Application of RNA interference in triatomine (Hemiptera: Reduviidae) studies

Insect Science

Volumn 20, Issue 1, 2013, Pages 40-52

  Paim, Rafaela M M ^a   Araujo, Ricardo N ^a   Lehane, Michael J ^b   Gontijo, Nelder F ^a   Pereira, Marcos H ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

DsRNA; Knockdown; Phenotype; RNAi; Triatomine

Indexed keywords

ANIMAL; DSRNA; GENE TRANSFER; GENETICS; HEMIPTERA; INSECT CONTROL; KNOCKDOWN; PHENOTYPE; REVIEW; RNA INTERFERENCE; RNAI; TRIATOMINE;

DSRNA; KNOCKDOWN; PHENOTYPE; RNAI; TRIATOMINE;

ANIMALS; GENE TRANSFER TECHNIQUES; HEMIPTERA; INSECT CONTROL; RNA INTERFERENCE;

HEMIPTERA; HEXAPODA; KINETOPLASTIDA; REDUVIIDAE; TRYPANOSOMA CRUZI; TRYPANOSOMATIDAE;

EID: 84872820185     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/j.1744-7917.2012.01540.x     Document Type: Review

References (78)

1. Allingham, P.G., Kerlin, R.L., Tellan, R.L., Briscoe, S.J. and Standfast, H.A. (1992) Passage of host immunoglobulin across the midgut epithelium into the hemolymph of blood-fed buffalo flies Haematobia-irritans exigua. Journal of Insect Physiology, 38, 9-17.
2. Arakane, Y., Specht, C.A., Kramer, K.J., Muthukrishnan, S. and Beeman, R.W. (2008) Chitin synthases are required for survival, fecundity and egg hatch in the red flour beetle, Tribolium castaneum. Insect Biochemistry and Molecular Biology, 38, 959-962.
3. Araujo, R.N., Campos, I.T., Tanaka, A.S., Santos, A., Gontijo, N.F., Lehane, M.J. and Pereira, M.H. (2007) Brasiliensin: a novel intestinal thrombin inhibitor from Triatoma brasiliensis (Hemiptera: Reduviidae) with an important role in blood intake. International Journal for Parasitology, 37, 1351-1358.
4. Araujo, R.N., Santos, A., Pinto, F.S., Gontijo, N.F., Lehane, M.J. and Pereira, M.H. (2006) RNA interference of the salivary gland nitrophorin 2 in the triatomine bug Rhodnius prolixus (Hemiptera: Reduviidae) by dsRNA ingestion or injection. Insect Biochemistry and Molecular Biology, 36, 683-693.
5. Araujo, R.N., Soares, A.C., Paim, R.M., Gontijo, N.F., Gontijo, A.F., Lehane, M.J. and Pereira, M.H. (2009) The role of salivary nitrophorins in the ingestion of blood by the triatomine bug Rhodnius prolixus (Reduviidae: Triatominae). Insect Biochemistry and Molecular Biology, 39, 83-89.
6. Assumpcao, T.C., Charneau, S., Santiago, P.B., Francischetti, I.M., Meng, Z., Araujo, C.N., Pham, V.M., Queiroz, R.M., de Castro, C.N., Ricart, C.A., Santana, J.M. and Ribeiro, J.M. (2011) Insight into the salivary transcriptome and proteome of Dipetalogaster maxima. Journal of Proteome Research, 10, 669-679.
7. Assumpcao, T.C., Francischetti, I.M., Andersen, J.F., Schwarz, A., Santana, J.M. and Ribeiro, J.M. (2008) An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas' disease. Insect Biochemistry and Molecular Biology, 38, 213-232.
8. Belles, X. (2010) Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annual Review of Entomology, 55, 111-128.
9. Bernstein, E., Caudy, A.A., Hammond, S.M. and Hannon, G.J. (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature, 409, 363-366.
10. Bischoff, V., Vignal, C., Duvic, B., Boneca, I.G., Hoffmann, J.A. and Royet, J. (2006) Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathogens, 2, e14.
11. Boisson, B., Jacques, J.C., Choumet, V., Martin, E., Xu, J., Vernick, K. and Bourgouin, C. (2006) Gene silencing in mosquito salivary glands by RNAi. FEBS Letters, 580, 1988-1992.
12. Bussacos, A.C., Nakayasu, E.S., Hecht, M.M., Assumpcao, T.C., Parente, J.A., Soares, C.M., Santana, J.M., Almeida, I.C. and Teixeira, A.R. (2011) Redundancy of proteins in the salivary glands of Panstrongylus megistus secures prolonged procurement for blood meals. Journal of Proteomics, 74, 1693-1700.
13. de la Fuente, J., Kocan, K.M., Almazan, C. and Blouin, E.F. (2007) RNA interference for the study and genetic manipulation of ticks. Trends in Parasitology, 23, 427-433.
14. de Marco, R., Lovato, D.V., Torquato, R.J., Clara, R.O., Buarque, D.S. and Tanaka, A.S. (2010) The first pacifastin elastase inhibitor characterized from a blood sucking animal. Peptides, 31, 1280-1286.
15. Dietzl, G., Chen, D., Schnorrer, F., Su, K.C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K. and Dickson, B.J. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature, 448, 151-156.
16. Elbashir, S.M., Lendeckel, W. and Tuschl, T. (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes & Development, 15, 188-200.
17. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E. and Mello, C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391, 806-811.
18. Fjose, A., Ellingsen, S., Wargelius, A. and Seo, H.C. (2001) RNA interference: mechanisms and applications. Biotechnology Annual Review, 7, 31-57.
19. Fresquet, N. and Lazzari, C.R. (2011) Response to heat in Rhodnius prolixus: the role of the thermal background. Journal of Insect Physiology, 57, 1446-1449.
20. Ghildiyal, M. and Zamore, P.D. (2009) Small silencing RNAs: an expanding universe. Nature Reviews Genetics, 10, 94-108.
21. Giordano, E., Rendina, R., Peluso, I. and Furia, M. (2002) RNAi triggered by symmetrically transcribed transgenes in Drosophila melanogaster. Genetics, 160, 637-648.
22. Guarneri, A.A., Diotaiuti, L., Gontijo, N.F., Gontijo, A.F. and Pereira, M.H. (2003) Blood-feeding performance of nymphs and adults of Triatoma brasiliensis on human hosts. Acta Tropica, 87, 361-370.
23. Gygi, S.P., Rochon, Y., Franza, B.R. and Aebersold, R. (1999) Correlation between protein and mRNA abundance in yeast. Molecular and Cellular Biology, 19, 1720-1730.
24. Hannon, G.J. (2002) RNA interference. Nature, 418, 244-251.
25. Hatfield, P.R. (1988) Detection and localization of antibody ingested with a mosquito bloodmeal. Medical and Veterinary Entomology, 2, 339-345.
26. Horn, T. and Boutros, M. (2010) E-RNAi: a web application for the multi-species design of RNAi reagents-2010 update. Nucleic Acids Research, 38, W332-W339.
27. Hrycaj, S., Mihajlovic, M., Mahfooz, N., Couso, J.P. and Popadic, A. (2008) RNAi analysis of nubbin embryonic functions in a hemimetabolous insect, Oncopeltus fasciatus. Evolution and Development, 10, 705-716.
28. Hughes, C.L. and Kaufman, T.C. (2000) RNAi analysis of deformed, proboscipedia and sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head. Development, 127, 3683-3694.
29. Huvenne, H. and Smagghe, G. (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. Journal of Insect Physiology, 56, 227-235.
30. Kan, L. and Kessler, J.A. (2005) New tool for an old problem: can RNAi efficiently resolve the issue of genetic redundancy? Bioessays, 27, 14-16.
31. Kang, S. and Hong, Y.S. (2008) RNA interference in infectious tropical diseases. Korean Journal of Parasitology, 46, 1-15.
32. Kato, H., Jochim, R.C., Gomez, E.A., Sakoda, R., Iwata, H., Valenzuela, J.G. and Hashiguchi, Y. (2010) A repertoire of the dominant transcripts from the salivary glands of the blood-sucking bug, Triatoma dimidiata, a vector of Chagas disease. Infection, Genetics and Evolution, 10, 184-191.
33. Konopova, B. and Jindra, M. (2008) Broad-Complex acts downstream of Met in juvenile hormone signaling to coordinate primitive holometabolan metamorphosis. Development, 135, 559-568.
34. Kulkarni, M.M., Booker, M., Silver, S.J., Friedman, A., Hong, P., Perrimon, N. and Mathey-Prevot, B. (2006) Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nature Methods, 3, 833-838.
35. Kuttenkeuler, D. and Boutros, M. (2004) Genome-wide RNAi as a route to gene function in Drosophila. Briefings in Functional Genomics and Proteomics, 3, 168-176.
36. Lackie, A.M. and Gavin, S. (1989) Uptake and persistence of ingested antibody in the mosquito Anopheles stephensi. Medical and Veterinary Entomology, 3, 225-230.
37. Lavore, A., Pagola, L., Esponda-Behrens, N. and Rivera-Pomar, R. (2012) The gap gene giant of Rhodnius prolixus is maternally expressed and required for proper head and abdomen formation. Developmental Biology, 361, 147-155.
38. Levin, D.M., Breuer, L.N., Zhuang, S., Anderson, S.A., Nardi, J.B. and Kanost, M.R. (2005) A hemocyte-specific integrin required for hemocytic encapsulation in the tobacco hornworm, Manduca sexta. Insect Biochemistry and Molecular Biology, 35, 369-380.
39. Lingel, A. and Sattler, M. (2005) Novel modes of protein-RNA recognition in the RNAi pathway. Current Opinion in Structural Biology, 15, 107-115.
40. Lipardi, C. and Paterson, B.M. (2009) Identification of an RNA-dependent RNA polymerase in Drosophila involved in RNAi and transposon suppression. Proceedings of the National Academic of Sciences of the United States of America, 106, 15645-15650.
41. Medeiros, M.N., Logullo, R., Ramos, I.B., Sorgine, M.H., Paiva-Silva, G.O., Mesquita, R.D., Machado, E.A., Coutinho, M.A., Masuda, H., Capurro, M.L., Ribeiro, J.M., Cardoso Braz, G.R. and Oliveira, P.L. (2011) Transcriptome and gene expression profile of ovarian follicle tissue of the triatomine bug Rhodnius prolixus. Insect Biochemistry and Molecular Biology, 41, 823-831.
42. Meister, G. and Tuschl, T. (2004) Mechanisms of gene silencing by double-stranded RNA. Nature, 431, 343-349.
43. Miller, S.C., Brown, S.J. and Tomoyasu, Y. (2008) Larval RNAi in Drosophila? Development Genes and Evolution, 218, 505-510.
44. Minakuchi, C., Namiki, T. and Shinoda, T. (2009) Kruppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Developmental Biology, 325, 341-350.
45. Moffat, J., Reiling, J.H. and Sabatini, D.M. (2007) Off-target effects associated with long dsRNAs in Drosophila RNAi screens. Trends in Pharmacological Sciences, 28, 149-151.
46. Mury, F.B., da Silva, J.R., Ferreira, L.S., dos Santos Ferreira, B., de Souza-Filho, G.A., de Souza-Neto, J.A., Ribolla, P.E., Silva, C.P., do Nascimento, V.V., Machado, O.L., Berbert-Molina, M.A. and Dansa-Petretski, M. (2009) Alpha-glucosidase promotes hemozoin formation in a blood-sucking bug: an evolutionary history. PLoS ONE, 4, e6966.
47. Mutti, N.S., Park, Y., Reese, J.C. and Reeck, G.R. (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. Journal of Insect Science, 6, 1-7.
48. Naito, Y., Yamada, T., Matsumiya, T., Ui-Tei, K., Saigo, K. and Morishita, S. (2005) dsCheck: highly sensitive off-target search software for double-stranded RNA-mediated RNA interference. Nucleic Acids Research, 33, W589-W591.
49. Nykanen, A., Haley, B. and Zamore, P.D. (2001) ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell, 107, 309-321.
50. Osta, M.A., Christophides, G.K. and Kafatos, F.C. (2004) Effects of mosquito genes on Plasmodium development. Science, 303, 2030-2032.
51. Paim, R.M., Araujo, R.N., Soares, A.C., Lemos, L.C., Tanaka, A.S., Gontijo, N.F., Lehane, M.J. and Pereira, M.H. (2011) Influence of the intestinal anticoagulant in the feeding performance of triatomine bugs (Hemiptera: Reduviidae). International Journal for Parasitology, 41, 765-773.
52. Panfilio, K.A. (2009) Late extraembryonic morphogenesis and its zen (RNAi)-induced failure in the milkweed bug Oncopeltus fasciatus. Developmental Biology, 333, 297-311.
53. Price, D.R. and Gatehouse, J.A. (2008) RNAi-mediated crop protection against insects. Trends in Biotechnology, 26, 393-400.
54. Qiu, S., Adema, C.M. and Lane, T. (2005) A computational study of off-target effects of RNA interference. Nucleic Acids Research, 33, 1834-1847.
55. Ramakrishnan, V.G., Aljamali, M.N., Sauer, J.R. and Essenberg, R.C. (2005) Application of RNA interference in tick salivary gland research. Journal of Biomolecular Techniques, 16, 297-305.
56. Ramasamy, M.S., Ramasamy, R., Kay, B.H. and Kidson, C. (1988) Anti-mosquito antibodies decrease the reproductive capacity of Aedes aegypti. Medical and Veterinary Entomology, 2, 87-93.
57. Randolt, K., Gimple, O., Geissendörfer, J., Reinders, J., Prusko, C., Mueller, M.J., Albert, S., Tautz, J. and Beier, H. (2008) Immune-related proteins induced in the hemolymph after aseptic and septic injury differ in honey bee worker larvae and adults. Archives of Insect Biochemistry and Physiology, 69, 155-167.
58. Ribeiro, J.M., Andersen, J., Silva-Neto, M.A., Pham, V.M., Garfield, M.K. and Valenzuela, J.G. (2004) Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochemistry and Molecular Biology, 34, 61-79.
59. Ribeiro, J.M. and Francischetti, I.M. (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annual Review of Entomology, 48, 73-88.
60. Ribeiro, J.M., Mans, B.J. and Arca, B. (2010) An insight into the sialome of blood-feeding nematocera. Insect Biochemistry and Molecular Biology, 40, 767-784.
61. Roignant, J.Y., Carre, C., Mugat, B., Szymczak, D., Lepesant, J.A. and Antoniewski, C. (2003) Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA, 9, 299-308.
62. Santos, A., Ribeiro, J.M., Lehane, M.J., Gontijo, N.F., Veloso, A.B., Sant' Anna, M.R., Nascimento Araujo, R., Grisard, E.C. and Pereira, M.H. (2007) The sialotranscriptome of the blood-sucking bug Triatoma brasiliensis (Hemiptera, Triatominae). Insect Biochemistry and Molecular Biology, 37, 702-712.
63. Sauer, J.R., McSwain, J.L., Bowman, A.S. and Essenberg, R.C. (1995) Tick salivary gland physiology. Annual Review of Entomology, 40, 245-267.
64. Schlein, Y., Sira, D.T. and Jacobson, R.L. (1976) The passage of serum immunoglobulins through the gut of Sarcophaga falculata, Pand. Annals of Tropical Medicine and Parasitology, 70, 227-230.
65. Schofield, C.J. and Galvao, C. (2009) Classification, evolution, and species groups within the Triatominae. Acta Tropica, 110, 88-100.
66. Semizarov, D., Frost, L., Sarthy, A., Kroeger, P., Halbert, D.N. and Fesik, S.W. (2003) Specificity of short interfering RNA determined through gene expression signatures. Proceedings of the National Academic of Sciences of the United States of America, 100, 6347-6352.
67. Sledz, C.A., Holko, M., de Veer, M.J., Silverman, R.H. and Williams, B.R. (2003) Activation of the interferon system by short-interfering RNAs. Nature Cell Biology, 5, 834-839.
68. Soares, C.A., Lima, C.M., Dolan, M.C., Piesman, J., Beard, C.B. and Zeidner, N.S. (2005) Capillary feeding of specific dsRNA induces silencing of the isac gene in nymphal Ixodes scapularis ticks. Insect Molecular Biology, 14, 443-452.
69. Terenius, O., Papanicolaou, A., Garbutt, J.S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., Albrechtsen, M., An, C., Aymeric, J.L., Barthel, A., Bebas, P., Bitra, K., Bravo, A., Chevalier, F., Collinge, D.P., Crava, C.M., de Maagd, R.A., Duvic, B., Erlandson, M., Faye, I., Felfoldi, G., Fujiwara, H., Futahashi, R., Gandhe, A.S., Gatehouse, H.S., Gatehouse, L.N., Giebultowicz, J.M., Gomez, I., Grimmelikhuijzen, C.J., Groot, A.T., Hauser, F., Heckel, D.G., Hegedus, D.D., Hrycaj, S., Huang, L., Hull, J.J., Iatrou, K., Iga, M., Kanost, M.R., Kotwica, J., Li, C., Li, J., Liu, J., Lundmark, M., Matsumoto, S., Meyering-Vos, M., Millichap, P.J., Monteiro, A., Mrinal, N., Niimi, T., Nowara, D., Ohnishi, A., Oostra, V., Ozaki, K., Papakonstantinou, M., Popadic, A., Rajam, M.V., Saenko, S., Simpson, R.M., Soberon, M., Strand, M.R., Tomita, S., Toprak, U., Wang, P., Wee, C.W., Whyard, S., Zhang, W., Nagaraju, J., Ffrench-Constant, R.H., Herrero, S., Gordon, K., Swevers, L. and Smagghe, G. (2010) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. Journal of Insect Physiology, 57, 231-245.
70. Timmons, L., Tabara, H., Mello, C.C. and Fire, A.Z. (2003) Inducible systemic RNA silencing in Caenorhabditis elegans. Molecular Biology of the Cell, 14, 2972-2983.
71. Tomoyasu, Y. and Denell, R.E. (2004) Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Development Genes and Evolution, 214, 575-578.
72. Tomoyasu, Y., Miller, S.C., Tomita, S., Schoppmeier, M., Grossmann, D. and Bucher, G. (2008) Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biology, 9, R10.
73. Tschuch, C., Schulz, A., Pscherer, A., Werft, W., Benner, A., Hotz-Wagenblatt, A., Barrionuevo, L.S., Lichter, P. and Mertens, D. (2008) Off-target effects of siRNA specific for GFP. BMC Molecular Biology, 9, 60.
74. Turner, C.T., Davy, M.W., MacDiarmid, R.M., Plummer, K.M., Birch, N.P. and Newcomb, R.D. (2006) RNA interference in the light brown apple moth, Epiphyas postvittana (Walker) induced by double-stranded RNA feeding. Insect Molecular Biology, 15, 383-391.
75. Walshe, D.P., Lehane, S.M., Lehane, M.J. and Haines, L.R. (2009) Prolonged gene knockdown in the tsetse fly Glossina by feeding double stranded RNA. Insect Molecular Biology, 18, 11-19.
76. Waters, J.C. and Swedlow, J.R. (2007) Interpreting fluorescence microscopy images and measurements. Evaluating Techniques in Biochemical Research (ed. D. Zuk ), pp. 37-42. Cell Press, Cambridge, MA
77. Winston, W.M., Molodowitch, C. and Hunter, C.P. (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science, 295, 2456-2459.
78. Zhou, X., Oi, F.M. and Scharf, M.E. (2006) Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proceedings of the National Academic of Sciences of the United States of America, 103, 4499-4504.