Deep Sequencing Analysis of the Ixodes ricinus Haemocytome
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, Research Support, N.I.H., Intramural, práce podpořená grantem
Grantová podpora
R01 AI093653
NIAID NIH HHS - United States
Intramural NIH HHS - United States
PubMed
25970599
PubMed Central
PMC4430169
DOI
10.1371/journal.pntd.0003754
PII: PNTD-D-15-00305
Knihovny.cz E-zdroje
- MeSH
- arachnida jako vektory genetika mikrobiologie MeSH
- genová knihovna MeSH
- hemocyty cytologie MeSH
- klíště genetika imunologie mikrobiologie MeSH
- klíšťová encefalitida mikrobiologie MeSH
- lymeská nemoc mikrobiologie MeSH
- molekulární sekvence - údaje MeSH
- proteiny členovců genetika MeSH
- sekvence nukleotidů MeSH
- sekvenční analýza DNA MeSH
- slinné žlázy cytologie MeSH
- stanovení celkové genové exprese MeSH
- transkriptom genetika MeSH
- vysoce účinné nukleotidové sekvenování MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Research Support, N.I.H., Intramural MeSH
- Geografické názvy
- Evropa MeSH
- Názvy látek
- proteiny členovců MeSH
BACKGROUND: Ixodes ricinus is the main tick vector of the microbes that cause Lyme disease and tick-borne encephalitis in Europe. Pathogens transmitted by ticks have to overcome innate immunity barriers present in tick tissues, including midgut, salivary glands epithelia and the hemocoel. Molecularly, invertebrate immunity is initiated when pathogen recognition molecules trigger serum or cellular signalling cascades leading to the production of antimicrobials, pathogen opsonization and phagocytosis. We presently aimed at identifying hemocyte transcripts from semi-engorged female I. ricinus ticks by mass sequencing a hemocyte cDNA library and annotating immune-related transcripts based on their hemocyte abundance as well as their ubiquitous distribution. METHODOLOGY/PRINCIPAL FINDINGS: De novo assembly of 926,596 pyrosequence reads plus 49,328,982 Illumina reads (148 nt length) from a hemocyte library, together with over 189 million Illumina reads from salivary gland and midgut libraries, generated 15,716 extracted coding sequences (CDS); these are displayed in an annotated hyperlinked spreadsheet format. Read mapping allowed the identification and annotation of tissue-enriched transcripts. A total of 327 transcripts were found significantly over expressed in the hemocyte libraries, including those coding for scavenger receptors, antimicrobial peptides, pathogen recognition proteins, proteases and protease inhibitors. Vitellogenin and lipid metabolism transcription enrichment suggests fat body components. We additionally annotated ubiquitously distributed transcripts associated with immune function, including immune-associated signal transduction proteins and transcription factors, including the STAT transcription factor. CONCLUSIONS/SIGNIFICANCE: This is the first systems biology approach to describe the genes expressed in the haemocytes of this neglected disease vector. A total of 2,860 coding sequences were deposited to GenBank, increasing to 27,547 the number so far deposited by our previous transcriptome studies that serves as a discovery platform for studies with I. ricinus biochemistry and physiology.
Zobrazit více v PubMed
de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE. Overview: Ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci. 2008;13:6938–46. PubMed
Kopacek P, Hajdusek O, Buresova V, Daffre S. Tick innate immunity. Adv Exp Med Biol. 2010;708:137–62. PubMed
Hajdusek O, Sima R, Ayllon N, Jalovecka M, Perner J, de la Fuente J, et al. Interaction of the tick immune system with transmitted pathogens. Front Cell Infect Microbiol. 2013;3:26 10.3389/fcimb.2013.00026 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(Pt 18):2843–64. PubMed
Santos IK, Valenzuela JG, Ribeiro JM, de Castro M, Costa JN, Costa AM, et al. Gene discovery in Boophilus microplus, the cattle tick: the transcriptomes of ovaries, salivary glands, and hemocytes. Ann N Y Acad Sci. 2004;1026:242–6. PubMed
Francischetti IM, My Pham V, Mans BJ, Andersen JF, Mather TN, Lane RS, et al. The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochem Mol Biol. 2005;35(10):1142–61. PubMed PMC
Mans BJ, Andersen JF, Schwan TG, Ribeiro JM. Characterization of anti-hemostatic factors in the argasid, Argas monolakensis: Implications for the evolution of blood-feeding in the soft tick family. Insect Biochem Mol Biol. 2008;38(1):22–41. PubMed PMC
Francischetti IM, Mans BJ, Meng Z, Gudderra N, Veenstra TD, Pham VM, et al. An insight into the sialome of the soft tick, Ornithodorus parkeri . Insect Biochem Mol Biol. 2008;38(1):1–21. PubMed PMC
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 10.1186/1471-2164-11-450 PubMed DOI PMC
Chmelar J, Oliveira CJ, Rezacova P, Francischetti IM, Kovarova Z, Pejler G, et al. A tick salivary protein targets cathepsin G and chymase and inhibits host inflammation and platelet aggregation. Blood. 2011;117(2):736–44. 10.1182/blood-2010-06-293241 PubMed DOI PMC
Ribeiro JM, Anderson JM, Manoukis NC, Meng Z, Francischetti IM. A further insight into the sialome of the tropical bont tick, Amblyomma variegatum . BMC Genomics. 2011;12:136 10.1186/1471-2164-12-136 PubMed DOI PMC
Francischetti IM, Anderson JM, Manoukis N, Pham VM, Ribeiro JM. An insight into the sialotranscriptome and proteome of the coarse bontlegged tick, Hyalomma marginatum rufipes . J Proteomics. 2011;74(12):2892–908. 10.1016/j.jprot.2011.07.015 PubMed DOI 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 10.1371/journal.pone.0028525 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 Cel Proteomics. 2014;In Press. PubMed 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. 10.1096/fj.13-232140 PubMed DOI PMC
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 10.1038/srep09103 PubMed DOI PMC
Liu XY, de la Fuente J, Cote M, Galindo RC, Moutailler S, Vayssier-Taussat M, et al. IrSPI, a tick serine protease inhibitor involved in tick feeding and Bartonella henselae infection. PLoS Negl Trop Dis. 2014;8(7):e2993 10.1371/journal.pntd.0002993 PubMed DOI PMC
Anderson JM, Sonenshine DE, Valenzuela JG. Exploring the mialome of ticks: an annotated catalogue of midgut transcripts from the hard tick, Dermacentor variabilis (Acari: Ixodidae). BMC Genomics. 2008;9:552 10.1186/1471-2164-9-552 PubMed DOI PMC
Jaworski DC, Zou Z, Bowen CJ, Wasala NB, Madden R, Wang Y, et al. Pyrosequencing and characterization of immune response genes from the American dog tick, Dermacentor variabilis (L.). Insect Mol Biol. 2010;19(5):617–30. 10.1111/j.1365-2583.2010.01037.x PubMed DOI PMC
Heekin AM, Guerrero FD, Bendele KG, Saldivar L, Scoles GA, Dowd SE, et al. The ovarian transcriptome of the cattle tick, Rhipicephalus (Boophilus) microplus, feeding upon a bovine host infected with Babesia bovis . Parasit Vectors. 2013;6:276 10.1186/1756-3305-6-276 PubMed DOI PMC
Heekin AM, Guerrero FD, Bendele KG, Saldivar L, Scoles GA, Dowd SE, et al. Gut transcriptome of replete adult female cattle ticks, Rhipicephalus (Boophilus) microplus, feeding upon a Babesia bovis-infected bovine host. Parasitol Res. 2013;112(9):3075–90. 10.1007/s00436-013-3482-4 PubMed DOI
Heekin AM, Guerrero FD, Bendele KG, Saldivar L, Scoles GA, Gondro C, et al. Analysis of Babesia bovis infection-induced gene expression changes in larvae from the cattle tick, Rhipicephalus (Boophilus) microplus . Parasit Vectors. 2012;5:162 10.1186/1756-3305-5-162 PubMed DOI PMC
Esteves E, Lara FA, Lorenzini DM, Costa GH, Fukuzawa AH, Pressinotti LN, et al. Cellular and molecular characterization of an embryonic cell line (BME26) from the tick Rhipicephalus (Boophilus) microplus . Insect Biochem Mol Biol. 2008;38(5):568–80. 10.1016/j.ibmb.2008.01.006 PubMed DOI PMC
Sojka D, Franta Z, Horn M, Caffrey CR, Mares M, Kopacek P. New insights into the machinery of blood digestion by ticks. Trends Parasitol. 2013;29(6):276–85. 10.1016/j.pt.2013.04.002 PubMed DOI
Buresova V, Hajdusek O, Franta Z, Loosova G, Grunclova L, Levashina EA, et al. Functional genomics of tick thioester-containing proteins reveal the ancient origin of the complement system. J Innate Immun. 2011;3(6):623–30. 10.1159/000328851 PubMed DOI
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 . Devel Comp Immunol. 2009;33(4):489–98. PubMed
Boldbaatar D, Umemiya-Shirafuji R, Liao M, Tanaka T, Xuan X, Fujisaki K. Multiple vitellogenins from the Haemaphysalis longicornis tick are crucial for ovarian development. J Insect Physiol. 2010;56(11):1587–98. 10.1016/j.jinsphys.2010.05.019 PubMed DOI
Donohue KV, Khalil SM, Sonenshine DE, Roe RM. Heme-binding storage proteins in the Chelicerata. J Insect Physiol. 2009;55(4):287–96. 10.1016/j.jinsphys.2009.01.002 PubMed DOI
Yuan D, Zou Q, Yu T, Song C, Huang S, Chen S, et al. Ancestral genetic complexity of arachidonic acid metabolism in Metazoa. Biochim Biophysica Acta. 2014;1841(9):1272–84. 10.1016/j.bbalip.2014.04.009 PubMed DOI
de Jong L, van der Kraan I, de Waal A. The kinetics of the hydroxylation of procollagen by prolyl 4-hydroxylase. Proposal for a processive mechanism of binding of the dimeric hydroxylating enzyme in relation to the high kcat/Km ratio and a conformational requirement for hydroxylation of-X-Pro-Gly- sequences. Biochim Biophysica Acta. 1991;1079(1):103–11. PubMed
Kelley DR, Rinn JL. Transposable elements reveal a stem cell specific class of long noncoding RNAs. Genome Biol. 2012;13(11):R107 10.1186/gb-2012-13-11-r107 PubMed DOI PMC
Fogaca AC, Lorenzini DM, Kaku LM, Esteves E, Bulet P, Daffre S. Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Devel Comp Immunol. 2004;28(3):191–200. PubMed
Silva FD, Rezende CA, Rossi DC, Esteves E, Dyszy FH, Schreier S, et al. Structure and mode of action of microplusin, a copper II-chelating antimicrobial peptide from the cattle tick Rhipicephalus (Boophilus) microplus . J Biol Chem. 2009;284(50):34735–46. 10.1074/jbc.M109.016410 PubMed DOI PMC
Bulet P, Stocklin R, Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol Rev. 2004;198:169–84. PubMed
Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol. 2003;3(9):710–20. PubMed
Wang Y, Zhu S. The defensin gene family expansion in the tick Ixodes scapularis . Devel Comp Immunol. 2011;35(11):1128–34. 10.1016/j.dci.2011.03.030 PubMed DOI
Calvo E, Pham VM, Lombardo F, Arca B, Ribeiro JM. The sialotranscriptome of adult male Anopheles gambiae mosquitoes. Insect Biochem Mol Biol. 2006;36(7):570–5. PubMed
Arca B, Lombardo F, Valenzuela JG, Francischetti IM, Marinotti O, Coluzzi M, et al. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae . J Exp Biol. 2005;208(Pt 20):3971–86. 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. PubMed PMC
Horackova J, Rudenko N, Golovchenko M, Havlikova S, Grubhoffer L. IrML—a gene encoding a new member of the ML protein family from the hard tick, Ixodes ricinus . J Vector Ecol. 2010;35(2):410–8. 10.1111/j.1948-7134.2010.00100.x PubMed DOI
Rudenko N, Golovchenko M, Edwards MJ, Grubhoffer L. Differential expression of Ixodes ricinus tick genes induced by blood feeding or Borrelia burgdorferi infection. J Med Entomol. 2005;42(1):36–41. PubMed
Nei M, Rooney AP. Concerted and birth-and-death evolution of multigene families. Annu Rev Genet. 2005;39:121–52. PubMed PMC
Rego RO, Hajdusek O, Kovar V, Kopacek P, Grubhoffer L, Hypsa V. Molecular cloning and comparative analysis of fibrinogen-related proteins from the soft tick Ornithodoros moubata and the hard tick Ixodes ricinus . Insect Biochem Mol Biol. 2005;35(9):991–1004. PubMed
Ferrandon D, Imler JL, Hoffmann JA. Sensing infection in Drosophila: Toll and beyond. Semin Immunol. 2004;16(1):43–53. PubMed
Kang D, Liu G, Lundstrom A, Gelius E, Steiner H. A peptidoglycan recognition protein in innate immunity conserved from insects to humans. Proc Natl Acad Sci U S A. 1998;95(17):10078–82. PubMed PMC
Fujita T, Matsushita M, Endo Y. The lectin-complement pathway—its role in innate immunity and evolution. Immunol Rev. 2004;198:185–202. PubMed
Krem MM, Di Cera E. Evolution of enzyme cascades from embryonic development to blood coagulation. Trends Biochem Sci. 2002;27(2):67–74. PubMed
Cerenius L, Soderhall K. The prophenoloxidase-activating system in invertebrates. Immunol Rev. 2004;198:116–26. PubMed
Kopacek P, Hajdusek O, Buresova V. Tick as a model for the study of a primitive complement system. Adv Exp Med Biol. 2012;710:83–93. 10.1007/978-1-4419-5638-5_9 PubMed DOI
Urbanova V, Hartmann D, Grunclova L, Sima R, Flemming T, Hajdusek O, et al. IrFC—An Ixodes ricinus injury-responsive molecule related to Limulus Factor C. Devel Comp Immunol. 2014;46:439–47. 10.1016/j.dci.2014.05.016 PubMed DOI
Kanost MR. Serine proteinase inhibitors in arthropod immunity. Devel Comp Immunol. 1999;23(4–5):291–301. PubMed
Francischetti IM, Mather TN, Ribeiro JM. Penthalaris, a novel recombinant five-Kunitz tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick vector of Lyme disease, Ixodes scapularis . Thromb Haemost. 2004;91(5):886–98. PubMed
Francischetti IM, Valenzuela JG, Andersen JF, Mather TN, Ribeiro JM. Ixolaris, a novel recombinant tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick, Ixodes scapularis: identification of factor X and factor Xa as scaffolds for the inhibition of factor VIIa/tissue factor complex. Blood. 2002;99(10):3602–12. PubMed
Turk V, Stoka V, Turk D. Cystatins: biochemical and structural properties, and medical relevance. Front Biosci. 2008;13:5406–20. PubMed
Kotsyfakis M, Karim S, Andersen JF, Mather TN, Ribeiro JM. Selective cysteine protease inhibition contributes to blood-feeding success of the tick Ixodes scapularis . J Biol Chem. 2007;282(40):29256–63. PubMed
Kotsyfakis M, Sa-Nunes A, Francischetti IM, Mather TN, Andersen JF, Ribeiro JM. Antiinflammatory and immunosuppressive activity of sialostatin L, a salivary cystatin from the tick Ixodes scapularis . J Biol Chem. 2006;281(36):26298–307. PubMed
Schwarz A, Valdes JJ, Kotsyfakis M. The role of cystatins in tick physiology and blood feeding. Ticks Tick Borne Dis. 2012;3(3):117–27. 10.1016/j.ttbdis.2012.03.004 PubMed DOI PMC
Gandhe AS, John SH, Nagaraju J. Noduler, a novel immune up-regulated protein mediates nodulation response in insects. J Immunol. 2007;179(10):6943–51. PubMed
Bao YY, Xue J, Wu WJ, Wang Y, Lv ZY, Zhang CX. An immune-induced reeler protein is involved in the Bombyx mori melanization cascade. Insect Biochem Mol Biol. 2011;41(9):696–706. 10.1016/j.ibmb.2011.05.001 PubMed DOI
Honda S, Kashiwagi M, Miyamoto K, Takei Y, Hirose S. Multiplicity, structures, and endocrine and exocrine natures of eel fucose-binding lectins. J Biol Chem. 2000;275(42):33151–7. PubMed
Armstrong PB, Quigley JP. Alpha2-macroglobulin: an evolutionarily conserved arm of the innate immune system. Dev Comp Immunol. 1999;23(4–5):375–90. PubMed
Urbanova V, Sima R, Sauman I, Hajdusek O, Kopacek P. Thioester-containing proteins of the tick Ixodes ricinus: Gene expression, response to microbial challenge and their role in phagocytosis of the yeast Candida albicans . Devel Comp Immunol. 2014;48(1):55–64. PubMed
Nurnberger T, Brunner F, Kemmerling B, Piater L. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev. 2004;198:249–66. PubMed
Pancer Z, Cooper MD. The evolution of adaptive immunity. Annu Rev Immunol. 2006;24:497–518. PubMed
Myllymaki H, Valanne S, Ramet M. The Drosophila imd signaling pathway. J Immunol. 2014;192(8):3455–62. 10.4049/jimmunol.1303309 PubMed DOI
Kleino A, Silverman N. The Drosophila IMD pathway in the activation of the humoral immune response. Devel Comp Immunol. 2014;42(1):25–35. 10.1016/j.dci.2013.05.014 PubMed DOI PMC
Severo MS, Sakhon OS, Choy A, Stephens KD, Pedra JH. The 'ubiquitous' reality of vector immunology. Cell Microbiol. 2013;15(7):1070–8 10.1111/cmi.12128 PubMed DOI PMC
Valanne S, Kleino A, Myllymaki H, Vuoristo J, Ramet M. Iap2 is required for a sustained response in the Drosophila Imd pathway. Devel Comp Immunol. 2007;31(10):991–1001. PubMed
Imler JL, Hoffmann JA. Signaling mechanisms in the antimicrobial host defense of Drosophila . Curr Opin Microbiol. 2000;3(1):16–22. PubMed
Barillas-Mury C, Han YS, Seeley D, Kafatos FC. Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection. Embo J. 1999;18(4):959–67. PubMed PMC
Liu L, Dai J, Zhao YO, Narasimhan S, Yang Y, Zhang L, et al. Ixodes scapularis JAK-STAT pathway regulates tick antimicrobial peptides, thereby controlling the agent of human granulocytic anaplasmosis. J Infect Dis. 2012;206(8):1233–41. PubMed PMC
Stuart LM, Ezekowitz RA. Phagocytosis and comparative innate immunity: learning on the fly. Nat Rev Immunol. 2008;8(2):131–41. 10.1038/nri2240 PubMed DOI
Aung KM, Boldbaatar D, Umemiya-Shirafuji R, Liao M, Xuenan X, Suzuki H, et al. Scavenger receptor mediates systemic RNA interference in ticks. PLoS One. 2011;6(12):e28407 10.1371/journal.pone.0028407 PubMed DOI PMC
Davis MM, Engstrom Y. Immune response in the barrier epithelia: lessons from the fruit fly Drosophila melanogaster . J Innate Immun. 2012;4(3):273–83. 10.1159/000332947 PubMed DOI PMC
Iwanaga S, Isawa H, Yuda M. Horizontal gene transfer of a vertebrate vasodilatory hormone into ticks. Nat Commun. 2014;5:3373 10.1038/ncomms4373 PubMed DOI
Serpins in Tick Physiology and Tick-Host Interaction
Tick Immune System: What Is Known, the Interconnections, the Gaps, and the Challenges
Sialomes and Mialomes: A Systems-Biology View of Tick Tissues and Tick-Host Interactions
BioProject
PRJNA183509
GENBANK
GBIH01000000
SRA
SRR641298, SRR641303, SRR641305, SRR641306, SRR641307, SRR641308, SRR641309, SRR641327, SRR641328, SRR641329, SRR641330, SRR641331