Pcdp1 is a central apparatus protein that binds Ca2+-calmodulin and regulates ciliary motility

Journal of Cell Biology

Volumn 189, Issue 3, 2010, Pages 601-612

  DiPetrillo, Christen G ^a   Smith, Elizabeth F ^a  

^a Dartmouth College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM ION; CALMODULIN; POLYPEPTIDE; PRIMARY CILIARY DYSKINESIA PROTEIN 1; PROTEIN FAP 221; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AXONEME; CHLAMYDOMONAS REINHARDTII; CILIARY MOTILITY; COMPLEX FORMATION; CONTROLLED STUDY; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; WAVEFORM;

ALGAL PROTEINS; ANIMALS; CALMODULIN; CALMODULIN-BINDING PROTEINS; CELL MOVEMENT; CHLAMYDOMONAS REINHARDTII; CILIA; MICE; PROTEINS; PROTOZOAN PROTEINS;

CHLAMYDOMONAS REINHARDTII; EUKARYOTA; MAMMALIA;

EID: 77951869322     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200912009     Document Type: Article

References (41)

1. Badano, J.L., N. Mitsuma, P.L. Beales, and N. Katsanis. 2006. The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7:125-148. doi:10.1146/annurev.genom.7.080505.115610
2. Bannai, H., M. Yoshimura, K. Takahashi, and C. Shingyoji. 2000. Calcium regulation of microtubule sliding in reactivated sea urchin sperm flagella. J. Cell Sci. 113:831-839.
3. Bessen, M., R.B. Fay, and G.B. Witman. 1980. Calcium control of waveform in isolated flagellar axonemes of Chlamydomonas. J. Cell Biol. 86:446-455. doi:10.1083/jcb.86.2.446
4. Brokaw, C.J., R. Josslin, and L. Bobrow. 1974. Calcium ion regulation of flagellar beat symmetry in reactivated sea urchin spermatozoa. Biochem. Biophys. Res. Commun. 58:795-800. doi:10.1016/S0006-291X(74)80487-0
5. Chin, D., and A.R. Means. 2000. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10:322-328. doi:10.1016/S0962-8924(00)01800-6
6. DiPetrillo, C., and E.F. Smith. 2009. Calcium regulation of ciliary motility: analysis of axonemal calcium binding proteins. In Methods in Cell Biology. Vol.92 Cilia: Motors and Regulation. S.J. King and G.J. Pazour, editors. Elsevier, St. Louis. 163-180.
7. Dutcher, S.K., B. Huang, and D.J. Luck. 1984. Genetic dissection of the central pair microtubules of the flagella of Chlamydomonas reinhardtii. J. Cell Biol. 98:229-236. doi:10.1083/jcb.98.1.229
8. Dymek, E.E., and E.F. Smith. 2007. A conserved CaM- and radial spoke associated complex mediates regulation of flagellar dynein activity. J. Cell Biol. 179:515-526. doi:10.1083/jcb.200703107
9. Frey, E., C.J. Brokaw, and C.K. Omoto. 1997. Reactivation at low ATP distinguishes among classes of paralyzed flagella mutants. Cell Motil. Cytoskeleton. 38:91-99. doi:10.1002/(SICI)1097-0169(1997)38:1<91:: AID-CM8>3.0.CO;2-K
10. Gorman, D.S., and R.P. Levine. 1965. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc. Natl. Acad. Sci. USA. 54:1665-1669. doi:10.1073/pnas.54.6.1665
11. Hayashi, S., and C. Shingyoji. 2009. Bending-induced switching of dynein activity in elastase-treated axonemes of sea urchin sperm-roles of Ca2+ and ADP. Cell Motil. Cytoskeleton. 66:292-301. doi:10.1002/cm.20360
12. Kindle, K.L. 1990. High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA. 87:1228-1232. doi:10.1073/pnas.87.3. 1228
13. Kwan, A.L., L. Li, D.C. Kulp, S.K. Dutcher, and G.D. Stormo. 2009. Improving gene-finding in Chlamydomonas reinhardtii:GreenGenie2. BMC Genomics. 10:210. doi:10.1186/1471-2164-10-210
14. Lechtreck, K.F., and G.B. Witman. 2007. Chlamydomonas reinhardtii hydin is a central pair protein required for flagellar motility. J. Cell Biol. 176:473-482. doi:10.1083/jcb.200611115
15. Lechtreck, K.F., P. Delmotte, M.L. Robinson, M.J. Sanderson, and G.B. Witman. 2008. Mutations in Hydin impair ciliary motility in mice. J. Cell Biol. 180:633-643. doi:10.1083/jcb.200710162
16. Lee, L., D.R. Campagna, J.L. Pinkus, H. Mulhern, T.A. Wyatt, J.H. Sisson, J.A. Pavlik, G.S. Pinkus, and M.D. Fleming. 2008. Primary ciliary dyskinesia in mice lacking the novel ciliary protein Pcdp1. Mol. Cell. Biol. 28:949-957. doi:10.1128/MCB.00354-07
17. Merchant, S.S., S.E. Prochnik, O. Vallon, E.H. Harris, S.J. Karpowicz, G.B. Witman, A. Terry, A. Salamov, L.K. Fritz-Laylin, L. Maréchal- Drouard, et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science. 318:245-250. doi:10.1126/science.1143609
18. Mitchell, D.R. 2009. The flagellar central pair apparatus. In The Chlamydomonas Sourcebook. Vol.Volume 3: Cell Motility and Behavior. G.B. Witman, editor. Elsevier, New York. 235-248.
19. Mitchell, D.R., and M. Nakatsugawa. 2004. Bend propagation drives central pair rotation in Chlamydomonas reinhardtii flagella. J. Cell Biol. 166:709-715. doi:10.1083/jcb.200406148
20. Mitchell, D.R., and W.S. Sale. 1999. Characterization of a Chlamydomonas insertional mutant that disrupts flagellar central pair microtubule-associated structures. J. Cell Biol. 144:293-304. doi: 10.1083/jcb.144.2.293
21. Molnar, A., A. Bassett, E. Thuenemann, F. Schwach, S. Karkare, S. Ossowski, D. Weigel, and D. Baulcombe. 2009. Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J. 58:165-174. doi:10.1111/j.1365-313X.2008.03767.x
22. Nakano, I., T. Kobayashi, M. Yoshimura, and C. Shingyoji. 2003. Centralpair-linked regulation of microtubule sliding by calcium in flagellar axonemes. J. Cell Sci. 116:1627-1636. doi:10.1242/jcs.00336
23. Nigg, E.A., and J.W. Raff. 2009. Centrioles, centrosomes, and cilia in health and disease. Cell. 139:663-678. doi:10.1016/j.cell.2009.10.036
24. Omoto, C.K., T. Yagi, E. Kurimoto, and R. Kamiya. 1996. Ability of paralyzed flagella mutants of Chlamydomonas to move. Cell Motil. Cytoskeleton. 33:88-94. doi:10.1002/(SICI)1097-0169(1996)33:2<88:: AID-CM2>3.0.CO;2-E
25. Ossowski, S., R. Schwab, and D. Weigel. 2008. Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53:674-690. doi:10.1111/j.1365-313X.2007.03328.x
26. Patel-King, R.S., S.E. Benashski, and S.M. King. 2002. A bipartite Ca2+- regulated nucleoside-diphosphate kinase system within the Chlamydomonas flagellum. The regulatory subunit p72. J. Biol. Chem. 277:34271-34279. doi:10.1074/jbc.M204137200
27. Patel-King, R.S., O. Gorbatyuk, S. Takebe, and S.M. King. 2004. Flagellar radial spokes contain a Ca2+-stimulated nucleoside diphosphate kinase. Mol. Biol. Cell. 15:3891-3902. doi:10.1091/mbc.E04-04-0352
28. Pazour, G.J., N. Agrin, J. Leszyk, and G.B. Witman. 2005. Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170:103-113. doi:10.1083/jcb. 200504008
29. Rupp, G., E. O'Toole, and M.E. Porter. 2001. The Chlamydomonas PF6 locus encodes a large alanine/proline-rich polypeptide that is required for assembly of a central pair projection and regulates flagellar motility. Mol. Biol. Cell. 12:739-751.
30. Sharma, N., N.F. Berbari, and B.K. Yoder. 2008. Ciliary dysfunction in developmental abnormalities and diseases. Curr. Top. Dev. Biol. 85:371-427. doi:10.1016/S0070-2153(08)00813-2
31. Smith, E.F. 2002. Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase. Mol. Biol. Cell. 13:3303-3313. doi:10.1091/mbc.E02-04-0185
32. Smith, E.F., and P. Yang. 2004. The radial spokes and central apparatus: mechano-chemical transducers that regulate flagellar motility. Cell Motil. Cytoskeleton. 57:8-17. doi:10.1002/cm.10155
33. Verdugo, P. 1980. Ca2+-dependent hormonal stimulation of ciliary activity. Nature. 283:764-765. doi:10.1038/283764a0
34. Wakabayashi, K., T. Yagi, and R. Kamiya. 1997. Ca2+-dependent waveform conversion in the flagellar axoneme of Chlamydomonas mutants lacking the central-pair/radial spoke system. Cell Motil. Cytoskeleton. 38:22-28. doi:10.1002/(SICI)1097-0169(1997)38:1<22::AID-CM3>3.0.CO;2-J
35. Wargo, M.J., and E.F. Smith. 2003. Asymmetry of the central apparatus defines the location of active microtubule sliding in Chlamydomonas flagella. Proc. Natl. Acad. Sci. USA. 100:137-142. doi:10.1073/pnas.0135800100
36. Wargo, M.J., M.A. McPeek, and E.F. Smith. 2004. Analysis of microtubule sliding patterns in Chlamydomonas flagellar axonemes reveals dynein activity on specific doublet microtubules. J. Cell Sci. 117:2533-2544. doi:10.1242/jcs.01082
37. Wargo, M.J., E.E. Dymek, and E.F. Smith. 2005. Calmodulin and PF6 are components of a complex that localizes to the C1 microtubule of the flagellar central apparatus. J. Cell Sci. 118:4655-4665. doi:10.1242/jcs.02585
38. Yagi, T., and R. Kamiya. 2000. Vigorous beating of Chlamydomonas axonemes lacking central pair/radial spoke structures in the presence of salts and organic compounds. Cell Motil. Cytoskeleton. 46:190-199. doi:10.1002/1097- 0169(200007)46:3<190::AID-CM4>3.0.CO;2-#
39. Yang, P., D.R. Diener, J.L. Rosenbaum, and W.S. Sale. 2001. Localization of calmodulin and dynein light chain LC8 in flagellar radial spokes. J. Cell Biol. 153:1315-1326. doi:10.1083/jcb.153.6.1315
40. Yoshimura, M., and C. Shingyoji. 1999. Effects of the central pair apparatus on microtubule sliding velocity in sea urchin sperm flagella. Cell Struct. Funct. 24:43-54. doi:10.1247/csf.24.43
41. Zhao, T., W. Wang, X. Bai, and Y. Qi. 2008. Gene silencing by artificial microRNAs in Chlamydomonas. Plant J. 58:157-164. doi:10.1111/j.1365-313X.2008. 03758.x