Characterization of a subtilisin-like protease with apical localization from microsporidian Nosema bombycis

Journal of Invertebrate Pathology

Volumn 112, Issue 2, 2013, Pages 166-174

  Dang, Xiaoqun ^a   Pan, Guoqing ^a   Li, Tian ^a   Lin, Lipeng ^a   Ma, Qiang ^a   Geng, Lina ^a   He, Yuanli ^a   Zhou, Zeyang ^a,b  

^a SOUTHWEST UNIVERSITY   (China)

^b CHONGQING NORMAL UNIVERSITY   (China)

Author keywords

Apical localization; Germination; Microsporidia; Nosema bombycis; Subtilisin

Indexed keywords

FUNGAL PROTEIN; SERINE PROTEINASE; SUBTILISIN;

ANIMAL; ARTICLE; BACTERIAL SPORE; BIOLOGICAL PEST CONTROL; BOMBYX; CHEMISTRY; ENZYMOLOGY; GENETICS; HOST PATHOGEN INTERACTION; INTESTINE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NOSEMA; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ANIMALS; BOMBYX; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; INTESTINES; MOLECULAR SEQUENCE DATA; NOSEMA; PEST CONTROL, BIOLOGICAL; SERINE PROTEASES; SPORES; SUBTILISIN;

BACTERIA (MICROORGANISMS); BOMBYX MORI; MICROSPORIDIA; NOSEMA; NOSEMA BOMBYCIS;

EID: 84871556525     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2012.10.009     Document Type: Article

References (68)

1. Aiyar A. The use of CLUSTAL W and CLUSTAL X for multiple sequence alignment. Methods Mol. Biol. 2000, 132:221-241.
2. Akiyoshi D.E., et al. Genomic survey of the non-cultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLoS Pathog. 2009, 5:e1000261.
3. Anderson E.D., VanSlyke J.K., et al. Activation of the furin endoprotease is a multiple-step process: requirements for acidification and internal propeptide cleavage. EMBO J. 1997, 7:1508-1518.
4. Bhat S.A., et al. Microsporidiosis of silkworm, Bombyx mori L. (Lepidoptera-bombycidae): a review. Afr. J. Agric. Res. 2009, 4:1519-1523.
5. Bishu K., et al. Sildenafil and B-type natriuretic peptide acutely phosphorylate titin and improve diastolic distensibility in vivo clinical perspective. Circulation 2011, 124:2882-2891.
6. Blackman M.J., et al. A subtilisin-like protein in secretory organelles of Plasmodium falciparum merozoites. J. Biol. Chem. 1998, 273:23398-23409.
7. Bohne W., et al. Developmental expression of a tandemly repeated, glycine-and serine-rich spore wall protein in the microsporidian pathogen Encephalitozoon cuniculi. Infect Immun. 2000, 68:2268-2275.
8. Cai S., et al. Identification of a Nosema bombycis (Microsporidia) spore wall protein corresponding to spore phagocytosis. Parasitology - Cambridge 2011, 138:1102-1109.
9. Capella-Gutierrez S., et al. Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol. 2012, 10:47.
10. Chou K.C., Shen H.B. Cell-PLoc: a package of Web servers for predicting subcellular localization of proteins in various organisms. Nat. Protoc. 2008, 3:153-162.
11. Cornman R.S., et al. Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog. 2009, 5:e1000466.
12. Corradi N., et al. The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat. Commun. 2010, 1:1-7.
13. Davail S., et al. Cold adaptation of proteins. Purification, characterization, and sequence of the heat-labile subtilisin from the antarctic psychrophile Bacillus TA41. J. Biol. Chem. 1994, 269:17448.
14. Delbac F., Polonais V. The microsporidian polar tube and its role in invasion. Molecular mechanisms of parasite invasion. 2008, 47:208-220.
15. Delbac F., et al. Immunocytochemical identification of spore proteins in two microsporidia, with emphasis on extrusion apparatus. J. Eukaryot Microbiol. 1998, 45:224-231.
16. Dereeper A., et al. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol. Biol. 2010, 10:8.
17. Dyrl v Bendtsen J., et al. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
18. Freestone P., et al. The universal stress protein, UspA, of Escherichia coil is phosphorylated in response to stasis. J. Mol. Biol. 1997, 274:318-324.
19. Geer L.Y., et al. CDART: protein homology by domain architecture. Genome Res. 2002, 12:1619.
20. Hayman J.R., et al. Role of sulfated glycans in adherence of the microsporidian Encephalitozoon intestinalis to host cells in vitro. Infect Immun. 2005, 73:841-845.
21. Horton P., et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007, 35:W585.
22. Hosaka M., Nagahama M., et al. Arg-X-Lys/Arg-Arg motif as a signal for precursor cleavage catalyzed by furin within the constitutive secretory pathway. J. Biolog. Chem. 1991, 19:12127-12130.
23. Humphrey W., et al. VMD: visual molecular dynamics. J. Mol. Graph. 1996, 14:33-38.
24. James T.Y., et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 2006, 443:818-822.
25. Jia Y., et al. Functional analysis of propeptide as an intramolecular chaperone for in vivo folding of subtilisin nattokinase. FEBS Lett. 2010, 584:4789-4796.
26. Käll L., Krogh A., et al. Advantages of combined transmembrane topology and signal peptide prediction - the Phobius web server. Nucleic Acids Res. 2007, 35:429-432.
27. Katinka M.D., et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 2001, 414:450-453.
28. Keeling P.J. Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet Biol. 2003, 38:298-309.
29. Keeling P.J., Fast N.M. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol. 2002, 56:93-116.
30. Kelley L.A., Sternberg M.J.E. Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.
31. Kim D.U., Yang C.H., et al. Identification of major autolytic cleavage site of subtilisin carlsberg. Korean Biochem. J. 1990, 1:58-61.
32. Koestler T., Ebersberger I. Zygomycetes, microsporidia, and the evolutionary ancestry of sex determination. Genome Biol. Evol. 2011, 3:186-194.
33. Lagal V., et al. Toxoplasma gondii protease TgSUB1 is required for cell surface processing of micronemal adhesive complexes and efficient adhesion of tachyzoites. Cell Microbiol. 2010, 12:1792-1808.
34. Li Y., et al. Identification of a novel spore wall protein (SWP26) from microsporidia Nosema bombycis. Int. J. Parasitol. 2009, 39:391-398.
35. Li H., et al. Proteases as regulators of pathogenesis: examples from the Apicomplexa. Biochim. Biophys. Acta - Proteins Proteom. 2012, 1824:177-185.
36. Li Z., et al. SWP5, a spore wall protein, interacts with polar tube proteins in the parasitic microsporidian Nosema bombycis. Eukaryotic Cell. 2012, 11:229-237.
37. Liang L., et al. The crystal structures of two cuticle-degrading proteases from nematophagous fungi and their contribution to infection against nematodes. FASEB J. 2010, 24:1391-1400.
38. McKerrow J.H., et al. The proteases and pathogenicity of parasitic protozoa. Annu. Rev. Microbiol. 1993, 47:821-853.
39. Miller S.A., et al. A conserved subtilisin-like protein TgSUB1 in microneme organelles of Toxoplasma gondii. J. Biol. Chem. 2001, 276:45341-45348.
40. Montero E., et al. A conserved subtilisin protease identified in Babesia divergens merozoites. J. Biol. Chem. 2006, 281:35717-35726.
41. Nageli K.W. Uber die neue Krankheit der Seidenraupe und verwandte Organismen. Bot. Z. 1857, 15:760-761.
42. Pan Guoqing., et al. Expression profiles of SWP25, SWP30 and SWP32 of Nosema bombycis. Sci. Sericult. 2009, 35:328-332.
43. 5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 2006, 443:548-552.
44. Pettersen E.F., et al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
45. Peuvel-Fanget I., et al. EnP1 and EnP2, two proteins associated with the Encephalitozoon cuniculi endospore, the chitin-rich inner layer of the microsporidian spore wall. Int. J. Parasitol. 2006, 36:309-318.
46. Que X., et al. The cathepsin B of Toxoplasma gondii, toxopain-1, is critical for parasite invasion and rhoptry protein processing. J. Biol. Chem. 2002, 277:25791-25797.
47. Rajkumar R. Characterization of rat odorant binding protein variants and its post-translational modifications (PTMs): LC-MS/MS analyses of protein eluted from 2D-polyacrylamide gel electrophoresis. J. Proteom. Bioinf. 2011, 4:210-217.
48. Rawlings N.D., et al. MEROPS: the peptidase database. Nucleic Acids Res. 2006, 34:D270-D272.
49. Ronnebaumer K., et al. Identification of novel developmentally regulated genes in Encephalitozoon cuniculi: an endochitinase, a chitin-synthase, and two subtilisin-like proteases are induced during meront-to-sporont differentiation. J Eukaryot Microbiol. 2006, 53:74-76.
50. Sajid M., et al. Maturation and specificity of Plasmodium falciparum subtilisin-like protease-1, a malaria merozoite subtilisin-like serine protease. J Biol Chem. 2000, 275:631-641.
51. Shah F.A., et al. Repeated in vitro subculturing alters spore surface properties and virulence of Metarhizium anisopliae. FEMS Microbiol. Lett. 2007, 276:60-66.
52. Siezen R.J., Leunissen J.A.M. Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci. 1997, 6:501-523.
53. Silmon de Monerri N.C., et al. Global identification of multiple substrates for PfSUB1, an essential malarial processing protease. Infect Immun. 2011, 79:1086-1097.
54. Small C.L.N., Bidochka M.J. Up-regulation of Pr1, a subtilisin-like protease, during conidiation in the insect pathogen Metarhizium anisopliae. Mycol. Res. 2005, 109:307-313.
55. Southern T.R., et al. EnP1, a microsporidian spore wall protein that enables spores to adhere to and infect host cells in vitro. Eukaryot Cell. 2007, 6:1354-1362.
56. Suda Y., et al. A screen for spore wall permeability mutants identifies a secreted protease required for proper spore wall assembly. PLoS One. 2009, 4:e7184.
57. Tamura K., et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
58. Tan X.H., et al. Relationship between the germination and spore wall proteins in Nosema bombycis. Acta Zool. Sinica 2008, 54:1068-1074.
59. Wanyiri J.W., et al. Proteolytic processing of the cryptosporidium glycoprotein gp40/15 by human furin and by a parasite-derived furin-like protease activity. Infect Immun. 2007, 75:184-197.
60. Wanyiri J.W., et al. Role of CpSUB1, a subtilisin-like protease, in Cryptosporidium parvum infection in vitro. Eukaryot Cell. 2009, 8:470-477.
61. Wiederstein M., Sippl M.J. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007, 35:W407-W410.
62. Williams B.A.P. Unique physiology of host-parasite interactions in microsporidia infections. Cell Microbiol. 2009, 11:1551-1560.
63. Wright C.S., Alden R.A., et al. Structure of subtilisin BPN' at 2.5 resolution. Nature 1969, 221:235-242.
64. Wu Z., et al. Proteomic analysis of spore wall proteins and identification of two spore wall proteins from Nosema bombycis (Microsporidia). Proteomics 2008, 8:2447-2461.
65. Wu Z., et al. SWP25, a novel protein associated with the Nosema bombycis endospore. J. Eukaryot Microbiol. 2009, 56:113-118.
66. Xu Y., et al. Identification of a new spore wall protein from Encephalitozoon cuniculi. Infect Immun. 2006, 74:239-247.
67. Yeoh S., et al. Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 2007, 131:1072-1083.
68. Yike I. Fungal proteases and their pathophysiological effects. Mycopathologia 2011, 171:299-323.