RNA interference for the identification of ectoparasite vaccine candidates

Parasite Immunology

Volumn 36, Issue 11, 2014, Pages 616-626

  Marr, E J ^a,b   Sargison, N D ^b   Nisbet, A J ^a   Burgess, S T G ^a  

^a MOREDUN RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Ectoparasite; Mite; RNA interference; Sea lice; Tick; Vaccine

Indexed keywords

ACARI; ARTHROPODA; IXODIDA; PHTHIRAPTERA;

ANTIGEN; VACCINE;

ANIMAL; DRUG DELIVERY SYSTEM; ECONOMICS; ECTOPARASITIC INFESTATIONS; GENETICS; HUMAN; IMMUNOLOGY; RNA INTERFERENCE; VETERINARY;

ANIMALS; ANTIGENS; DRUG DELIVERY SYSTEMS; ECTOPARASITIC INFESTATIONS; HUMANS; RNA INTERFERENCE; VACCINES;

EID: 84922334232     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12132     Document Type: Review

References (131)

1. Willadsen P. Immunological control of ectoparasites: past achievements and future research priorities. Genet Anal 1999; 15: 131-137.
2. Schnettler E, Ratinier M, Watson M, et al. RNA interference targets arbovirus replication in Culicoides cells. J Virol 2013; 87: 2441-2454.
3. Campbell EM, Budge GE & Bowman AS. Gene-knockdown in the honey bee mite Varroa destructor by a non-invasive approach: studies on a glutathione S-transferase. Parasit Vectors 2010; 3: 73.
4. de Castro JJ. Sustainable tick and tickborne disease control in livestock improvement in developing countries. Vet Parasitol 1997; 71: 77-97.
5. Dalton JP & Mulcahy G. Parasite vaccines-a reality? Vet Parasitol 2001; 98: 149-167.
6. Willadsen P. Novel vaccines for ectoparasites. Vet Parasitol 1997; 71: 209-222.
7. Coop RL, Taylor MA, Jacobs DE & Jackson F. Ectoparasites: recent advances in control. Trends Parasitol 2002; 18: 55-56.
8. Sargison ND, Jackson F, Bartley DJ, Wilson DJ, Stenhouse LJ & Penny CD. Observations on the emergence of multiple anthelmintic resistance in sheep flocks in the south-east of Scotland. Vet Parasitol 2007; 145: 65-76.
9. Sargison ND, Jackson F, Bartley DJ & Moir AC. Failure of moxidectin to control benzimidazole-, levamisole- and ivermectin-resistant Teladorsagia circumcincta in a sheep flock. Vet Rec 2005; 156: 105-109.
10. Bartley DJ, Jackson E, Sargison N & Jackson F. Further characterisation of a triple resistant field isolate of Teladorsagia from a Scottish lowland sheep farm. Vet Parasitol 2005; 134: 261-266.
11. Coles GC. Drug-resistant parasites of sheep: an emerging problem in Britain? Parasitol Today 1998; 14: 86-88.
12. Currie BJ, Harumal P, McKinnon M & Walton SF. First documentation of in vivo and in vitro ivermectin resistance in Sarcoptes scabiei. Clin Infect Dis 2004; 39: e8-e12.
13. Sargison N, Scott P & Jackson F. Multiple anthelmintic resistance in sheep. Vet Rec 2001; 149: 778-779.
14. McArthur CL, Bartley DJ, Shaw DJ & Matthews JB. Assessment of ivermectin efficacy against gastrointestinal nematodes in cattle on four Scottish farms. Vet Rec 2011; 169: 658.
15. Bartley DJ, McArthur CL, Devin LM, et al. Characterisation of macrocyclic lactone resistance in two field-derived isolates of Cooperia oncophora. Vet Parasitol 2012; 190: 454-460.
16. Pruett JH. Immunological control of arthropod ectoparasites-a review. Int J Parasitol 1999; 29: 25-32.
17. Mathieson BR & Lehane MJ. Isolation of the gram-negative bacterium, Serratia marcescens, from the sheep scab mite, Psoroptes ovis. Vet Rec 1996; 138: 210-211.
18. Jayawardena KG, Heller-Haupt A, Woodland RM & Varma MG. Antigens of the sheep scab mite Psoroptes ovis. Folia Parasitol (Praha) 1998; 45: 239-244.
19. Nong X, Fang C, Wang J, et al. Acaricidal activity of extract from Eupatorium adenophorum against the Psoroptes cuniculi and Sarcoptes scabiei in vitro. Vet Parasitol 2012; 187: 345-349.
20. Shen F, Xing M, Liu L, et al. Efficacy of trans-cinnamaldehyde against Psoroptes cuniculi in vitro. Parasitol Res 2012; 110: 1321-1326.
21. Walton SF, McKinnon M, Pizzutto S, Dougall A, Williams E & Currie BJ. Acaricidal activity of Melaleuca alternifolia (tea tree) oil: in vitro sensitivity of Sarcoptes scabiei var hominis to terpinen-4-ol. Arch Dermatol 2004; 140: 563-566.
22. James PJ & Callander JT. Dipping and jetting with tea tree (Melaleuca alternifolia) oil formulations control lice (Bovicola ovis) on sheep. Vet Parasitol 2012; 189: 338-343.
23. Talbert R & Wall R. Toxicity of essential and non-essential oils against the chewing louse, Bovicola (Werneckiella) ocellatus. Res Vet Sci 2012; 93: 831-835.
24. Heimerdinger A, Olivo CJ, Molento MB, et al. Alcoholic extract of lemongrass (Cymbopogon citratus) on the control of Boophilus microplus in cattle. Rev Bras Parasitol Vet 2006; 15: 37-39.
25. Koc S, Oz E, Aydin L & Cetin H. Acaricidal activity of the essential oils from three Lamiaceae plant species on Rhipicephalus turanicus Pom. (Acari: Ixodidae). Parasitol Res 2012; 111: 1863-1865.
26. Horak IG, Camicas JL & Keirans JE. The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): a world list of valid tick names. Exp Appl Acarol 2002; 28: 27-54.
27. Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Pena A & Horak IG. Comments on controversial tick (Acari: Ixodida) species names and species described or resurrected from 2003 to 2008. Exp Appl Acarol 2009; 48: 311-327.
28. Ellse L, Burden FA & Wall R. Control of the chewing louse Bovicola (Werneckiella) ocellatus in donkeys, using essential oils. Med Vet Entomol 2013; 27: 408-413.
29. Hamiduzzaman MM, Sinia A, Guzman-Novoa E & Goodwin PH. Entomopathogenic fungi as potential biocontrol agents of the ecto-parasitic mite, Varroa destructor, and their effect on the immune response of honey bees (Apis mellifera L.). J Invertebr Pathol 2012; 111: 237-243.
30. Perrucci S, Zini A, Donadio E, Mancianti F & Fichi G. Isolation of Scopulariopsis spp. fungi from Psoroptes cuniculi body surface and evaluation of their entomopathogenic role. Parasitol Res 2008; 102: 957-962.
31. Lekimme M, Mignon B, Tombeux S, Focant C, Marechal F & Losson B. In vitro entomopathogenic activity of Beauveria bassiana against Psoroptes spp. (Acari: Psoroptidae). Vet Parasitol 2006; 139: 196-202.
32. Fernandes EK, Bittencourt VR & Roberts DW. Perspectives on the potential of entomopathogenic fungi in biological control of ticks. Exp Parasitol 2012; 130: 300-305.
33. Mochi DA, Monteiro AC, Machado AC & Yoshida L. Efficiency of entomopathogenic fungi in the control of eggs and larvae of the horn fly Haematobia irritans (Diptera: Muscidae). Vet Parasitol 2010; 167: 62-66.
34. Cuisance D, Barre N & de Deken R. Ectoparasites of animals: methods of ecological, biological, genetic and mechanical control. Rev Sci Tech 1994; 13: 1305-1356.
35. Willadsen P. The molecular revolution in the development of vaccines against ectoparasites. Vet Parasitol 2001; 101: 353-368.
36. Knox DP & Redmond DL. Parasite vaccines - recent progress and problems associated with their development. Parasitology 2006; 133: S1-S8.
37. Wall R & Strong L. Environmental consequences of treating cattle with the antiparasitic drug ivermectin. Nature 1987; 327: 418-421.
38. Willadsen P, Riding GA, McKenna RV, et al. Immunologic control of a parasitic arthropod. Identification of a protective antigen from Boophilus microplus. J Immunol 1989; 143: 1346-1351.
39. Smith WD & Pettit DM. Immunization against sheep scab: preliminary identification of fractions of Psoroptes ovis which confer protective effects. Parasite Immunol 2004; 26: 307-314.
40. Smith WD, van den Broek A, Huntley J, et al. Approaches to vaccines for Psoroptes ovis (sheep scab). Res Vet Sci 2001; 70: 87-91.
41. Nisbet AJ & Huntley JF. Progress and opportunities in the development of vaccines against mites, fleas and myiasis-causing flies of veterinary importance. Parasite Immunol 2006; 28: 165-172.
42. Nisbet AJ, Halliday AM, Parker L, et al. Psoroptes ovis: identification of vaccine candidates by immunoscreening. Exp Parasitol 2008; 120: 194-199.
43. Mounsey KE, Willis C, Burgess ST, Holt DC, McCarthy J & Fischer K. Quantitative PCR-based genome size estimation of the astigmatid mites Sarcoptes scabiei, Psoroptes ovis and Dermatophagoides pteronyssinus. Parasit Vectors 2012; 5: 3.
44. Pagel Van Zee J, Geraci NS, Guerrero FD, et al. Tick genomics: the Ixodes genome project and beyond. Int J Parasitol 2007; 37: 1297-1305.
45. Almazan C, Lagunes R, Villar M, et al. Identification and characterization of Rhipicephalus (Boophilus) microplus candidate protective antigens for the control of cattle tick infestations. Parasitol Res 2010; 106: 471-479.
46. Kocan KM, Blouin E & de la Fuente J. RNA interference in ticks. J Vis Exp 2011; 47: e2474.
47. Campbell EM, Burdin M, Hoppler S & Bowman AS. Role of an aquaporin in the sheep tick Ixodes ricinus: assessment as a potential control target. Int J Parasitol 2010; 40: 15-23.
48. Torres L, Almazan C, Ayllon N, et al. Functional genomics of the horn fly, Haematobia irritans (Linnaeus, 1758). BMC Genomics 2011; 12: 105.
49. Dalvin S, Frost P, Biering E, et al. Functional characterisation of the maternal yolk-associated protein (LsYAP) utilising systemic RNA interference in the salmon louse (Lepeophtheirus salmonis) (Crustacea: Copepoda). Int J Parasitol 2009; 39: 1407-1415.
50. Eichner C, Nilsen F, Grotmol S & Dalvin S. A method for stable gene knock-down by RNA interference in larvae of the salmon louse (Lepeophtheirus salmonis). Exp Parasitol 2014; 140: 44-51.
51. Trosse C, Nilsen F & Dalvin S. RNA interference mediated knockdown of the KDEL receptor and COPB2 inhibits digestion and reproduction in the parasitic copepod Lepeophtheirus salmonis. Comp Biochem Physiol B Biochem Mol Biol 2014; 170: 1-9.
52. Campbell EM, Pert CC & Bowman AS. RNA-interference methods for gene-knockdown in the sea louse, Lepeophtheirus salmonis: studies on a putative prostaglandin E synthase. Parasitology 2009; 136: 867-874.
53. Grbic M, Khila A, Lee KZ, et al. Mity model: Tetranychus urticae, a candidate for chelicerate model organism. BioEssays 2007; 29: 489-496.
54. Grbic M, Van Leeuwen T, Clark RM, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 2011; 479: 487-492.
55. Khila A & Grbic M. Gene silencing in the spider mite Tetranychus urticae: dsRNA and siRNA parental silencing of the Distal-less gene. Dev Genes Evol 2007; 217: 241-251.
56. Cerutti H & Casas-Mollano JA. On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 2006; 50: 81-99.
57. Roger AJ & Hug LA. The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation. Philos Trans R Soc Lond B Biol Sci 2006; 361: 1039-1054.
58. Waterhouse PM, Wang MB & Lough T. Gene silencing as an adaptive defence against viruses. Nature 2001; 411: 834-842.
59. Pennisi E. The CRISPR craze. Science 2013; 341: 833-836.
60. Makarova KS, Grishin NV, Shabalina SA, Wolf YI & Koonin EV. A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 2006; 1: 7.
61. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE & Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391: 806-811.
62. de la Fuente J & Kocan KM. Strategies for development of vaccines for control of ixodid tick species. Parasite Immunol 2006; 28: 275-283.
63. Gu L & Knipple DC. Recent advances in RNA interference research in insects: implications for future insect pest management strategies. Crop Prot 2013; 45: 36-40.
64. Zamore PD. RNA interference: listening to the sound of silence. Nat Struct Biol 2001; 8: 746-750.
65. Lee YS, Nakahara K, Pham JW, et al. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 2004; 117: 69-81.
66. Meister G & Tuschl T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004; 431: 343-349.
67. Sontheimer EJ. Assembly and function of RNA silencing complexes. Nat Rev Mol Cell Biol 2005; 6: 127-138.
68. Matranga C, Tomari Y, Shin C, Bartel DP & Zamore PD. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 2005; 123: 607-620.
69. Filipowicz W. RNAi: the nuts and bolts of the RISC machine. Cell 2005; 122: 17-20.
70. Aljamali MN, Bior AD, Sauer JR & Essenberg RC. RNA interference in ticks: a study using histamine binding protein dsRNA in the female tick Amblyomma americanum. Insect Mol Biol 2003; 12: 299-305.
71. Kurscheid S, Lew-Tabor AE, Rodriguez Valle M, et al. Evidence of a tick RNAi pathway by comparative genomics and reverse genetics screen of targets with known loss-of-function phenotypes in Drosophila. BMC Mol Biol 2009; 10: 26.
72. Kavi HH, Fernandez HR, Xie W & Birchler JA. RNA silencing in Drosophila. FEBS Lett 2005; 579: 5940-5949.
73. Hoa NT, Keene KM, Olson KE & Zheng L. Characterization of RNA interference in an Anopheles gambiae cell line. Insect Biochem Mol Biol 2003; 33: 949-957.
74. Nijhof AM, Taoufik A, de la Fuente J, Kocan KM, de Vries E & Jongejan F. Gene silencing of the tick protective antigens, Bm86, Bm91 and subolesin, in the one-host tick Boophilus microplus by RNA interference. Int J Parasitol 2007; 37: 653-662.
75. Ramakrishnan VG, Aljamali MN, Sauer JR & Essenberg RC. Application of RNA interference in tick salivary gland research. J Biomol Tech 2005; 16: 297-305.
76. Garcia S, Billecocq A, Crance JM, Prins M, Garin D & Bouloy M. Viral suppressors of RNA interference impair RNA silencing induced by a Semliki Forest virus replicon in tick cells. J Gen Virol 2006; 87: 1985-1989.
77. Scott JG, Michel K, Bartholomay LC, et al. Towards the elements of successful insect RNAi. J Insect Physiol 2013; 59: 1212-1221.
78. Karim S, Troiano E & Mather TN. Functional genomics tool: gene silencing in Ixodes scapularis eggs and nymphs by electroporated dsRNA. BMC Biotechnol 2010; 10: 1.
79. Gong H, Umemiya R, Zhou J, et al. Blocking the secretion of saliva by silencing the HlYkt6 gene in the tick Haemaphysalis longicornis. Insect Biochem Mol Biol 2009; 39: 372-381.
80. Huvenne H & Smagghe G. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol 2010; 56: 227-235.
81. Barnard AC, Nijhof AM, Fick W, Stutzer C & Maritz-Olivier C. RNAi in arthropods: insight into the machinery and applications for understanding the pathogen-vector interface. Genes (Basel) 2012; 3: 702-741.
82. Jongejan F & Uilenberg G. The global importance of ticks. Parasitology 2004; 129: S3-S14.
83. de la Fuente J, Kocan KM, Almazan C & Blouin EF. RNA interference for the study and genetic manipulation of ticks. Trends Parasitol 2007; 23: 427-433.
84. Torrissen O, Jones S, Asche F, et al. Salmon lice-impact on wild salmonids and salmon aquaculture. J Fish Dis 2013; 36: 171-194.
85. Sigoillot FD, Lyman S, Huckins JF, et al. A bioinformatics method identifies prominent off-targeted transcripts in RNAi screens. Nat Methods 2012; 9: 363-366.
86. Sterck L, Billiau K, Abeel T, Rouze P & Van de Peer Y. ORCAE: online resource for community annotation of eukaryotes. Nat Methods 2012; 9: 1041.
87. Kwon DH, Park JH & Lee SH. Screening of lethal genes for feeding RNAi by leaf disc-mediated systematic delivery of dsRNA in Tetranychus urticae. Pestic Biochem Physiol 2013; 105: 69-75.
88. Winter J, Jung S, Keller S, Gregory RI & Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11: 228-234.
89. Wheeler BM, Heimberg AM, Moy VN, et al. The deep evolution of metazoan microRNAs. Evol Dev 2009; 11: 50-68.
90. Barrero RA, Keeble-Gagnere G, Zhang B, et al. Evolutionary conserved microRNAs are ubiquitously expressed compared to tick-specific miRNAs in the cattle tick Rhipicephalus (Boophilus) microplus. BMC Genomics 2011; 12: 328.
91. Kirkness EF, Haas BJ, Sun W, et al. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA 2010; 107: 12168-12173.
92. Massirer KB, Perez SG, Mondol V & Pasquinelli AE. The miR-35-41 family of microRNAs regulates RNAi sensitivity in Caenorhabditis elegans. PLoS Genet 2012; 8: e1002536.
93. Devaney E, Winter AD & Britton C. microRNAs: a role in drug resistance in parasitic nematodes? Trends Parasitol 2010; 26: 428-433.
94. Lew-Tabor AE, Kurscheid S, Barrero R, et al. Gene expression evidence for off-target effects caused by RNA interference-mediated gene silencing of Ubiquitin-63E in the cattle tick Rhipicephalus microplus. Int J Parasitol 2011; 41: 1001-1014.
95. Kulkarni MM, Booker M, Silver SJ, et al. Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nat Methods 2006; 3: 833-838.
96. Seinen E, Burgerhof JG, Jansen RC & Sibon OC. RNAi experiments in D. melanogaster: solutions to the overlooked problem of off-targets shared by independent dsRNAs. PLoS ONE 2010; 5: e13119.
97. Tzelos T, Matthews JB, Whitelaw B & Knox DP. Marker genes for activation of the RNA interference (RNAi) pathway in the free-living nematode Caenorhabditis elegans and RNAi development in the ovine nematode Teladorsagia circumcincta. J Helminthol 2013; 1-9. [Epub ahead of print].
98. Zhu KY. RNA interference: a powerful tool in entomological research and a novel approach for insect pest management. Insect Sci 2013; 20: 1-3.
99. Sijen T, Fleenor J, Simmer F, et al. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 2001; 107: 465-476.
100. Smardon A, Spoerke JM, Stacey SC, Klein ME, Mackin N & Maine EM. EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Curr Biol 2000; 10: 169-178.
101. Dalmay T, Hamilton A, Rudd S, Angell S & Baulcombe DC. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 2000; 101: 543-553.
102. Tomoyasu Y, Miller SC, Tomita S, Schoppmeier M, Grossmann D & Bucher G. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol 2008; 9: R10.
103. Drinnenberg IA, Weinberg DE, Xie KT, et al. RNAi in budding yeast. Science 2009; 326: 544-550.
104. Lee JM, Kojin Y, Tatsuke T, Mon H, Miyagawa Y & Kusakabe T. Coexpression of Escherichia coli RNase III in silkworm cells improves the efficiency of RNA interference induced by long hairpin dsRNAs. Insect Sci 2013; 20: 69-77.
105. Willadsen P. Anti-tick vaccines. Parasitology 2004; 129: S367-S387.
106. de la Fuente J, Almazan C, Blas-Machado U, et al. The tick protective antigen, 4D8, is a conserved protein involved in modulation of tick blood ingestion and reproduction. Vaccine 2006; 24: 4082-4095.
107. de la Fuente J, Almazan C, Naranjo V, Blouin EF & Kocan KM. Synergistic effect of silencing the expression of tick protective antigens 4D8 and Rs86 in Rhipicephalus sanguineus by RNA interference. Parasitol Res 2006; 99: 108-113.
108. de la Fuente J, Almazan C, Blouin EF, Naranjo V & Kocan KM. RNA interference screening in ticks for identification of protective antigens. Parasitol Res 2005; 96: 137-141.
109. de la Fuente J, Manzano-Roman R, Naranjo V, et al. Identification of protective antigens by RNA interference for control of the lone star tick, Amblyomma americanum. Vaccine 2010; 28: 1786-1795.
110. Nijhof AM, Balk JA, Postigo M, Rhebergen AM, Taoufik A & Jongejan F. Bm86 homologues and novel ATAQ proteins with multiple epidermal growth factor (EGF)-like domains from hard and soft ticks. Int J Parasitol. 2010; 40: 1587-97.
111. Kamath RS & Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 2003; 30: 313-321.
112. Kamath RS, Fraser AG, Dong Y, et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003; 421: 231-237.
113. Yoon KS, Strycharz JP, Baek JH, et al. Brief exposures of human body lice to sublethal amounts of ivermectin over-transcribes detoxification genes involved in tolerance. Insect Mol Biol 2011; 20: 687-699.
114. Narasimhan S, Montgomery RR, DePonte K, et al. Disruption of Ixodes scapularis anticoagulation by using RNA interference. Proc Natl Acad Sci USA 2004; 101: 1141-1146.
115. Soares CA, Lima CM, Dolan MC, Piesman J, Beard CB & Zeidner NS. Capillary feeding of specific dsRNA induces silencing of the isac gene in nymphal Ixodes scapularis ticks. Insect Mol Biol 2005; 14: 443-452.
116. Kocan KM, Manzano-Roman R & de la Fuente J. Transovarial silencing of the subolesin gene in three-host ixodid tick species after injection of replete females with subolesin dsRNA. Parasitol Res 2007; 100: 1411-1415.
117. Mitchell RD 3rd, Ross E, Osgood C, et al. Molecular characterization, tissue-specific expression and RNAi knockdown of the first vitellogenin receptor from a tick. Insect Biochem Mol Biol 2007; 37: 375-388.
118. Kocan KM, de la Fuente J, Manzano-Roman R, Naranjo V, Hynes WL & Sonenshine DE. Silencing expression of the defensin, varisin, in male Dermacentor variabilis by RNA interference results in reduced Anaplasma marginale infections. Exp Appl Acarol 2008; 46: 17-28.
119. Decrem Y, Mariller M, Lahaye K, et al. The impact of gene knock-down and vaccination against salivary metalloproteases on blood feeding and egg laying by Ixodes ricinus. Int J Parasitol 2008; 38: 549-560.
120. Buresova V, Hajdusek O, Franta Z, Sojka D & Kopacek P. IrAM-An alpha2-macroglobulin from the hard tick Ixodes ricinus: characterization and function in phagocytosis of a potential pathogen Chryseobacterium indologenes. Dev Comp Immunol 2009; 33: 489-498.
121. Franta Z, Sojka D, Frantova H, et al. IrCL1 - the haemoglobinolytic cathepsin L of the hard tick, Ixodes ricinus. Int J Parasitol 2011; 41: 1253-1262.
122. Hajdusek O, Sojka D, Kopacek P, et al. Knockdown of proteins involved in iron metabolism limits tick reproduction and development. Proc Natl Acad Sci USA 2009; 106: 1033-1038.
123. Aljamali MN, Sauer JR & Essenberg RC. RNA interference: applicability in tick research. Exp Appl Acarol 2002; 28: 89-96.
124. Karim S, Ramakrishnan VG, Tucker JS, Essenberg RC & Sauer JR. Amblyomma americanum salivary glands: double-stranded RNA-mediated gene silencing of synaptobrevin homologue and inhibition of PGE2 stimulated protein secretion. Insect Biochem Mol Biol 2004; 34: 407-413.
125. Karim S, Ramakrishnan VG, Tucker JS, Essenberg RC & Sauer JR. Amblyomma americanum salivary gland homolog of nSec1 is essential for saliva protein secretion. Biochem Biophys Res Commun 2004; 324: 1256-1263.
126. Miyoshi T, Tsuji N, Islam MK, Kamio T & Fujisaki K. Gene silencing of a cubilin-related serine proteinase from the hard tick Haemaphysalis longicornis by RNA interference. J Vet Med Sci 2004; 66: 1471-1473.
127. Liao M, Zhou J, Hatta T, et al. Molecular characterization of Rhipicephalus (Boophilus) microplus Bm86 homologue from Haemaphysalis longicornis ticks. Vet Parasitol 2007; 146: 148-157.
128. Boldbaatar D, Sikalizyo Sikasunge C, Battsetseg B, Xuan X & Fujisaki K. Molecular cloning and functional characterization of an aspartic protease from the hard tick Haemaphysalis longicornis. Insect Biochem Mol Biol 2006; 36: 25-36.
129. Hill CA & Wikel SK. The Ixodes scapularis genome project: an opportunity for advancing tick research. Trends Parasitol 2005; 21: 151-153.
130. Manzano-Roman R, Diaz-Martin V, Oleaga A, Siles-Lucas M & Perez-Sanchez R. Subolesin/akirin orthologs from Ornithodoros spp. soft ticks: cloning, RNAi gene silencing and protective effect of the recombinant proteins. Vet Parasitol 2012; 185: 248-259.
131. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W & Tirry L. Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: A review. Insect Biochem Molec 2010; 40: 563-572.