The flagellum-mitogen-activated protein kinase connection in Trypanosomatids: A key sensory role in parasite signalling and development?

Cellular Microbiology

Volumn 11, Issue 5, 2009, Pages 710-718

  Rotureau, Brice ^a   Morales, Miguel A ^b,c   Bastin, Philippe ^a   Späth, Gerald F ^b,c  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE;

EUKARYOTE; EUKARYOTIC FLAGELLUM; FLAGELLUM; LEISHMANIA; NONHUMAN; PARASITE VIRULENCE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUORUM SENSING; SENSE ORGAN; SHORT SURVEY; SIGNAL TRANSDUCTION; TRYPANOSOMA BRUCEI;

EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAGELLA; MAP KINASE SIGNALING SYSTEM; MODELS, BIOLOGICAL; TRYPANOSOMATINA; VIRULENCE;

EUKARYOTA; HEXAPODA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 64049086801     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01295.x     Document Type: Short Survey

References (70)

1. Absalon, S., Kohl, L., Branche, C., Blisnick, T., Toutirais, G., Rusconi, F., et al. (2007) Basal body positioning is controlled by flagellum formation in Trypanosoma brucei. PLoS ONE 2: E437.
2. Absalon, S., Blisnick, T., Kohl, L., Toutirais, G., Dore, G., Julkowska, D., et al. (2008a) Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes. Mol Biol Cell 19: 929-944.
3. Absalon, S., Blisnick, T., Bonhivers, M., Kohl, L., Cayet, N., Toutirais, G., et al. (2008b) Flagellum elongation is required for correct structure, orientation and function of the flagellar pocket in Trypanosoma brucei. J Cell Sci 121: 3704-3716.
4. 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.
5. Adhiambo, C., Blisnick, T., Toutirais, G., Delannoy, E., and Bastin, P. (2009) A novel function for the atypical small G protein Rab-like 5 in flagellum assembly of trypanosomes. J Cell Sci 122: 834-841.
6. Bastin, P., Sherwin, T., and Gull, K. (1998) Paraflagellar rod is vital for trypanosome motility. Nature 391: 548.
7. Bastin, P., Pullen, T.J., Sherwin, T., and Gull, K. (1999) Protein transport and flagellum assembly dynamics revealed by analysis of the paralysed trypanosome mutant snl-1. J Cell Sci 112: 3769-3777.
8. Bengs, F., Scholz, A., Kuhn, D., and Wiese, M. (2005) LmxMPK9, a mitogen-activated protein kinase homologue affects flagellar length in Leishmania mexicana. Mol Microbiol 55: 1606-1615.
9. Berman, S.A., Wilson, N.F., Haas, N.A., and Lefebvre, P.A. (2003) A novel MAP kinase regulates flagellar length in Chlamydomonas. Curr Biol 13: 1145-1149.
10. Blaineau, C., Tessier, M., Dubessay, P., Tasse, L., Crobu, L., Pages, M., and Bastien, P. (2007) A novel microtubule-depolymerizing kinesin involved in length control of a eukaryotic flagellum. Curr Biol 17: 778-782.
11. Bonhivers, M., Nowacki, S., Landrein, N., and Robinson, D.R. (2008) Biogenesis of the trypanosome endo-exocytotic organelle is cytoskeleton mediated. PLoS Biol 6: E105.
12. Bradley, B.A., and Quarmby, L.M. (2005) A NIMA-related kinase, Cnk2p, regulates both flagellar length and cell size in Chlamydomonas. J Cell Sci 118: 3317-3326.
13. Bridges, D.J., Pitt, A.R., Hanrahan, O., Brennan, K., Voorheis, H.P., Herzyk, P., etal. (2008) Characterisation of the plasma membrane subproteome of bloodstream form Trypanosoma brucei. Proteomics 8: 83-99.
14. Broadhead, R., Dawe, H.R., Farr, H., Griffiths, S., Hart, S.R., Portman, N., et al. (2006) Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440: 224-227.
15. Burghoorn, J., Dekkers, M.P., Rademakers, S., de Jong, T., Willemsen, R., and Jansen, G. (2007) Mutation of the MAP kinase DYF-5 affects docking and undocking of kinesin-2 motors and reduces their speed in the cilia of Caenorhabditis elegans. Proc Natl Acad Sci U S A 104: 7157-7162.
16. Chen, J., Knowles, H.J., Hebert, J.L., and Hackett, B.P. (1998) Mutation of the mouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry. J Clin Invest 102: 1077-1082.
17. Cuchillo-Ibanez, I., Seereeram, A., Byers, H.L., Leung, K.Y., Ward, M.A., Anderton, B.H., and Hanger, D.P. (2008) Phosphorylation of tau regulates its axonal transport by controlling its binding to kinesin. FASEB J 22: 3186-3195.
18. 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.
19. Domenicali Pfister, D., Burkard, G., Morand, S., Renggli, C.K., Roditi, I., and Vassella, E. (2006) A mitogen-activated protein kinase controls differentiation of bloodstream forms of Trypanosoma brucei. Eukaryot Cell 5: 1126-1135.
20. Dubruille, R., Laurencon, A., Vandaele, C., Shishido, E., Coulon-Bublex, M., Swoboda, P., et al. (2002) Drosophila regulatory factor X is necessary for ciliated sensory neuron differentiation. Development 129: 5487-5498.
21. El-Sayed, N.M., Myler, P.J., Blandin, G., Berriman, M., Crabtree, J., Aggarwal, G., et al. (2005) Comparative genomics of Trypanosomatid parasitic protozoa. Science 309: 404-409.
22. Erdmann, M., Scholz, A., Melzer, I.M., Schmetz, C., and Wiese, M. (2006) Interacting protein kinases involved in the regulation of flagellar length. Mol Biol Cell 17: 2035-2045.
23. Fenn, K., and Matthews, K.R. (2007) The cell biology of Trypanosoma brucei differentiation. Curr Opin Microbiol 10: 539-546.
24. Guttinger, A., Schwab, C., Morand, S., Roditi, I., and Vassella, E. (2007) A mitogen-activated protein kinase of Trypanosoma brucei confers resistance to temperature stress. Mol Biochem Parasitol 153: 203-206.
25. Horiuchi, D., Collins, C.A., Bhat, P., Barkus, R.V., Diantonio, A., and Saxton, W.M. (2007) Control of a kinesin-cargo linkage mechanism by JNK pathway kinases. Curr Biol 17: 1313-1317.
26. Hua, S.B., and Wang, C.C. (1994) Differential accumulation of a protein kinase homolog in Trypanosoma brucei. J Cell Biochem 54: 20-31.
27. Hua, S.B., and Wang, C.C. (1997) Interferon-gamma activation of a mitogen-activated protein kinase, KFR1, in the bloodstream form of Trypanosoma brucei. J Biol Chem 272: 10797-10803.
28. Kamhawi, S., Ramalho-Ortigao, M., Pham, V.M., Kumar, S., Lawyer, P.G., Turco, S.J., et al. (2004) A role for insect galectins in parasite survival. Cell 119: 329-341.
29. Kohl, L., and Bastin, P. (2005) The flagellum of trypanosomes. Int Rev Cytol 244: 227-285.
30. 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.
31. Kollien, A.H., Schmidt, J., and Schaub, G.A. (1998) Modes of association of Trypanosoma cruzi with the intestinal tract of the vector Triatoma infestans. Acta Trop 70: 127-141.
32. Kovacs, J.J., Whalen, E.J., Liu, R., Xiao, K., Kim, J., Chen, M., et al. (2008) Beta-arrestin-mediated localization of smoothened to the primary cilium. Science 320: 1777-1781.
33. LaCount, D.J., Barrett, B., and Donelson, J.E. (2002) Trypanosoma brucei FLA1 is required for flagellum attachment and cytokinesis. J Biol Chem 277: 17580-17588.
34. Lukong, K.E., and Richard, S. (2008) Breast tumor kinase BRK requires kinesin-2 subunit KAP3A in modulation of cell migration. Cell Signal 20: 432-442.
35. Maga, J.A., Sherwin, T., Francis, S., Gull, K., and LeBowitz, J.H. (1999) Genetic dissection of the Leishmania paraflagellar rod, a unique flagellar cytoskeleton structure. J Cell Sci 112: 2753-2763.
36. Marszalek, J.R., Liu, X., Roberts, E.A., Chui, D., Marth, J.D., Williams, D.S., and Goldstein, L.S. (2000) Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102: 175-187.
37. Molla-Herman, A., Boularan, C., Ghossoub, R., Scott, M.G., Burtey, A., Zarka, M., et al. (2008) Targeting of beta-arrestin2 to the centrosome and primary cilium: Role in cell proliferation control. PLoS ONE 3: e3728.
38. Morales, M.A., Renaud, O., Faigle, W., Shorte, S.L., and Spath, G.F. (2007) Over-expression of Leishmania major MAP kinases reveals stage-specific induction of phosphotransferase activity. Int J Parasitol 37: 1187-1199.
39. Morales, M.A., Watanabe, R., Laurent, C., Lenormand, P., Rousselle, J.C., Namane, A., and Spath, G.F. (2008) Phosphoproteomic analysis of Leishmania donovani pro- and amastigote stages. Proteomics 8: 350-363.
40. Muller, I.B., Domenicali-Pfister, D., Roditi, I., and Vassella, E. (2002) Stage-specific requirement of a mitogen-activated protein kinase by Trypanosoma brucei. Mol Biol Cell 13: 3787-3799.
41. Naula, C., Parsons, M., and Mottram, J.C. (2005) Protein kinases as drug targets in trypanosomes and Leishmania. Biochim Biophys Acta 1754: 151-159.
42. Oberholzer, M., Marti, G., Baresic, M., Kunz, S., Hemphill, A., and Seebeck, T. (2007) The Trypanosoma brucei cAMP phosphodiesterases TbrPDEB1 and TbrPDEB2: Flagellar enzymes that are essential for parasite virulence. FASEB J 21: 720-731.
43. Parsons, M., Worthey, E.A., Ward, P.N., and Mottram, J.C. (2005) Comparative analysis of the kinomes of three pathogenic Trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 6: 127.
44. Pullen, T.J., Ginger, M.L., Gaskell, S.J., and Gull, K. (2004) Protein targeting of an unusual, evolutionarily conserved adenylate kinase to a eukaryotic flagellum. Mol Biol Cell 15: 3257-3265.
45. Qin, H., Diener, D.R., Geimer, S., Cole, D.G., and Rosenbaum, J.L. (2004) Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J Cell Biol 164: 255-266.
46. Qin, H., Burnette, D.T., Bae, Y.K., Forscher, P., Barr, M.M., and Rosenbaum, J.L. (2005) Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Curr Biol 15: 1695-1699.
47. 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.
48. Rocha, G.M., Brandao, B.A., Mortara, R.A., Attias, M., de Souza, W., and Carvalho, T.M. (2006) The flagellar attachment zone of Trypanosoma cruzi epimastigote forms. J Struct Biol 154: 89-99.
49. Rosenbaum, J.L., and Witman, G.B. (2002) Intraflagellar transport. Nat Rev Mol Cell Biol 3: 813-825.
50. Sahin, A., Espiau, B., Marchand, C., and Merlin, G. (2008) Flagellar length depends on LdARL-3A GTP/GDP unaltered cycling in Leishmania amazonensis. Mol Biochem Parasitol 157: 83-87.
51. 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.
52. Scholey, J.M. (2008) Intraflagellar transport motors in cilia: Moving along the cell's antenna. J Cell Biol 180: 23-29.
53. Sherwin, T., and Gull, K. (1989) The cell division cycle of Trypanosoma brucei: Timing of event markers and cytoskeletal modulations. Philos Trans R Soc Lond B Biol Sci 323: 573-588.
54. Singla, V., and Reiter, J.F. (2006) The primary cilium as the cell's antenna: Signaling at a sensory organelle. Science 313: 629-633.
55. Stuart, K., Brun, R., Croft, S., Fairlamb, A., Gurtler, R.E., McKerrow, J., et al. (2008) Kinetoplastids: Related protozoan pathogens, different diseases. J Clin Invest 118: 1301-1310.
56. Stubbs, J.L., Oishi, I., Izpisua Belmonte, J.C., and Kintner, C. (2008) The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat Genet 40: 1454-1460.
57. Swoboda, P., Adler, H.T., and Thomas, J.H. (2000) The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C.elegans. Mol Cell 5: 411-421.
58. Tam, L.W., Wilson, N.F., and Lefebvre, P.A. (2007) A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J Cell Biol 176: 819-829.
59. Tetley, L., and Vickerman, K. (1985) Differentiation in Trypanosoma brucei: Host-parasite cell junctions and their persistence during acquisition of the variable antigen coat. J Cell Sci 74: 1-19.
60. Vaughan, S., Kohl, L., Ngai, I., Wheeler, R.J., and Gull, K. (2008) A repetitive protein essential for the flagellum attachment zone filament structure and function in Trypanosoma brucei. Protist 159: 127-136.
61. Wang, Q., Melzer, I.M., Kruse, M., Sander-Juelch, C., and Wiese, M. (2005) LmxMPK4, a mitogen-activated protein (MAP) kinase homologue essential for promastigotes and amastigotes of Leishmania mexicana. Kinetoplastid Biol Dis 4: 6.
62. Weise, F., Stierhof, Y.D., Kuhn, C., Wiese, M., and Overath, P. (2000) Distribution of GPI-anchored proteins in the protozoan parasite Leishmania, based on an improved ultrastructural description using high-pressure frozen cells. J Cell Sci 113: 4587-4603.
63. Wiese, M. (1998) A mitogen-activated protein (MAP) kinase homologue of Leishmania mexicana is essential for parasite survival in the infected host. EMBO J 17: 2619-2628.
64. Wiese, M. (2007) Leishmania MAP kinases - familiar proteins in an unusual context. Int J Parasitol 37: 1053-1062.
65. Wiese, M., Wang, Q., and Gorcke, I. (2003) Identification of mitogen-activated protein kinase homologues from Leishmania mexicana. Int J Parasitol 33: 1577-1587.
66. Wilson, N.F., Iyer, J.K., Buchheim, J.A., and Meek, W. (2008) Regulation of flagellar length in Chlamydomonas. Semin Cell Dev Biol 19: 494-501.
67. Wissing, J., Jansch, L., Nimtz, M., Dieterich, G., Hornberger, R., Keri, G., et al. (2007) Proteomics analysis of protein kinases by target class-selective prefractionation and tandem mass spectrometry. Mol Cell Proteomics 6: 537-547.
68. Wu, C., Ramirez, A., Cui, B., Ding, J., Delcroix, J.D., Valletta, J.S., et al. (2007) A functional dynein-microtubule network is required for NGF signaling through the Rap1/MAPK pathway. Traffic 8: 1503-1520.
69. Yu, X., Ng, C.P., Habacher, H., and Roy, S. (2008) Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nat Genet 40: 1445-1453.
70. Zilberstein, D., and Shapira, M. (1994) The role of pH and temperature in the development of Leishmania parasites. Annu Rev Microbiol 48: 449-470.