Modulation of a cytoskeletal calpain-like protein induces major transitions in trypanosome morphology

Journal of Cell Biology

Volumn 206, Issue 3, 2014, Pages 377-384

  Hayes, Polly ^a   Varga, Vladimir ^a   Olego Fernandez, Sofia ^a   Sunter, Jack ^a   Ginger, Michael L ^a,b   Gull, Keith ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CLPGM6 PROTEIN; CYTOSKELETON PROTEIN; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL GROWTH; CELL MEMBRANE; CELL SHAPE; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; EPIMASTIGOTE; FLAGELLUM; GENE SEQUENCE; IMMUNOFLUORESCENCE; KINETOPLAST; KINETOSOME; LEISHMANIA MAJOR; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN MODIFICATION; PROTOZOAL GENETICS; SOUTHERN BLOTTING; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; WESTERN BLOTTING;

CALPAIN; CELL DIVISION; CELL PROLIFERATION; CELL SHAPE; CYTOSKELETAL PROTEINS; FLAGELLA; PHENOTYPE; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84905965155     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201312067     Document Type: Article

References (33)

1. Beisson, J., and T.M. Sonneborn. 1965. Cytoplasmic inheritance of the organization of the cell cortex in Paramecium aurelia. Proc. Natl. Acad. Sci. USA. 53:275-282. http://dx.doi.org/10.1073/pnas.53.2.275
2. Brun, R., and Schönenberger. 1979. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop. 36:289-292.
3. Davidge, J.A., E. Chambers, H.A. Dickinson, K. Towers, M.L. Ginger, P.G. McKean, and K. Gull. 2006. Trypanosome IFT mutants provide insight into the motor location for mobility of the flagella connector and flagellar membrane formation. J. Cell Sci. 119:3935-3943. http://dx.doi.org/10 .1242/jcs.03203
4. Ersfeld, K., H. Barraclough, and K. Gull. 2005. Evolutionary relationships and protein domain architecture in an expanded calpain superfamily in kinetoplastid parasites. J. Mol. Evol. 61:742-757. http://dx.doi.org/10 .1007/s00239-004-0272-8
5. Gluenz, E., M.L. Povelones, P.T. Englund, and K. Gull. 2011. The kinetoplast duplication cycle in Trypanosoma brucei is orchestrated by cytoskeletonmediated cell morphogenesis. Mol. Cell. Biol. 31:1012-1021. http://dx .doi.org/10.1128/MCB.01176-10
6. Hoare, C.A., and F.G. Wallace. 1966. Developmental stages of trypanosomatid flagellates: a new terminology. Nature. 212:1385-1386. http://dx.doi.org/ 10.1038/2121385a0
7. Inoue, M., Y. Nakamura, K. Yasuda, N. Yasaka, T. Hara, A. Schnaufer, K. Stuart, and T. Fukuma. 2005. The 14-3-3 proteins of Trypanosoma brucei function in motility, cytokinesis, and cell cycle. J. Biol. Chem. 280:14085- 14096. http://dx.doi.org/10.1074/jbc.M412336200
8. Kohl, L., T. Sherwin, and K. Gull. 1999. Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. J. Eukaryot. Microbiol. 46:105-109. http://dx.doi.org/10.1111/ j.1550-7408.1999.tb04592.x
9. Kohl, L., D. Robinson, and P. Bastin. 2003. Novel roles for the flagellum in cell morphogenesis and cytokinesis of trypanosomes. EMBO J. 22:5336- 5346. http://dx.doi.org/10.1093/emboj/cdg518
10. Kolev, N.G., K. Ramey-Butler, G.A.M. Cross, E. Ullu, and C. Tschudi. 2012. Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein. Science. 338:1352-1353. http://dx.doi .org/10.1126/science.1229641
11. Lacomble, S., S. Vaughan, C. Gadelha, M.K. Morphew, M.K. Shaw, J.R. McIntosh, and K. Gull. 2009. Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. J. Cell Sci. 122:1081-1090. http:// dx.doi.org/10.1242/jcs.045740
12. LaCount, D.J., B. Barrett, and J.E. Donelson. 2002. Trypanosoma brucei FLA1 is required for flagellum attachment and cytokinesis. J. Biol. Chem. 277:17580-17588. http://dx.doi.org/10.1074/jbc.M200873200
13. Matthews, K.R. 2011. Controlling and coordinating development in vectortransmitted parasites. Science. 331:1149-1153. http://dx.doi.org/10.1126/ science.1198077
14. McCulloch, R., E. Vassella, P. Burton, M. Boshart, and J.D. Barry. 2004. Transformation of monomorphic and pleomorphic Trypanosoma brucei. Methods Mol. Biol. 262:53-86.
15. Moreira-Leite, F.F., T. Sherwin, L. Kohl, and K. Gull. 2001. A trypanosome structure involved in transmitting cytoplasmic information during cell division. Science. 294:610-612. http://dx.doi.org/10.1126/science.1063775
16. Morrissette, N.S., and L.D. Sibley. 2002. Cytoskeleton of apicomplexan parasites. Microbiol. Mol. Biol. Rev. 66:21-38. http://dx.doi.org/10.1128/ MMBR.66.1.21-38.2002
17. Müller, N., A. Hemphill, M. Imboden, G. Duvallet, R.H. Dwinger, and T. Seebeck. 1992. Identification and characterization of two repetitive non-variable antigens from African trypanosomes which are recognized early during infection. Parasitology. 104:111-120. http://dx.doi.org/10 .1017/S0031182000060856
18. Nilsson, D., K. Gunasekera, J. Mani, M. Osteras, L. Farinelli, L. Baerlocher, I. Roditi, and T. Ochsenreiter. 2010. Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog. 6:e1001037. http://dx.doi.org/ 10.1371/journal.ppat.1001037
19. Ogbadoyi, E.O., D.R. Robinson, and K. Gull. 2003. A high-order transmembrane structural linkage is responsible for mitochondrial genome positioning and segregation by flagellar basal bodies in trypanosomes. Mol. Biol. Cell. 14:1769-1779. http://dx.doi.org/10.1091/mbc.E02-08-0525
20. Peacock, L., M. Bailey, M. Carrington, and W. Gibson. 2014. Meiosis and haploid gametes in the pathogen Trypanosoma brucei. Curr. Biol. 24:181- 186. http://dx.doi.org/10.1016/j.cub.2013.11.044
21. Piel, M., and P.T. Tran. 2009. Cell shape and cell division in fission yeast. Curr. Biol. 19:R823-R827. http://dx.doi.org/10.1016/j.cub.2009.08.012
22. Poon, S.K., L. Peacock, W. Gibson, K. Gull, and S. Kelly. 2012. A modular and optimized single marker system for generating Trypanosoma brucei cell lines expressing T7 RNA polymerase and the tetracycline repressor. Open Biol. 2:110037. http://dx.doi.org/10.1098/rsob.110037
23. Reynolds, E.S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17:208-212. http://dx.doi.org/ 10.1083/jcb.17.1.208
24. Schneider, C.A., W.S. Rasband, and K.W. Eliceiri. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods. 9:671-675. http://dx.doi.org/ 10.1038/nmeth.2089
25. Sharma, R., E. Gluenz, L. Peacock, W. Gibson, K. Gull, and M. Carrington. 2009. The heart of darkness: growth and form of Trypanosoma brucei in the tsetse fly. Trends Parasitol. 25:517-524. http://dx.doi.org/10.1016/j.pt .2009.08.001
26. Sherwin, T., and K. Gull. 1989. The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeletal modulations. Philos. Trans. R. Soc. Lond. B Biol. Sci. 323:573-588. http://dx.doi.org/10.1098/ rstb.1989.0037
27. Subota, I., B. Rotureau, T. Blisnick, S. Ngwabyt, M. Durand-Dubief, M. Engstler, and P. Bastin. 2011. ALBA proteins are stage regulated during trypanosome development in the tsetse fly and participate in differentiation. Mol. Biol. Cell. 22:4205-4219. http://dx.doi.org/10.1091/mbc.E11-06-0511
28. Urwyler, S., E. Studer, C.K. Renggli, and I. Roditi. 2007. A family of stage-specific alanine-rich proteins on the surface of epimastigote forms of Trypanosoma brucei. Mol. Microbiol. 63:218-228. http://dx.doi.org/10 .1111/j.1365-2958.2006.05492.x
29. Vaughan, S., L. Kohl, I. Ngai, R.J. Wheeler, and K. Gull. 2008. A repetitive protein essential for the flagellum attachment zone filament structure and function in Trypanosoma brucei. Protist. 159:127-136. http://dx.doi.org/ 10.1016/j.protis.2007.08.005
30. Wickstead, B., K. Ersfeld, and K. Gull. 2002. Targeting of a tetracycline-inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol. Biochem. Parasitol. 125:211-216. http://dx .doi.org/10.1016/S0166-6851(02)00238-4
31. Wirtz, E., S. Leal, C. Ochatt, and G.A. Cross. 1999. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:89-101. http://dx.doi.org/10.1016/S0166-6851(99)00002-X
32. Woods, A., T. Sherwin, R. Sasse, T.H. MacRae, A.J. Baines, and K. Gull. 1989. Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J. Cell Sci. 93:491-500.
33. Zhou, Q., B. Liu, Y. Sun, and C.Y. He. 2011. A coiled-coil- and C2-domaincontaining protein is required for FAZ assembly and cell morphology in Trypanosoma brucei. J. Cell Sci. 124:3848-3858. http://dx.doi.org/10.1242/jcs.087676