Purification of a chymotrypsin-like enzyme present on adult Schistosoma mansoni worms from infected mice and its characterization as a host carboxylesterase

Parasitology

Volumn 143, Issue 5, 2016, Pages 646-657

  Igetei, Joseph E ^a,b   Liddell, Susan ^a   El Faham, Marwa ^a,c   Doenhoff, Michael J ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF BENIN   (Nigeria)

^c ALEXANDRIA UNIVERSITY   (Egypt)

Author keywords

carboxylesterase 1C; host derived enzyme; immune evasion; mice; Schistosoma mansoni

Indexed keywords

1 NAPHTHYL ACETATE; ALCOHOL; CARBOXYLESTERASE; CHROMOGENIC SUBSTRATE; CHYMOTRYPSIN; ESTER DERIVATIVE; HYDROLYASE; SODIUM CHLORIDE; N-ACETYLPHENYLALANINE BETA-NAPHTHYL ESTER; PHENYLALANINE; SERUM ALBUMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BLOOD VESSEL; CONTROLLED STUDY; ENZYME PURIFICATION; FEMALE; HOST PARASITE INTERACTION; HYDROLYSIS; IMMUNE EVASION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PURIFICATION; SCHISTOSOMA MANSONI; TANDEM MASS SPECTROMETRY; WORM; ANALOGS AND DERIVATIVES; ANIMAL; BIOMPHALARIA; CHEMISTRY; ENZYMOLOGY; IMMUNODIFFUSION; IMMUNOPRECIPITATION; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR WEIGHT; POLYACRYLAMIDE GEL ELECTROPHORESIS; RABBITS AND HARES; RAT;

ANIMALS; BIOMPHALARIA; CARBOXYLESTERASE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HYDROLYSIS; IMMUNODIFFUSION; IMMUNOPRECIPITATION; MICE; MOLECULAR WEIGHT; PHENYLALANINE; RABBITS; RATS; SCHISTOSOMA MANSONI; SERUM ALBUMIN; TANDEM MASS SPECTROMETRY;

EID: 84959219254     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182016000184     Document Type: Article

References (51)

1. Bahar, F. G., Ohura, K., Ogihara, T., Imai, T. (2012). Species difference of esterase expression and hydrolase activity in plasma. Journal of Pharmaceutical Sciences 101, 3979-3988.
2. Bailey, G. S. (1996). Ouchterlony double immunodiffusion". In The Protein Protocols Handbook (pdf). VII: Immunochemical Techniques (ed. Walker John, M.), pp. 749-752. Humana Press, Totowa, New Jersey.
3. Bernhard, O. K., Kapp, E. A., Simpson, R. J. (2007). Enhanced analysis of the mouse plasma proteome using cysteine-containing tryptic glycopeptides. Journal of Proteome Research 6, 987-995.
4. Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B.,rade, 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., El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature 460, 352-358.
5. Beyer, N. H., Schou, C., Houen, G., Heegaard, N. H. (2008). Extraction and identification of electroimmunoprecipitated proteins from agarose gels. Journal of Immunological Methods 330, 24-33.
6. Brayer, G. D., Delbaere, L. T. J., James, M. N. G. (1979). Molecular-structure of the alpha-lytic protease from myxobacter-495 at 2-8-a resolution. Journal of Molecular Biology 131, 743-775.
7. Brouwers, J. F., Smeenk, I. M., van Golde, L.M., Tielens, A. G. (1997). The incorporation, modification and turnover of fatty acids in adult Schistosoma mansoni. Molecular and Biochemical Parasitology 88, 175-185.
8. Cerasoli, D. M., Maxwell, D.M., Lenz, D. E. (2000). Generation of genetically modified mice with low serum carboxylesterase. FASEB Journal 14, A1476-A1476.
9. Chen, Y. Y., Lin, S. Y., Yeh, Y. Y., Hsiao, H. H., Wu, C. Y., Chen, S. T., Wang, A. H. (2005). A modified protein precipitation procedure for efficient removal of albumin from serum. Electrophoresis 26, 2117-2127.
10. Choudhury, S. R. (1974). Isolation and properties of an esterase isoenzyme of rat serum. Histochemical Journal 6, 369-372.
11. Cioli, D., Knopf, P. M., Senft, A. W. (1977). A study of Schistosoma mansoni transferred into permissive and nonpermissive hosts. International Journal of Parasitology 7, 293-297.
12. Colantonio, D.A., Dunkinson, C., Bovenkamp, D. E., Van Eyk, J. E. (2005). Effective removal of albumin from serum. Proteomics 5, 3831-3835.
13. Damian, R. T., Greene, N. D., Hubbard, W. J. (1973). Occurrence of mouse alpha 2-macroglobulin antigenic determinants on Schistosomamansoni adults, with evidence on their nature. Journal of Parasitology 59, 64-73.
14. Darani, H. Y., Doenhoff, M.J. (2008). An association between Schistosoma mansoni worms and an enzymatically-active protease/peptidase in mouse blood. Parasitology 135, 467-472.
15. Darani, H. Y., Curtis, R. H., McNeice, C., Price, H. P., Sayers, J. R., Doenhoff, M.J. (1997). Schistosoma mansoni: anomalous immunogenic properties of a 27 kDa larval serine protease associated with protective immunity. Parasitology 115 (Pt 3), 237-247.
16. Dinguirard, N., Yoshino, T. P. (2006). Potential role of a CD36-like class B scavenger receptor in the binding of modified low-density lipoprotein (acLDL) to the tegumental surface of Schistosoma mansoni sporocysts. Molecular and Biochemical Parasitology 146, 219-230.
17. Doenhoff, M., Bickle, Q., Long, E., Bain, J., McGregor, A. (1978). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. I. Demonstration of resistance to reinfection using a model system that involves perfusion of mice within three weeks of challenge. Journal of Helminthology 52, 173-186.
18. Doenhoff, M. J., Modha, J., Curtis, R. H., Adeoye, G. O. (1988). Immunological identification of Schistosoma mansoni peptidases. Molecular and Biochemical Parasitology 31, 233-240.
19. Dunne, D. W., Agnew, A. M., Modha, J., Doenhoff, M. J. (1986). Schistosoma mansoni egg antigens: preparation of rabbit antisera with monospecific immunoprecipitating activity, and their use in antigen characterization. Parasite Immunology 8, 575-586.
20. Duysen, E. G., Koentgen, F., Wiliams, G. R., Timperey, C. M., Schopfer, L. M., Cerasoli, D. M., Lockridge, O. (2011). Production of ES1 plasma carboxylesterase knockout mice for toxicity studies. Chemical Research in Toxicology 24, 1891-1898.
21. Furlong, S. T. (1991). Unique roles for lipids in Schistosoma mansoni. Parasitology Today 7, 59-62.
22. Furlong, S. T., Thibault, K. S., Rogers, R. A. (1992). Fluorescent phospholipids preferentially accumulate in sub-tegumental cells of schistosomula of Schistosoma mansoni. Journal of Cell Science 103 (Pt 3), 823-830.
23. Genetta, T. L., Deustachio, P., Kadner, S. S., Finlay, T. H. (1988). Cdna cloning of esterase-1, the major esterase-activity in mouse plasma. Biochemical and Biophysical Research Communications 151, 1364-1370.
24. Ghesquiere, B., Van Damme, J., Martens, L., Vandekerckhove, J., Gevaert, K. (2006). Proteome-wide characterization of N-glycosylation events by diagonal chromatography. Journal of Proteome Research 5, 2438-2447.
25. Goudie, R. B., Horne, C. H., Wilkinson, P. C. (1966). A simple method for producing antibody specific to a single selected diffusible antigen. Lancet 2, 1224-1226.
26. Holmes, R. S., Wright, M. W., Laulederkind, S. J., Cox, L. A., Hosokawa, M., Imai, T., Ishibashi, S., Lehner, R., Miyazaki, M., Perkins, E. J., Potter, P. M., Redinbo, M. R., Robert, J., Satoh, T., Yamashita, T., Yan, B., Yokoi, T., Zechner, R., Maltais, L. J. (2010). Recommended nomenclature for five mammalian carboxylesterase gene families: human, mouse, and rat genes and proteins. Mammalian Genome 21, 427-441.
27. Hosokawa, M. (2008). Structure and catalytic properties of carboxylesterase isozymes involved in metabolic activation of prodrugs. Molecules 13, 412-431.
28. Kemp, W. M., Damian, R. T., Greene, N. D., Lushbaugh, W. B. (1976). Immunocytochemical localization of mouse alpha 2-macroglobulin-like antigenic determinants on schistosoma-mansoni adults. Journal of Parasitology 62, 413-419.
29. Krishnasamy, S., Teng, A. L., Dhand., R., Schultz., R. M., NJ, G. (1998). Molecular cloning, characterization, and differential expression pattern of mouse lung surfactant convertase. American Journal of Physiology 275(5 Pt 1), L969-L975.
30. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
31. Li, B., Sedlacek, M., Manoharan, I., Boopathy, R., Duysen, E. G., Masson, P., Lockridge, O. (2005). Butyrylcholinesterase, paraoxonase, and albumin esterase, but not carboxylesterase, are present in human plasma. Biochemical Pharmacology 70, 1673-1684.
32. Mancini, G., Carbonara, A. O., Heremans, J. F. (1965). Immunochemical quantitation of antigens by single radial immunodiffusion. Immunochemistry 2, 235-254.
33. McLaren, D. J., Clegg, J. A., Smithers, S. R. (1975). Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology 70, 67-75.
34. Meyer, F., Meyer, H., Bueding, E. (1970). Lipid metabolism in the parasitic and free-living flatworms, Schistosoma mansoni and Dugesia dorotocephala. Biochimica et Biophysica Acta 210, 257-266.
35. Modha, J., Parikh, V., Gauldie, J., Doenhoff, M. J. (1988). An association between schistosomes and contrapsin, a mouse serine protease inhibitor (serpin). Parasitology 96 (Pt 1), 99-109.
36. Munger, J. S., Shi, G. P., Mark, E. A., Chin, D. T., Gerard, C., Chapman, H. A. (1991). A serine esterase released by human alveolar macrophages is closely related to liver microsomal carboxylesterases. Journal of Biological Chemistry 266, 18832-18838.
37. Otto, J., Ronai, A., von Deimling, O. (1981). Purification and characterization of esterase 1F, the albumin esterase of the house mouse (Mus musculus). European Journal of Biochemistry 116, 285-291.
38. Papayannopoulos, I. A. (1995). The interpretation of collision-induced dissociation tandem masssSpectra of peptides. Mass Spectrometry Reviews 14, 49-73.
39. Pearse, A. G. E. (1968). Histochemistry, Theoretical and Applied. Little, Brown; distributed by William & Wilkins, Boston.
40. Satoh, T., Hosokawa, M. (2006). Structure, function and regulation of carboxylesterases. Chemico-Biological Interactions 162, 195-211.
41. Simpson, A. J., Hackett, F., Kelly, C., Knight, M., Payares, G., Omer-Ali, P., Lillywhite, J., Fleck, S. L., Smithers, S. R. (1986). The recognition of Schistosoma mansoni surface antigens by antibodies from patients infected with S. mansoni and S. haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 261-270.
42. Skelly, P. J. (2004). Intravascular schistosomes and complement. Trends in Parasitology 20, 370-374.
43. Smith, T. M., Brooks, T. J., Jr., Lockard, V. G. (1970). In vitro studies on cholesterol metabolism in the blood fluke Schistosoma mansoni. Lipids 5, 854-856.
44. Smithers, S. R., Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695-700.
45. Smithers, S. R., Terry, R. J., Hockley, D. J. (1969). Host antigens in schistosomiasis. Proceedings of the Royal Society of London B, Biological Sciences 171, 483-494.
46. Standley, C. J., Mugisha, L., Dobson, A. P., Stothard, J. R. (2012). Zoonotic schistosomiasis in non-human primates: past, present and future activities at the human-wildlife interface in Africa. Journal of Helminthology 86, 131-140.
47. Steen, H., Mann, M. (2004). The ABC's (and XYZ's) of peptide sequencing. Nature Reviews Molecular Cell Biology 5, 699-711.
48. Stoops, J. K., Horgan, D. J., Runnegar, M. T., De Jersey, J., Webb, E. C., Zerner, B. (1969). Carboxylesterases (EC 3•1•1). Kinetic studies on carboxylesterases. Biochemistry 8, 2026-2033.
49. Studier, F. W. (1973). Analysis of bacteriophage T7 early RNAs and proteins on slab gels. Journal of Molecular Biology 79, 237-248.
50. Takai, S., Matsuda, A., Usami, Y., Adachi, T., Sugiyama, T., Katagiri, Y., Tatematsu, M., Hirano, K. (1997). Hydrolytic profile for ester-or amide-linkage by carboxylesterases pI 5•3 and 4•5 from human liver. Biological and Pharmaceutical Bulletin 20, 869-873.
51. Xie, M., Yang, D., Liu, L., Xue, B., Yan, B. (2002). Human and rodent carboxylesterases: immunorelatedness, overlapping substrate specificity, differential sensitivity to serine enzyme inhibitors, and tumorrelated expression. Drug Metabolism and Disposition 30, 541-547.