Ecotin-like serine peptidase inhibitor ISP1 of Leishmania major plays a role in flagellar pocket dynamics and promastigote differentiation

Cellular Microbiology

Volumn 14, Issue 8, 2012, Pages 1271-1286

  Morrison, Lesley S ^a   Goundry, Amy ^a   Faria, Marilia S ^b   Tetley, Laurence ^a   Eschenlauer, Sylvain C ^a   Westrop, Gareth D ^c   Dostalova, Anna ^d   Volf, Petr ^d   Coombs, Graham H ^c   Lima, Ana Paula C A ^b   Mottram, Jeremy C ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^d CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT ECOTIN LIKE SERINE PROTEINASE INHIBITOR 1; RECOMBINANT ECOTIN LIKE SERINE PROTEINASE INHIBITOR 2; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIUM CULTURE; BACTERIUM MUTANT; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; ENZYME INHIBITION; EXOSOME; FLAGELLUM; HEMIDESMOSOME; HOMEOSTASIS; LEISHMANIA MAJOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE;

ANIMALS; CELLS, CULTURED; FLAGELLA; GENE KNOCKOUT TECHNIQUES; HOST-PARASITE INTERACTIONS; LEISHMANIA MAJOR; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED BALB C; PROTEASE INHIBITORS; PROTEIN TRANSPORT; PROTEINASE INHIBITORY PROTEINS, SECRETORY; PROTOZOAN PROTEINS; SECRETORY VESICLES; SERINE PROTEASES;

LEISHMANIA MAJOR; MURINAE;

EID: 84864011343     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01798.x     Document Type: Article

References (51)

1. Absalon, S., Blisnick, T., Bonhivers, M., Kohl, L., Cayet, N., Toutirais, G., etal. (2008) Flagellum elongation is required for correct structure, orientation and function of the flagellar pocket in Trypanosoma brucei. J Cell Sci 121: 3704-3716.
2. Ambit, A., Woods, K.L., Coombs, G.H., and Mottram, J.C. (2011) Morphological events during the cell cycle of Leishmania major. Eukaryot Cell 10: 1429-1438.
3. 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.
4. Besteiro, S., Coombs, G.H., and Mottram, J.C. (2004) A potential role for ICP, a leishmanial inhibitor of cysteine peptidases, in the interaction between host and parasite. Mol Microbiol 54: 1224-1236.
5. Besteiro, S., Williams, R.A.M., Morrison, L.S., Coombs, G.H., and Mottram, J.C. (2006) Endosome sorting and autophagy are essential for differentiation and virulence of Leishmania major. J Biol Chem 281: 11384-11396.
6. Blaineau, C., Tessier, M., Dubessay, P., Tasse, L., Crobu, L., Pages, M., etal. (2007) A novel microtubule-depolymerizing kinesin involved in length control of a eukaryotic flagellum. Curr Biol 17: 778-782.
7. Broadhead, R., Dawe, H.R., Farr, H., Griffiths, S., Hart, S.R., Portman, N., etal. (2006) Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440: 224-227.
8. Chung, C.H., Ives, H.E., Almeda, S., and Goldberg, A.L. (1983) Purification from Escherichia coli of a periplasmic protein that is a potent inhibitor of pancreatic proteases. J Biol Chem 258: 11032-11038.
9. Cihakova, J., and Volf, P. (1997) Development of different Leishmania major strains in the vector sandflies Phlebotomus papatasi and P. duboscqi. Ann Trop Med Parasitol 91: 267-279.
10. Cocucci, E., Racchetti, G., and Meldolesi, J. (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol 19: 43-51.
11. Dillon, R.J., and Lane, R.P. (1993) Bloodmeal digestion in the midgut of Phlebotomus papatasi and Phlebotomus langeroni. Med Vet Entomol 7: 225-232.
12. Dostalova, A., Votypka, J., Favreau, A., Barbian, K., Volf, P., Valenzuela, J., etal. (2011) The midgut transcriptome of Phlebotomus (Larroussius) perniciosus, a vector of Leishmania infantum: comparison of sugar fed and blood fed sand flies. BMC Genomics 12: 223.
13. Eggers, C.T., Murray, I.A., Delmar, V.A., Day, A.G., and Craik, C.S. (2004) The periplasmic serine protease inhibitor ecotin protects bacteria against neutrophil elastase. Biochem J 379: 107-118.
14. 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.
15. Eschenlauer, S.C., Faria, M.S., Morrison, L.S., Bland, N., Ribeiro-Gomes, F.L., DosReis, G.A., etal. (2009) Influence of parasite encoded inhibitors of serine peptidases in early infection of macrophages with Leishmania major. Cell Microbiol 11: 106-120.
16. Faria, M., Reis, F.C.G., Azevedo-Pereira, R.L., Morrison, L.S., Mottram, J.C., and Lima, A.P.C.A. (2011) Leishmania inhibitor of serine peptidase inhibitor 2 prevents TLR4 activation by neutrophil elastase promoting parasite survival in murine macrophages. J Immunol 186: 411-422.
17. Field, M.C., and Carrington, M. (2009) The trypanosome flagellar pocket. Nat Rev Microbiol 7: 775-786.
18. Gluenz, E., Hoog, J.L., Smith, A.E., Dawe, H.R., Shaw, M.K., and Gull, K. (2010a) Beyond 9+0: noncanonical axoneme structures characterize sensory cilia from protists to humans. FASEB J 24: 3117-3121.
19. Gluenz, E., Ginger, M.L., and McKean, P.G. (2010b) Flagellum assembly and function during the Leishmania life cycle. Curr Opin Microbiol 13: 473-479.
20. Gossage, S.M., Rogers, M.E., and Bates, P.A. (2003) Two separate growth phases during the development of Leishmania in sand flies: implications for understanding the life cycle. Int J Parasitol 33: 1027-1034.
21. Gouveia, J.J., Vasconcelos, E.J., Pacheco, A.C., Araujo-Filho, R., Maia, A.R., Kamimura, M.T., etal. (2007) Intraflagellar transport complex in Leishmania spp. In silico genome-wide screening and annotation of gene function. Genet Mol Res 6: 766-798.
22. Harder, S., Thiel, M., Clos, J., and Bruchhaus, I. (2010) Characterization of a subunit of the outer dynein arm docking complex necessary for correct flagellar assembly in Leishmania donovani. PLoS Negl Trop Dis 4: e586.
23. Hart, S.R., Lau, K.W., Hao, Z., Broadhead, R., Portman, N., Huhmer, A., etal. (2009) Analysis of the trypanosome flagellar proteome using a combined electron transfer/collisionally activated dissociation strategy. J Am Soc Mass Spectrom 20: 167-175.
24. Ivens, A.C., Peacock, C.S., Worthey, E.A., Murphy, L., Aggarwal, G., Berriman, M., etal. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436-442.
25. Katta, S.S., Tammana, T.V.S., Sahasrabuddhe, A.A., Bajpai, V.K., and Gupta, C.M. (2010) Trafficking activity of myosin XXI is required in assembly of Leishmania flagellum. J Cell Sci 123: 2035-2044.
26. Killick-Kendrick, R., Molyneux, D.H., and Ashford, R.W. (1974a) Leishmania in phlebotomid sandflies. I. Modifications of the flagellum associated with attachment to the mid-gut and oesophageal valve of the sandfly. Proc R Soc Lond B Biol Sci 187: 409-419.
27. Killick-Kendrick, R., Molyneux, D.H., and Ashford, R.W. (1974b) Ultrastructural observations on the attachment of Leishmania in the sandfly. Trans R Soc Trop Med Hyg 68: 269.
28. McConville, M.J., Mullin, K.A., Ilgoutz, S.C., and Teasdale, R.D. (2002) Secretory pathway of trypanosomatid parasites. Microbiol Mol Biol Rev 66: 122-154.
29. Molyneux, D.H., and Killick-Kendrick, R. (1987) Morphology, ultrastructure and life cycles. In The Leishmaniases in Biology and Medicine. Peters, W., and Killick-Kendrick, R. (eds). San Diego, CA: Academic Press, pp. 121-176.
30. Munday, J.C., McLuskey, K., Brown, E., Coombs, G.H., and Mottram, J.C. (2011) Oligopeptidase B-deficient mutants of Leishmania major. Mol Biochem Parasitol 175: 49-57.
31. Murray, H.W., Berman, J.D., Davies, C.R., and Saravia, N.G. (2005) Advances in leishmaniasis. Lancet 366: 1561-1577.
32. Rogers, M.B., Hilley, J.D., Dickens, N.J., Wilkes, J.M., Bates, P.A., Depledge, D.P., etal. (2011) Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res 21: 2129-2142.
33. 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.
34. Rogers, M.E., Ilg, T., Nikolaev, A.V., Ferguson, M.A., and Bates, P.A. (2004) Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 430: 463-467.
35. Rogers, M.E., Hajmová, M., Joshi, M.B., Sadlova, J., Dwyer, D.M., Volf, P., and Bates, P.A. (2008) Leishmania chitinase facilitates colonization of sand fly vectors and enhances transmission to mice. Cell Microbiol 10: 1363-1373.
36. Rotureau, B., Morales, M.A., Bastin, P., and Spath, G.F. (2009) The flagellum-mitogen-activated protein kinase connection in Trypanosomatids: a key sensory role in parasite signalling and development? Cell Microbiol 11: 710-718.
37. Sacks, D.L., Hieny, S., and Sher, A. (1985) Identification of cell surface carbohydrate and antigen changes between non-infective and infective developmental stages of Leishmania major promastigotes. J Immunol 135: 564-569.
38. Sadlova, J., and Volf, P. (2009) Peritrophic matrix of Phlebotomus duboscqi and its kinetics during Leishmania major development. Cell Tissue Res 337: 313-325.
39. Sant'Anna, M.R., Diaz-Albiter, H., Mubaraki, M., Dillon, R.J., and Bates, P.A. (2009) Inhibition of trypsin expression in Lutzomyia longipalpis using RNAi enhances the survival of Leishmania. Parasit Vectors 2: 62.
40. Santrich, C., Moore, L., Sherwin, T., Bastin, P., Brokaw, C., Gull, K., etal. (1997) A motility function for the paraflagellar rod of Leishmania parasites revealed by PFR-2 gene knockouts. Mol Biochem Parasitol 90: 95-109.
41. Silverman, J.M., Chan, S.K., Robinson, D.P., Dwyer, D.M., Nandan, D., Foster, L.J., etal. (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biol 9: R35.
42. Silverman, J.M., Clos, J., de'Oliveira, C.C., Shirvani, O., Fang, Y., Wang, C., etal. (2010) An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci 123: 842-852.
43. Stegmayer, C., Kehlenbach, A., Tournaviti, S., Wegehingel, S., Zehe, C., Denny, P., etal. (2005) Direct transport across the plasma membrane of mammalian cells of Leishmania HASPB as revealed by a CHO export mutant. J Cell Sci 118: 517-527.
44. Stierhof, Y.-D., Ilg, T., Russell, D.G., Hohenberg, H., and Overath, P. (1994) Characterization of polymer release from the flagellar pocket of Leishmania mexicana promastigotes. J Cell Biol 125: 321-331.
45. Telleria, E.L., de Araujo, A.P., Secundino, N.F., d'Avila-Levy, C.M., and Traub-Cseko, Y.M. (2010) Trypsin-like serine proteases in Lutzomyia longipalpis - expression, activity and possible modulation by Leishmania infantum chagasi. PLoS ONE 5: e10697.
46. Volf, P., and Volfova, V. (2011) Establishment and maintenance of sand fly colonies. J Vector Ecol 36 (Suppl. 1):S1-S9.
47. Volf, P., Hajmova, M., Sadlova, J., and Votypka, J. (2004) Blocked stomodeal valve of the insect vector: similar mechanism of transmission in two trypanosomatid models. Int J Parasitol 34: 1221-1227.
48. Wiese, M., Kuhn, D., and Grunfelder, C.G. (2003) Protein kinase involved in flagellar-length control. Eukaryot Cell 2: 769-777.
49. Wilson, R., Bates, M.D., Dostalova, A., Jecna, L., Dillon, R.J., Volf, P., etal. (2010) Stage-specific adhesion of Leishmania promastigotes to sand fly midguts assessed using an improved comparative binding assay. PLoS Negl Trop Dis 4: e816.
50. Yang, S.Q., Wang, C.I., Gillmor, S.A., Fletterick, R.J., and Craik, C.S. (1998) Ecotin: a serine protease inhibitor with two distinct and interacting binding sites. J Mol Biol 279: 945-957.
51. Zilberstein, D., and Shapira, M. (1994) The role of pH and temperature in the development of Leishmania parasites. Annu Rev Microbiol 48: 449-470.