A quantitative proteomic analysis of the tegumental proteins from Schistosoma mansoni schistosomula reveals novel potential therapeutic targets

International Journal for Parasitology

Volumn 45, Issue 8, 2015, Pages 505-516

  Sotillo, Javier ^a   Pearson, Mark ^a   Becker, Luke ^a   Mulvenna, Jason ^b   Loukas, Alex ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

ITRAQ; Proteomics; Schistosoma mansoni; Schistosomula; Tegument

Indexed keywords

CALPAIN; GLUCOSE TRANSPORTER; HEAT SHOCK PROTEIN; HELMINTH PROTEIN; PEPTIDASE; PROTEIN SM29; STEROL; TEGUMENTAL PROTEIN; THROMBOSPONDIN 1; THROMBOSPONDIN 2; UNCLASSIFIED DRUG;

ANTIGEN; ENZYME; GLUCOSE; MEMBRANE; PEPTIDE; PROTEIN; PROTEOMICS; QUANTITATIVE ANALYSIS; STEROL;

ANTIGEN DETECTION; APICAL MEMBRANE; ARTICLE; CELL LABELING; CONTROLLED STUDY; DRUG TARGETING; IN VITRO STUDY; NONHUMAN; PARASITE DEVELOPMENT; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SCHISTOSOMULUM; WORM TEGUMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; GENETICS; HUMAN; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; SCHISTOSOMIASIS MANSONI; SNAIL;

MAMMALIA; SCHISTOSOMA MANSONI;

ANIMALS; HELMINTH PROTEINS; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PROTEOMICS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SNAILS;

EID: 84929654703     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2015.03.004     Document Type: Article

References (76)

1. Basch P.F. Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. J. Parasitol. 1981, 67:179-185.
2. 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., El-Sayed N.M. The genome of the blood fluke Schistosoma mansoni. Nature 2009, 460:352-358.
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. Braschi S., Wilson R.A. Proteins exposed at the adult schistosome surface revealed by biotinylation. Mol. Cell. Proteomics 2006, 5:347-356.
5. Brink L.H., McLaren D.J., Smithers S.R. Schistosoma mansoni: a comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology 1977, 74:73-86.
6. Brouwers J.F., Smeenk I.M., van Golde L.M., Tielens A.G. The incorporation, modification and turnover of fatty acids in adult Schistosoma mansoni. Mol. Biochem. Parasitol. 1997, 88:175-185.
7. Cantacessi C., Campbell B.E., Visser A., Geldhof P., Nolan M.J., Nisbet A.J., Matthews J.B., Loukas A., Hofmann A., Otranto D., Sternberg P.W., Gasser R.B. A portrait of the "SCP/TAPS" proteins of eukaryotes-developing a framework for fundamental research and biotechnological outcomes. Biotechnol. Adv. 2009, 27:376-388.
8. Clegg J.A., Smithers S.R. The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. Int. J. Parasitol. 1972, 2:79-98.
9. Colley D.G., Bustinduy A.L., Secor W.E., King C.H. Human schistosomiasis. Lancet 2014, 383:2253-2264.
10. Colley D.G., Wikel S.K. Schistosoma mansoni: simplified method for the production of schistosomules. Exp. Parasitol. 1974, 35:44-51.
11. Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
12. Curwen R.S., Ashton P.D., Sundaralingam S., Wilson R.A. Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Mol. Cell. Proteomics 2006, 5:835-844.
13. Da'dara A.A., Faghiri Z., Krautz-Peterson G., Bhardwaj R., Skelly P.J. Schistosome Na, K-ATPase as a therapeutic target. Trans. R. Soc. Trop. Med. Hyg. 2013, 107:74-82.
14. De la Torre Escudero E., Manzano-Roman R., Valero L., Oleaga A., Perez-Sanchez R., Hernandez-Gonzalez A., Siles-Lucas M. Comparative proteomic analysis of Fasciola hepatica juveniles and Schistosoma bovis schistosomula. J. Proteomics 2011, 74:1534-1544.
15. Devaney E. Thermoregulation in the life cycle of nematodes. Int. J. Parasitol. 2006, 36:641-649.
16. Diemert D.J., Pinto A.G., Freire J., Jariwala A., Santiago H., Hamilton R.G., Periago M.V., Loukas A., Tribolet L., Mulvenna J., Correa-Oliveira R., Hotez P.J., Bethony J.M. Generalized urticaria induced by the Na-ASP-2 hookworm vaccine: implications for the development of vaccines against helminths. J. Allergy Clin. Immunol. 2012, 130(169-176):e166.
17. Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007, 2:953-971.
18. Fitzpatrick J.M., Peak E., Perally S., Chalmers I.W., Barrett J., Yoshino T.P., Ivens A.C., Hoffmann K.F. Anti-schistosomal intervention targets identified by lifecycle transcriptomic analyses. PLoS Negl. Trop. Dis. 2009, 3:e543.
19. Ginestet C. Ggplot2: Elegant Graphics for Data Analysis. J. R. Stat. Soc. Ser. A Stat. Soc. 2011, 174:245-246.
20. Gobert G.N., Tran M.H., Moertel L., Mulvenna J., Jones M.K., McManus D.P., Loukas A. Transcriptional changes in Schistosoma mansoni during early schistosomula development and in the presence of erythrocytes. PLoS Negl. Trop. Dis. 2010, 4:e600.
21. Gryseels B., Polman K., Clerinx J., Kestens L. Human schistosomiasis. Lancet 2006, 368:1106-1118.
22. Hawdon J.M., Narasimhan S., 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. 1999, 99:149-165.
23. Hedstrom R., Culpepper J., Schinski V., Agabian N., Newport G. Schistosome heat-shock proteins are immunologically distinct host-like antigens. Mol. Biochem. Parasitol. 1988, 29:275-282.
24. Hockley D., McLaren D. The outer membrane of Schistosoma mansoni. Trans. R. Soc. Trop. Med. Hyg. 1971, 65:432.
25. 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, 3:13-25.
26. Hong Y., Peng J., Jiang W., Fu Z., Liu J., Shi Y., Li X., Lin J. Proteomic analysis of Schistosoma japonicum schistosomulum proteins that are differentially expressed among hosts differing in their susceptibility to the infection. Mol. Cell. Proteomics 2011, 10(M110):006098.
27. Hong Y., Sun A., Zhang M., Gao F., Han Y., Fu Z., Shi Y., Lin J. Proteomics analysis of differentially expressed proteins in schistosomula and adult worms of Schistosoma japonicum. Acta Trop. 2013, 126:1-10.
28. James C., Hicks M., Webbe G., Nelson G.S. Proceedings: Schistosoma haematobium and bladder cancer. Parasitology 1974, 69. viii-ix.
29. 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.
30. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74:5383-5392.
31. King C.H. It's Time to Dispel the Myth of "Asymptomatic" Schistosomiasis. PLoS Negl. Trop. Dis. 2015, 9:e0003504.
32. King C.H., Dickman K., Tisch D.J. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 2005, 365:1561-1569.
33. Krautz-Peterson G., Simoes M., Faghiri Z., Ndegwa D., Oliveira G., Shoemaker C.B., Skelly P.J. Suppressing glucose transporter gene expression in schistosomes impairs parasite feeding and decreases survival in the mammalian host. PLoS Pathog. 2010, 6:e1000932.
34. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
35. Kusel J.R., Al-Adhami B.H., Doenhoff M.J. The schistosome in the mammalian host: understanding the mechanisms of adaptation. Parasitology 2007, 134:1477-1526.
36. Loukas A., Tran M., Pearson M.S. Schistosome membrane proteins as vaccines. Int. J. Parasitol. 2007, 37:257-263.
37. Mayer D.A., Fried B. The role of helminth infections in carcinogenesis. Adv. Parasitol. 2007, 65:239-296.
38. Mazier D., Mattei D. Parasite heat-shock proteins and host responses: the balance between protection and immunopathology. Springer Semin. Immunopathol. 1991, 13:37-53.
39. McManus D.P., Loukas A. Current status of vaccines for schistosomiasis. Clin. Microbiol. Rev. 2008, 21:225-242.
40. Miller P., Wilson R.A. Migration of the schistosomula of Schistosoma mansoni from the lungs to the hepatic portal system. Parasitology 1980, 80:267-288.
41. Morris G.P., Threadgold L.T. Ultrastructure of the tegument of adult Schistosoma mansoni. J. Parasitol. 1968, 54:15-27.
42. 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.
43. Nesvizhskii A.I., Keller A., Kolker E., Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75:4646-4658.
44. Ohta N., Kumagai T., Maruyama H., Yoshida A., He Y., Zhang R. Research on calpain of Schistosoma japonicum as a vaccine candidate. Parasitol. Int. 2004, 53:175-181.
45. Parker-Manuel S.J., Ivens A.C., Dillon G.P., Wilson R.A. Gene expression patterns in larval Schistosoma mansoni associated with infection of the mammalian host. PLoS Negl. Trop. Dis. 2011, 5:e1274.
46. Pearce E.J., MacDonald A.S. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2002, 2:499-511.
47. Pinheiro C.S., Martins V.P., Assis N.R., Figueiredo B.C., Morais S.B., Azevedo V., Oliveira S.C. Computational vaccinology: an important strategy to discover new potential S. mansoni vaccine candidates. J. Biomed. Biotechnol. 2011, 2011:503068.
48. Protasio A.V., Dunne D.W., Berriman M. Comparative study of transcriptome profiles of mechanical- and skin-transformed Schistosoma mansoni schistosomula. PLoS Negl. Trop. Dis. 2013, 7:e2091.
49. Quezada L.A., Sajid M., Lim K.C., McKerrow J.H. A blood fluke serine protease inhibitor regulates an endogenous larval elastase. J. Biol. Chem. 2012, 287:7074-7083.
50. Roberts S.M., MacGregor A.N., Vojvodic M., Wells E., Crabtree J.E., Wilson R.A. Tegument surface membranes of adult Schistosoma mansoni: development of a method for their isolation. Mol. Biochem. Parasitol. 1983, 9:105-127.
51. Rofatto H.K., Parker-Manuel S.J., Barbosa T.C., Tararam C.A., Alan Wilson R., Leite L.C., Farias L.P. Tissue expression patterns of Schistosoma mansoni Venom Allergen-Like proteins 6 and 7. Int. J. Parasitol. 2012, 42:613-620.
52. Salter J.P., Lim K.C., Hansell E., Hsieh I., McKerrow J.H. Schistosome invasion of human skin and degradation of dermal elastin are mediated by a single serine protease. J. Biol. Chem. 2000, 275:38667-38673.
53. Samuelson J.C., Caulfield J.P., David J.R. Schistosoma mansoni: post-transformational surface changes in schistosomula grown in vitro and in mice. Exp. Parasitol. 1980, 50:369-383.
54. Schulte L., Lovas E., Green K., Mulvenna J., Gobert G.N., Morgan G., Jones M.K. Tetraspanin-2 localisation in high pressure frozen and freeze-substituted Schistosoma mansoni adult males reveals its distribution in membranes of tegumentary vesicles. Int. J. Parasitol. 2013, 43:785-793.
55. Schwartz D.A. Helminths in the induction of cancer II. Schistosoma haematobium and bladder cancer. Trop. Geogr. Med. 1981, 33:1-7.
56. Searle B.C. Scaffold: a bioinformatic tool for validating MS/MS-based proteomic studies. Proteomics 2010, 10:1265-1269.
57. Shadforth I.P., Dunkley T.P., Lilley K.S., Bessant C. I-Tracker: for quantitative proteomics using iTRAQ. BMC Genomics 2005, 6:145.
58. Skelly P.J., Alan Wilson R. Making sense of the schistosome surface. Adv. Parasitol. 2006, 63:185-284.
59. Skelly P.J., Da'dara A.A., Li X.H., Castro-Borges W., Wilson R.A. Schistosome feeding and regurgitation. PLoS Pathog. 2014, 10:e1004246.
60. Skelly P.J., Shoemaker C.B. Rapid appearance and asymmetric distribution of glucose transporter SGTP4 at the apical surface of intramammalian-stage Schistosoma mansoni. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3642-3646.
61. Skelly P.J., Shoemaker C.B. The Schistosoma mansoni host-interactive tegument forms from vesicle eruptions of a cyton network. Parasitology 2001, 122(Pt 1):67-73.
62. Smith D.B., Davern K.M., Board P.G., Tiu W.U., Garcia E.G., Mitchell G.F. Mr 26,000 antigen of Schistosoma japonicum recognized by resistant WEHI 129/J mice is a parasite glutathione S-transferase. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:8703-8707.
63. Sotillo J., Valero L., Sanchez Del Pino M.M., Fried B., Esteban J.G., Marcilla A., Toledo R. Identification of antigenic proteins from Echinostoma caproni (Trematoda) recognized by mouse immunoglobulins M, A and G using an immunoproteomic approach. Parasite Immunol. 2008, 30:271-279.
64. Steinmann P., Keiser J., Bos R., Tanner M., Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 2006, 6:411-425.
65. 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.
66. 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.
67. Tribolet L., Cantacessi C., Pickering D.A., Navarro S., Doolan D.L., Trieu A., Fei H., Chao Y., Hofmann A., Gasser R.B., Giacomin P.R., Loukas A. Probing of a human proteome microarray with a recombinant pathogen protein reveals a novel mechanism by which hookworms suppress B-cell receptor signaling. J. Infect. Dis. 2015, 211:416-425.
68. Tucker M.S., Karunaratne L.B., Lewis F.A., Freitas T.C., Liang Y.S. Schistosomiasis. Curr. Protoc. Immunol. 2013, 103:1. Unit 19 11.
69. 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.
70. van der Werf M.J., de Vlas S.J., Brooker S., Looman C.W., Nagelkerke N.J., Habbema J.D., Engels D. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop. 2003, 86:125-139.
71. Wilson R.A. Proteomics at the schistosome-mammalian host interface: any prospects for diagnostics or vaccines?. Parasitology 2012, 139:1178-1194.
72. Wilson R.A., Barnes P.E. The formation and turnover of the membranocalyx on the tegument of Schistosoma mansoni. Parasitology 1977, 74:61-71.
73. Wilson R.A., Coulson P.S. Immune effector mechanisms against schistosomiasis: looking for a chink in the parasite's armour. Trends Parasitol. 2009, 25:423-431.
74. Yoshino T.P., Brown M., Wu X.J., Jackson C.J., Ocadiz-Ruiz R., Chalmers I.W., Kolb M., Hokke C.H., Hoffmann K.F. Excreted/secreted Schistosoma mansoni venom allergen-like 9 (SmVAL9) modulates host extracellular matrix remodelling gene expression. Int. J. Parasitol. 2014, 44:551-563.
75. Yu J., Wang S., Li W., Dai G., Xu S., He Z., Peng X., Zhou S., Liu X. Cloning, expression and protective immunity evaluation of the full-length cDNA encoding succinate dehydrogenase iron-sulfur protein of Schistosoma japonicum. Sci. China C. Life Sci. 2007, 50:221-227.
76. Zhang M., Hong Y., Han Y., Han H., Peng J., Qiu C., Yang J., Lu K., Fu Z., Lin J. Proteomic analysis of tegument-exposed proteins of female and male Schistosoma japonicum worms. J. Proteome. Res. 2013, 12:5260-5270.