2:e1.
34. Piperno G. 1990. Functional diversity of dyneins. Cell Motil Cytoskeleton 17:147-149.
35. 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.
36. Piperno G, Ramamis 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.
37. Porter ME. 1996. Axonemal dyneins: Assembly, organization, and regulation. Curr Opin Cell Biol 8:10-17.
38. Porter ME, Knott JA, Myster SH, Farlow SJ. 1996. The dynein gene family in Chlamydomonas reinhardtii. Genetics 14:569-585.
39. Rasmussen K, Serr M, Gepner J, Gibbons I, Hays TS. 1994. A family of dynein genes in Drosophila melanogaster. Mol Biol Cell 5:45-55.
40. Rosenbaum JL, Witman GB. 2002. Intraflagellar transport. Nat Rev Mol Cell Biol 3:813-825.
41. Sailaja G, Lincoln LM, Chen J, Asai DJ. 2001. Evaluating the dynein heavy chain gene family in Tetrahymena. Methods Mol Biol 161:17-27.
42. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
43. Sakakibara H, Kojima H, Sakai Y, Katayama E, Oiwa K. 1999. Inner-arm dynein c of Chlamydomonas flagella is a single-headed processive motor. Nature 400:586-590.
44. Scholey JM. 2003. Intraflagellar transport. Annu Rev Cell Dev Biol 19:423-443.
45. 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.
46. Sokal RR, Michener CD. 1958. A statistical method for evaluating systematic relationships. Univ Kans Sci Bull 28:1409-1438.
47. 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.
48. Vale RD. 2003. The molecular motor toolbox for intracellular transport. Cell 112:467-480.
49. Vernon GG, Neesen J, Woolley DM. 2005. Further studies on knockout mice lacking a functional dynein heavy chain (MDHC7). I. Evidence for a structural deficit in the axoneme. Cell Motil Cytoskeleton 61:65-73.
50. Warner FD, Perreault JG, McIlvain JH. 1985. Rebinding of Tetrahymena 13S and 21S dynein ATPases to extracted doublet microtubules. The inner row and outer row dynein arms. J Cell Sci 77:263-287.
51. Woolley DM. 1997. Studies on the eel sperm flagellum. I. The structure of the inner dynein arm complex. J Cell Sci 110:85-94.
52. 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.