Investigation of the proteolytic functions of an expanded cercarial elastase gene family in Schistosoma mansoni

PLoS Neglected Tropical Diseases

Volumn 6, Issue 4, 2012, Pages

  Ingram, Jessica R ^a,c   Rafi, Salma B ^a   Eroy Reveles, A Alegra ^a,d   Ray, Manisha ^a   Lambeth, Laura ^a   Hsieh, Ivy ^b   Ruelas, Debbie ^b   Lim, K C ^b   Sakanari, Judy ^a   Craik, Charles S ^a   Jacobson, Matthew P ^a   McKerrow, James H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d SAN FRANCISCO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELASTASE; ISOENZYME; MESSENGER RNA; PANCREATIC ELASTASE;

ARTICLE; CERCARIA; ELASTASE GENE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; GENE; GENE SEQUENCE; HOST; LARVAL STAGE; LIFE CYCLE STAGE; NONBIOLOGICAL MODEL; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; SEQUENCE ALIGNMENT; SNAIL; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; BAGG ALBINO MOUSE; BINDING SITE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; HAMSTER; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; MOUSE; PROTEIN BINDING; SEQUENCE HOMOLOGY; SYRIAN HAMSTER;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CERCARIA; CRICETINAE; GENE EXPRESSION PROFILING; MESOCRICETUS; MICE; MICE, INBRED BALB C; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PANCREATIC ELASTASE; PROTEIN BINDING; PROTEOLYSIS; SCHISTOSOMA MANSONI; SEQUENCE HOMOLOGY, AMINO ACID; SNAILS;

EID: 84861220352     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001589     Document Type: Article

References (33)

1. Chitsulo L, Engels D, Montresor A, Savioli L, (2000) The global status of schistosomiasis and its control. Acta Trop 77: 41-51.
2. Brown M, Miiro G, Nkurunziza P, Watera C, Quigley MA, et al. (2006) Schistosoma mansoni, nematode infections, and progression to active tuberculosis among HIV-1-infected Ugandans. Am J Trop Med Hyg 74: 819-825.
3. Booth M, Vennervald BJ, Kenty L, Butterworth AE, Kariuki HC, et al. (2004) Micro-geographical variation in exposure to Schistosoma mansoni and malaria, and exacerbation of splenomegaly in Kenyan school-aged children. BMC Infect Dis 4: 13 doi:10.1186/1471-2334-4-13.
4. McKerrow JH, Salter J, (2002) Invasion of skin by Schistosoma cercariae. Trends Parasitol 18: 193-195.
5. Knudsen GM, Medzihradszky KF, Lim K-C, Hansell E, McKerrow JH, (2005) Proteomic analysis of Schistosoma mansoni cercarial secretions. Mol Cell Proteomics 4: 1862-1875 doi:10.1074/mcp.M500097-MCP200.
6. Curwen RS, Ashton PD, Sundaralingam S, Wilson RA, (2006) Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Mol Cell Proteomics 5: 835-844 doi:10.1074/mcp.M500313-MCP200.
7. Salter JP, Choe Y, Albrecht H, Franklin C, Lim K-C, et al. (2002) Cercarial elastase is encoded by a functionally conserved gene family across multiple species of schistosomes. J Biol Chem 277: 24618-24624 doi:10.1074/jbc.M202364200.
8. Young ND, Jex AR, Li B, Liu S, Yang L, et al. (2012) Whole-genome sequence of Schistosoma haematobium. Nat Genet.doi:10.1038/ng.1065.
9. Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 345-351 doi:10.1038/nature08140.
10. Dvorák J, Mashiyama ST, Braschi S, Sajid M, Knudsen GM, et al. (2008) Differential use of protease families for invasion by schistosome cercariae. Biochimie 90: 345-358 doi:10.1016/j.biochi.2007.08.013.
11. Dolecková K, Kasný M, Mikes L, Cartwright J, Jedelský P, et al. (2009) The functional expression and characterisation of a cysteine peptidase from the invasive stage of the neuropathogenic schistosome Trichobilharzia regenti. Int J Parasitol 39: 201-211 doi:10.1016/j.ijpara.2008.06.010.
12. Ingram J, Knudsen G, Lim KC, Hansell E, Sakanari J, et al. (2011) Proteomic Analysis of Human Skin Treated with Larval Schistosome Peptidases Reveals Distinct Invasion Strategies among Species of Blood Flukes. PLoS Negl Trop Dis 5: e1337 doi:10.1371/journal.pntd.0001337.t001.
13. Abdulla M-H, Ruelas DS, Wolff B, Snedecor J, Lim K-C, et al. (2009) Drug Discovery for Schistosomiasis: Hit and Lead Compounds Identified in a Library of Known Drugs by Medium-Throughput Phenotypic Screening. PLoS Negl Trop Dis 3: e478 doi:10.1371/journal.pntd.0000478.t001.
14. Salter JP, Lim KC, Hansell E, Hsieh I, McKerrow JH, (2000) Schistosome invasion of human skin and degradation of dermal elastin are mediated by a single serine protease. J Biol Chem 275: 38667-38673 doi:10.1074/jbc.M006997200.
15. Brown CM, Ray M, Eroy-Reveles AA, Egea P, Tajon C, et al. (2011) Peptide length and leaving-group sterics influence potency of peptide phosphonate protease inhibitors. Chem Biol 18: 48-57 doi:10.1016/j.chembiol.2010.11.007.
16. Li CY, Lam KW, Yam LT, (1973) Esterases in human leukocytes. J Histochem Cytochem 21: 1-12.
17. Bhattacharya A, Tejero R, Montelione GT, (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66: 778-795 doi:10.1002/prot.21165.
18. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948 doi:10.1093/bioinformatics/btm404.
19. Hackey JR, Stirewalt MA, (1956) Penetration of host skin by cercariae of Schistosoma mansoni. I. Observed entry into skin of mouse, hamster, rat, monkey and man. J Parasitol 42: 565-580.
20. Lopez Quezada LA, Sajid M, Lim KC, McKerrow JH, (2011) A blood fluke serine protease inhibitor regulates an endogenous larval elastase. Journal of Biological Chemistry doi:10.1074/jbc.M111.313304.
21. Fishelson Z, Amiri P, Friend DS, Marikovsky M, Petitt M, et al. (1992) Schistosoma mansoni: cell-specific expression and secretion of a serine protease during development of cercariae. Exp Parasitol 75: 87-98.
22. Cohen FE, Gregoret LM, Amiri P, Aldape K, Railey J, et al. (1991) Arresting tissue invasion of a parasite by protease inhibitors chosen with the aid of computer modeling. Biochemistry 30: 11221-11229.
23. Remington SJ, Woodbury RG, Reynolds RA, Matthews BW, Neurath H, (1988) The structure of rat mast cell protease II at 1.9-A resolution. Biochemistry 27: 8097-8105.
24. Perona JJ, Craik CS, (1995) Structural basis of substrate specificity in the serine proteases. Protein Sci 4: 337-360 doi:10.1002/pro.5560040301.
25. Perona JJ, Craik CS, (1997) Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J Biol Chem 272: 29987-29990.
26. Lynch VJ, (2007) Inventing an arsenal: adaptive evolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evol Biol 7: 2 doi:10.1186/1471-2148-7-2.
27. Rogers MB, Hilley JD, Dickens NJ, Wilkes J, Bates PA, et al. (2011) Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Research doi:10.1101/gr.122945.111.
28. Jackson AP, (2007) Tandem gene arrays in Trypanosoma brucei: Comparative phylogenomic analysis of duplicate sequence variation. BMC Evol Biol 7: 54 doi:10.1186/1471-2148-7-54.
29. Robinson M, Dalton J, Donnelly S, (2008) Helminth pathogen cathepsin proteases: it's a family affair. Trends in Biochemical Sciences 33: 601-608 doi:10.1016/j.tibs.2008.09.001.
30. Mello LV, O'Meara H, Rigden DJ, Paterson S, (2009) Identification of novel aspartic proteases from Strongyloides ratti and characterisation of their evolutionary relationships, stage-specific expression and molecular structure. BMC Genomics 10: 611 doi:10.1186/1471-2164-10-611.
31. Hansell E, Braschi S, Medzihradszky KF, Sajid M, Debnath M, et al. (2008) Proteomic analysis of skin invasion by blood fluke larvae. PLoS Negl Trop Dis 2: e262 doi:10.1371/journal.pntd.0000262.
32. Gobert GN, Tran MH, Moertel L, Mulvenna J, Jones MK, et al. (2010) Transcriptional Changes in Schistosoma mansoni during Early Schistosomula Development and in the Presence of Erythrocytes. PLoS Negl Trop Dis 4: e600 doi:10.1371/journal.pntd.0000600.t002.
33. McKerrow J, Pino-Heiss S, Lindquist R, (1985) Purification and characterization of an elastinolytic proteinase secreted by cercariae of Schistosoma mansoni. J Bio Chem Mar 25;260 (6): 3703-7.