Trafficking activity of myosin XXI is required in assembly of Leishmania flagellum

Journal of Cell Science

Volumn 123, Issue 12, 2010, Pages 2035-2044

  Katta, Santharam S ^a   Tammana, Trinadh V Satish ^a   Sahasrabuddhe, Amogh A ^a   Bajpai, Virendra K ^a   Gupta, Chhitar M ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

Intraflagellar transport; Myosin; Trafficking; Trypanosomatids

Indexed keywords

ACTIN; MYOSIN; MYOSIN XXI; UNCLASSIFIED DRUG;

ACTIN MYOSIN INTERACTION; ARTICLE; CELL SURVIVAL; EPISOME; EUKARYOTIC CELL; FLAGELLUM; GENE; GENE DELETION; INTRACELLULAR TRANSPORT; LEISHMANIA; MYO21 GENE; NONHUMAN; PLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ACTINS; FLAGELLA; LEISHMANIA; MYOSINS; PROTEIN BINDING; PROTEIN TRANSPORT; PROTOZOAN PROTEINS;

EUKARYOTA; PROTOZOA; TRYPANOSOMATIDAE;

EID: 77953549937     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.064725     Document Type: Article

References (62)

1. Absalon, S., Blisnick, T., Kohl, L., Toutirais, G., Doré, G., Julkowska, D., Tavenet, A. and Bastin, P. (2008). Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes. Mol. Biol. Cell 19, 929-944.
2. Adhiambo, C., Forney, J. D., Asai, D. J. and LeBowitz, J. H. (2005). The two cytoplasmic dynein-2 isoforms in Leishmania mexicana perform separate functions. Mol. Biochem. Parasitol. 143, 216-225.
3. Allen, C. L., Goulding, D. and Field, M. C. (2003). Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J. 22, 4991-5002.
4. Bakalara, N., Seyfang, A., Baltz, T. and Davis, C. (1995). Trypanosoma brucei and Trypanosoma cruzi: life cycle-regulated protein tyrosine phosphatase activity. Exp. Parasitol. 81, 302-312. (Pubitemid 26025568)
5. Bastin, P., Matthews, K. R. and Gull, K. (1996). The paraflagellar rod of Kinetoplastida: solved and unsolved questions. Parasitol. Today 12, 302-307.
6. Bloodgood, R. A. (2000). Protein targeting to flagella of trypanosomatid protozoa. Cell. Biol. Int. 24, 857-862.
7. Briggs, L. J., McKean, P. G., Baines, A., Moreira-Leite, F., Davidge, J., Vaughan, S. and Gull, K. (2004). The flagella connector of Trypanosoma brucei: an unusual mobile transmembrane junction. J. Cell Sci. 117, 1641-1651.
8. Broadhead, R., Dawe, H. R., Farr, H., Griffiths, S., Hart, S. R., Portman, N., Shaw, M. K., Ginger, M. L., Gaskell, S. J., McKean, P. G. et al. (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224-227.
9. Cole, D. G. and Snell, W. J. (2009). SnapShot: Intraflagellar transport. Cell 137, 784-784.
10. Cramer, L. (2008). Organelle transport: dynamic actin tracks for myosin motors. Curr. Biol. 18, R1066-R1068.
11. Cruz, A. K., Titus, R. and Beverley, S. M. (1993). Plasticity in chromosome number and testing of essential genes in Leishmania by targeting. Proc. Natl. Acad. Sci. USA 90, 1599-1603. (Pubitemid 23058221)
12. Cuvillier, A., Redon, F., Antoine, J. C., Chardin, P., DeVos, T. and Merlin, G. (2000). LdARL-3A, a Leishmania promastigote-specific ADP-ribosylation factor-like protein, is essential for flagellum integrity. J. Cell Sci. 113, 2065-2074. (Pubitemid 30386510)
13. Cuvillier, A., Miranda, J. C., Ambit, A., Barral, A. and Merlin, G. (2003). Abortive infection of Lutzomyia longipalpis insect vectors by aflagellated LdARL-3A-Q70L overexpressing Leishmania amazonensis parasites. Cell. Microbiol. 5, 717-728. (Pubitemid 37185048)
14. Davidge, J. A., Chambers, E., Dickinson, H. A., Towers, K., Ginger, M. L., McKean, P. G. and Gull, K. (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. (Pubitemid 44650867)
15. Debrabant, A., Gottlieb, M. and Dwyer, D. M. (1995). Isolation and characterization of the gene encoding the surface membrane 3′- nucleotidase/nuclease of Leishmania donovani. Mol. Biochem. Parasitol. 71, 51-63.
16. Desjeux, P. (2004). Leishmaniasis. Nat. Rev. Microbiol. 9, 692.
17. Dumas, C., Ouellette, M., Tovar, J., Cunningham, M. L., Fairlamb, A. H., Tamar, S., Olivier, M. and Papadopoulou, B. (1997). Disruption of the trypanothione reductase gene of Leishmania decreases its ability to survive oxidative stress in macrophages. EMBO J. 16, 2590-2598. (Pubitemid 27226198)
18. El-Sayed, N. M., Myler, P. J., Blandin, G., Berriman, M., Crabtree, J., Aggarwal, G., Caler, E., Renauld, H., Worthey, E. A., Hertz-Fowler, C. et al. (2005). Comparative genomics of trypanosomatid parasitic protozoa. Science 309, 404-409.
19. Ersfeld, K. and Gull, K. (2001). Targeting of cytoskeletal proteins to the flagellum of Trypanosoma brucei. J. Cell Sci. 114, 141-148.
20. Field, M. C. and Carrington, M. (2009). The trypanosome flagellar pocket. Nat. Rev. Microbiol. 7, 775-786.
21. Foth, B. J., Goedecke, M. C. and Soldati, D. (2006). New insights into myosin evolution and classification. Proc. Natl. Acad. Sci. USA 103, 3681-3686.
22. García-Salcedo, J. A., Pérez-Morga, D., Gijón, P., Dilbeck, V., Pays, E. and Nolan, D. P. (2004). A differential role for actin during the life cycle of Trypanosoma brucei. EMBO J. 23, 780-789. (Pubitemid 38418745)
23. Ghedin, E., Debrabant, A., Engel, J. C. and Dwyer, D. M. (2001). Secretory and endocytic pathways converge in a dynamic endosomal system in a primitive protozoan. Traffic. 2,175-188. (Pubitemid 32487549)
24. Ha, D. S., Schwarz, J. K., Turcob, S. J. and Beverley, S. M. (1996). Use of the green fluorescent protein as a marker in transfected Leishmania. Mol. Biochem. Parasitol. 77, 57-64. (Pubitemid 26186162)
25. Hayashi, M., Hirono, M. and Kamiya, R. (2001). Recovery of flagellar dynein function in a Chlamydomonas actin/dynein-deficient mutant upon introduction of muscle actin by electroporation. Cell Motil. Cytoskeleton. 49, 146-153. (Pubitemid 32708948)
26. Ismach, R., Cianci, C. M., Caulfield, J. P., Langer, P. J., Hein, A. and McMahon-Pratt, D. (1989). Flagellar membrane and paraxial rod proteins of Leishmania: characterization employing monoclonal antibodies. J. Protozool. 36, 617-624.
27. Jensen, A. T., Curtis, J., Montgomery, J., Handman, E. and Theander, T. G. (2001). Molecular and immunological characterization of the glucose regulated protein 78 of Leishmania donovani. Biochim. Biophys. Acta 1549, 73-87. (Pubitemid 32879350)
28. Karcher, R. L., Deacon, S. W. and Gelfand, V. I. (2002). Motor-cargo interactions: the key to transport specificity. Trends Cell Biol. 12, 21-27.
29. Kato-Minoura, T., Hirono, M. and Kamiya, R. (1997). Chlamydomonas inner-arm dynein mutant, ida5, has a mutation in an actin-encoding gene. J. Cell Biol. 137, 649-656. (Pubitemid 27200667)
30. Katta, S. S., Sahasrabuddhe, A. A. and Gupta, C. M. (2009). Flagellar localization of a novel isoform of myosin, myosin XXI, in Leishmania. Mol. Biochem. Parasitol. 164, 105-110.
31. Kohl, L., Robinson, D. and Bastin, P. (2003). Novel roles for the flagellum in cell morphogenesis and cytokinesis of trypanosomes. EMBO J. 22, 5336-5346 (Pubitemid 37279944)
32. Krendel, M. and Mooseker, M. S. (2005). Myosins: tails (and heads) of functional diversity. Physiology (Bethesda). 20, 239-251. (Pubitemid 41215198)
33. Liu, X., Vansant, G., Udovichenko, I. P., Wolfrum, U. and Williams, D. S. (1997). Myosin VIIa, the product of the Usher 1B syndrome gene, is concentrated in the connecting cilia of photoreceptor cells. Cell Motil. Cytoskeleton. 37, 240-252.
34. Liu, X., Udovichenko, I. P., Brown, S. D., Steel, K. P. and Williams, D. S. (1999). Myosin VIIa participates in opsin transport through the photoreceptor cilium. J. Neurosci. 19, 6267-6274.
35. Minoura, T. K. (2005). Impaired flagellar regeneration due to uncoordinated expression of two divergent actin genes in Chlamydomonas. Zool. Sci. 22, 571-577.
36. Moreira-Leite, F. F., Sherwin, T., Kohl, L., Gull, K. (2001). A trypanosome structure involved in transmitting cytoplasmic information during cell division. Science 294, 610-612.
37. Mottram, J. C., McCready, B. P., Brown, K. G. and Grant, K. M. (1996). Gene disruptions indicate an essential function for the LmmCRK1 cdc2-related kinase of Leishmania mexicana. Mol. Microbiol. 22, 573-583.
38. Mullin, K. A., Foth, B. J., Ilgoutz, S. C., Callaghan, J. M., Zawadzki, J. L., McFadden, G. I. and McConville, M. J. (2001). Regulated degradation of an endoplasmic reticulum membrane protein in a tubular lysosome in Leishmania mexicana. Mol. Biol. Cell 12, 2364-2377.
39. Muto, E., Masaki, E., Masafumi, H. C. and Kamiya, R. (1994). Immunological detection of actin in the 14s ciliary dynein of Tetrahymena. FEBS Lett. 343, 173-176.
40. Nayak, R. C., Sahasrabuddhe, A. A., Bajpai, V. K. and Gupta, C. M. (2005). A novel homologue of coronin colocalizes with actin in filament-like structures in Leishmania. Mol. Biochem. Parasitol. 143, 152-164.
41. Odronitz, F. and Kollmar, M. (2007). Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol. 8, R196.
42. Overath, P., Stierhof, Y.-D. and Wiese, M. (1997). Endocytosis and secretion in trypanosomatid parasites: tumultuous traffic in a pocket. Trends Cell Biol. 7, 27-33.
43. Pazour, G. J., Dickert, B. L. and Witman, G. B. (1999). The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J. Cell Biol. 144, 473-481.
44. Pedersen, L. B. and Rosenbaum, J. L. (2008). Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr. Top. Dev. Biol. 85, 23-61.
45. Ralston, K. S. and Hill, K. L. (2008). The flagellum of Trypanosoma brucei: new tricks from an old dog. Int. J. Parasitol. 38, 869-884.
46. Rogers, M. E., Chance, M. L. and Bates, P. A. (2002). The role of promastigote secretory gel in the origin and transmission of the infective stage of Leishmania mexicana by the sandfly Lutzomyia longipalpis. Parasitology. 124, 495-507.
47. Rosenbaum, J. L. and Witman, G. B. (2002). Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3, 813-825.
48. Ross, J. L., Ali, M. Y. and Warshaw, D. M. (2008). Cargo transport: molecular motors navigate a complex cytoskeleton. Curr. Opin. Cell Biol. 20, 41-47.
49. Rotureau, B., Morales, M. A., Bastin, P. and Späth, G. F. (2009). The flagellum-MAP kinase connection in Trypanosomatids: a key sensory role in parasite signaling and development? Cell Microbiol. Epub ahead of print.
50. Sahasrabuddhe, A. A., Bajpai, V. K. and Gupta, C. M. (2004). A novel form of actin in Leishmania: molecular characterisation, subcellular localisation and association with subpellicular microtubules. Mol. Biochem. Parasitol. 134, 105-114.
51. Sahin, A., Espiau, B., Tetaud, E., Cuvillier, A., Lartigue, L., Ambit, A., Robinson, D. R. and Merlin, G. (2008). The Leishmania ARL-1 and Golgi traffic. PLoS One. 3, e1620.
52. Santrich, C., Moore, L., Sherwin, T., Bastin, P., Brokaw, C., Gull, K. and LeBowitz, J. H. (1997). A motility function for the paraflagellar rod of Leishmania parasites revealed by PFR-2 gene knockouts. Mol. Biochem. Parasitol. 90, 95-109.
53. Scholey, J. M. (2003). Intraflagellar transport. Annu. Rev. Cell Dev. Biol. 19, 423-443.
54. Semenova, I., Burakov, A., Berardone, N., Zaliapin, I., Slepchenko, B., Svitkina, T., Kashina, A. and Rodionov, V. (2008). Actin dynamics is essential for myosin-based transport of membrane organelles. Curr. Biol. 28, 1581-1586.
55. Tammana, T. V., Sahasrabuddhe, A. A., Mitra, K., Bajpai, V. K. and Gupta, C. M. (2008). Actin-depolymerizing factor, ADF/cofilin, is essentially required in assembly of Leishmania flagellum. Mol. Microbiol. 70, 837-852.
56. Tovar, J., Wilkinson, S., Mottram, J. C. and Fairlamb, A. H. (1998). Evidence that trypanothione reductase is an essential enzyme in Leishmania by targeted replacement of the tryA gene locus. Mol. Microbiol. 29, 653-660.
57. Tull, D., Vince, J. E., Callaghan, J. M., Naderer, T., Spurck, T., McFadden, G. I., Currie, G., Ferguson, K., Bacic, A. and McConville, M. J. (2004). SMP-1, a member of a new family of small myristoylated proteins in kinetoplastid parasites, is targeted to the flagellum membrane in Leishmania. Mol. Biol. Cell 15, 4775-4786.
58. Wicks, S. R., de Vries, C. J., van Luenen, H. G. and Plasterk, R. H. (2000). CHE-3, a cytosolic dynein heavy chain, is required for sensory cilia structure and function in Caenorhabditis elegans. Dev. Biol. 221, 295-307.
59. Woolner, S. and Bement, W. M. (2009). Unconventional myosins acting unconventionally. Trends Cell Biol. 19, 245-252.
60. Yanagisawa, H. and Kamiya, R. (2001). Association between actin and light chains in Chlamydomonas flagellar innerarm dyneins. Biochem. Biophy. Res. Comm. 288, 443-447.
61. Zakai, H. A., Chance, M. L. and Bates, P. A. (1998). In vitro stimulation of metacyclogenesis in Leishmania braziliensis, L. donovani, L. major and L. mexicana. Parasitology. 116, 305-309.
62. Zheng, M., Beck, M., Müller. J., Chen, T., Wang, X., Wang, F., Wang, Q., Wang, Y., Baluska, F., Logan, D. C., et al. (2009). Actin turnover is required for myosin-dependent mitochondrial movements in Arabidopsis root hairs. PLoS One. 18, e5961.