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Serine protease inhibitors of parasitic helminths

Published online by Cambridge University Press:  06 February 2012

ADEBAYO J. MOLEHIN ,
GEOFFREY N. GOBERT  and
DONALD P. McMANUS
ADEBAYO J. MOLEHIN*
Affiliation:
Molecular Parasitology Laboratory, Department of Biology, Queensland Institute of Medical Research, 300 Herston Road, Herston, Queensland, Australia 4006 School of Population Health, The University of Queensland, Herston Road, Herston, Queensland, Australia4006
GEOFFREY N. GOBERT
Affiliation:
Molecular Parasitology Laboratory, Department of Biology, Queensland Institute of Medical Research, 300 Herston Road, Herston, Queensland, Australia 4006
DONALD P. McMANUS
Affiliation:
Molecular Parasitology Laboratory, Department of Biology, Queensland Institute of Medical Research, 300 Herston Road, Herston, Queensland, Australia 4006
*
*Corresponding author: Molecular Parasitology Laboratory, Department of Biology, Queensland Institute of Medical Research, 300 Herston Road, Herston, Queensland, Australia4006. Tel: +61 73362 0405. Fax: +61 73362 0104. E-mail: adebayo.molehin@qimr.edu.au
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Summary

Serine protease inhibitors (serpins) are a superfamily of structurally conserved proteins that inhibit serine proteases and play key physiological roles in numerous biological systems such as blood coagulation, complement activation and inflammation. A number of serpins have now been identified in parasitic helminths with putative involvement in immune regulation and in parasite survival through interference with the host immune response. This review describes the serpins and smapins (small serine protease inhibitors) that have been identified in Ascaris spp., Brugia malayi, Ancylostoma caninum Onchocerca volvulus, Haemonchus contortus, Trichinella spiralis, Trichostrongylus vitrinus, Anisakis simplex, Trichuris suis, Schistosoma spp., Clonorchis sinensis, Paragonimus westermani and Echinococcus spp. and discusses their possible biological functions, including roles in host-parasite interplay and their evolutionary relationships.

Keywords

serine protease inhibitorsserpinssmall serine protease inhibitorssmapins biochemical characterizationparasitic helminths
Type
Review Article
Information
Parasitology , Volume 139 , Issue 6 , May 2012 , pp. 681 - 695
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Aguinaldo, A. M., Turbeville, J. M., Linford, L. S., Rivera, M. C., Garey, J. R., Raff, R. A. and Lake, J. A. (1997). Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489–493. doi: 10.1038/387489a0CrossRefGoogle ScholarPubMed
Audicana, M. T. and Kennedy, M. W. (2008). Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiology Reviews 21, 360–379, table of contents. doi: 21/2/360 [pii]CrossRefGoogle ScholarPubMed
Axelsson, U. and Laurell, C. B. (1965). Hereditary variants of serum alpha-1-antitrypsin. American Journal of Human Genetics 17, 466–472.Google ScholarPubMed
Babin, D. R., Peanasky, R. J. and Goos, S. M. (1984). The isoinhibitors of chymotrypsin/elastase from Ascaris lumbricoides: the primary structure. Archives of Biochemistry and Biophysics 232, 143–161. doi: 0003-9861(84)90530-7 [pii]CrossRefGoogle ScholarPubMed
Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M. A., Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G. and El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature, London 460, 352–358. doi: nature08160 [pii]CrossRefGoogle ScholarPubMed
Blanton, R. E., Licate, L. S. and Aman, R. A. (1994). Characterization of a native and recombinant Schistosoma haematobium serine protease inhibitor gene product. Molecular and Biochemical Parasitology 63, 1–11. doi: 0166-6851(94)90003-5 [pii]CrossRefGoogle ScholarPubMed
Cappello, M., Vlasuk, G. P., Bergum, P. W., Huang, S. and Hotez, P. J. (1995). Ancylostoma caninum anticoagulant peptide: a hookworm-derived inhibitor of human coagulation factor Xa. Proceedings of the National Academy of Sciences, USA 92, 6152–6156.CrossRefGoogle ScholarPubMed
Carrell, R. W. and Owen, M. C. (1985). Plakalbumin, alpha 1-antitrypsin, antithrombin and the mechanism of inflammatory thrombosis. Nature, London 317, 730–732.CrossRefGoogle ScholarPubMed
Carrell, R. W., Stein, P. E., Fermi, G. and Wardell, M. R. (1994). Biological implications of a 3 A structure of dimeric antithrombin. Structure 2, 257–270.CrossRefGoogle ScholarPubMed
Chertov, O., Ueda, H., Xu, L. L., Tani, K., Murphy, W. J., Wang, J. M., Howard, O. M., Sayers, T. J. and Oppenheim, J. J. (1997). Identification of human neutrophil-derived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. Journal of Experimental Medicine 186, 739–747.CrossRefGoogle ScholarPubMed
Chopin, V., Bilfinger, T. V., Stefano, G. B., Matias, I. and Salzet, M. (1997). Amino-acid-sequence determination and biological activity of cytin, a naturally occurring specific chymotrypsin inhibitor from the leech Theromyzon tessulatum. European Journal of Biochemistry 249, 733–738.CrossRefGoogle ScholarPubMed
Chopin, V., Matias, I., Stefano, G. B. and Salzet, M. (1998 a). Amino acid sequence determination and biological activity of therin, a naturally occuring specific trypsin inhibitor from the leech Theromyzon tessulatum. European Journal of Biochemistry 254, 565–570.CrossRefGoogle ScholarPubMed
Chopin, V., Stefano, G. B. and Salzet, M. (1998 b). Amino-acid-sequence determination and biological activity of tessulin, a naturally occurring trypsin-chymotrypsin inhibitor isolated from the leech Theromyzon tessulatum. European Journal of Biochemistry 258, 662–668.CrossRefGoogle ScholarPubMed
de Silva, N. R., Brooker, S., Hotez, P. J., Montresor, A., Engels, D. and Savioli, L. (2003). Soil-transmitted helminth infections: updating the global picture. Trends in Parasitology 19, 547–551. doi: S1471492203002757 [pii]CrossRefGoogle ScholarPubMed
Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M. and Gascuel, O. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36, W465–469. doi: gkn180 [pii]CrossRefGoogle ScholarPubMed
Duggan, B. M., Dyson, H. J. and Wright, P. E. (1999). Inherent flexibility in a potent inhibitor of blood coagulation, recombinant nematode anticoagulant protein c2. European Journal of Biochemistry 265, 539–548. doi: ejb781 [pii]CrossRefGoogle Scholar
Elliott, P. R., Lomas, D. A., Carrell, R. W. and Abrahams, J. P. (1996). Inhibitory conformation of the reactive loop of alpha 1-antitrypsin. Nature Structural Biology 3, 676–681.CrossRefGoogle ScholarPubMed
Elliott, P. R., Pei, X. Y., Dafforn, T. R. and Lomas, D. A. (2000). Topography of a 2.0 A structure of alpha1-antitrypsin reveals targets for rational drug design to prevent conformational disease. Protein Science 9, 1274–1281. doi: 10.1110/ps.9.7.1274CrossRefGoogle ScholarPubMed
Engh, R., Lobermann, H., Schneider, M., Wiegand, G., Huber, R. and Laurell, C. B. (1989). The S variant of human alpha 1-antitrypsin, structure and implications for function and metabolism. Protein Engineering 2, 407–415.CrossRefGoogle Scholar
Ford, L., Guiliano, D. B., Oksov, Y., Debnath, A. K., Liu, J., Williams, S. A., Blaxter, M. L. and Lustigman, S. (2005). Characterization of a novel filarial serine protease inhibitor, Ov-SPI-1, from Onchocerca volvulus, with potential multifunctional roles during development of the parasite. Journal of Biological Chemistry 280, 40845–40856. doi: M504434200 [pii]CrossRefGoogle ScholarPubMed
Gettins, P. G. (2002). Serpin structure, mechanism, and function. Chemical Reviews 102, 4751–4804. doi: cr010170+[pii]CrossRefGoogle ScholarPubMed
Ghedin, E., Wang, S., Spiro, D., Caler, E., Zhao, Q., Crabtree, J., Allen, J. E., Delcher, A. L., Guiliano, D. B., Miranda-Saavedra, D., Angiuoli, S. V., Creasy, T., Amedeo, P., Haas, B., El-Sayed, N. M., Wortman, J. R., Feldblyum, T., Tallon, L., Schatz, M., Shumway, M., Koo, H., Salzberg, S. L., Schobel, S., Pertea, M., Pop, M., White, O., Barton, G. J., Carlow, C. K., Crawford, M. J., Daub, J., Dimmic, M. W., Estes, C. F., Foster, J. M., Ganatra, M., Gregory, W. F., Johnson, N. M., Jin, J., Komuniecki, R., Korf, I., Kumar, S., Laney, S., Li, B. W., Li, W., Lindblom, T. H., Lustigman, S., Ma, D., Maina, C. V., Martin, D. M., McCarter, J. P., McReynolds, L., Mitreva, M., Nutman, T. B., Parkinson, J., Peregrin-Alvarez, J. M., Poole, C., Ren, Q., Saunders, L., Sluder, A. E., Smith, K., Stanke, M., Unnasch, T. R., Ware, J., Wei, A. D., Weil, G., Williams, D. J., Zhang, Y., Williams, S. A., Fraser-Liggett, C., Slatko, B., Blaxter, M. L. and Scott, A. L. (2007). Draft genome of the filarial nematode parasite Brugia malayi. Science 317, 1756–1760. doi: 317/5845/1756 [pii]CrossRefGoogle ScholarPubMed
Ghendler, Y., Arnon, R. and Fishelson, Z. (1994). Schistosoma mansoni: isolation and characterization of Smpi56, a novel serine protease inhibitor. Experimental Parasitology 78, 121–131. doi: S0014-4894(84)71013-7 [pii]CrossRefGoogle ScholarPubMed
Gils, A. and Declerck, P. J. (1998). Structure-function relationships in serpins: current concepts and controversies. Thrombosis and Haemostasis 80, 531–541. doi: 98100531 [pii]Google Scholar
Goodwin, R. L., Baumann, H. and Berger, F. G. (1996). Patterns of divergence during evolution of alpha 1-proteinase inhibitors in mammals. Molecular Biology and Evolution 13, 346–358.CrossRefGoogle ScholarPubMed
Gooptu, B., Hazes, B., Chang, W. S., Dafforn, T. R., Carrell, R. W., Read, R. J. and Lomas, D. A. (2000). Inactive conformation of the serpin alpha(1)-antichymotrypsin indicates two-stage insertion of the reactive loop: implications for inhibitory function and conformational disease. Proceedings of the National Academy of Sciences, USA 97, 67–72.CrossRefGoogle ScholarPubMed
Grasberger, B. L., Clore, G. M. and Gronenborn, A. M. (1994). High-resolution structure of Ascaris trypsin inhibitor in solution: direct evidence for a pH-induced conformational transition in the reactive site. Structure 2, 669–678.CrossRefGoogle ScholarPubMed
Graur, D. and Li, W. H. (1988). Evolution of protein inhibitors of serine proteinases: positive Darwinian selection or compositional effects? Journal of Molecular Evolution 28, 131–135.CrossRefGoogle ScholarPubMed
Guiliano, D. B., Hong, X., McKerrow, J. H., Blaxter, M. L., Oksov, Y., Liu, J., Ghedin, E. and Lustigman, S. (2004). A gene family of cathepsin L-like proteases of filarial nematodes are associated with larval molting and cuticle and eggshell remodeling. Molecular and Biochemical Parasitology 136, 227–242.CrossRefGoogle ScholarPubMed
Hashmi, S., Britton, C., Liu, J., Guiliano, D. B., Oksov, Y. and Lustigman, S. (2002). Cathepsin L is essential for embryogenesis and development of Caenorhabditis elegans. Journal of Biological Chemistry 277, 3477–3486. doi: 10.1074/jbc.M106117200CrossRefGoogle ScholarPubMed
He, Y., Luo, X., Zhang, X., Yu, X., Lin, J., Li, Y., Li, Y. and Liu, S. (1999). Immunological characteristics of natural resistance in Microtus fortis to infection with Schistosoma japonicum. Chinese Medical Journal (English Edition) 112, 649–654.Google ScholarPubMed
Hill, R. E. and Hastie, N. D. (1987). Accelerated evolution in the reactive centre regions of serine protease inhibitors. Nature, London 326, 96–99. doi: 10.1038/326096a0CrossRefGoogle ScholarPubMed
Hirst, C. E., Buzza, M. S., Bird, C. H., Warren, H. S., Cameron, P. U., Zhang, M., Ashton-Rickardt, P. G. and Bird, P. I. (2003). The intracellular granzyme B inhibitor, proteinase inhibitor 9, is up-regulated during accessory cell maturation and effector cell degranulation, and its overexpression enhances CTL potency. Journal of Immunology 170, 805–815.CrossRefGoogle ScholarPubMed
Hogan, B. J. (1980). Function of the gut in the parasitic roundworm Ascaris lumbricoides var. suum. Proceedings of the South Dakota Academy of Sciences 59, 283.Google Scholar
Hopkins, P. C., Carrell, R. W. and Stone, S. R. (1993). Effects of mutations in the hinge region of serpins. Biochemistry 32, 7650–7657.CrossRefGoogle ScholarPubMed
Huang, W., Haas, T. A., Biesterfeldt, J., Mankawsky, L., Blanton, R. E. and Lee, X. (1999). Purification and crystallization of a novel membrane-anchored protein: the Schistosoma haematobium serpin. Acta Crystallographica. Section D, Biological Crystallography 55, 350–352. doi: 10.1107/S0907444998008658CrossRefGoogle ScholarPubMed
Huber, R. and Carrell, R. W. (1989). Implications of the three-dimensional structure of alpha 1-antitrypsin for structure and function of serpins. Biochemistry 28, 8951–8966.CrossRefGoogle ScholarPubMed
Hunt, L. T. and Dayhoff, M. O. (1980). A surprising new protein superfamily containing ovalbumin, antithrombin-III, and alpha 1-proteinase inhibitor. Biochemical and Biophysical Research Communications 95, 864–871. doi: 0006-291X(80)90867-0 [pii]CrossRefGoogle ScholarPubMed
Huntington, J. A., Read, R. J. and Carrell, R. W. (2000). Structure of a serpin-protease complex shows inhibition by deformation. Nature, London 407, 923–926. doi: 10.1038/35038119CrossRefGoogle ScholarPubMed
Hwang, J. H., Lee, W. G., Na, B. K., Lee, H. W., Cho, S. H. and Kim, T. S. (2009). Identification and characterization of a serine protease inhibitor of Paragonimus westermani. Parasitology Research 104, 495–501. doi: 10.1007/s00436-008-1219-6CrossRefGoogle ScholarPubMed
Irving, J. A., Pike, R. N., Lesk, A. M. and Whisstock, J. C. (2000). Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Research 10, 1845–1864.CrossRefGoogle ScholarPubMed
Jex, A. R., Liu, S., Li, B., Young, N. D., Hall, R. S., Li, Y., Yang, L., Zeng, N., Xu, X., Xiong, Z., Chen, F., Wu, X., Zhang, G., Fang, X., Kang, Y., Anderson, G. A., Harris, T. W., Campbell, B. E., Vlaminck, J., Wang, T., Cantacessi, C., Schwarz, E. M., Ranganathan, S., Geldhof, P., Nejsum, P., Sternberg, P. W., Yang, H., Wang, J. and Gasser, R. B. (2011). Ascaris suum draft genome. Nature, London 479, 529–533. doi: 10.1038/nature10553CrossRefGoogle ScholarPubMed
Jiang, D., Zhan, B., Mayor, R. S., Gillespie, P., Keegan, B., Bottazzi, M. E. and Hotez, P. (2011). Ac-AP-12, a novel factor Xa anticoagulant peptide from the esophageal glands of adult Ancylostoma caninum. Molecular and Biochemical Parasitology 177, 42–48. doi: S0166-6851(11)00034-X [pii]CrossRefGoogle ScholarPubMed
Juhasz, S. and Nemeth, I. (1979). Proteolytic enzymes and enzyme inhibitors in Ascaris suum. IV. Estimation of molecular weights of chymotrypsin inhibitors and an intestinal protease by gel chromatography. Acta Veterinaria Academiae Scientiarum Hungaricae 27, 217–224.Google Scholar
Kang, J. M., Sohn, W. M., Ju, J. W., Kim, T. S. and Na, B. K. (2010). Identification and characterization of a serine protease inhibitor of Clonorchis sinensis. Acta Tropica 116, 134–140. doi: S0001-706X(10)00180-4 [pii]CrossRefGoogle ScholarPubMed
Khan, M. S., Singh, P., Azhar, A., Naseem, A., Rashid, Q., Kabir, M. A. and Jairajpuri, M. A. (2011). Serpin InhibitionMechanism: A Delicate Balance between Native Metastable State and Polymerization. Journal of Amino Acids 2011, 1–10.CrossRefGoogle Scholar
Knox, D. P. (2007). Proteinase inhibitors and helminth parasite infection. Parasite Immunology 29, 57–71. doi: PIM913 [pii]CrossRefGoogle ScholarPubMed
Kobayashi, Y., Ishizaki, S., Shimakura, K., Nagashima, Y. and Shiomi, K. (2007 a). Molecular cloning and expression of two new allergens from Anisakis simplex. Parasitology Research 100, 1233–1241. doi: 10.1007/s00436-006-0396-4CrossRefGoogle ScholarPubMed
Kobayashi, Y., Shimakura, K., Ishizaki, S., Nagashima, Y. and Shiomi, K. (2007 b). Purification and cDNA cloning of a new heat-stable allergen from Anisakis simplex. Molecular and Biochemical Parasitology 155, 138–145. doi: S0166-6851(07)00171-5 [pii]CrossRefGoogle ScholarPubMed
Lawrence, D. A., Olson, S. T., Palaniappan, S. and Ginsburg, D. (1994). Serpin reactive center loop mobility is required for inhibitor function but not for enzyme recognition. Journal of Biological Chemistry 269, 27657–27662.CrossRefGoogle Scholar
Li, J., Zhang, W. B., Wilson, M., Ito, A. and McManus, D. P. (2003). A novel recombinant antigen for immunodiagnosis of human cystic echinococcosis. Journal of Infectious Diseases 188, 1951–1960. doi: JID31042 [pii]CrossRefGoogle ScholarPubMed
Li, Z., King, C. L., Ogundipe, J. O., Licate, L. S. and Blanton, R. E. (1995). Preferential recognition by human IgE and IgG4 of a species-specific Schistosoma haematobium serine protease inhibitor. Journal of Infectious Diseases 171, 416–422.CrossRefGoogle ScholarPubMed
Lomas, D. A., Elliott, P. R., Chang, W. S., Wardell, M. R. and Carrell, R. W. (1995). Preparation and characterization of latent alpha 1-antitrypsin. Journal of Biological Chemistry 270, 5282–5288.CrossRefGoogle ScholarPubMed
Lu, C. C., Nguyen, T., Morris, S., Hill, D. and Sakanari, J. A. (1998). Anisakis simplex: mutational bursts in the reactive site centers of serine protease inhibitors from an ascarid nematode. Experimental Parasitology 89, 257–261. doi: S0014–4894(98)94284-9 [pii]CrossRefGoogle ScholarPubMed
Lun, Z. R., Gasser, R. B., Lai, D. H., Li, A. X., Zhu, X. Q., Yu, X. B. and Fang, Y. Y. (2005). Clonorchiasis: a key foodborne zoonosis in China. Lancet Infectious Diseases 5, 31–41. doi: S1473309904012526 [pii]CrossRefGoogle ScholarPubMed
MacLennan, K., McLean, K. and Knox, D. P. (2005). Serpin expression in the parasitic stages of Trichostrongylus vitrinus, an ovine intestinal nematode. Parasitology 130, 349–357.CrossRefGoogle ScholarPubMed
Maizels, R. M., Bundy, D. A., Selkirk, M. E., Smith, D. F. and Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature, London 365, 797–805. doi: 10.1038/365797a0CrossRefGoogle ScholarPubMed
Marshall, C. J. (1993). Evolutionary relationships among the serpins. Philosophical Transactions of the Royal Society of London, B 342, 101–119. doi: 10.1098/rstb.1993.0141Google ScholarPubMed
Martzen, M. R., Geise, G. L., Hogan, B. J. and Peanasky, R. J. (1985). Ascaris suum: localization by immunochemical and fluorescent probes of host proteases and parasite proteinase inhibitors in cross-sections. Experimental Parasitology 60, 139–149. doi: 0014-4894(85)90016-5 [pii]CrossRefGoogle ScholarPubMed
Martzen, M. R., Geise, G. L. and Peanasky, R. J. (1986). Ascaris suum: immunoperoxidase and fluorescent probe analysis of host proteases and parasite proteinase inhibitors in developing eggs and second stage larvae. Experimental Parasitology 61, 138–145. doi: 0014-4894(86)90145-1 [pii]CrossRefGoogle ScholarPubMed
Meeusen, E. N., Balic, A. and Bowles, V. (2005). Cells, cytokines and other molecules associated with rejection of gastrointestinal nematode parasites. Veterinary Immunology and Immunopathology 108, 121–125. doi: S0165-2427(05)00207-2 [pii]CrossRefGoogle ScholarPubMed
Merckelbach, A. and Ruppel, A. (2007). Biochemical properties of an intracellular serpin from Echinococcus multilocularis. Molecular and Biochemical Parasitology 156, 84–88. doi: S0166-6851(07)00216-2 [pii]CrossRefGoogle ScholarPubMed
Michael, E., Bundy, D. A. and Grenfell, B. T. (1996). Re-assessing the global prevalence and distribution of lymphatic filariasis. Parasitology 112 (Pt 4), 409–428.CrossRefGoogle ScholarPubMed
Mieszczanek, J., Harrison, L. M., Vlasuk, G. P. and Cappello, M. (2004). Anticoagulant peptides from Ancylostoma caninum are immunologically distinct and localize to separate structures within the adult hookworm. Molecular and Biochemical Parasitology 133, 319–323. doi: S0166685103003153 [pii]CrossRefGoogle ScholarPubMed
Miller, H. R. P. (1984). The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Veterinary Immunology and Immunopathology 6, 167–259.CrossRefGoogle ScholarPubMed
Mitreva, M., Jasmer, D. P., Zarlenga, D. S., Wang, Z., Abubucker, S., Martin, J., Taylor, C. M., Yin, Y., Fulton, L., Minx, P., Yang, S. P., Warren, W. C., Fulton, R. S., Bhonagiri, V., Zhang, X., Hallsworth-Pepin, K., Clifton, S. W., McCarter, J. P., Appleton, J., Mardis, E. R. and Wilson, R. K. (2011). The draft genome of the parasitic nematode Trichinella spiralis. Nature Genetics 43, 228–235. doi: ng.769 [pii]CrossRefGoogle ScholarPubMed
Modha, J. and Doenhoff, M. J. (1994). Schistosoma mansoni host-parasite relationship: interaction of contrapsin with adult worms. Parasitology 109, 487–495.CrossRefGoogle ScholarPubMed
Monard, D., Reinhard, E., Meier, R., ▪, J., ▪, S., Farmer, L., Rovelli, G. and Ortmann, R. (1990). Steps in establishing a biological relevance for glial-derived nexin. Serine Proteases and Their Serpin Inhibitors in the Nervous System 69–78.Google Scholar
Mottonen, J., Strand, A., Symersky, J., Sweet, R. M., Danley, D. E., Geoghegan, K. F., Gerard, R. D. and Goldsmith, E. J. (1992). Structural basis of latency in plasminogen activator inhibitor-1. Nature, London 355, 270–273. doi: 10.1038/355270a0CrossRefGoogle ScholarPubMed
Nagano, I., Wu, Z., Nakada, T., Matsuo, A. and Takahashi, Y. (2001). Molecular cloning and characterization of a serine proteinase inhibitor from Trichinella spiralis. Parasitology 123, 77–83.CrossRefGoogle ScholarPubMed
Nathoo, S., Rasums, A., Katz, J., Ferguson, W. S. and Finlay, T. H. (1982). Purification and properties of two different alpha 1-protease inhibitors from mouse plasma. Archives of Biochemistry and Biophysics 219, 306–315.CrossRefGoogle ScholarPubMed
Peanasky, R. J., Bentz, Y., Paulson, B., Graham, D. L. and Babin, D. R. (1984). The isoinhibitors of chymotrypsin/elastase from Ascaris lumbricoides: isolation by affinity chromatography and association with the enzymes. Archives of Biochemistry and Biophysics 232, 127–134. doi: 0003-9861(84)90528-9 [pii]CrossRefGoogle ScholarPubMed
Peterson, F. C., Gordon, N. C. and Gettins, P. G. (2000). Formation of a noncovalent serpin-proteinase complex involves no conformational change in the serpin. Use of 1H-15N HSQC NMR as a sensitive nonperturbing monitor of conformation. Biochemistry 39, 11884–11892. doi: bi001152+[pii]CrossRefGoogle ScholarPubMed
Poole, C. B., Jin, J. and McReynolds, L. A. (2003). Cloning and biochemical characterization of blisterase, a subtilisin-like convertase from the filarial parasite, Onchocerca volvulus. Journal of Biological Chemistry 278, 36183–36190. doi: 10.1074/jbc.M302601200CrossRefGoogle ScholarPubMed
Prevot, P. P., Adam, B., Boudjeltia, K. Z., Brossard, M., Lins, L., Cauchie, P., Brasseur, R., Vanhaeverbeek, M., Vanhamme, L. and Godfroid, E. (2006). Anti-hemostatic effects of a serpin from the saliva of the tick Ixodes ricinus. Journal of Biological Chemistry 281, 26361–26369. doi: M604197200 [pii]CrossRefGoogle ScholarPubMed
Quezada, L. A. and McKerrow, J. H. (2011). Schistosome serine protease inhibitors: parasite defense or homeostasis? Anais da Academia Brasileira de Ciencias 83, 663–672. doi: S0001-37652011000200025 [pii]CrossRefGoogle ScholarPubMed
Rawlings, N. D., Tolle, D. P. and Barrett, A. J. (2004). Evolutionary families of peptidase inhibitors. The Biochemical Journal 378, 705–716. doi: 10.1042/BJ20031825CrossRefGoogle ScholarPubMed
Rhoads, M. L., Fetterer, R. H. and Hill, D. E. (2000 a). Trichuris suis: A secretory serine protease inhibitor. Experimental Parasitology 94, 1–7. doi: 10.1006/expr.1999.4466CrossRefGoogle ScholarPubMed
Rhoads, M. L., Fetterer, R. H., Hill, D. E. and Urban, J. F. Jr. (2000 b). Trichuris suis: a secretory chymotrypsin/elastase inhibitor with potential as an immunomodulator. Experimental Parasitology 95, 36–44. doi: 10.1006/expr.2000.4502CrossRefGoogle ScholarPubMed
Ritchie, H. and Booth, N. A. (1998). Secretion of plasminogen activator inhibitor 2 by human peripheral blood monocytes occurs via an endoplasmic reticulum-golgi-independent pathway. Experimental Cell Research 242, 439–450. doi: S0014-4827(98)94118-0 [pii]CrossRefGoogle ScholarPubMed
Sanchez, F., March, F., Mercader, M., Coll, P., Munoz, C. and Prats, G. (1991). Immunochemical localization of major hydatid fluid antigens in protoscoleces and cysts of Echinococcus granulosus from human origin. Parasite Immunology 13, 583–592.CrossRefGoogle ScholarPubMed
Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009).Google Scholar
Shepherd, J. C., Aitken, A. and McManus, D. P. (1991). A protein secreted in vivo by Echinococcus granulosus inhibits elastase activity and neutrophil chemotaxis. Molecular & Biochemical Parasitology 44, 81–90. doi: 0166-6851(91)90223-S [pii]CrossRefGoogle ScholarPubMed
Silverman, G. A., Whisstock, J. C., Bottomley, S. P., Huntington, J. A., Kaiserman, D., Luke, C. J., Pak, S. C., Reichhart, J. M. and Bird, P. I. (2010). Serpins flex their muscle: I. Putting the clamps on proteolysis in diverse biological systems. Journal of Biological Chemistry 285, 24299–24305. doi: R110.112771 [pii]CrossRefGoogle ScholarPubMed
Spakulová, M., Orosová, M. and Mackiewicz, J. S. (2011). Cytogenetics and chromosomes of tapeworms (Platyhelminthes, Cestoda). Advances in Parasitology 74, 177–230.CrossRefGoogle ScholarPubMed
Stanley, P. and Stein, P. E. (2003). BmSPN2, a serpin secreted by the filarial nematode Brugia malayi, does not inhibit human neutrophil proteinases but plays a noninhibitory role. Biochemistry 42, 6241–6248. doi: 10.1021/bi0271650CrossRefGoogle ScholarPubMed
Stassens, P., Bergum, P. W., Gansemans, Y., Jespers, L., Laroche, Y., Huang, S., Maki, S., Messens, J., Lauwereys, M., Cappello, M., Hotez, P. J., Lasters, I. and Vlasuk, G. P. (1996). Anticoagulant repertoire of the hookworm Ancylostoma caninum. Proceedings of the National Academy of Sciences, USA 93, 2149–2154.CrossRefGoogle ScholarPubMed
Takahara, H. and Sinohara, H. (1983 a). [Contrapsin, a novel trypsin inhibitor in the mouse plasma]. Seikagaku (Journal of Japanese Biochemical Society) 55, 1426–1433.Google ScholarPubMed
Takahara, H. and Sinohara, H. (1983 b). Inhibitory spectrum of mouse contrapsin and alpha-1-antitrypsin against mouse serine proteases. Journal of Biochemistry 93, 1411–1419.CrossRefGoogle ScholarPubMed
van Gent, D., Sharp, P., Morgan, K. and Kalsheker, N. (2003). Serpins: structure, function and molecular evolution. The International Journal of Biochemistry & Cell Biology 35, 1536–1547. doi: Doi: 10.1016/s1357-2725(03)00134-1CrossRefGoogle ScholarPubMed
Whisstock, J. C., Silverman, G. A., Bird, P. I., Bottomley, S. P., Kaiserman, D., Luke, C. J., Pak, S. C., Reichhart, J. M. and Huntington, J. A. (2010). Serpins flex their muscle: II. Structural insights into target peptidase recognition, polymerization, and transport functions. Journal of Biological Chemistry 285, 24307–24312. doi: R110.141408 [pii]CrossRefGoogle ScholarPubMed
Yan, Y., Liu, S., Song, G., Xu, Y. and Dissous, C. (2005). Characterization of a novel vaccine candidate and serine proteinase inhibitor from Schistosoma japonicum (Sj serpin). Veterinary Parasitology 131, 53–60. doi: S0304-4017(05)00208-6 [pii]CrossRefGoogle ScholarPubMed
Yang, Y., Hu, D., Wang, L., Liang, C., Hu, X., Wang, X., Chen, J., Xu, J. and Yu, X. (2009). Molecular cloning and characterization of a novel serpin gene of Clonorchis sinensis, highly expressed in the stage of metacercaria. Parasitology Research 106, 221–225. doi: 10.1007/s00436-009-1654-zCrossRefGoogle ScholarPubMed
Ye, S., Cech, A. L., Belmares, R., Bergstrom, R. C., Tong, Y., Corey, D. R., Kanost, M. R. and Goldsmith, E. J. (2001). The structure of a Michaelis serpin-protease complex. Nature Structural Biology 8, 979–983. doi: 10.1038/nsb1101-979CrossRefGoogle ScholarPubMed
Yenbutr, P. and Scott, A. L. (1995). Molecular cloning of a serine proteinase inhibitor from Brugia malayi. Infection and Immunity 63, 1745–1753.CrossRefGoogle ScholarPubMed
Yi, D., Xu, L., Yan, R. and Li, X. (2010). Haemonchus contortus: cloning and characterization of serpin. Experimental Parasitology 125, 363–370. doi: S0014-4894(10)00087-1 [pii]CrossRefGoogle ScholarPubMed
Zang, X., Atmadja, A. K., Gray, P., Allen, J. E., Gray, C. A., Lawrence, R. A., Yazdanbakhsh, M. and Maizels, R. M. (2000). The serpin secreted by Brugia malayi microfilariae, Bm-SPN-2, elicits strong, but short-lived, immune responses in mice and humans. Journal of Immunology 165, 5161–5169.CrossRefGoogle ScholarPubMed
Zang, X. and Maizels, R. M. (2001). Serine proteinase inhibitors from nematodes and the arms race between host and pathogen. Trends in Biochemical Sciences 26, 191–197. doi: Doi: 10.1016/s0968-0004(00)01761-8CrossRefGoogle ScholarPubMed
Zang, X., Yazdanbakhsh, M., Jiang, H., Kanost, M. R. and Maizels, R. M. (1999). A novel serpin expressed by blood-borne microfilariae of the parasitic nematode Brugia malayi inhibits human neutrophil serine proteinases. Blood 94, 1418–1428.CrossRefGoogle ScholarPubMed
Zhang, M., Park, S. M., Wang, Y., Shah, R., Liu, N., Murmann, A. E., Wang, C. R., Peter, M. E. and Ashton-Rickardt, P. G. (2006). Serine protease inhibitor 6 protects cytotoxic T cells from self-inflicted injury by ensuring the integrity of cytotoxic granules. Immunity 24, 451–461. doi: S1074-7613(06)00138-5 [pii]CrossRefGoogle ScholarPubMed
Zhang, W., Li, J., Jones, M. K., Zhang, Z., Zhao, L., Blair, D. and McManus, D. P. (2010). The Echinococcus granulosus antigen B gene family comprises at least 10 unique genes in five subclasses which are differentially expressed. PLoS Neglected Tropical Diseases 4, e784. doi: e784 [pii]CrossRefGoogle ScholarPubMed
Zhang, W., Li, J. and McManus, D. P. (2003). Concepts in immunology and diagnosis of hydatid disease. Clinical Microbiology Reviews 16, 18–36.CrossRefGoogle ScholarPubMed