Three-dimensional organization of basal bodies from wild-type and δ-tubulin deletion strains of Chlamydomonas reinhardtii

Molecular Biology of the Cell

Volumn 14, Issue 7, 2003, Pages 2999-3012

  O'Toole, Eileen T ^a   Giddings, Thomas H ^a   McIntosh, J Richard ^a   Dutcher, Susan K ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA TUBULIN; ISOPROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CELL STRUCTURE; CELL TYPE; CHLAMYDOMONAS REINHARDTII; FLAGELLUM; GENE DELETION; KINETOSOME; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; STELLATE CELL; STRAIN DIFFERENCE; STRUCTURE ANALYSIS; SUPPRESSOR CELL; THREE DIMENSIONAL IMAGING; TOMOGRAPHY;

ANIMALS; CENTRIOLES; CHLAMYDOMONAS REINHARDTII; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, ELECTRON; MICROTUBULES; MUTATION; TUBULIN;

ALGAE; CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; PROTOZOA;

EID: 0038159661     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-11-0755     Document Type: Article

References (46)

1. Adams, G.M.W., Wright, R.L., and Jarvik, J.W. (1985). Defective temporal and spatial control of flagellar assembly in a mutant of Chlamydomonas reinhardtii with variable flagellar number. J. Cell Biol. 100, 955-964.
2. Bullitt, E., Rout, M.P., Kilmartin, J.V., and Akey, C.W. (1997). The yeast spindle pole body is assemble around a central crystal of Spc42p. Cell 89, 1077-1086.
3. Cavalier-Smith, T. (1974). Basal bodies and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardtii. J. Cell Sci. 16, 529-556.
4. Chang, P., and Stearns, T. (2000). δ-Tubulin and ε-tubulin: two new human centrosomal tubulins reveal new aspects of centrosome structure and function. Nat. Cell Biol. 2, 30-35.
5. Dippel, R.V. (1968). The development of basal bodies in Paramecium. Proc. Natl. Acad. Sci. USA 61, 461-468.
6. Doxsey, S. (2001). Re-evaluating centrosome function. Nat. Rev. Mol. Cell. Biol. 2, 688-698.
7. Dutcher, S.K. (2001). The tubulin fraternity: alpha to eta. Curr. Opin. Cell Biol. 13, 49-54.
8. Dutcher, S.K., Morrissette, N.S., Preble, A.M., Rackley, C., and Stanga, J. (2002). Epsilon tubulin is an essential component of the centriole. Mol. Biol. Cell 13, 3859-3869.
9. Dutcher, S.K., and Trabuco, E.C. (1998). The UNI3 gene is required for assembly of basal bodies of Chlamydomonas and encodes δ-tubulin, a new member of the tubulin superfamily. Mol. Biol. Cell 9, 1293-1308.
10. Ehler, L.L., Holmes, J.A., and Dutcher, S.K. (1995). Loss of spatial control of the mitotic spindle apparatus in a Chlamydomonas reinhardtii mutant strain lacking basal bodies. Genetics 141, 945-960.
11. Frank, J. (1992). Introduction: principles of electron tomography. In: Electron Tomography: Three Dimensional Imaging with the Transmission Electron Microscope, ed. J. Frank, New York: Plenum Press, 1-13.
12. Garreau de Loubresse, N., Ruiz, F., Beisson, J., and Klotz, C. (2001). Role of delta-tubulin and the C-tubule in assembly of Paramecium basal bodies. BMC Cell Biol. 2, 4-10.
13. Goodenough, U. W., and St. Clair, H. S. (1975). BALD-2: a mutation affecting the formation of doublet and triplet sets of MTs in Chlamydomonas reinhardtii. J. Cell Biol. 66:480-491.
14. Holmes, J.A., and Dutcher, S.K. (1989). Cellular asymmetry in Chlamydomonas reinhardtii. J. Cell Sci. 94, 273-285.
15. Hoops, H.J., and Witman, G.B. (1983). Outer doublet heterogeneity reveals structural polarity related to beat direction in Chlamydomonas flagella. J. Cell Biol. 97, 902-908.
16. Huang, B., Ramanis, Z., Dutcher, S., and Luck, D.L. (1982). Uniflagellar mutants of Chlamydomonass: evidence for the role of basal bodies in transmission of positional information. Cell 29, 745-753.
17. Johnson, U.G., and Porter, K.R. (1968). Fine structure of cell division in Chlamydomonas reinhardtii. Basal bodies and microtubules. J. Cell Biol. 38, 403-425.
18. Kellogg, D.R., Moritz, M., and Alberts, B.A. (1994). The centrosome and cellular organization. Annu. Rev. Biochem. 63, 639-674.
19. Kremer, J.R., Mastronarde, D.N., and McIntosh, J.R. (1996). Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76.
20. Ladinsky, M.S., Kremer, J.R., Furcinitti, P.S., McIntosh, J.R., and Howell, K.E. (1994). HVEM tomography of the trans-Golgi network: structural insights and identification of a lace-like vesicle coat. J. Cell Biol. 127, 29-38.
21. Ladinsky, M.S., Mastronarde, D.N., McIntosh, J.R., Howell, K.E., and Staehelin, L.A. (1999). Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144, 1135-1149.
22. Lange, B.M., and Gull, K. (1995). Molecular marker for centriole maturation in the mammalian cell cycle. J. Cell Biol. 130, 919-927.
23. Lechtreck, K-F., Teltenkötter, A., and Grunow, A. (1999). A 210 kDa protein is located in a membrane-microtubule linker at the distal end of mature and nascent basal bodies. J. Cell Sci. 112, 1633-1644.
24. LeDizet, M., and Piperno, G. (1986). Cytoplasmic microtubules containing acetylated alpha-tubulin in Chlamydomonas reinhardtii: spatial arrangement and properties. J. Cell Biol. 103, 13-22.
25. Marsh, B.J., Mastronarde, D.N., Buttle, K.F., Howell, K.E., and McIntosh, J.R. (2001). Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc. Natl. Acad. Sci. USA 98, 2399-2406.
26. Mastronarde, D.N. (1997). Dual-axis tomography: an approach with alignment methods that preserve resolution. J. Struct. Biol. 120, 343-352.
27. Moritz, M., Braunfeld, M.B., Fung, J.C., Sedat, J.W., Alberts, B.M., and Agard, D.A. (1995a). Three-dimensional structural characterization of centrosomes from early Drosophila embryos. J. Cell Biol. 130, 1149-1159.
28. Moritz, M., Braunfeld, M.B., Guenebaut, V., Heuser, J., and Agard, D.A. (2000). Structure of the γ-tubulin ring complex: a template for microtubule nucleation. Nat. Cell Biol. 2, 365-370.
29. Moritz, M., Braunfeld, M.B., Sedat, J.W., Alberts, B., and Agard, D.A. (1995b). Microtuble nucleation by γ-tubulin-containing rings in the centrosome. Nature 378, 638-640.
30. Oakley, B.R. (2000). An abundance of tubulins. Trends Cell. Biol. 10, 537-542.
31. O'Toole, E.T., Winey, M., and McIntosh, J.R. (1999). High voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 10, 2017-2031.
32. Piel, M., Meyer, P., Khodjakov, A., Reider, C.L., and Bornens, M. (2000). The respective contributions of mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149, 317-329.
33. Preble, A.M., Giddings, T.H., and Dutcher, S.K. (2000). Basal bodies and centrioles: their function and structure. Curr. Top. Dev. Biol. 49, 207-233.
34. Preble, A.M., Giddings, T.H., and Dutcher, S.K. (2001). Extragenic bypass supressors of mutations in the essential gene BLD2 promote assembly of basal bodies with abnormal microtubules in Chlamydomonas reinhardtii. Genetics 157, 163-181.
35. Quarmby, L.M., and Lohret, T.A. (1999). Microtubule severing. Cell Motil. Cytoskeleton 43, 1-9.
36. Ringo, D.L. (1967). Flagellar motion and fine structure of the flagellar apparatus in Chlamydomonas. J. Cell Biol. 33, 543-571.
37. Salisbury, J.L., Baron, A.T., and Sanders, M.A. (1988). The centrin-based cytoskeleton of Chlamydomonas reinhardtii: distribution in interphase and mitotic cells. J. Cell Biol. 107, 635-641.
38. Sanders, M.A., and Salisbury, J.L. (1989). Centrin-mediated microtubule severing during flagellar excision in Chlamydomonas reinhardtii. J. Cell Biol. 108, 1751-1760.
39. Sanders, M.A., and Salisbury, J.L. (1994). Centrin plays an essential role in microtubule severing during flagellar excision in Chlamydomonas reinhardtii. J. Cell Biol. 124, 795-805.
40. Schiebel E. (2000). Two new tubulins differ in a split decision. Nat. Cell Biol. 2, E3-E4.
41. Silflow, C.D., Liu, B., LaVoie, M., Richardson, E.A., and Palevitz, B.A. (1999). γ-Tubulin in Chlamydomonas: characterization of the gene and localization of the gene product in cells. Cell Motil. Cytoskeleton 42, 285-297.
42. Silflow, C. D., LaVoie, M., Tam L-W., Tousey, S., Sanders, M., Wu, W., Borodovsky, M., and Lefebvre, P.A. (2001). The Vfl1 protein in Chlamydomonas localizes in a rotationally asymmetric pattern at the distal ends of basal bodies. J. Cell Biol. 153, 63-74.
43. Smrzka, O.W., Delgehyr, N., and Bornens, M. (2000). Tissue-specific expression and subcellular localization of mammalian δ-tubulin. Curr. Biol. 10, 413-416.
44. Taillon, B.E., Adler, S.A., Suhan, J.P., and Jarvik, J.W. (1992). Mutational analysis of centrin: an EF-hand protein associated with three distinct contractile fibers in the basal body apparatus of Chlamydomonas. J. Cell Biol. 119, 1613-1624.
45. Wright, R.L., Chojnacki, B., and Jarvik, J.W. (1983). Abnormal basal-body number, location, and orientation in a striated fiber-defective mutant of Chlamydomonas reinhardtii. J. Cell Biol. 96, 1697-1707.
46. Wright, R.L., Salisbury, J., and Jarvik, J.W. (1985). A nucleus-basal body connector in Chlamydomonas reinhardtii that may function in basal body localization or segregation. J. Cell Biol. 101, 1903-1912.