Sialome diversity of ticks revealed by RNAseq of single tick salivary glands
Language English Country United States Media electronic-ecollection
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
Z01 AI000810
Intramural NIH HHS - United States
PubMed
29652888
PubMed Central
PMC5919021
DOI
10.1371/journal.pntd.0006410
PII: PNTD-D-17-02057
Knihovny.cz E-resources
- MeSH
- Ixodes genetics metabolism MeSH
- Rabbits MeSH
- Humans MeSH
- Sequence Analysis, RNA MeSH
- Salivary Glands metabolism MeSH
- Saliva metabolism MeSH
- Gene Expression Profiling MeSH
- Transcriptome * MeSH
- Computational Biology MeSH
- High-Throughput Nucleotide Sequencing methods MeSH
- Animals MeSH
- Check Tag
- Rabbits MeSH
- Humans MeSH
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
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.
See more in PubMed
Gregson JD. Observations on the movement of fluids in the vicinity of the mouthparts of naturally feeding
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 PubMed DOI PMC
Karim S, Ribeiro JM. An Insight into the sialome of the Lone Star tick, PubMed DOI PMC
Schwarz A, von Reumont BM, Erhart J, Chagas AC, Ribeiro JM, Kotsyfakis M. De novo 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 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 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, 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 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 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 PubMed DOI
Ribeiro JM. PubMed
Valenzuela JG, Charlab R, Mather TN, Ribeiro JM. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, PubMed DOI
Daix V, Schroeder H, Praet N, Georgin JP, Chiappino I, Gillet L, et al. 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 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 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 ( PubMed DOI
Kurtenbach K, De Michelis S, Etti S, Schafer SM, Sewell HS, Brade V, et al. Host association of 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, PubMed DOI
de Castro MH, de Klerk D, Pienaar R, Rees DJG, Mans BJ. Sialotranscriptomics of PubMed DOI PMC
Schneider BS, Karim S, Ribeiro JMC. An Insight into the Sialome of the Lone Star Tick, PubMed DOI PMC
Insight Into the Dynamics of the Ixodes ricinus Nymphal Midgut Proteome
Lyme disease transmission by severely impaired ticks
Tick Immune System: What Is Known, the Interconnections, the Gaps, and the Challenges
The Central Role of Salivary Metalloproteases in Host Acquired Resistance to Tick Feeding
Novel targets and strategies to combat borreliosis