Tetraspanin-2 localisation in high pressure frozen and freeze-substituted Schistosoma mansoni adult males reveals its distribution in membranes of tegumentary vesicles

International Journal for Parasitology

Volumn 43, Issue 10, 2013, Pages 785-793

  Schulte, Leigh ^a,b   Lovas, Erica ^b   Green, Kathryn ^b   Mulvenna, Jason ^a   Gobert, Geoffrey N ^a   Morgan, Garry ^b   Jones, Malcolm K ^a,b  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cryo electron microscopy; Electron tomography; Schistosoma mansoni; Tegument; Tetraspanins

Indexed keywords

TETRASPANIN; TETRASPANIN 2; UNCLASSIFIED DRUG; URANYL ACETATE;

ANTIBODY; ELECTRON MICROSCOPY; FLATWORM; FREEZING; HIGH PRESSURE; MEMBRANE; PARASITE; PROTEIN; SPATIAL DISTRIBUTION; TOMOGRAPHY;

ADULT ANIMAL; ANIMAL EXPERIMENT; APICAL MEMBRANE; ARTICLE; CONTROLLED STUDY; CRYOPRESERVATION; CRYOSUBSTITUTION; ELECTRON TOMOGRAPHY; FREEZING; HIGH PRESSURE FREEZING; IMMUNOELECTRON MICROSCOPY; IMMUNOLOCALIZATION; INTEGUMENT; LOW TEMPERATURE PROCEDURES; MALE; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PROTEIN LOCALIZATION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS;

SCHISTOSOMA; SCHISTOSOMA MANSONI;

EID: 84881550105     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2013.04.003     Document Type: Article

References (39)

1. Boucheix C., Rubinstein E. Tetraspanins. Cell. Mol. Life Sci. 2001, 58:1189-1205.
2. Braschi S., Wilson R.A. Proteins exposed at the adult schistosome surface revealed by biotinylation. Mol. Cell. Proteomics 2006, 5:347-356.
3. Braschi S., Borges W.C., Wilson R.A. Proteomic analysis of the schistosome tegument and its surface membranes. Mem. Inst. Oswaldo Cruz 2006, 101(Suppl. 1):205-212.
4. Cardoso F.C., Macedo G.C., Gava E., Kitten G.T., Mati V.L., de Melo A.L., Caliari M.V., Almeida G.T., Venancio T.M., Verjovski-Almeida S., Oliveira S.C. Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Negl. Trop. Dis. 2008, 2:e308.
5. Charrin S., le Naour F., Silvie O., Milhiet P.E., Boucheix C., Rubinstein E. Lateral organization of membrane proteins: tetraspanins spin their web. Biochem. J. 2009, 420:133-154.
6. Cogswell A.A., Collins J.J., Newmark P.A., Williams D.L. Whole mount in situ hybridization methodology for Schistosoma mansoni. Mol. Biochem. Parasitol. 2011, 178:46-50.
7. Cohen C., Reinhardt B., Castellani L., Norton P., Stirewalt M. Schistosome surface spines are "crystals" of actin. J. Cell. Biol. 1982, 95:987-988.
8. Dillon G.P., Feltwell T., Skelton J., Coulson P.S., Wilson R.A., Ivens A.C. Altered patterns of gene expression underlying the enhanced immunogenicity of radiation-attenuated schistosomes. PLoS Negl. Trop. Dis. 2008, 2:e240.
9. Dubochet J. The physics of rapid cooling and its implications for cryoimmobilization of cells. Methods Cell Biol. 2007, 79:7-21.
10. Gobert G.N., Stenzel D.J., McManus D.P., Jones M.K. The ultrastructural architecture of the adult Schistosoma japonicum tegument. Int. J. Parasitol. 2003, 33:1561-1575.
11. Griffiths G., Burke B., Lucocq J. Fine Structure Immunocytochemistry 1993, Springer-Verlag, Berlin and New York.
12. Gryseels B., Polman K., Clerinx J., Kestens L. Human schistosomiasis. Lancet 2006, 368:1106-1118.
13. Hockley D.J. Ultrastructure of the tegument of Schistosoma. Adv. Parasitol. 1973, 11:233-305.
14. Hockley D.J., McLaren D.J. Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. Int. J. Parasitol. 1973, 3:13-20.
15. Jabbar A., Crawford S., Młocicki D., Świderski Z.P., Conn D.B., Jones M.K., Beveridge I., Lightowlers M.W. Ultrastructural reconstruction of Taenia ovis oncospheres from serial sections. Int. J. Parasitol. 2010, 40:1419-1431.
16. Jabbar A., Kyngdon C.T., Gauci C.G., Walduck A.K., McCowan C., Jones M.K., Beveridge I., Lightowlers M.W. Localisation of three host-protective oncospheral antigens of Taenia ovis. Int. J. Parasitol. 2010, 40:579-589.
17. Jones M.K., Gobert G.N., Zhang L., Sunderland P., McManus D.P. The cytoskeleton and motor proteins of human schistosomes and their roles in surface maintenance and host-parasite interactions. Bioessays 2004, 26:752-765.
18. Jones M.K., Bong S.H., Green K.M., Holmes P., Duke M., Loukas A., McManus D.P. Correlative and dynamic imaging of the hatching biology of Schistosoma japonicum from eggs prepared by high pressure freezing. PLoS Negl. Trop. Dis. 2008, 2:e334.
19. Khampoosa P., Jones M., Lovas E., Srisawangwong T., Laha T., Piratae S., Thammasiri C., Suwannatrai A., Sripanidkulchai B., Eursitthichai V., Tesana S. Light and electron microscopy observations of embryogenesis and egg development in the human liver fluke, Opisthorchis viverrini (Platyhelminthes, Digenea). Parasitol. Res. 2012, 110:799-808.
20. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996, 116:71-76.
21. Loukas A., Tran M., Pearson M.S. Schistosome membrane proteins as vaccines. Int. J. Parasitol. 2007, 37:257-263.
22. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 2005, 152:36-51.
23. Mulvenna J., Moertel L., Jones M.K., Nawaratna S., Lovas E.M., Gobert G.N., Colgrave M., Jones A., Loukas A., McManus D.P. Exposed proteins of the Schistosoma japonicum tegument. Int. J. Parasitol. 2010, 40:543-554.
24. Noske A.B., Costin A.J., Morgan G.P., Marsh B.J. Expedited approaches to whole cell electron tomography and organelle mark-up in situ in high-pressure frozen pancreatic islets. J. Struct. Biol. 2008, 161:298-313.
25. Pearson M.S., Pickering D.A., McSorley H.J., Bethony J.M., Tribolet L., Dougall A.M., Hotez P.J., Loukas A. Enhanced protective efficacy of a chimeric form of the schistosomiasis vaccine antigen SmTSP-2. PLoS Negl. Trop. Dis. 2012, 6:e1564.
26. Pérez-Sánchez R., Ramajo-Hernández A., Ramajo-Martín V., Oleaga A. Proteomic analysis of the tegument and excretory-secretory products of adult Schistosoma bovis worms. Proteomics 2006, 6:S226-S236.
27. Piratae S., Tesana S., Jones M.K., Brindley P.J., Loukas A., Lovas E., Eursitthichai V., Sripa B., Thanasuwan S., Laha T. Molecular characterization of a tetraspanin from the human liver fluke, Opisthorchis viverrini. PLoS Negl. Trop. Dis. 2012, 6:e1939.
28. Rana S., Zoller M. Exosome target cell selection and the importance of exosomal tetraspanins: a hypothesis. Biochem. Soc. Trans. 2011, 39:559-562.
29. Rubinstein E. The complexity of tetraspanins. Biochem. Soc. Trans. 2011, 39:501-505.
30. Skelly P.J., Wilson R.A. Making sense of the schistosome surface. Adv. Parasitol. 2006, 63:185-284.
31. Świderski Z., Bakhoum A.S., Młocicki D., Miquel J. Ultrastructural studies on egg envelopes surrounding the miracidia of Mediogonimus jourdanei Mas-Coma et Rocamora, 1978 (Digenea, Microphalloidea, Prosthogonimidae). Acta Parasitol. 2010, 55:245-253.
32. Tran M.H., Pearson M.S., Bethony J.M., Smyth D.J., Jones M.K., Duke M., Don T.A., McManus D.P., Correa-Oliveira R., Loukas A. Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nat. Med. 2006, 12:835-840.
33. Tran M.H., Freitas T.C., Cooper L., Gaze S., Gatton M.L., Jones M.K., Lovas E., Pearce E.J., Loukas A. Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathog. 2010, 6:e1000840.
34. van Balkom B.W., van Gestel R.A., Brouwers J.F., Krijgsveld J., Tielens A.G., Heck A.J., van Hellemond J.J. Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome. J. Proteome Res. 2005, 4:958-966.
35. Wilson R.A. The saga of schistosome migration and attrition. Parasitology 2009, 136:1581-1592.
36. Wilson R.A. Proteomics at the schistosome-mammalian host interface: any prospects for diagnostics or vaccines?. Parasitology 2012, 139:1178-1194.
37. Wilson R.A., Barnes P.E. The tegument of Schistosoma mansoni: observations on formation, structure and composition of cytoplasmic inclusions in relation to tegument function. Parasitology 1974, 68:239-258.
38. Wilson R.A., Barnes P.E. The formation and turnover of the membranocalyx on the tegument of Schistosoma mansoni. Parasitology 1977, 74:61-71.
39. Zhang W., Li J., Duke M., Jones M.K., Kuang L., Zhang J., Blair D., Li Y., McManus D.P. Inconsistent protective efficacy and marked polymorphism limits the value of Schistosoma japonicum tetraspanin-2 as a vaccine target. PLoS Negl. Trop. Dis. 2011, 5:e1166.