Centrin3 in trypanosomes maintains the stability of a flagellar inner-arm dynein for cell motility

Nature Communications

Volumn 5, Issue , 2014, Pages

  Wei, Ying ^a,b,c   Hu, Huiqing ^a   Lun, Zhao Rong ^b,c   Li, Ziyin ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b Ministry of Education   (United States)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CENTRIN; CENTRIN 3; DYNEIN ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; CENTRIN3 PROTEIN, TRYPANOSOMA BRUCEI BRUCEI; CONTRACTILE PROTEIN; PROTOZOAL PROTEIN;

CELL ORGANELLE; CILIATE; FLAGELLATE; MOTILITY; PARASITIC DISEASE; STABILIZATION;

ARTICLE; AXONEME; CELL MOTILITY; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; GENE SILENCING; GENETIC STABILITY; KINETOSOME; MASS SPECTROMETRY; NONHUMAN; TRYPANOSOMA BRUCEI; FLAGELLUM; GENETICS; METABOLISM; PHYSIOLOGY; TRYPANOSOMA BRUCEI BRUCEI;

CALCIUM-BINDING PROTEINS; CONTRACTILE PROTEINS; DYNEINS; FLAGELLA; GENE KNOCKDOWN TECHNIQUES; PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84901951097     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5060     Document Type: Article

References (44)

1. Taillon, B. E., Adler, S. A., Suhan, J. P. & Jarvik, J. W. 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 (1992). (Pubitemid 23006558)
2. Koblenz, B., Schoppmeier, J., Grunow, A. & Lechtreck, K. F. Centrin deficiency in Chlamydomonas causes defects in basal body replication, segregation and maturation. J. Cell. Sci. 116, 2635-2646 (2003). (Pubitemid 36857217)
3. Melkonian, M. Centrin-mediated cell motility: a novel cell motility mechanism in eukaryotic cells. Bot. Acta 102, 3-4 (1989).
4. Geimer, S. & Melkonian, M. Centrin scaffold in Chlamydomonas reinhardtii revealed by immunoelectron microscopy. Eukaryot. Cell 4, 1253-1263 (2005). (Pubitemid 41004138)
5. Piperno, G., Ramanis, Z., Smith, E. F. & Sale, W. S. Three distinct inner dynein arms in Chlamydomonas flagella: molecular composition and location in the axoneme. J. Cell Biol. 110, 379-389 (1990).
6. Guerra, C., Wada, Y., Leick, V., Bell, A. & Satir, P. Cloning, localization, and axonemal function of Tetrahymena centrin. Mol. Biol. Cell 14, 251-261 (2003). (Pubitemid 36106034)
7. He, C. Y., Pypaert, M. & Warren, G. Golgi duplication in Trypanosoma brucei requires Centrin2. Science 310, 1196-1198 (2005). (Pubitemid 41681748)
8. Selvapandiyan, A., Kumar, P., Salisbury, J. L., Wang, C. C. & Nakhasi, H. L. Role of centrins 2 and 3 in organelle segregation and cytokinesis in Trypanosoma brucei. PLoS ONE 7, e45288 (2012).
9. Selvapandiyan, A. et al. Centrin1 is required for organelle segregation and cytokinesis in Trypanosoma brucei. Mol. Biol. Cell 18, 3290-3301 (2007). (Pubitemid 47378671)
10. Shi, J. et al. Centrin4 coordinates cell and nuclear division in T. brucei. J. Cell. Sci. 121, 3062-3070 (2008).
11. Wang, M., Gheiratmand, L. & He, C. Y. An interplay between Centrin2 and Centrin4 on the bi-lobed structure in Trypanosoma brucei. Mol. Microbiol. 83, 1153-1161 (2012).
12. Ikeda, K. N. & de Graffenried, C. L. Polo-like kinase is necessary for flagellum inheritance in Trypanosoma brucei. J. Cell. Sci. 125, 3173-3184 (2012).
13. Zhou, Q. et al. A comparative proteomic analysis reveals a new bi-lobe protein required for bi-lobe duplication and cell division in Trypanosoma brucei. PLoS ONE 5, e9660 (2010).
14. Schimanski, B., Nguyen, T. N. & Gunzl, A. Highly efficient tandem affinity purification of trypanosome protein complexes based on a novel epitope combination. Eukaryot. Cell 4, 1942-1950 (2005). (Pubitemid 41636886)
15. Springer, A. L. et al. Silencing of a putative inner arm dynein heavy chain results in flagellar immotility in Trypanosoma brucei. Mol. Biochem. Parasitol. 175, 68-75 (2011).
16. Zukas, R., Chang, A. J., Rice, M. & Springer, A. L. Structural analysis of flagellar axonemes from inner arm dynein knockdown strains of Trypanosoma brucei. Biocell 36, 133-141 (2012).
17. Dean, S. & Gull, K. A proteomics analysis of the trypanosome transition zone. The 5th Kinetoplastid Molecular Cell Biology Meeting 272 (Woods Hole, MA, 21-25 April 2013).
18. Wickstead, B. & Gull, K. Dyneins across eukaryotes: a comparative genomic analysis. Traffic. 8, 1708-1721 (2007). (Pubitemid 350066684)
19. de Graffenried, C. L., Anrather, D., Von Raussendorf, F. &Warren, G. Polo-like kinase phosphorylation of bilobe-resident TbCentrin2 facilitates flagellar inheritance in Trypanosoma brucei. Mol. Biol. Cell 24, 1947-1963 (2013).
20. Broadhead, R. et al. Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224-227 (2006). (Pubitemid 43372101)
21. Oberholzer, M. et al. Independent analysis of the flagellum surface and matrix proteomes provides insight into flagellum signaling in mammalian-infectious Trypanosoma brucei. Mol. Cell. Proteomics 10, M111 010538 (2011).
22. Piperno, G., Mead, K. & Shestak, W. The inner dynein arms I2 interact with a "dynein regulatory complex" in Chlamydomonas flagella. J. Cell Biol. 118, 1455-1463 (1992).
23. Yanagisawa, H. A. & Kamiya, R. Association between actin and light chains in Chlamydomonas flagellar inner-arm dyneins. Biochem. Biophys. Res. Commun. 288, 443-447 (2001). (Pubitemid 33022503)
24. King, S. M. Purification of axonemal dyneins and dynein-associated components from Chlamydomonas. Methods Cell. Biol. 92, 31-48 (2009).
25. Hu, H. et al. An orphan kinesin in trypanosomes cooperates with a kinetoplastid-specific kinesin to maintain cell morphology by regulating subpellicular microtubules. J. Cell. Sci. 125, 4126-4136 (2012).
26. Hu, L., Hu, H. & Li, Z. A kinetoplastid-specific kinesin is required for cytokinesis and for maintenance of cell morphology in Trypanosoma brucei. Mol. Microbiol. 83, 565-578 (2012).
27. Wei, Y., Hu, H., Lun, Z. R. & Li, Z. The cooperative roles of two kinetoplastidspecific kinesins in cytokinesis and in maintaining cell morphology in bloodstream trypanosomes. PLoS ONE 8, e73869 (2013).
28. Duquesnoy, P. et al. Loss-of-function mutations in the human ortholog of Chlamydomonas reinhardtii ODA7 disrupt dynein arm assembly and cause primary ciliary dyskinesia. Am. J. Hum. Genet. 85, 890-896 (2009).
29. Bastin, P., MacRae, T. H., Francis, S. B., Matthews, K. R. & Gull, K. Flagellar morphogenesis: protein targeting and assembly in the paraflagellar rod of trypanosomes. Mol. Cell. Biol. 19, 8191-8200 (1999). (Pubitemid 30414013)
30. Bastin, P., Ellis, K., Kohl, L. & Gull, K. Flagellum ontogeny in trypanosomes studied via an inherited and regulated RNA interference system. J. Cell. Sci. 113(Pt 18): 3321-3328 (2000).
31. Johnson, K. A. & Rosenbaum, J. L. Polarity of flagellar assembly in Chlamydomonas. J. Cell Biol. 119, 1605-1611 (1992).
32. Piperno, G., Mead, K. & Henderson, S. Inner dynein arms but not outer dynein arms require the activity of kinesin homologue protein KHP1(FLA10) to reach the distal part of flagella in Chlamydomonas. J. Cell Biol. 133, 371-379 (1996).
33. Lindemann, C. B. & Lesich, K. A. Flagellar and ciliary beating: the proven and the possible. J. Cell. Sci. 123, 519-528 (2010).
34. Ralston, K. S., Kabututu, Z. P., Melehani, J. H., Oberholzer, M. & Hill, K. L. The Trypanosoma brucei flagellum: moving parasites in new directions. Annu. Rev. Microbiol. 63, 335-362 (2009).
35. Ridgley, E., Webster, P., Patton, C. & Ruben, L. Calmodulin-binding properties of the paraflagellar rod complex from Trypanosoma brucei. Mol. Biochem. Parasitol. 109, 195-201 (2000). (Pubitemid 30665418)
36. Ginger, M. L. et al. Calmodulin is required for paraflagellar rod assembly and flagellum-cell body attachment in trypanosomes. Protist 164, 528-540 (2013).
37. Wirtz, E., Leal, S., Ochatt, C. & Cross, G. A. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99, 89-101 (1999). (Pubitemid 29127189)
38. Wang, Z., Morris, J. C., Drew, M. E. & Englund, P. T. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 275, 40174-40179 (2000). (Pubitemid 32064646)
39. Dang, H. Q. & Li, Z. The Cdc45. Mcm2-7. GINS protein complex in trypanosomes regulates DNA replication and interacts with two Orc1-like proteins in the origin recognition complex. J. Biol. Chem. 286, 32424-32435 (2011).
40. Bastin, P., Pullen, T. J., Sherwin, T. & Gull, K. Protein transport and flagellum assembly dynamics revealed by analysis of the paralysed trypanosome mutant snl-1. J. Cell. Sci. 112(Pt 21): 3769-3777 (1999).
41. Baron, D. M., Ralston, K. S., Kabututu, Z. P. & Hill, K. L. Functional genomics in Trypanosoma brucei identifies evolutionarily conserved components of motile flagella. J. Cell. Sci. 120, 478-491 (2007). (Pubitemid 46332511)
42. Robinson, D., Beattie, P., Sherwin, T. & Gull, K. Microtubules, tubulin, and microtubule-associated proteins of trypanosomes. Methods. Enzymol. 196, 285-299 (1991).
43. Kabututu, Z. P., Thayer, M., Melehani, J. H. & Hill, K. L. CMF70 is a subunit of the dynein regulatory complex. J. Cell. Sci. 123, 3587-3595 (2010).
44. Li, Z. et al. An easily dissociated 26 S proteasome catalyzes an essential ubiquitin-mediated protein degradation pathway in Trypanosoma brucei. J. Biol. Chem. 277, 15486-15498 (2002). (Pubitemid 34967815)