Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover

PLoS Pathogens

Volumn 6, Issue 4, 2010, Pages 1-10

  Tran, Mai H ^a,b   Freitas, Tori C ^b   Cooper, Leanne ^a   Gaze, Soraya ^a   Gatton, Michelle L ^a   Jones, Malcolm K ^a,c   Lovas, Erica ^c   Pearce, Edward J ^b   Loukas, Alex ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; LUCIFERASE; MESSENGER RNA; TETRASPANIN; TETRASPANIN 1; TETRASPANIN 2; UNCLASSIFIED DRUG; HELMINTH PROTEIN; MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; ELECTROPORATION; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; GENETIC TRANSCRIPTION; HOST PARASITE INTERACTION; IN VITRO STUDY; MESENTERY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; RNA INTERFERENCE; SCHISTOSOMA MANSONI; SCHISTOSOMULUM; TRANSCRIPTION REGULATION; ULTRASTRUCTURE; WORM TEGUMENT; ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; GENE; GENETICS; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHISTOSOMIASIS MANSONI; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

MUS; SCHISTOSOMA MANSONI;

ANIMALS; BLOTTING, WESTERN; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENES, HELMINTH; HELMINTH PROTEINS; MEMBRANE PROTEINS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, MESSENGER; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI;

EID: 77954037090     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000840     Document Type: Article

References (62)

1. Fenwick A, Rollinson D, Southgate V (2006) Implementation of human schistosomiasis control: Challenges and prospects. Adv Parasitol 61: 567-622.
2. Gryseels B, Polman K, Clerinx J, Kestens L (2006) Human schistosomiasis. Lancet 368: 1106-1118.
3. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411-425.
4. Miller P, Wilson RA (1980) Migration of the schistosomula of Schistosoma mansoni from the lungs to the hepatic portal system. Parasitology 80: 267-288.
5. Jones MK, Gobert GN, Zhang L, Sunderland P, McManus DP (2004) The cytoskeleton and motor proteins of human schistosomes and their roles in surface maintenance and host-parasite interactions. Bioessays 26: 752-765.
6. Smithers SR, McLaren DJ, Ramalho-Pinto FJ (1977) Immunity to schistosomes: the target. Am J Trop Med Hyg 26: 11-19.
7. Smithers SR, Terry RJ (1976) The immunology of schistosomiasis. Adv Parasitol 14: 399-422.
8. Loukas A, Tran M, Pearson MS (2007) Schistosome membrane proteins as vaccines. Int J Parasitol 37: 257-263.
9. Verjovski-Almeida S, De Marco R, Martins EA, Guimaraes PE, Ojopi EP, et al. (2003) Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nat Genet 35: 148-157.
10. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352-358.
11. Braschi S, Curwen RS, Ashton PD, Verjovski-Almeida S, Wilson A (2006) The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6: 1471-1482.
12. Gaugitsch HW, Hofer E, Huber NE, Schnabl E, Baumruker T (1991) A new superfamily of lymphoid and melanoma cell proteins with extensive homology to Schistosoma mansoni antigen Sm23. Eur J Immunol 21: 377-383.
13. Smyth D, McManus DP, Smout MJ, Laha T, Zhang W, et al. (2003) Isolation of cDNAs encoding secreted and transmembrane proteins from Schistosoma mansoni by a signal sequence trap method. Infect Immun 71: 2548-2554.
14. Braschi S, Borges WC, Wilson RA (2006) Proteomic analysis of the schistosome tegument and its surface membranes. Mem Inst Oswaldo Cruz 101 Suppl 1: 205-212.
15. Kovalenko OV, Metcalf DG, De Grado WF, Hemler ME (2005) Structural organization and interactions of transmembrane domains in tetraspanin proteins. BMC Struct Biol 5: 11.
16. Hemler ME (2001) Specific tetraspanin functions. J Cell Biol 155: 1103-1107.
17. Stipp CS, Kolesnikova TV, Hemler ME (2003) Functional domains in tetraspanin proteins. Trends Biochem Sci 28: 106-112.
18. Boucheix C, Duc GH, Jasmin C, Rubinstein E (2001) Tetraspanins and malignancy. Expert Rev Mol Med 2001: 1-17.
19. Hemler ME (2003) Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol 19: 397-422.
20. Wright MD, Moseley GW, van Spriel AB (2004) Tetraspanin microdomains in immune cell signalling and malignant disease. Tissue Antigens 64: 533-542.
21. Higginbottom A, Takahashi Y, Bolling L, Coonrod SA, White JM, et al. (2003) Structural requirements for the inhibitory action of the CD9 large extracellular domain in sperm/oocyte binding and fusion. Biochem Biophys Res Commun 311: 208-214.
22. Lazo PA (2007) Functional implications of tetraspanin proteins in cancer biology. Cancer Sci 98: 1666-1677.
23. Rubinstein E, Ziyyat A, Prenant M, Wrobel E, Wolf JP, et al. (2006) Reduced fertility of female mice lacking CD81. Dev Biol 290: 351-358.
24. Barraud-Lange V, Naud-Barriant N, Bomsel M, Wolf JP, Ziyyat A (2007) Transfer of oocyte membrane fragments to fertilizing spermatozoa. FASEB J 21: 3446-3449.
25. Gordon-Alonso M, Yanez-Mo M, Barreiro O, Alvarez S, Munoz-Fernandez MA, et al. (2006) Tetraspanins CD9 and CD81 modulate HIV-1- induced membrane fusion. J Immunol 177: 5129-5137.
26. Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, et al. (2003) Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 278: 41624-41630.
27. Yalaoui S, Zougbede S, Charrin S, Silvie O, Arduise C, et al. (2008) Hepatocyte permissiveness to Plasmodium infection is conveyed by a short and structurally conserved region of the CD81 large extracellular domain. PLoS Pathog 4: e1000010. doi:10.1371/journal.ppat.1000010.
28. Tran MH, Pearson MS, Bethony JM, Smyth DJ, Jones MK, et al. (2006) Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nature Med 12: 835-840.
29. van Balkom BW, van Gestel RA, Brouwers JF, Krijgsveld J, Tielens AG, et al. (2005) Mass spectrometric analysis of the Schistosoma mansoni tegumental subproteome. J Proteome Res 4: 958-966.
30. Braschi S, Wilson RA (2006) Proteins exposed at the adult schistosome surface revealed by biotinylation. Mol Cell Proteomics 5: 347-356.
31. Correnti JM, Pearce EJ (2004) Transgene expression in Schistosoma mansoni: introduction of RNA into schistosomula by electroporation. Mol Biochem Parasitol 137: 75-79.
32. Skelly PJ, Da'dara A, Harn DA (2003) Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. Int J Parasitol 33: 363-369.
33. Freitas TC, Jung E, Pearce EJ (2007) TGF-beta signaling controls embryo development in the parasitic flatworm Schistosoma mansoni. PLoS Pathog 3: e52. doi:10.1371/journal.ppat.0030052.
34. Boyle JP, Wu XJ, Shoemaker CB, Yoshino TP (2003) Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Mol Biochem Parasitol 128: 205-215.
35. Hockley DJ, McLaren DJ (1973) Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. Int J Parasitol 3: 13-25.
36. Basch PF (1981) Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. J Parasitol 67: 179-185.
37. Schmidt J, Bodor O, Gohr L, Kunz W (1996) Paramyosin isoforms of Schistosoma mansoni are phosphorylated and localized in a large variety of muscle types. Parasitology 112: 459-467.
38. Cousin CE, Stirewalt MA, Dorsey CH, Watson LP (1986) Schistosoma mansoni: comparative development of schistosomules produced by artificial techniques. J Parasitol 72: 606-609.
39. Da'dara AA, Li YS, Xiong T, Zhou J, Williams GM, et al. (2008) DNA-based vaccines protect against zoonotic schistosomiasis in water buffalo. Vaccine 26: 3617-3625.
40. Ndegwa D, Krautz-Peterson G, Skelly PJ (2007) Protocols for gene silencing in schistosomes. Exp Parasitol 117: 284-291.
41. Pearce EJ, Freitas TC (2008) Reverse genetics and the study of the immune response to schistosomes. Parasite Immunol 30: 215-221.
42. Correnti JM, Brindley PJ, Pearce EJ (2005) Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol Biochem Parasitol 143: 209-215.
43. Morales ME, Rinaldi G, Gobert GN, Kines KJ, Tort JF, et al. (2008) RNA interference of Schistosoma mansoni cathepsin D, the apical enzyme of the hemoglobin proteolysis cascade. Mol Biochem Parasitol 157: 160-168.
44. Faghiri Z, Skelly PJ (2009) The role of tegumental aquaporin from the human parasitic worm, Schistosoma mansoni, in osmoregulation and drug uptake. FASEB J 23: 2780-2789.
45. Hemler ME (2008) Targeting of tetraspanin proteins - potential benefits and strategies. Nature Rev Drug Discov 7: 747-758.
46. Moribe H, Yochem J, Yamada H, Tabuse Y, Fujimoto T, et al. (2004) Tetraspanin protein (TSP-15) is required for epidermal integrity in Caenorhabditis elegans. J Cell Sci 117: 5209-5220.
47. Yamada M, Sumida Y, Fujibayashi A, Fukaguchi K, Sanzen N, et al. (2008) The tetraspanin CD151 regulates cell morphology and intracellular signaling on laminin-511. FEBS J 275: 3335-3351.
48. Szollosi J, Horejsi V, Bene L, Angelisova P, Damjanovich S (1996) Supramolecular complexes of MHC class I, MHC class II, CD20, and tetraspan molecules (CD53, CD81, and CD82) at the surface of a B cell line JY. J Immunol 157: 2939-2946.
49. Kropshofer H, Spindeldreher S, Rohn TA, Platania N, Grygar C, et al. (2002) Tetraspan microdomains distinct from lipid rafts enrich select peptide-MHC class II complexes. Nature Immunol 3: 61-68.
50. Sheng KC, van Spriel AB, Gartlan KH, Sofi M, Apostolopoulos V, et al. (2009) Tetraspanins CD37 and CD151 differentially regulate Ag presentation and Tcell co-stimulation by DC. Eur J Immunol 39: 50-55.
51. Sher A, Hall BF, Vadas MA (1978) Acquisition of murine major histocompatibility complex gene products by schistosomula of Schistosoma mansoni. J Exp Med 148: 46-57.
52. Le Naour F, Andre M, Greco C, Billard M, Sordat B, et al. (2006) Profiling of the tetraspanin web of human colon cancer cells. Mol Cell Proteomics 5: 845-857.
53. Liu L, He B, Liu WM, Zhou D, Cox JV, et al. (2007) Tetraspanin CD151 promotes cell migration by regulating integrin trafficking. J Biol Chem 282: 31631-31642.
54. Yang XH, Richardson AL, Torres-Arzayus MI, Zhou P, Sharma C, et al. (2008) CD151 accelerates breast cancer by regulating alpha 6 integrin function, signaling, and molecular organization. Cancer Res 68: 3204-3213.
55. Deissler H, Kuhn EM, Lang GE (2007) Tetraspanin CD9 is involved in the migration of retinal microvascular endothelial cells. Int J Mol Med 20: 643-652.
56. James ER, Taylor MG (1976) Transformation of cercariae to schistosomula: a quantitative comparison of transformation techniques and of infectivity by different injection routes of the organisms produced. J Helminthol 50: 223-233.
57. Salafsky B, Fusco AC, Whitley K, Nowicki D, Ellenberger B (1988) Schistosoma mansoni: analysis of cercarial transformation methods. Exp Parasitol 67: 116-127.
58. Lazdins JK, Stein MJ, David JR, Sher A (1982) Schistosoma mansoni: rapid isolation and purification of schistosomula of different developmental stages by centrifugation on discontinuous density gradients of Percoll. Exp Parasitol 53: 39-44.
59. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
60. Pearce EJ, James SL, Dalton J, Barrall A, Ramos C, et al. (1986) Immunochemical characterization and purification of Sm-97, a Schistosoma mansoni antigen monospecifically recognized by antibodies from mice protectively immunized with a nonliving vaccine. J Immunol 137: 3593-3600.
61. Griffiths G (1993) Fine Structure Immunocytochemistry Springer: Berlin, 459 p.
62. Bartley PB, Ramm GA, Jones MK, Ruddell RG, Li Y, McManus DP (2006) A contributory role for activated hepatic stellate cells in the dynamics of Schistosoma japonicum egg-induced fibrosis. Int J Parasitol 36: 993-1001.