Molecular characterization of centriole assembly in ciliated epithelial cells

Journal of Cell Biology

Volumn 178, Issue 1, 2007, Pages 31-42

  Vladar, Eszter K ^a   Stearns, Tim ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MOLECULAR MARKER;

ANIMAL CELL; ARTICLE; AXONEME; CELL ACTIVITY; CELL CULTURE; CELL GRANULE; CELL MEMBRANE; CELL STRUCTURE; CENTRIOLE; CENTROSOME; CILIATED EPITHELIUM; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; EPITHELIUM CELL; FLAGELLUM; KINETOSOME; MAMMAL CELL; MORPHOLOGICAL TRAIT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SPINDLE CELL; TRACHEA MUCOSA; UPREGULATION;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE; CELLS, CULTURED; CENTRIOLES; CILIA; CROSSES, GENETIC; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GREEN FLUORESCENT PROTEINS; HUMANS; LENTIVIRUS; LENTIVIRUS INFECTIONS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NIH 3T3 CELLS; TRACHEA; TRANSDUCTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA;

EID: 34347394349     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200703064     Document Type: Article

References (52)

1. Avidor-Reiss, T., A.M. Maer, E. Koundakjian, A. Polyanovsky, T. Keil, S. Subramaniam, and C.S. Zuker. 2004. Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell. 117:527-539.
2. Borok, Z., J.E. Harboe-Schmidt, S.L. Brody, Y. You, B. Zhou, X. Li, P.M. Cannon, K.J. Kim, E.D. Crandall, and N. Kasahara. 2001. Vesicular stomatitis virus G-pseudotyped lentivirus vectors mediate efficient apical transduction of polarized quiescent primary alveolar epithelial cells. J. Virol. 75:11747-11754.
3. Chapman, M.J., M.F. Dolan, and L. Margulis. 2000. Centrioles and kinetosomes: form, function, and evolution. Q. Rev. Biol. 75:409-429.
4. Christensen, S.T., C.F. Guerra, A. Awan, D.N. Wheatley, and P. Satir. 2003. Insulin receptor-like proteins in Tetrahymena thermophila ciliary membranes. Curr. Biol. 13:R50-R52.
5. Dammermann, A., and A. Merdes. 2002. Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J. Cell Biol. 159:255-266.
6. Dammermann, A., T. Muller-Reichert, L. Pelletier, B. Habermann, A. Desai, and K. Oegema. 2004. Centriole assembly requires both centriolar and pericentriolar material proteins. Dev. Cell. 7:815-829.
7. Dirksen, E.R. 1991. Centriole and basal body formation during ciliogenesis revisited. Biol. Cell. 72:31-38.
8. Dull, T., R. Zufferey, M. Kelly, R.J. Mandel, M. Nguyen, D. Trono, and L. Naldini. 1998. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:8463-8471.
9. Dutcher, S.K., and E.C. Trabuco. 1998. The UNI3 gene is required for assembly of basal bodies of Chlamydomonas and encodes delta-tubulin, a new member of the tubulin superfamily. Mol. Biol. Cell. 9:1293-1308.
10. Follenzi, A., L.E. Ailles, S. Bakovic, M. Geuna, and L. Naldini. 2000. Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat. Genet. 25:217-222.
11. Garreau de Loubresse, N., F. Ruiz, J. Beisson, and C. Klotz. 2001. Role of delta-tubulin and the C-tubule in assembly of Paramecium basal bodies. BMC Cell Biol. 2:4.
12. Gomperts, B.N., X. Gong-Cooper, and B.P. Hackett. 2004. Foxj1 regulates basal body anchoring to the cytoskeleton of ciliated pulmonary epithelial cells. J. Cell Sci. 117:1329-1337.
13. Hagiwara, H., N. Ohwada, and K. Takata. 2004. Cell biology of normal and abnormal ciliogenesis in the ciliated epithelium. Int. Rev. Cytol. 234:101-141.
14. Jurczyk, A., A. Gromley, S. Redick, J. San Agustin, G. Witman, G.J. Pazour, D.J. Peters, and S. Doxsey. 2004. Pericentrin forms a complex with intra-flagellar transport proteins and polycystin-2 and is required for primary cilia assembly. J. Cell Biol. 166:637-643.
15. Keller, L.C., E.P. Romijn, I. Zamora, J.R. Yates III, and W.F. Marshall. 2005. Proteomic analysis of isolated Chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr. Biol. 15:1090-1098.
16. Kim, H.K., J.G. Kang, S. Yumura, C.J. Walsh, J.W. Cho, and J. Lee. 2005. De novo formation of basal bodies in Naegleria gruberi: regulation by phosphorylation. J. Cell Biol. 169:719-724.
17. Kim, J.C., J.L. Badano, S. Sibold, M.A. Esmail, J. Hill, B.E. Hoskins, C.C. Leitch, K. Venner, S.J. Ansley, A.J. Ross, et al. 2004. The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat. Genet. 36:462-470.
18. Kubo, A., and S. Tsukita. 2003. Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cell-cycle-dependent assembly/disassembly. J. Cell Sci. 116:919-928.
19. Kubo, A., H. Sasaki, A. Yuba-Kubo, S. Tsukita, and N. Shiina. 1999. Centriolar satellites: molecular characterization, ATP-dependent movement toward centrioles and possible involvement in ciliogenesis. J. Cell Biol. 147:969-980.
20. La Terra, S., C.N. English, P. Hergert, B.F. McEwen, G. Sluder, and A. Khodjakov. 2005. The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. J. Cell Biol. 168:713-722.
21. Laoukili, J., E. Perret, S. Middendorp, O. Houcine, C. Guennou, F. Marano, M. Bornens, and F. Tournier. 2000. Differential expression and cellular distribution of centrin isoforms during human ciliated cell differentiation in vitro. J. Cell Sci. 113:1355-1364.
22. Leidel, S., M. Delattre, L. Cerutti, K. Baumer, and P. Gonczy. 2005. SAS-6 de-fines a protein family required for centrosome duplication in C. elegans and in human cells. Nat. Cell Biol. 7:115-125.
23. Levy, Y.Y., E.Y. Lai, S.P. Remillard, M.B. Heintzelman, and C. Fulton. 1996. Centrin is a conserved protein that forms diverse associations with centrioles and MTOCs in Naegleria and other organisms. Cell Motil. Cytoskeleton. 33:298-323.
24. Li, J.B., J.M. Gerdes, C.J. Haycraft, Y. Fan, T.M. Teslovich, H. May-Simera, H. Li, O.E. Blacque, L. Li, C.C. Leitch, et al. 2004. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell. 117:541-552.
25. Luders, J., and T. Stearns. 2007. Microtubule-organizing centres: a re-evaluation. Nat. Rev. Mol. Cell Biol. 8:161-167.
26. Marshall, W.F., and S. Nonaka. 2006. Cilia: tuning in to the cell's antenna. Curr. Biol. 16:R604-R614.
27. Murcia, N.S., W.G. Richards, B.K. Yoder, M.L. Mucenski, J.R. Dunlap, and R.P. Woychik. 2000. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development. 127:2347-2355.
28. Muresan, V., H.C. Joshi, and J.C. Besharse. 1993. Gamma-tubulin in differentiated cell types: localization in the vicinity of basal bodies in retinal photo-receptors and ciliated epithelia. J. Cell Sci. 104:1229-1237.
29. Mykytyn, K., R.F. Mullins, M. Andrews, A.P. Chiang, R.E. Swiderski, B. Yang, T. Braun, T. Casavant, E.M. Stone, and V.C. Sheffield. 2004. Bardet-Biedl syndrome type 4 (BBS4)-null mice implicate Bbs4 in flagella formation but not global cilia assembly. Proc. Natl. Acad. Sci. USA. 101:8664-8669.
30. Olsen, B. 2005. Nearly all cells in vertebrates and many cells in invertebrates contain primary cilia. Matrix Biol. 24:449-450.
31. Ostrowski, L.E., J.R. Hutchins, K. Zakel, and W.K. O'Neal. 2003. Targeting expression of a transgene to the airway surface epithelium using a ciliated cell-specific promoter. Mol. Ther. 8:637-645.
32. Pazour, G.J., B.L. Dickert, Y. Vucica, E.S. Seeley, J.L. Rosenbaum, G.B. Witman, and D.G. Cole. 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151:709-718.
33. Pazour, G.J., N. Agrin, J. Leszyk, and G.B. Witman. 2005. Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170:103-113.
34. Pelletier, L., E. O'Toole, A. Schwager, A.A. Hyman, and T. Muller-Reichert. 2006. Centriole assembly in Caenorhabditis elegans. Nature. 444:619-623.
35. Praetorius, H.A., and K.R. Spring. 2005. A physiological view of the primary cilium. Annu. Rev. Physiol. 67:515-529.
36. Preble, A.M., T.H. Giddings Jr., and S.K. Dutcher. 2001. Extragenic bypass suppressors of mutations in the essential gene BLD2 promote assembly of basal bodies with abnormal microtubules in Chlamydomonas reinhardtii. Genetics. 157:163-181.
37. Rawlins, E.L., L.E. Ostrowski, S.H. Randell, and B.L. Hogan. 2007. Lung development and repair: contribution of the ciliated lineage. Proc. Natl. Acad. Sci. USA. 104:410-417.
38. Robert, A., G. Margall-Ducos, J.E. Guidotti, O. Bregerie, C. Celati, C. Brechot, and C. Desdouets. 2007. The intraflagellar transport component IFT88/ polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells. J. Cell Sci. 120:628-637.
39. Ross, A.J., L.A. Dailey, L.E. Brighton, and R.B. Devlin. 2007. Transcriptional profiling of mucociliary differentiation in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. DOI:10.1165/rcmb.2006- 0466OC.
40. Rubinson, D.A., C.P. Dillon, A.V. Kwiatkowski, C. Sievers, L. Yang, J. Kopinja, D.L. Rooney, M.M. Ihrig, M.T. McManus, F.B. Gertler, et al. 2003. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33:401-406.
41. Scholey, J.M., and K.V. Anderson. 2006. Intraflagellar transport and cilium-based signaling. Cell. 125:439-442.
42. Sorokin, S.P. 1968. Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J. Cell Sci. 3:207-230.
43. Stemm-Wolf, A.J., G. Morgan, T.H. Giddings Jr., E.A. White, R. Marchione, H.B. McDonald, and M. Winey. 2005. Basal body duplication and maintenance require one member of the Tetrahymena thermophila centrin gene family. Mol. Biol. Cell. 16:3606-3619.
44. Taillon, B.E., S.A. Adler, J.P. Suhan, and J.W. Jarvik. 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. Taulman, P.D., C.J. Haycraft, D.F. Balkovetz, and B.K. Yoder. 2001. Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol. Biol. Cell. 12:589-599.
46. Teilmann, S.C., A.G. Byskov, P.A. Pedersen, D.N. Wheatley, G.J. Pazour, and S.T. Christensen. 2005. Localization of transient receptor potential ion channels in primary and motile cilia of the female murine reproductive organs. Mol. Reprod. Dev. 71:444-452.
47. Tichelaar, J.W., S.E. Wert, R.H. Costa, S. Kimura, and J.A. Whitsett. 1999. HNF-3/forkhead homologue-4 (HFH-4) is expressed in ciliated epithelial cells in the developing mouse lung. J. Histochem. Cytochem. 47:823-832.
48. Toskala, E., S.M. Smiley-Jewell, V.J. Wong, D. King, and C.G. Plopper. 2005. Temporal and spatial distribution of ciliogenesis in the tracheobronchial airways of mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 289:L454-L459.
49. Tsou, M.F., and T. Stearns. 2006a. Controlling centrosome number: licenses and blocks. Curr. Opin. Cell Biol. 18:74-78.
50. Tsou, M.F., and T. Stearns. 2006b. Mechanism limiting centrosome duplication to once per cell cycle. Nature. 442:947-951.
51. Ventura, A., A. Meissner, C.P. Dillon, M. McManus, P.A. Sharp, L. Van Parijs, R. Jaenisch, and T. Jacks. 2004. Cre-lox-regulated conditional RNA interference from transgenes. Proc. Natl. Acad. Sci. USA. 101:10380-10385.
52. You, Y., E.J. Richer, T. Huang, and S.L. Brody. 2002. Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am. J. Physiol. Lung Cell. Mol. Physiol. 283:L1315-L1321.