Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation

Molecular and Biochemical Parasitology

Volumn 164, Issue 1, 2009, Pages 32-44

  Wu, Xiao Jun ^a   Sabat, Greg ^b   Brown, James F ^b   Zhang, Mengzi ^a   Taft, Andrew ^a   Peterson, Nathan ^a   Harms, Amy ^b   Yoshino, Timothy P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Excretory secretory proteins (ESP); In vitro culture; Larval transformation proteins (LTP); Miracidium sporocyst; Proteomics; Schistosoma mansoni

Indexed keywords

BINDING PROTEIN; FERRITIN; HEAT SHOCK PROTEIN; HEME BINDING PROTEIN; OXIDOREDUCTASE; POLYCLONAL ANTIBODY; PROTEINASE; PROTEINASE INHIBITOR; SECRETORY PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VENOM ALLERGEN LIKE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; HOST PARASITE INTERACTION; IMMUNOLOCALIZATION; INTEGUMENT; LARVAL DEVELOPMENT; LIQUID CHROMATOGRAPHY; MIRACIDIUM; MOLLUSC; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; PROTEOMICS; SCHISTOSOMA MANSONI; SPOROCYST; SYNCYTIUM; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

ANIMALS; HELMINTH PROTEINS; IMMUNOHISTOCHEMISTRY; LIFE CYCLE STAGES; OOCYSTS; PROTEOMICS; SCHISTOSOMA MANSONI;

GASTROPODA; SCHISTOSOMA MANSONI;

EID: 58549116678     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2008.11.005     Document Type: Article

References (58)

1. Basch P.F., and DiConza J.J. The miracidium-sporocyst transition in Schistosoma mansoni: surface changes in vitro with ultrastructural correlation. J Parasitol 60 (1974) 935-941
2. Pan C.T. Schistosoma mansoni: the ultrastructure of larval morphogenesis in Biomphalaria glabrata and of associated hot-parasite interactions. Jpn J Med Sci Biol 49 (1996) 129-149
3. Lodes M.J., and Yoshino T.P. Characterization of excretory-secretory proteins synthesized in vitro by Schistosoma mansoni primary sporocysts. J Parasitol 75 (1989) 853-862
4. DeGaffe G., and Loker E.S. Susceptibility of Biomphalaria glabrata to infection with Echinostoma parensei: correlation with the effect of parasite secretory-excretory products on host hemocyte spreading. J Invertebr Pathol 71 (1998) 64-72
5. Bayne C.J., and Yoshino T.P. Determinants of compatibility in mollusk-trematode parasitism. Amer Zool 29 (1989) 399-407
6. Yoshino T.P., and Vasta G.R. Parasite-invertebrate host immune interactions. Adv Comp Environ Physiol 24 (1996) 125-167
7. Adema C.M., and Loker E.S. Specificity and immunobiology of larval digenean-snail associations. In: Fried B., and Graczyk T.K. (Eds). Advances in Trematode Biology (1997), CRC Press, Boca Raton 229-264
8. Yoshino T.P., Lodes M.J., Rege A.A., and Chappell C.L. Proteinase activity in miracidia, transformation excretory-secretory products, and primary sporocysts of Schistosoma mansoni. J Parasitol 79 (1993) 23-31
9. Sullivan J.T. Mitotic responses to injected extracts of larval and adult Schistosoma mansoni in Biomphalaria glabrata: effects of dose and colchicine treatment. J Parasitol 93 (2007) 213-215
10. Vermeire J.J., and Yoshino T.P. Antioxidant gene expression and function in in vitro-developing Schistosoma mansoni mother sporocysts: possible role in self-protection. Parasitology 134 (2007) 1369-1378
11. Lodes M.J., and Yoshino T.P. The effect of schistosome excretory-secretory products on Biomphalaria glabrata hemocyte motility. J Invertebr Pathol 56 (1990) 75-85
12. Connors V.A., and Yoshino T.P. In vitro effect of larval Schistosoma mansoni excretory-secretory products on phagocytosis-stimulated superoxide production in hemocytes from Biomphalaria glabrata. J Parasitol 76 (1990) 895-902
13. Zahoor Z., Davies A.J., Kirk R.S., Rollinson D., and Walker A.J. Disruption of ERK signaling in Biomphalaria glabrata defence cells by Schistosoma mansoni: Implications for parasite survival in the snail host. Dev Comp Immunol 32 (2008) 1561-1571
14. Guillou F., Roger E., Mone Y., et al. Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Mol Biochem Parasitol 155 (2007) 45-56
15. Lodes M.J., Connors V.A., and Yoshino T.P. Isolation and functional characterization of snail hemocyte-modulating polypeptides from primary sporocysts of Schistosoma mansoni. Mol Biochem Parasitol 49 (1991) 1-10
16. Chernin E. Observations on hearts explanted in vitro from the snail Australorbis glabratus. J Parasitol 39 (1963) 353-364
17. Yoshino T.P., and Laursen J.R. Production of Schistosoma mansoni daughter sporocysts from mother sporocysts maintained in synxenic culture with Biomphalaria glabrata embryonic (Bge) cells. J Parasitol 81 (1995) 714-722
18. Castillo M.G., Wu X.J., Dinguirard N., Nyame A.K., Cummings R.D., and Yoshino T.P. Surface membrane proteins of Biomphalaria glabrata embryonic cells bind fucosly determinants on the tegumental surface of Schistosoma mansoni primary sporocysts. J Parasitol 93 (2007) 832-840
19. Nickel W. Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6 (2005) 607-614
20. Bendtsen J.D., Jensen L.J., Blom N., von Heijne G., and Brunak S. Feature-based prediction of non-classical and leaderless protein secretion. Prot Eng Design Sel 17 (2004) 349-356
21. Samuelson J.C., and Caulfield J.P. Role of pleated septate junctions in the epithelium of miracidia of Schistosoma mansoni during transformation to sporocysts in vitro. Tiss Cell 17 (1985) 667-682
22. Bayne C.J., Hahn U.K., and Bender R.C. Mechanisms of molluscan host resistance and of parasite strategies for survival. Parasitology 123 (2001) S159-S167
23. Davids B.J., and Yoshino T.P. Schistosoma mansoni: Excretory-secretory polypeptides exhibit selective binding to plasma components of the snail Biomphalaria glabrata. Exp Parasitol 81 (1995) 292-301
24. Johnston L.A., and Yoshino T.P. Larval Schistosoma mansoni excretory-secretory glycoproteins (ESPs) Bind to hemocytes of Biomphalaria glabrata (Gastropoda) via surface carbohydrate binding receptors. J Parasitol 87 (2001) 786-793
25. Wymelenberg A.V., Sabat G., Mozuch M., Kersten P.J., Cullen D., and Blanchette R.A. Structure, organization, and transcriptional regulation of a family of copper radical oxidase genes in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 72 (2006) 4871-4877
26. Dunn T.S., and Yoshino T.P. Schistosoma mansoni: origin and expression of a tegumental surface antigen on the miracidium and primary sporocyst. Exp Parasitol 67 (1988) 67-81
27. Loker E.S., Bayne C.J., Buckley P.M., and Kruse K.T. Ultrastructure of encapsulation of Schistosoma mansoni mother sporocysts by hemocytes of juveniles of the 10-R2 strain of Biomphalaria glabrata. J Parasitol 68 (1982) 84-94
28. Mambula S.S., and Calderwood S.K. Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J Immunol 177 (2006) 7849-7857
29. Danielsen E.M., van Deurs B., and Hansen G.H. "Nonclassical" secretion of annexin A2 to the luminal side of the enterocyte brush border membrane. Biochemistry 42 (2003) 14670-14676
30. Bottger A., Strasser D., Alexandrova O., et al. Genetic screen for signal peptides in Hydra reveal novel secreted proteins and evidence for non-classical protein secretion. Eur J Cell Biol 85 (2006) 1107-1117
31. Cass C.L., Johnson J.R., Califf L.L., et al. Proteomic analysis of Schistosoma mansoni egg secretions. Mol Biochem Parasitol 155 (2007) 84-93
32. Knudsen G.M., Medzihradszky K.F., Lim K.C., Hansell E., and McKerrow J.H. Proteomic analysis of Schistosoma mansoni ceercarial secretions. Mol Cell Proteomics 4 (2005) 1862-1875
33. Curwen R.S., Ashton P.D., Sundaralingam S., and Wilson R.A. Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Mol Cell Proteomics 5.5 (2006) 835-844
34. Salter J.P., Lim K.C., Hansell E., Hsieh I., and McKerrow J.H. Schistosome invasion of human skin and degradation of dermal elastin are mediated by a single serine protease. J Biol Chem 275 (2000) 38667-38673
35. Armstrong P.B. Proteases and protease inhibitors: balance of activities in host-pathogen interaction. Immunobiology 211 (2006) 263-281
36. Bahgat M., Doenhoff M., Kirschfink M., and Ruppel A. Serine protease and phenoloxidase activities in hemocytes of Biomphalaria glabrata snails with varying susceptibility to infection with the parasite Schistosoma mansoni. Parasitol Res 88 (2002) 489-494
37. Myers J., Ittiprasert W., Raghavan N., Miller A., and Knight M. Differences in cysteine protease activity in Schistosoma mansoni-resistant and-susceptible Biomphalaria glabrata and characterization of the hepatopancreas cathepsin B full-length cDNA. J Parasitol 94 (2008) 659-668
38. Mitta G., Galinier R., Tissevre P., et al. Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev Comp Immunol 29 (2005) 393-407
39. Lockyer A.E., Spinks J.N., Walker A.J., et al. Biomphalaria glabrata transcriptome: Identification of cell-signalling, transcription control and immune-related genes from open reading frame expressed sequence tags (ORESTES). Dev Comp Immunol 31 (2007) 763-782
40. Hanelt B., Lun C.M., and Adema C.M. Comparative ORESTES-sampling of transcriptomes of immune-challenged Biomphalaria glabrata snails. J Invertebr Pathol 99 (2008) 192-203
41. Alger H.M., and Williams D.L. The disulfide redox system of Schistosoma mansoni and the importance of a multifunctional enzyme, thioredoxin glutathione reductase. Mol Biochem Parasitol 121 (2002) 129-139
42. Cordell P.A., Futers S., Grant P.J., and Pease R.J. The human hydroxyacylglutathione hydrolase (HAGH) gene encodes both cytosolic and mitochondrial forms of glyoxalase II. J Biol Chem 279 (2004) 28653-28661
43. Hahn U.K., Bender R.C., and Bayne C.J. Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J Parasitol 87 (2001) 292-299
44. 2 than susceptible snails. J Parasitol 91 (2005) 275-279
45. Hintze K.J., and Theil E.C. Cellular regulation and molecular interactions of the ferritins. Cell Mol Life Sci 63 (2006) 591-600
46. Chalmers I.W., McArdle A.J., Coulson R.M., et al. Developmentally regulated expression, alternative splicing and distinct sub-groupings in members of the Schistosoma mansoni venom allergen-like (SmVAL) gene family. BMC Genomics 9 (2008) 89 [PMCID: PMC2270263]
47. Yeats C., Bentley S., and Bateman A. New knowledge from old: in silico discovery of novel protein domains in Streptomyces coelicolor. BMC Microbiol 3 (2003) 3 [PMCID: PMC151604]
48. Hoffman D.R. Structural biology of allergens from stinging and biting insects. Curr Opin Allergy Clin Immunol 8 (2008) 338-342
49. Milne T.J., Abbenante G., Tyndall J.D., Halliday J., and Lewis R.J. Isolation and characterization of a cone snail protease with homology to CRISP proteins of the pathogenesis-related protein superfamily. J Biol Chem 278 (2003) 31105-31110
50. Hawdon J.M., Narasimhan S., and Hotez P.J. Ancylostoma secreted protein 2: cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Mol Biochem Parasitol 99 (1999) 149-165
51. Murray J., Gregory W.F., Gomez-Escobar N., Atmadia A.K., and Maizels R.M. Expression and immune recognition of Brugia malayi VAL-1, a homologue of vespid venom and Ancylostoma secreted proteins. Mol Biochem Parasitol 118 (2001) 89-96
52. Yatsuda A.P., Krijgsveld J., Cornelissen A.W., Heck A.J., and de Vries E. Comprehensive analysis of the secreted proteins of the parasite Haemochus contortus reveals extensive variation and differential immune recognition. J Biol Chem 278 (2003) 16941-16951
53. Ali F., Brown A., Stanssens P., Timothy L.M., Soule H.R., and Pritchard D.I. Vaccination with neutrophil inhibitory factor reduces the fecundity of the hookworm Ancylostoma ceylanicum. Parasite Immunol 23 (2001) 237-249
54. Hahn U.K., Bender R.C., and Bayne C.J. Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. J Parasitol 87 (2001) 778-785
55. Holmfeldt P., Brannstrom K., Sellin M.E., Segerman B., Carlsson S.R., and Gullberg M. The Schistosoma mansoni protein Sm16/SmSLP/SmSPO-1 is a membrane-binding protein that lacks the proposed microtubule-regulatory activity. Mol Biochem Parasitol 156 (2007) 225-234
56. Moss S.E., and Morgan R.O. The annexins. Genome Biol 5 (2004) 219
57. Rao K.V., and Ramaswamy K. Cloning and expression of a gene encoding Sm16, an anti-inflammatory protein from Schistosoma mansoni. Mol Biochem Parasitol 108 (2000) 101-108
58. Lehr T., Geyer H., Maaß K., Doenhoff M.J., and Geyer R. Structural characterization of N-glycans from the freshwater snail Biomphalaria glabrata cross-reacting with Schistosoma mansoni glycoconjugates. Glycobiology 17 (2007) 82-103