Mining a differential sialotranscriptome of Rhipicephalus microplus guides antigen discovery to formulate a vaccine that reduces tick infestations

. 2017 Apr 26 ; 10 (1) : 206. [epub] 20170426

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid28446245
Odkazy

PubMed 28446245
PubMed Central PMC5406933
DOI 10.1186/s13071-017-2136-2
PII: 10.1186/s13071-017-2136-2
Knihovny.cz E-zdroje

BACKGROUND: Ticks cause massive damage to livestock and vaccines are one sustainable substitute for the acaricides currently heavily used to control infestations. To guide antigen discovery for a vaccine that targets the gamut of parasitic strategies mediated by tick saliva and enables immunological memory, we exploited a transcriptome constructed from salivary glands from all stages of Rhipicephalus microplus ticks feeding on genetically tick-resistant and susceptible bovines. RESULTS: Different levels of host anti-tick immunity affected gene expression in tick salivary glands; we thus selected four proteins encoded by genes weakly expressed in ticks attempting to feed on resistant hosts or otherwise abundantly expressed in ticks fed on susceptible hosts; these sialoproteins mediate four functions of parasitism deployed by male ticks and that do not induce antibodies in naturally infected, susceptible bovines. We then evaluated in tick-susceptible heifers an alum-adjuvanted vaccine formulated with recombinant proteins. Parasite performance (i.e. weight and numbers of females finishing their parasitic cycle) and titres of antigen-specific antibodies were significantly reduced or increased, respectively, in vaccinated versus control heifers, conferring an efficacy of 73.2%; two of the antigens were strong immunogens, rich in predicted T-cell epitopes and challenge infestations boosted antibody responses against them. CONCLUSION: Mining sialotranscriptomes guided by the immunity of tick-resistant hosts selected important targets and infestations boosted immune memory against salivary antigens.

Zobrazit více v PubMed

Estrada-Pena A, Bouattour A, Camicas JL, Guglielmone A, Horak I, Jongejan F, et al. The known distribution and ecological preferences of the tick subgenus Boophilus (Acari: Ixodidae) in Africa and Latin America. Exp Appl Acarol. 2006;38:219–35. doi: 10.1007/s10493-006-0003-5. PubMed DOI

Graf JF, Gogolewski R, Leach-Bing N, Sabatini GA, Molento MB, Bordin EL, et al. Tick control: an industry point of view. Parasitology. 2004;129(Suppl):S427–42. doi: 10.1017/S0031182004006079. PubMed DOI

Brossard M, Wikel SK. Immunology of interactions between ticks and hosts. Med Vet Entomol. 1997;11:270–6. doi: 10.1111/j.1365-2915.1997.tb00406.x. PubMed DOI

Willadsen P, Bird P, Cobon GS, Hungerford J. Commercialisation of a recombinant vaccine against Boophilus microplus. Parasitology. 1995;110(Suppl):S43–50. doi: 10.1017/S0031182000001487. PubMed DOI

Rodriguez M, Penichet ML, Mouris AE, Labarta V, Luaces LL, Rubiera R, et al. Control of Boophilus microplus populations in grazing cattle vaccinated with a recombinant Bm86 antigen preparation. Vet Parasitol. 1995;57:339–49. doi: 10.1016/0304-4017(94)00678-6. PubMed DOI

Willadsen P, Riding GA, McKenna RV, Kemp DH, Tellam RL, Nielsen JN, et al. Immunologic control of a parasitic arthropod. Identification of a protective antigen from Boophilus microplus. J. Immunol. 1989;143:1346–51. PubMed

Riding GA, Jarmey J, McKenna RV, Pearson R, Cobon GS, Willadsen P. A protective “concealed” antigen from Boophilus microplus. Purification, localization, and possible function. J. Immunol. 1994;153:5158–66. PubMed

Francischetti IM, Sa-Nunes A, Mans BJ, Santos IM, Ribeiro JM. The role of saliva in tick feeding. Front Biosci. 2009;14:2051–88. doi: 10.2741/3363. PubMed DOI PMC

de la Fuente J, Rodriguez M, Montero C, Redondo M, Garcia-Garcia JC, Mendez L, et al. Vaccination against ticks (Boophilus spp.): the experience with the Bm86-based vaccine Gavac. Genet Anal. 1999;15:143–8. doi: 10.1016/S1050-3862(99)00018-2. PubMed DOI

Garcia-Garcia JC, Gonzalez IL, Gonzalez DM, Valdes M, Mendez L, Lamberti J, et al. Sequence variations in the Boophilus microplus Bm86 locus and implications for immunoprotection in cattle vaccinated with this antigen. Exp Appl Acarol. 1999;23:883–95. doi: 10.1023/A:1006270615158. PubMed DOI

Andreotti R. Performance of two Bm86 antigen vaccin formulation against tick using crossbreed bovines in stall test. Rev Bras Parasitol Vet. 2006;15:97–100. PubMed

Parizi LF, Pohl PC, Masuda A, Vaz IS. New approaches toward anti-Rhipicephalus (Boophilus) microplus tick vaccine. Rev Bras Parasitol Vet. 2009;18:1–7. doi: 10.4322/rbpv.01801001. PubMed DOI

Schetters T, Bishop R, Crampton M, Kopáček P, Lew-Tabor A, Maritz-Olivier C, et al. Cattle tick vaccine researchers join forces in CATVAC. Parasit Vectors. 2016;9:105. doi: 10.1186/s13071-016-1386-8. PubMed DOI PMC

Lew-Tabor AE, Rodriguez VM. A review of reverse vaccinology approaches for the development of vaccines against ticks and tick borne diseases. Ticks Tick Borne Dis. 2016;7:573–85. doi: 10.1016/j.ttbdis.2015.12.012. PubMed DOI

Zinkernagel RM. Immunological memory ≠ protective immunity. Cell Mol Life Sci. 2012;69:1635–40. doi: 10.1007/s00018-012-0972-y. PubMed DOI PMC

Guerrero FD, Miller RJ, Rousseau M-E, Sunkara S, Quackenbush J, Lee Y, et al. BmiGI: a database of cDNAs expressed in Boophilus microplus, the tropical/southern cattle tick. Insect Biochem and Mol Biol. 2005;35:585–95. doi: 10.1016/j.ibmb.2005.01.020. PubMed DOI

Bellgard MI, Moolhuijzen PM, Guerrero FD, Schibeci D, Rodriguez-Valle M, Peterson DG, et al. CattleTickBase: An integrated Internet-based bioinformatics resource for Rhipicephalus (Boophilus) microplus. Int J Parasitol. 2012;42:161–9. doi: 10.1016/j.ijpara.2011.11.006. PubMed DOI

Seifert GW. Variations between and within breeds of cattle in resistance to field infestations of cattle tick (Boophilus microplus) Aust J Agr Res. 1971;22:159–68. doi: 10.1071/AR9710159. DOI

Wambura PN, Gwakisa PS, Silayo RS, Rugaimukamu EA. Breed-associated resistance to tick infestation in Bos indicus and their crosses with Bos taurus. Vet Parasitol. 1998;77:63–70. doi: 10.1016/S0304-4017(97)00229-X. PubMed DOI

Piper EK, Jonsson NN, Gondro C, Lew-Tabor AE, Moolhuijzen P, Vance ME, et al. Immunological profiles of Bos taurus and Bos indicus cattle infested with the cattle tick, Rhipicephalus (Boophilus) microplus. Clin Vaccine Immunol. 2009;16:1074–86. doi: 10.1128/CVI.00157-09. PubMed DOI PMC

Ribeiro JM, Alarcon-Chaidez F, Francischetti IM, Mans BJ, Mather TN, Valenzuela JG, et al. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem Mol Biol. 2006;36:111–29. doi: 10.1016/j.ibmb.2005.11.005. PubMed DOI

Maruyama SR, Anatriello E, Anderson JM, Ribeiro JM, Brandao LG, Valenzuela JG, et al. The expression of genes coding for distinct types of glycine-rich proteins varies according to the biology of three metastriate ticks, Rhipicephalus (Boophilus) microplus, Rhipicephalus sanguineus and Amblyomma cajennense. BMC Genomics. 2010;11:363. doi: 10.1186/1471-2164-11-363. PubMed DOI PMC

Valenzuela JG, Francischetti IM, Pham VM, Garfield MK, Mather TN, Ribeiro JM. Exploring the sialome of the tick Ixodes scapularis. J Exp Biol. 2002;205:2843–64. PubMed

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Huang X, Madan A. CAP3: a DNA sequence assembly program. Genome Res. 1999;9:868–77. doi: 10.1101/gr.9.9.868. PubMed DOI PMC

Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–9. doi: 10.1038/75556. PubMed DOI PMC

Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, Bryant SH. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 2002;30:281–3. doi: 10.1093/nar/30.1.281. PubMed DOI PMC

Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003;4:41. doi: 10.1186/1471-2105-4-41. PubMed DOI PMC

Bateman A, Birney E, Durbin R, Eddy SR, Howe KL, Sonnhammer EL. The Pfam protein families database. Nucleic Acids Res. 2000;28:263–6. doi: 10.1093/nar/28.1.263. PubMed DOI PMC

Letunic I, Goodstadt L, Dickens NJ, Doerks T, Schultz J, Mott R, et al. Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res. 2002;30:242–4. doi: 10.1093/nar/30.1.242. PubMed DOI PMC

LIBEST_014697 BEA cDNA library. https://www.ncbi.nlm.nih.gov/nucest/?term=LIBEST_014697.

Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004;340:783–95. doi: 10.1016/j.jmb.2004.05.028. PubMed DOI

Larsen JEP, Lund O, Nielsen M. Improved method for predicting linear B-cell epitopes. Immunome Res. 2006;2:2. doi: 10.1186/1745-7580-2-2. PubMed DOI PMC

Zhang Q, Wang P, Kim Y, Haste-Andersen P, Beaver J, Bourne PE, et al. Immune epitope database analysis resource (IEDB-AR) Nucleic Acids Res. 2008;36:W513–8. doi: 10.1093/nar/gkn254. PubMed DOI PMC

Lew-Tabor AE, Valle MR, Moolhuijzen PM, Bruyeres A, Belgard M. Screening of anti-peptide antibodies in vitro to identify potential cattle tick vaccine antigens. Medimond International Proceedings. Melbourne, Australia; 2010. p. 97–102.

Bian H, Hammer J. Discovery of promiscuous HLA-II-restricted T cell epitopes with TEPITOPE. Methods. 2004;34:468–75. doi: 10.1016/j.ymeth.2004.06.002. PubMed DOI

Nielsen M, Lund O. NN-align. An artificial neural network-based alignment algorithm for MHC class II peptide binding prediction. BMC Bioinformatics. 2009;10:296. doi: 10.1186/1471-2105-10-296. PubMed DOI PMC

Nielsen M, Lundegaard C, Lund O. Prediction of MHC class II binding affinity using SMM-align, a novel stabilization matrix alignment method. BMC Bioinformatics. 2007;8:238. doi: 10.1186/1471-2105-8-238. PubMed DOI PMC

Bird PI, Pak SC, Worrall DM, Bottomley SP. Production of recombinant serpins in Escherichia coli. Methods. 2004;32:169–76. doi: 10.1016/S1046-2023(03)00208-1. PubMed DOI

Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Meth. 2012;9:671–5. doi: 10.1038/nmeth.2089. PubMed DOI PMC

Canales M, Almazan C, Naranjo V, Jongejan F, de la Fuente J. Vaccination with recombinant Boophilus annulatus Bm86 ortholog protein, Ba86, protects cattle against B. annulatus and B. microplus infestations. BMC Biotechnol. 2009;9:29. PubMed PMC

Hajdusek O, Almazan C, Loosova G, Villar M, Canales M, Grubhoffer L, et al. Characterization of ferritin 2 for the control of tick infestations. Vaccine. 2010;28:2993–8. doi: 10.1016/j.vaccine.2010.02.008. PubMed DOI

Carvalho WA, Maruyama SR, Franzin AM, Abatepaulo AR, Anderson JM, Ferreira BR, et al. Rhipicephalus (Boophilus) microplus: clotting time in tick-infested skin varies according to local inflammation and gene expression patterns in tick salivary glands. Exp Parasitol. 2010;124:428–35. doi: 10.1016/j.exppara.2009.12.013. PubMed DOI PMC

Ribeiro JM. How ticks make a living. Parasitol Today. 1995;11:91–3. doi: 10.1016/0169-4758(95)80162-6. PubMed DOI

Anatriello E, Ribeiro JM, de Miranda-Santos IK, Brandao LG, Anderson JM, Valenzuela JG, et al. An insight into the sialotranscriptome of the brown dog tick, Rhipicephalus sanguineus. BMC Genomics. 2010;11:450. doi: 10.1186/1471-2164-11-450. PubMed DOI PMC

Wang M, Guerrero FD, Pertea G, Nene VM. Global comparative analysis of ESTs from the southern cattle tick, Rhipicephalus (Boophilus) microplus. BMC Genomics. 2007;8:368. doi: 10.1186/1471-2164-8-368. PubMed DOI PMC

Parker JM, Guo D, Hodges RS. New hydrophilicity scale derived from high-performance liquid chromatography peptide retention data: correlation of predicted surface residues with antigenicity and X-ray-derived accessible sites. Biochemistry. 1986;25:5425–32. doi: 10.1021/bi00367a013. PubMed DOI

Husband AJ, Brandon MR, Lascelles AK. Absorption and endogenous production of immunoglobulins in calves. Aust J Exp Biol Med Sci. 1972;50:491–8. doi: 10.1038/icb.1972.41. PubMed DOI

Ribeiro JM. Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect Agents Dis. 1995;4:143–52. PubMed

Carvalho WA, Bechara GH, More DD, Ferreira BR, da Silva JS, de Miranda Santos IK. Rhipicephalus (Boophilus) microplus: distinct acute phase proteins vary during infestations according to the genetic composition of the bovine hosts, Bos taurus and Bos indicus. Exp Parasitol. 2008;118:587–91. doi: 10.1016/j.exppara.2007.10.006. PubMed DOI

Arredouani M, Matthys P, Kasran A, Baumann H, Ceuppen JL. Haptoglobin and the Th1/Th2 balance: hints from in vitro and in vivo studies. Redox Rep. 2001;6:369–71. doi: 10.1179/135100001101536481. PubMed DOI

Oh SK, Ross S, Walker J, Zeisel S. Role of a SER immune suppressor in immune surveillance. Immunology. 1988;64:73–9. PubMed PMC

Trager W. Acquired immunity to ticks. J Parasitol. 1939;25:57–81. doi: 10.2307/3272160. DOI

Ribeiro JM. Role of saliva in tick/host interactions. Exp Appl Acarol. 1989;7:15–20. doi: 10.1007/BF01200449. PubMed DOI

Brown SJ, Shapiro SZ, Askenase PW. Characterization of tick antigens inducing host immune resistance. I. Immunization of guinea pigs with Amblyomma americanum-derived salivary gland extracts and identification of an important salivary gland protein antigen with guinea pig anti-tick antibodies. J Immunol. 1984;133:3319–25. PubMed

Shapiro SZ, Buscher G, Dobbelaere DA. Acquired resistance to Rhipicephalus appendiculatus (Acari: Ixodidae): identification of an antigen eliciting resistance in rabbits. J Med Entomol. 1987;24:147–54. doi: 10.1093/jmedent/24.2.147. PubMed DOI

Richards SA, Stutzer C, Bosman A-M, Maritz-Olivier C. Transmembrane proteins - mining the cattle tick transcriptome. Ticks Tick Borne Dis. 2015;6:695–710. doi: 10.1016/j.ttbdis.2015.06.002. PubMed DOI

Rodriguez-Valle M, Lew-Tabor A, Gondro C, Moolhuijzen P, Vance M, Guerrero FD, et al. Comparative microarray analysis of Rhipicephalus (Boophilus) microplus expression profiles of larvae pre-attachment and feeding adult female stages on Bos indicus and Bos taurus cattle. BMC Genomics. 2010;11:437. doi: 10.1186/1471-2164-11-437. PubMed DOI PMC

Gaze S, Driguez P, Pearson MS, Mendes T, Doolan DL, Trieu A, et al. An immunomics approach to schistosome antigen discovery: antibody signatures of naturally resistant and chronically infected individuals from endemic areas. PLoS Pathog. 2014;10 doi: 10.1371/journal.ppat.1004033. PubMed DOI PMC

Almazan C, Kocan KM, Blouin EF, de la Fuente J. Vaccination with recombinant tick antigens for the control of Ixodes scapularis adult infestations. Vaccine. 2005;23:5294–8. doi: 10.1016/j.vaccine.2005.08.004. PubMed DOI

Schuijt TJ, Narasimhan S, Daffre S, DePonte K, Hovius JW, Van’t Veer C, et al. Identification and characterization of Ixodes scapularis antigens that elicit tick immunity using yeast surface display. PLoS One. 2011;6 doi: 10.1371/journal.pone.0015926. PubMed DOI PMC

Almazan C, Lagunes R, Villar M, Canales M, Rosario-Cruz R, Jongejan F, et al. Identification and characterization of Rhipicephalus (Boophilus) microplus candidate protective antigens for the control of cattle tick infestations. Parasitol Res. 2010;106:471–9. doi: 10.1007/s00436-009-1689-1. PubMed DOI PMC

Prudencio CR, Marra AO, Cardoso R, Goulart LR. Recombinant peptides as new immunogens for the control of the bovine tick, Rhipicephalus (Boophilus) microplus. Vet Parasitol. 2010;172:122–31. doi: 10.1016/j.vetpar.2010.04.012. PubMed DOI

Seixas A, Oliveira P, Termignoni C, Logullo C, Masuda A, da Silva Vaz I., Jr Rhipicephalus (Boophilus) microplus embryo proteins as target for tick vaccine. Vet Immunol Immunopathol. 2012;148:149–56. doi: 10.1016/j.vetimm.2011.05.011. PubMed DOI

Hope M, Jiang X, Gough J, Cadogan L, Josh P, Jonsson N, et al. Experimental vaccination of sheep and cattle against tick infestation using recombinant 5’-nucleotidase. Parasite Immunol. 2010;32:135–42. doi: 10.1111/j.1365-3024.2009.01168.x. PubMed DOI PMC

Garcia-Garcia JC, Montero C, Redondo M, Vargas M, Canales M, Boue O, et al. Control of ticks resistant to immunization with Bm86 in cattle vaccinated with the recombinant antigen Bm95 isolated from the cattle tick, Boophilus microplus. Vaccine. 2000;18:2275–87. doi: 10.1016/S0264-410X(99)00548-4. PubMed DOI

Kumar A, Garg R, Yadav CL, Vatsya S, Kumar RR, Sugumar P, et al. Immune responses against recombinant tick antigen, Bm95, for the control of Rhipicephalus (Boophilus) microplus ticks in cattle. Vet Parasitol. 2009;165:119–24. doi: 10.1016/j.vetpar.2009.06.030. PubMed DOI

Nuttall PA, Trimnell AR, Kazimirova M, Labuda M. Exposed and concealed antigens as vaccine targets for controlling ticks and tick-borne diseases. Parasite Immunol. 2006;28:155–63. doi: 10.1111/j.1365-3024.2006.00806.x. PubMed DOI

Dai J, Narasimhan S, Zhang L, Liu L, Wang P, Fikrig E. Tick histamine release factor is critical for Ixodes scapularis engorgement and transmission of the lyme disease agent. PLoS Pathog. 2010;6:e1001205. doi: 10.1371/journal.ppat.1001205. PubMed DOI PMC

Ali A, Parizi LF, Guizzo MG, Tirloni L, Seixas A, Vaz I da S, et al. Immunoprotective potential of a Rhipicephalus (Boophilus) microplus metalloprotease. Vet Parasitol. 2015;207:107–14. PubMed

Guerrero FD, Andreotti R, Bendele KG, Cunha RC, Miller RJ, Yeater K, et al. Rhipicephalus (Boophilus) microplus aquaporin as an effective vaccine antigen to protect against cattle tick infestations. Parasit Vectors. 2014;7:475. PubMed PMC

Rodríguez-Mallon A, Encinosa PE, Méndez-Pérez L, Bello Y, Rodríguez Fernández R, Garay H, et al. High efficacy of a 20 amino acid peptide of the acidic ribosomal protein P0 against the cattle tick, Rhipicephalus microplus. Ticks Tick Borne Dis. 2015;6:530–7. doi: 10.1016/j.ttbdis.2015.04.007. PubMed DOI

Igawa T, Tsunoda H, Tachibana T, Maeda A, Mimoto F, Moriyama C, et al. Reduced elimination of IgG antibodies by engineering the variable region. Protein Eng Des Sel. 2010;23:385–92. doi: 10.1093/protein/gzq009. PubMed DOI

Coloma MJ, Trinh RK, Martinez AR, Morrison SL. Position effects of variable region carbohydrate on the affinity and in vivo behavior of an anti-(1- > 6) dextran antibody. J Immunol. 1999;162:2162–70. PubMed

Ishino T, Wang M, Mosyak L, Tam A, Duan W, Svenson K, et al. Engineering a monomeric Fc domain modality by N-glycosylation for the half-life extension of biotherapeutics. J Biol Chem. 2013;288:16529–37. doi: 10.1074/jbc.M113.457689. PubMed DOI PMC

Schroeder H, Skelly PJ, Zipfel PF, Losson B, Vanderplasschen A. Subversion of complement by hematophagous parasites. Dev Comp Immunol. 2009;33:5–13. doi: 10.1016/j.dci.2008.07.010. PubMed DOI PMC

Vordermeier M, Whelan AO, Hewinson RG. Recognition of mycobacterial epitopes by T cells across mammalian species and use of a program that predicts human HLA-DR binding peptides to predict bovine epitopes. Infect Immun. 2003;71:1980–7. doi: 10.1128/IAI.71.4.1980-1987.2003. PubMed DOI PMC

Jones GJ, Bagaini F, Hewinson RG, Vordermeier HM. The use of binding-prediction models to identify M. bovis-specific antigenic peptides for screening assays in bovine tuberculosis. Vet Immunol Immunopathol. 2011;141:239–45. doi: 10.1016/j.vetimm.2011.03.006. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...