Development of functional genomic tools in trematodes: RNA interference and luciferase reporter gene activity in Fasciola hepatica

PLoS Neglected Tropical Diseases

Volumn 2, Issue 7, 2008, Pages

  Rinaldi, Gabriel ^a,b   Morales, Maria E ^a   Cancela, Martin ^b   Castillo, Estela ^c   Brindley, Paul J ^a,d   Tort, José F ^b  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^c UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^d GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSOL AMINOPEPTIDASE; DOUBLE STRANDED DNA; LUCIFERASE; MESSENGER RNA; FIREFLY LUCIFERASE; HELMINTH PROTEIN;

ARTICLE; ASSAY; DRUG TARGETING; ELECTROPORATION; ENZYME ACTIVITY; FASCIOLA HEPATICA; FASCIOLIASIS; FUNCTIONAL GENOMICS; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; HOST PARASITE INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; REPORTER GENE; RNA INTERFERENCE; TRANSCRIPTOMICS; TRANSGENE; TREMATODE; ANIMAL; ENZYMOLOGY; EVALUATION; GENETICS; GENOMICS; HUMAN; LIVER; METABOLISM; METHODOLOGY; PARASITOLOGY; SNAIL;

ANIMALS; FASCIOLA HEPATICA; FASCIOLIASIS; GENES, REPORTER; GENOMICS; HELMINTH PROTEINS; HUMANS; LEUCYL AMINOPEPTIDASE; LIVER; LUCIFERASES, FIREFLY; RNA INTERFERENCE; SNAILS;

EID: 56149093397     PISSN: None     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pntd.0000260     Document Type: Article

References (55)

1. Kalinna BH, Brindley PJ (2007) Manipulating the manipulators: advances in parasitic helminth transgenesis and RNAi. Trends Parasitol 23: 197-204.
2. Brindley PJ, Pearce EJ (2007) Genetic manipulation of schistosomes. Int J Parasitol 37: 465-473.
3. Wilson RA, Ashton PD, Braschi S, Dillon GP, Berriman M, et al. (2007) 'Oming in on schistosomes: prospects and limitations for post-genomics. Trends Parasitol 23: 14-20.
4. Geldhof P, Visser A, Clark D, Saunders G, Britton C, et al. (2007) RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology 134: 609-619.
5. Wippersteg V, Kapp K, Kunz W, Grevelding CG (2002) Characterisation of the cysteine protease ER60 in transgenic Schistosoma mansoni larvae. Int J Parasitol 32: 1219-1224.
6. Wippersteg V, Kapp K, Kunz W, Jackstadt WP, Zahner H, et al. (2002) HSP70-controlled GFP expression in transiently transformed schistosomes. Mol Biochem Parasitol 120: 141-150.
7. Wippersteg V, Ribeiro F, Liedtke S, Kusel JR, Grevelding CG (2003) The uptake of Texas Red-BSA in the excretory system of schistosomes and its colocalisation with ER60 promoter-induced GFP in transiently transformed adult males. Int J Parasitol 33: 1139-1143.
8. Wippersteg V, Sajid M, Walshe D, Khiem D, Salter JP, et al. (2005) Biolistic transformation of Schistosoma mansoni with 5′ flanking regions of two peptidase genes promotes tissue-specific expression. Int J Parasitol 35: 583-589.
9. Davis RE, Parra A, LoVerde PT, Ribeiro E, Glorioso G, et al. (1999) Transient expression of DNA and RNA in parasitic helminths by using particle bombardment. Proc Natl Acad Sci U S A 96: 8687-8692.
10. Heyers O, Walduck AK, Brindley PJ, Bleiss W, Lucius R, et al. (2003) Schistosoma mansoni miracidia transformed by particle bombardment infect Biomphalaria glabrata snails and develop into transgenic sporocysts. Exp Parasitol 105: 174-178.
11. Rossi A, Wippersteg V, Klinkert MQ, Grevelding CG (2003) Cloning of 5′ and 3′ flanking regions of the Schistosoma mansoni calcineurin A gene and their characterization in transiently transformed parasites. Mol Biochem Parasitol 130: 133-138.
12. Correnti JM, Pearce EJ (2004) Transgene expression in Schistosoma mansoni: introduction of RNA into schistosomula by electroporation. Mol Biochem Parasitol 137: 75-79.
13. Yuan XS, Shen JL, Wang XL, Wu XS, Liu DP, et al. (2005) Schistosoma japonicum: a method for transformation by electroporation. Exp Parasitol 111: 244-249.
14. Morales ME, Mann VH, Kines KJ, Gobert GN, Fraser MJ Jr., et al. (2007) piggyBac transposon mediated transgenesis of the human blood fluke, Schistosoma mansoni. Faseb J..
15. Kines KJ, Mann VH, Morales ME, Shelby BD, Kalinna BH, et al. (2006) Transduction of Schistosoma mansoni by vesicular stomatitis virus glycoprotein-pseudotyped Moloney murine leukemia retrovirus. Exp Parasitol 112: 209-220.
16. 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.
17. 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.
18. 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.
19. Osman A, Niles EG, Verjovski-Almeida S, LoVerde PT (2006) Schistosoma mansoni TGF-beta receptor II: role in host ligand-induced regulation of a schistosome target gene. PLoS Pathog 2: e54. doi:10.1371/ journal.ppat.0020054.
20. Krautz-Peterson G, Radwanska M, Ndegwa D, Shoemaker CB, Skelly PJ (2007) Optimizing gene suppression in schistosomes using RNA interference. Mol Biochem Parasitol 153: 194-202.
21. Cheng GF, Lin JJ, Shi Y, Jin YX, Fu ZQ, et al. (2005) Dose-dependent inhibition of gynecophoral canal protein gene expression in vitro in the schistosome (Schistosoma japonicum) by RNA interference. Acta Biochim Biophys Sin (Shanghai) 37: 386-390.
22. Dinguirard N, Yoshino TP (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. Mol Biochem Parasitol 146: 219-230.
23. Delcroix M, Sajid M, Caffrey CR, Lim KC, Dvorak J, et al. (2006) A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J Biol Chem 281: 39316-39329.
24. Reddien PW, Bermange AL, Murfitt KJ, Jennings JR, Sanchez Alvarado A (2005) Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev Cell 8: 635-649.
25. Newmark PA (2005) Opening a new can of worms: a large-scale RNAi screen in planarians. Dev Cell 8: 623-624.
26. Newmark PA, Reddien PW, Cebria F, Sanchez Alvarado A (2003) Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc Natl Acad Sci U S A 100 Suppl 1: 11861-11865.
27. Sanchez Alvarado A (2003) The freshwater planarian Schmidtea mediterranea: embryogenesis, stem cells and regeneration. Curr Opin Genet Dev 13: 438-444.
28. Haas BJ, Berriman M, Hirai H, Cerqueira GG, Loverde PT, et al. (2007) Schistosoma mansoni genome: Closing in on a final gene set. Exp Parasitol.
29. Liu F, Lu J, Hu W, Wang SY, Cui SJ, et al. (2006) New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathog 2: e29. doi:10.1371/ journal.ppat.0020029.
30. Verjovski-Almeida S, DeMarco R, Martins EA, Guimaraes PE, Ojopi EP, et al. (2003) Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nat Genet 35: 148-157.
31. Verjovski-Almeida S, Leite LC, Dias-Neto E, Menck CF, Wilson RA (2004) Schistosome transcriptome: insights and perspectives for functional genomics. Trends Parasitol 20: 304-308.
32. Hu W, Yan Q, Shen DK, Liu F, Zhu ZD, et al. (2003) Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nat Genet 35: 139-147.
33. Spiliotis M, Lechner S, Tappe D, Scheller C, Krohne G, et al. (2007) Transient transfection of Echinococcus multilocularis primary cells and complete in vitro regeneration of metacestode vesicles. Int J Parasitol.
34. Ohashi H, Umeda N, Hirazawa N, Ozaki Y, Miura C, et al. (2007) Expression of vasa (vas)-related genes in germ cells and specific interference with gene functions by double-stranded RNA in the monogenean, Neobenedenia girellae. Int J Parasitol 37: 515-523.
35. McGonigle L, Mousley A, Marks NJ, Brennan GP, Dalton JP, et al. (2008) The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration. Int J Parasitol 38: 149-155.
36. Spithill TW, Smooker PM, Copeman B (1999) Fasciola gigantica: epidemiology, control, immunology and molecular biology. In: Dalton JP, ed (1999) Fasciolosis. Wallingford: CAB International Publishing. pp 465-525.
37. Mas-Coma S (2005) Epidemiology of fascioliasis in human endemic areas. J Helminthol 79: 207-216.
38. Garcia HH, Moro PL, Schantz PM (2007) Zoonotic helminth infections of humans: echinococcosis, cysticercosis and fascioliasis. Curr Opin Infect Dis 20: 489-494.
39. Keiser J, Engels D, Buscher G, Utzinger J (2005) Triclabendazole for the treatment of fascioliasis and paragonimiasis. Expert Opin Investig Drugs 14: 1513-1526.
40. Brennan GP, Fairweather I, Trudgett A, Hoey E, McCoy, et al. (2007) Understanding triclabendazole resistance. Exp Mol Pathol 82: 104-109.
41. Jefferies JR, Campbell AM, van Rossum AJ, Barrett J, Brophy PM (2001) Proteomic analysis of Fasciola hepatica excretory-secretory products. Proteomics 1: 1128-1132.
42. Morphew RM, Wright HA, LaCourse EJ, Woods DJ, Brophy PM (2007) Comparative proteomics of excretory-secretory proteins released by the liver fluke Fasciola hepatica in sheep host bile and during in vitro culture ex host. Mol Cell Proteomics 6: 963-972.
43. 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.
44. Basch PF (1981) Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. J Parasitol 67: 179-185.
45. Carmona C, Dowd AJ, Smith AM, Dalton JP (1993) Cathepsin L proteinase secreted by Fasciola hepatica in vitro prevents antibody-mediated eosinophil attachment to newly excysted juveniles. Mol Biochem Parasitol 62: 9-17.
46. Acosta D, Cancela M, Piacenza L, Roche L, Carmona C, et al. (2007) Fasciola hepatica leucine aminopeptidase, a promising candidate for vaccination against ruminant fasciolosis. Mol Biochem Parasitol doi:10.1016/j.molbiopara. 2007.11.011.
47. Correnti JM, Jung E, Freitas TC, Pearce EJ (2007) Transfection of Schistosoma mansoni by electroporation and the description of a new promoter sequence for transgene expression. Int J Parasitol 37: 1107-1115.
48. Smith MA, Clegg JA (1981) Improved culture of Fasciola hepatica in vitro. Z Parasitenkd 66: 9-15.
49. Fairweather I, Threadgold LT, Hanna REB (1999) Development of Fasciola hepatica in the mammalian host. In: Dalton JP, ed (1999) Fasciolosis. New York: CABI Publishing. pp 47-104.
50. Morales ME, Rinaldi G, Gobert GN, Kines KJ, Tort JF, et al. (2007) RNA interference of Schistosoma mansoni cathepsin D, the apical enzyme of the hemoglobin proteolysis cascade. Mol Biochem Parasitol doi:10.1016/ j.molbiopara.2007.10.009.
51. Cancela M, Acosta D, Rinaldi G, Silva E, Duran R, et al. (2008) A distinctive repertoire of cathepsins is expressed by juvenile invasive Fasciola hepatica. Biochimie Accepted.
52. Knox DP, Geldhof P, Visser A, Britton C (2007) RNA interference in parasitic nematodes of animals: a reality check? Trends Parasitol 23: 105-107.
53. Viney ME, Thompson FJ (2007) Two hypotheses to explain why RNA interference does not work in animal parasitic nematodes. Int J Parasitol.
54. Winston WM, Sutherlin M, Wright AJ, Feinberg EH, Hunter CP (2007) Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc Natl Acad Sci U S A 104: 10565-10570.
55. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756-1760.