Deep Sequencing Analysis of the Ixodes ricinus Haemocytome

. 2015 May ; 9 (5) : e0003754. [epub] 20150513

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

Perzistentní odkaz   https://www.medvik.cz/link/pmid25970599

Grantová podpora
R01 AI093653 NIAID NIH HHS - United States
Intramural NIH HHS - United States

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.

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PubMed

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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 PubMed

Santos IK, Valenzuela JG, Ribeiro JM, de Castro M, Costa JN, Costa AM, et al. Gene discovery in 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 PubMed PMC

Mans BJ, Andersen JF, Schwan TG, Ribeiro JM. Characterization of anti-hemostatic factors in the argasid, 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, 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, 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, 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, PubMed DOI PMC

Karim S, Singh P, Ribeiro JM. A deep insight into the sialotranscriptome of the Gulf Coast tick, 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 PMC

Schwarz A, von Reumont BM, Erhart J, Chagas AC, Ribeiro JM, Kotsyfakis M. De novo PubMed DOI PMC

Kotsyfakis M, Schwarz A, Erhart J, Ribeiro JM. Tissue- and time-dependent transcription in 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 PubMed DOI PMC

Anderson JM, Sonenshine DE, Valenzuela JG. Exploring the mialome of ticks: an annotated catalogue of midgut transcripts from the hard tick, 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, PubMed DOI PMC

Heekin AM, Guerrero FD, Bendele KG, Saldivar L, Scoles GA, Dowd SE, et al. The ovarian transcriptome of the cattle tick, 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, PubMed DOI

Heekin AM, Guerrero FD, Bendele KG, Saldivar L, Scoles GA, Gondro C, et al. Analysis of 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 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 PubMed

Boldbaatar D, Umemiya-Shirafuji R, Liao M, Tanaka T, Xuan X, Fujisaki K. Multiple vitellogenins from the 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 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 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 PubMed DOI

Calvo E, Pham VM, Lombardo F, Arca B, Ribeiro JM. The sialotranscriptome of adult male 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, 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, PubMed DOI

Rudenko N, Golovchenko M, Edwards MJ, Grubhoffer L. Differential expression of 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 PubMed

Ferrandon D, Imler JL, Hoffmann JA. Sensing infection in 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, 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, 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 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 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 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 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 PubMed DOI

Kleino A, Silverman N. The 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 PubMed

Imler JL, Hoffmann JA. Signaling mechanisms in the antimicrobial host defense of PubMed

Barillas-Mury C, Han YS, Seeley D, Kafatos FC. PubMed PMC

Liu L, Dai J, Zhao YO, Narasimhan S, Yang Y, Zhang L, et al. 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 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

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