Sialome diversity of ticks revealed by RNAseq of single tick salivary glands

. 2018 Apr ; 12 (4) : e0006410. [epub] 20180413

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29652888

Grantová podpora
Z01 AI000810 Intramural NIH HHS - United States

Ticks salivate while feeding on their hosts. Saliva helps blood feeding through host anti-hemostatic and immunomodulatory components. Previous transcriptomic and proteomic studies revealed the complexity of tick saliva, comprising hundreds of polypeptides grouped in several multi-genic families such as lipocalins, Kunitz-domain containing peptides, metalloproteases, basic tail secreted proteins, and several other families uniquely found in ticks. These studies also revealed that the composition of saliva changes with time; expression of transcripts from the same family wax and wane as a function of feeding time. Here, we examined whether host immune factors could influence sialome switching by comparing sialomes of ticks fed naturally on a rabbit, to ticks artificially fed on defibrinated blood depleted of immune components. Previous studies were based on transcriptomes derived from pools of several individuals. To get an insight into the uniqueness of tick sialomes, we performed transcriptomic analyses of single salivary glands dissected from individual adult female I. ricinus ticks. Multivariate analysis identified 1,279 contigs differentially expressed as a function of time and/or feeding mode. Cluster analysis of these contigs revealed nine clusters of differentially expressed genes, four of which appeared consistently across several replicates, but five clusters were idiosyncratic, pointing to the uniqueness of sialomes in individual ticks. The disclosure of tick quantum sialomes reveals the unique salivary composition produced by individual ticks as they switch their sialomes throughout the blood meal, a possible mechanism of immune evasion.

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Gregson JD. Observations on the movement of fluids in the vicinity of the mouthparts of naturally feeding Dermacentor andersoni Stiles. Parasitol. 1967;57:1–8.

Francischetti IMB, Sá-Nunes A, Mans BJ, Santos IM, Ribeiro JMC. The role of saliva in tick feeding. Frontiers in Biosciences. 2009;14:2051–88. PubMed PMC

Andersen JF, Ribeiro JMC. Salivary Kratagonists: Scavengers of Host Physiological Effectors During Blood Feeding In: Wikel S, Aksoy S, Dimopoulos G, editors. Arthropod Vector: Controller of Disease Transmission, Volume 2 2. London,: Elsevier/Academic Press; 2017. p. 51–63.

Trager W. Acquired immunity to ticks. J Parasitol. 1939;25:57–81.

Kotsyfakis M, Schwarz A, Erhart J, Ribeiro JM. Tissue- and time-dependent transcription in Ixodes ricinus salivary glands and midguts when blood feeding on the vertebrate host. Sci Rep. 2015;5:9103 Epub 2015/03/15. doi: 10.1038/srep09103 ; PubMed Central PMCID: PMC4357865. PubMed DOI PMC

Karim S, Ribeiro JM. An Insight into the sialome of the Lone Star tick, Amblyomma americanum, with a glimpse on its time dependent gene expression. PLoS One. 2015;10(7):e0131292 doi: 10.1371/journal.pone.0131292 ; PubMed Central PMCID: PMC4489193. PubMed DOI PMC

Schwarz A, von Reumont BM, Erhart J, Chagas AC, Ribeiro JM, Kotsyfakis M. De novo Ixodes ricinus salivary gland transcriptome analysis using two next-generation sequencing methodologies. Faseb J. 2013;27(12):4745–56. Epub 2013/08/22. doi: 10.1096/fj.13-232140 ; PubMed Central PMCID: PMC3834774. PubMed DOI PMC

Schwarz A, Tenzer S, Hackenberg M, Erhart J, Gerhold-Ay A, Mazur J, et al. A systems level analysis reveals transcriptomic and proteomic complexity in Ixodes ricinus midgut and salivary glands during early attachment and feeding. Mol Cell Proteomics. 2014;13(10):2725–35. Epub 2014/07/23. doi: 10.1074/mcp.M114.039289 ; PubMed Central PMCID: PMC4188998. PubMed DOI PMC

Berends ET, Mohan S, Miellet WR, Ruyken M, Rooijakkers SH. Contribution of the complement Membrane Attack Complex to the bactericidal activity of human serum. Mol Immunol. 2015;65(2):328–35. Epub 2015/03/01. doi: 10.1016/j.molimm.2015.01.020 . PubMed DOI

Perner J, Sobotka R, Šíma R, Konvičková J, Sojka D, Oliveira PLd, et al. Acquisition of exogenous haem is essential for tick reproduction. eLife. 2016;5 doi: 10.7554/eLife.12318 PubMed DOI PMC

Krober T, Guerin PM. In vitro feeding assays for hard ticks. Trends Parasitol. 2007; 23(9):445–9. Epub 2007/08/08. doi: 10.1016/j.pt.2007.07.010 . PubMed DOI

Perner J, Provazník J, Schrenková J, Urbanová V, Ribeiro JMC, Kopáček P. RNA-seq analyses of the midgut from blood- and serum-fed Ixodes ricinus ticks. Scientific Reports. 2016;6:36695 doi: 10.1038/srep36695 PubMed DOI PMC

Birol I, Jackman SD, Nielsen CB, Qian JQ, Varhol R, Stazyk G, et al. De novo transcriptome assembly with ABySS. Bioinformatics. 2009;25(21):2872–7. Epub 2009/06/17. doi: 10.1093/bioinformatics/btp367 . PubMed DOI

Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I. ABySS: a parallel assembler for short read sequence data. Genome Res. 2009;19(6):1117–23. Epub 2009/03/03. doi: 10.1101/gr.089532.108 ; PubMed Central PMCID: PMC2694472. PubMed DOI PMC

Miller JR, Koren S, Sutton G. Assembly algorithms for next-generation sequencing data. Genomics. 2010;95(6):315–27. Epub 2010/03/10. doi: 10.1016/j.ygeno.2010.03.001 ; PubMed Central PMCID: PMC2874646. PubMed DOI PMC

Liu Y, Schmidt B, Maskell DL. Parallelized short read assembly of large genomes using de Bruijn graphs. BMC Bioinformatics. 2011;12:354 Epub 2011/08/27. doi: 10.1186/1471-2105-12-354 ; PubMed Central PMCID: PMC3167803. PubMed DOI PMC

Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience. 2012;1(1):18 doi: 10.1186/2047-217X-1-18 ; PubMed Central PMCID: PMC3626529. PubMed DOI PMC

Huang X, Madan A. CAP3: A DNA sequence assembly program. Genome Res. 1999;9(9):868–77. . PubMed PMC

Karim S, Singh P, Ribeiro JM. A deep insight into the sialotranscriptome of the gulf coast tick, Amblyomma maculatum. PLoS One. 2011;6(12):e28525 Epub 2012/01/05. doi: 10.1371/journal.pone.0028525 ; PubMed Central PMCID: PMC3244413. PubMed DOI PMC

Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402. PubMed PMC

Nielsen H, Brunak S, von Heijne G. Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng. 1999;12(1):3–9. . PubMed

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. Epub 2009/11/17. doi: 10.1093/bioinformatics/btp616 ; PubMed Central PMCID: PMC2796818. PubMed DOI PMC

Howe EA, Sinha R, Schlauch D, Quackenbush J. RNA-Seq analysis in MeV. Bioinformatics. 2011;27(22):3209–10. Epub 2011/10/07. doi: 10.1093/bioinformatics/btr490 ; PubMed Central PMCID: PMC3208390. PubMed DOI PMC

Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A. 1998;95(25):14863–8. ; PubMed Central PMCID: PMC24541. PubMed PMC

Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, et al. gplots: Various R programming tools for plotting data. R package version 2141. 2015;2(14).

Shamir R, Maron-Katz A, Tanay A, Linhart C, Steinfeld I, Sharan R, et al. EXPANDER—an integrative program suite for microarray data analysis. BMC Bioinformatics. 2005;6:232 Epub 2005/09/24. doi: 10.1186/1471-2105-6-232 ; PubMed Central PMCID: PMC1261157. PubMed DOI PMC

Ribeiro JM, Topalis P, Louis C. AnoXcel: an Anopheles gambiae protein database. Insect Mol Biol. 2004;13(5):449–57. doi: 10.1111/j.0962-1075.2004.00503.x . PubMed DOI

Sharan R, Maron-Katz A, Shamir R. CLICK and EXPANDER: a system for clustering and visualizing gene expression data. Bioinformatics. 2003;19(14):1787–99. Epub 2003/09/27. . PubMed

Cox JS, Walter P. A Novel Mechanism for Regulating Activity of a Transcription Factor That Controls the Unfolded Protein Response. Cell. 1996;87(3):391–404. doi: 10.1016/s0092-8674(00)81360-4 PubMed DOI

Souid S, Lepesant J-A, Yanicostas C. The xbp-1 gene is essential for development in Drosophila. Development Genes and Evolution. 2007;217(2):159–67. doi: 10.1007/s00427-006-0124-1 PubMed DOI

Francischetti IM, Mather TN, Ribeiro JM. Tick saliva is a potent inhibitor of endothelial cell proliferation and angiogenesis. Thromb Haemost. 2005;94(1):167–74. doi: 10.1267/THRO05010167 ; PubMed Central PMCID: PMC2893037. 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(2):111–29. doi: 10.1016/j.ibmb.2005.11.005 . PubMed DOI

Ribeiro JM. Ixodes dammini: salivary anti-complement activity. Exp Parasitol. 1987;64(3):347–53. . PubMed

Valenzuela JG, Charlab R, Mather TN, Ribeiro JM. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. J Biol Chem. 2000;275(25):18717–23. doi: 10.1074/jbc.M001486200 . PubMed DOI

Daix V, Schroeder H, Praet N, Georgin JP, Chiappino I, Gillet L, et al. Ixodes ticks belonging to the Ixodes ricinus complex encode a family of anticomplement proteins. Insect Mol Biol. 2007;16(2):155–66. doi: 10.1111/j.1365-2583.2006.00710.x . PubMed DOI

Couvreur B, Beaufays J, Charon C, Lahaye K, Gensale F, Denis V, et al. Variability and action mechanism of a family of anticomplement proteins in Ixodes ricinus. PLoS One. 2008;3(1):e1400 doi: 10.1371/journal.pone.0001400 ; PubMed Central PMCID: PMC2151134. PubMed DOI PMC

Chmelar J, Kotal J, Kopecky J, Pedra JH, Kotsyfakis M. All For One and One For All on the Tick-Host Battlefield. Trends Parasitol. 2016;32(5):368–77. doi: 10.1016/j.pt.2016.01.004 ; PubMed Central PMCID: PMC4851932. PubMed DOI PMC

de Taeye SW, Kreuk L, van Dam AP, Hovius JW, Schuijt TJ. Complement evasion by Borrelia burgdorferi: it takes three to tango. Trends Parasitol. 2013;29(3):119–28. doi: 10.1016/j.pt.2012.12.001 . PubMed DOI

Kuo MM, Lane RS, Giclas PC. A comparative study of mammalian and reptilian alternative pathway of complement-mediated killing of the Lyme disease spirochete (Borrelia burgdorferi). J Parasitol. 2000;86(6):1223–8. doi: 10.1645/0022-3395(2000)086[1223:ACSOMA]2.0.CO;2 . PubMed DOI

Kurtenbach K, De Michelis S, Etti S, Schafer SM, Sewell HS, Brade V, et al. Host association of Borrelia burgdorferi sensu lato—the key role of host complement. Trends Microbiol. 2002;10(2):74–9. . PubMed

Bowman AS, Sauer JR. Tick salivary glands: function, physiology and future. Parasitology. 2005;129(07):S67 doi: 10.1017/s0031182004006468 PubMed DOI

Binnington KC. Sequential changes in salivary gland structure during attachment and feeding of the cattle tick, Boophilus microplus. Int J Parasitol. 1978;8(2):97–115. doi: 10.1016/0020-7519(78)90004-8 PubMed DOI

de Castro MH, de Klerk D, Pienaar R, Rees DJG, Mans BJ. Sialotranscriptomics of Rhipicephalus zambeziensis reveals intricate expression profiles of secretory proteins and suggests tight temporal transcriptional regulation during blood-feeding. Parasites & Vectors. 2017;10(1). doi: 10.1186/s13071-017-2312-4 PubMed DOI PMC

Schneider BS, Karim S, Ribeiro JMC. An Insight into the Sialome of the Lone Star Tick, Amblyomma americanum, with a Glimpse on Its Time Dependent Gene Expression. PLoS One. 2015;10(7):e0131292 doi: 10.1371/journal.pone.0131292 PubMed DOI PMC

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