Tick Immune System: What Is Known, the Interconnections, the Gaps, and the Challenges
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
33737931
PubMed Central
PMC7962413
DOI
10.3389/fimmu.2021.628054
Knihovny.cz E-zdroje
- Klíčová slova
- cell-mediated immunity, immune signaling pathway, immune system, microbiota, tick-borne pathogen,
- MeSH
- buněčná imunita * MeSH
- humorální imunita * MeSH
- interakce hostitele a parazita MeSH
- klíšťata imunologie metabolismus MeSH
- lidé MeSH
- nemoci přenášené klíšťaty imunologie metabolismus přenos MeSH
- slinné žlázy imunologie metabolismus MeSH
- sliny imunologie metabolismus MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
Ticks are ectoparasitic arthropods that necessarily feed on the blood of their vertebrate hosts. The success of blood acquisition depends on the pharmacological properties of tick saliva, which is injected into the host during tick feeding. Saliva is also used as a vehicle by several types of pathogens to be transmitted to the host, making ticks versatile vectors of several diseases for humans and other animals. When a tick feeds on an infected host, the pathogen reaches the gut of the tick and must migrate to its salivary glands via hemolymph to be successfully transmitted to a subsequent host during the next stage of feeding. In addition, some pathogens can colonize the ovaries of the tick and be transovarially transmitted to progeny. The tick immune system, as well as the immune system of other invertebrates, is more rudimentary than the immune system of vertebrates, presenting only innate immune responses. Although simpler, the large number of tick species evidences the efficiency of their immune system. The factors of their immune system act in each tick organ that interacts with pathogens; therefore, these factors are potential targets for the development of new strategies for the control of ticks and tick-borne diseases. The objective of this review is to present the prevailing knowledge on the tick immune system and to discuss the challenges of studying tick immunity, especially regarding the gaps and interconnections. To this end, we use a comparative approach of the tick immune system with the immune system of other invertebrates, focusing on various components of humoral and cellular immunity, such as signaling pathways, antimicrobial peptides, redox metabolism, complement-like molecules and regulated cell death. In addition, the role of tick microbiota in vector competence is also discussed.
Department of Parasitology Institute of Biomedical Sciences University of São Paulo São Paulo Brazil
Institute of Parasitology Biology Centre Czech Academy of Sciences Ceske Budejovice Czechia
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Dantas-Torres F, Fernandes Martins T, Munoz-Leal S, Onofrio VC, Barros-Battesti DM. Ticks (Ixodida: Argasidae, Ixodidae) of Brazil: Updated species checklist and taxonomic keys. Ticks Tick Borne Dis (2019) 10:101252. 10.1016/j.ttbdis.2019.06.012 PubMed DOI
Dantas-Torres F. Species Concepts: What about ticks? Trends Parasitol (2018) 34:1017–26. 10.1016/j.pt.2018.09.009 PubMed DOI
Koch HG, Sauer JR. Quantity of blood ingested by four species of hard ticks (Acari:Ixodidae) fed on domestic dogs. Ann Entomol Soc Am (1984) 77:142–6. 10.1093/aesa/77.2.142 DOI
Grisi L, Leite RC, Martins JR, Barros AT, Andreotti R, Cancado PH, et al. . Reassessment of the potential economic impact of cattle parasites in Brazil. Rev Bras Parasitol Vet (2014) 23:150–6. 10.1590/S1984-29612014042 PubMed DOI
Bowman AS, Sauer JR. Tick salivary glands: function, physiology and future. Parasitology (2004) 129(Suppl):S67–81. 10.1017/s0031182004006468 PubMed DOI
Kazimirova M, Stibraniova I. Tick salivary compounds: their role in modulation of host defences and pathogen transmission. Front Cell Infect Microbiol (2013) 3:43. 10.3389/fcimb.2013.00043 PubMed DOI PMC
Kotal J, Langhansova H, Lieskovska J, Andersen JF, Francischetti IM, Chavakis T, et al. . Modulation of host immunity by tick saliva. J Proteomics (2015) 128:58–68. 10.1016/j.jprot.2015.07.005 PubMed DOI PMC
Simo L, Kazimirova M, Richardson J, Bonnet SI. The essential role of tick salivary glands and saliva in tick feeding and pathogen transmission. Front Cell Infect Microbiol (2017) 7:281. 10.3389/fcimb.2017.00281 PubMed DOI PMC
Dantas-Torres F, Chomel BB, Otranto D. Ticks and tick-borne diseases: a one health perspective. Trends Parasitol (2012) 28:437–46. 10.1016/j.pt.2012.07.003 PubMed DOI
Stanek G, Strle F. Lyme borreliosis-from tick bite to diagnosis and treatment. FEMS Microbiol Rev (2018) 42:233–58. 10.1093/femsre/fux047 PubMed DOI
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
Brey PT. The contribution of the Pasteur scholl of insect immunity. In: Brey PT, Hultmark D, editors. Molecular Mechanisms of Immune Responses in Insects. London: Chapman & Hall; (1998). p. 1–39.
Steiner H, Hultmark D, Engstrom A, Bennich H, Boman HG. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature (1981) 292:246–8. 10.1038/292246a0 PubMed DOI
Selsted ME, Brown DM, DeLange RJ, Lehrer RI. Primary structures of MCP-1 and MCP-2, natural peptide antibiotics of rabbit lung macrophages. J Biol Chem (1983) 258:14485–9. PubMed
Selsted ME, Harwig SS, Ganz T, Schilling JW, Lehrer RI. Primary structures of three human neutrophil defensins. J Clin Invest (1985) 76:1436–9. 10.1172/JCI112121 PubMed DOI PMC
Boman HG, Hultmark D. Cell-free immunity in insects. Annu Rev Microbiol (1987) 41:103–26. 10.1146/annurev.mi.41.100187.000535 PubMed DOI
Ashida M. The prophenoloxidase cascade in insect immunity. Res Immunol (1990) 141:908–10. 10.1016/0923-2494(90)90191-z PubMed DOI
Johansson MW, Soderhall K. Cellular immunity in crustaceans and the proPO system. Parasitol Today (1989) 5:171–6. 10.1016/0169-4758(89)90139-7 PubMed DOI
Kopacek P, Hall M, Soderhall K. Characterization of a clotting protein, isolated from plasma of the freshwater crayfish Pacifastacus leniusculus. Eur J Biochem (1993) 213:591–7. 10.1111/j.1432-1033.1993.tb17798.x PubMed DOI
Iwanaga S, Miyata T, Tokunaga F, Muta T. Molecular mechanism of hemolymph clotting system in Limulus. Thromb Res (1992) 68:1–32. 10.1016/0049-3848(92)90124-s PubMed DOI
Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA. Phylogenetic perspectives in innate immunity. Science (1999) 284:1313–8. 10.1126/science.284.5418.1313 PubMed DOI
Hultmark D. Drosophila immunity: paths and patterns. Curr Opin Immunol (2003) 15:12–9. 10.1016/s0952-7915(02)00005-5 PubMed DOI
Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell (1996) 86:973–83. 10.1016/s0092-8674(00)80172-5 PubMed DOI
Imler JL. Overview of Drosophila immunity: a historical perspective. Dev Comp Immunol (2014) 42:3–15. 10.1016/j.dci.2013.08.018 PubMed DOI
Engstrom Y, Kadalayil L, Sun SC, Samakovlis C, Hultmark D, Faye I. kappa B-like motifs regulate the induction of immune genes in Drosophila. J Mol Biol (1993) 232:327–33. 10.1006/jmbi.1993.1392 PubMed DOI
Belvin MP, Anderson KV. A conserved signaling pathway: the Drosophila Toll-Dorsal pathway. Annu Rev Cell Dev Biol (1996) 12:393–416. 10.1146/annurev.cellbio.12.1.393 PubMed DOI
Michel K, Kafatos FC. Mosquito immunity against Plasmodium. Insect Biochem Mol Biol (2005) 35:677–89. 10.1016/j.ibmb.2005.02.009 PubMed DOI
Garcia GR, Maruyama SR, Malardo T, Zangirolamo AF, Gardinassi LG. The biology of hematophagous arthropods addressed by molecular high-throughput approaches. Austin J Trop Med Hyg (2015) 1:1004–10.
Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, et al. . Immunity-related genes and gene families in Anopheles gambiae. Science (2002) 298:159–65. 10.1126/science.1077136 PubMed DOI
Palmer WJ, Jiggins FM. Comparative genomics reveals the origins and diversity of arthropod immune systems. Mol Biol Evol (2015) 32:2111–29. 10.1093/molbev/msv093 PubMed DOI PMC
Rosa RD, Capelli-Peixoto J, Mesquita RD, Kalil SP, Pohl PC, Braz GR, et al. . Exploring the immune signalling pathway-related genes of the cattle tick Rhipicephalus microplus: From molecular characterization to transcriptional profile upon microbial challenge. Dev Comp Immunol (2016) 59:1–14. 10.1016/j.dci.2015.12.018 PubMed DOI
Zumaya-Estrada FA, Martinez-Barnetche J, Lavore A, Rivera-Pomar R, Rodriguez MH. Comparative genomics analysis of triatomines reveals common first line and inducible immunity-related genes and the absence of Imd canonical components among hemimetabolous arthropods. Parasit Vectors (2018) 11:48. 10.1186/s13071-017-2561-2 PubMed DOI PMC
Smith AA, Pal U. Immunity-related genes in Ixodes scapularis-perspectives from genome information. Front Cell Infect Microbiol (2014) 4:116. 10.3389/fcimb.2014.00116 PubMed DOI PMC
Barnard AC, Nijhof AM, Fick W, Stutzer C, Maritz-Olivier C. RNAi in arthropods: insight into the machinery and applications for understanding the pathogen-vector interface. Genes (Basel) (2012) 3:702–41. 10.3390/genes3040702 PubMed DOI PMC
Sun D, Guo Z, Liu Y, Zhang Y. Progress and prospects of CRISPR/Cas systems in insects and other arthropods. Front Physiol (2017) 8:608. 10.3389/fphys.2017.00608 PubMed DOI PMC
Geraci NS, Spencer Johnston J, Paul Robinson J, Wikel SK, Hill CA. Variation in genome size of argasid and ixodid ticks. Insect Biochem Mol Biol (2007) 37:399–408. 10.1016/j.ibmb.2006.12.007 PubMed DOI
Barrero RA, Guerrero FD, Black M, McCooke J, Chapman B, Schilkey F, et al. . Gene-enriched draft genome of the cattle tick Rhipicephalus microplus: assembly by the hybrid Pacific Biosciences/Illumina approach enabled analysis of the highly repetitive genome. Int J Parasitol (2017) 47:569–83. 10.1016/j.ijpara.2017.03.007 PubMed DOI
Gulia-Nuss M, Nuss AB, Meyer JM, Sonenshine DE, Roe RM, Waterhouse RM, et al. . Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat Commun (2016) 7:10507. 10.1038/ncomms10507 PubMed DOI PMC
Jia N, Wang J, Shi W, Du L, Sun Y, Zhan W, et al. . Large-scale comparative analyses of tick genomes elucidate their genetic diversity and vector capacities. Cell (2020) 182:1328–40.e13. 10.1016/j.cell.2020.07.023 PubMed DOI
Romano D, Stefanini C, Canale A, Benelli G. Artificial blood feeders for mosquito and ticks-where from, where to? Acta Trop (2018) 183:43–56. 10.1016/j.actatropica.2018.04.009 PubMed DOI
Bell-Sakyi L, Darby A, Baylis M, Makepeace BL. The tick cell biobank: a global resource for in vitro research on ticks, other arthropods and the pathogens they transmit. Ticks Tick Borne Dis (2018) 9:1364–71. 10.1016/j.ttbdis.2018.05.015 PubMed DOI PMC
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. 10.2741/3200 PubMed DOI
Verhulst NO, Boulanger N JS. Impact of skin microbiome on attractiveness to arthropod vectors and pathogen transmission. In: Boulanger N, editor. Skin and Arthropod Vectors. Academic Press; (Cambridge, Massachusetts, EUA: ) (2018). p. 55–81. 10.1016/B978-0-12-811436-0.00003-4 DOI
Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol (2007) 25:697–743. 10.1146/annurev.immunol.25.022106.141615 PubMed DOI
Kitsou C, Pal U. Ixodes immune responses against Lyme disease pathogens. Front Cell Infect Microbiol (2018) 8:176. 10.3389/fcimb.2018.00176 PubMed DOI PMC
Lindsay SA, Wasserman SA. Conventional and non-conventional Drosophila Toll signaling. Dev Comp Immunol (2014) 42:16–24. 10.1016/j.dci.2013.04.011 PubMed DOI PMC
Oliva Chavez AS, Shaw DK, Munderloh UG, Pedra JH. Tick humoral responses: marching to the beat of a different drummer. Front Microbiol (2017) 8:223. 10.3389/fmicb.2017.00223 PubMed DOI PMC
Shaw DK, Wang X, Brown LJ, Chavez AS, Reif KE, Smith AA, et al. . Infection-derived lipids elicit an immune deficiency circuit in arthropods. Nat Commun (2017) 8:14401. 10.1038/ncomms14401 PubMed DOI PMC
Capelli-Peixoto J, Carvalho DD, Johnson WC, Scoles GA, Fogaca AC, Daffre S, et al. . The transcription factor Relish controls Anaplasma marginale infection in the bovine tick Rhipicephalus microplus. Dev Comp Immunol (2017) 74:32–9. 10.1016/j.dci.2017.04.005 PubMed DOI
Tanji T, Yun EY, Ip YT. Heterodimers of NF-kappaB transcription factors DIF and Relish regulate antimicrobial peptide genes in Drosophila. Proc Natl Acad Sci USA (2010) 107:14715–20. 10.1073/pnas.1009473107 PubMed DOI PMC
Paradkar PN, Duchemin JB, Voysey R, Walker PJ. Dicer-2-dependent activation of Culex Vago occurs via the TRAF-Rel2 signaling pathway. PloS Negl Trop Dis (2014) 8:e2823. 10.1371/journal.pntd.0002823 PubMed DOI PMC
Paradkar PN, Trinidad L, Voysey R, Duchemin JB, Walker PJ. Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway. Proc Natl Acad Sci USA (2012) 109:18915–20. 10.1073/pnas.1205231109 PubMed DOI 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) 206:1233–41. 10.1093/infdis/jis484 PubMed DOI PMC
Mansfield KL, Cook C, Ellis RJ, Bell-Sakyi L, Johnson N, Alberdi P, et al. . Tick-borne pathogens induce differential expression of genes promoting cell survival and host resistance in Ixodes ricinus cells. Parasit Vectors (2017) 10:81. 10.1186/s13071-017-2011-1 PubMed DOI PMC
Kleino A, Silverman N. The Drosophila IMD pathway in the activation of the humoral immune response. Dev Comp Immunol (2014) 42:25–35. 10.1016/j.dci.2013.05.014 PubMed DOI PMC
Nishide Y, Kageyama D, Yokoi K, Jouraku A, Tanaka H, Futahashi R, et al. . Functional crosstalk across IMD and Toll pathways: insight into the evolution of incomplete immune cascades. Proc Biol Sci (2019) 286:20182207. 10.1098/rspb.2018.2207 PubMed DOI PMC
Salcedo-Porras N, Guarneri A, Oliveira PL, Lowenberger C. Rhodnius prolixus: identification of missing components of the IMD immune signaling pathway and functional characterization of its role in eliminating bacteria. PloS One (2019) 14:e0214794. 10.1371/journal.pone.0214794 PubMed DOI PMC
McClure Carroll EE, Wang X, Shaw DK, O’Neal AJ, Oliva Chavez AS, Brown LJ, et al. . p47 licenses activation of the immune deficiency pathway in the tick Ixodes scapularis. Proc Natl Acad Sci USA (2019) 116:205–10. 10.1073/pnas.1808905116 PubMed DOI PMC
Silverman N, Zhou R, Erlich RL, Hunter M, Bernstein E, Schneider D, et al. . Immune activation of NF-kappaB and JNK requires Drosophila TAK1. J Biol Chem (2003) 278:48928–34. 10.1074/jbc.M304802200 PubMed DOI
Dostert C, Jouanguy E, Irving P, Troxler L, Galiana-Arnoux D, Hetru C, et al. . The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat Immunol (2005) 6:946–53. 10.1038/ni1237 PubMed DOI
Osman D, Buchon N, Chakrabarti S, Huang YT, Su WC, Poidevin M, et al. . Autocrine and paracrine unpaired signaling regulate intestinal stem cell maintenance and division. J Cell Sci (2012) 125:5944–9. 10.1242/jcs.113100 PubMed DOI
Narasimhan S, Rajeevan N, Liu L, Zhao YO, Heisig J, Pan J, et al. . Gut microbiota of the tick vector Ixodes scapularis modulate colonization of the Lyme disease spirochete. Cell Host Microbe (2014) 15:58–71. 10.1016/j.chom.2013.12.001 PubMed DOI PMC
Smith AA, Navasa N, Yang X, Wilder CN, Buyuktanir O, Marques A, et al. . Cross-species interferon signaling boosts microbicidal activity within the tick vector. Cell Host Microbe (2016) 20:91–8. 10.1016/j.chom.2016.06.001 PubMed DOI PMC
Abraham NM, Liu L, Jutras BL, Yadav AK, Narasimhan S, Gopalakrishnan V, et al. . Pathogen-mediated manipulation of arthropod microbiota to promote infection. Proc Natl Acad Sci USA (2017) 114:E781–E90. 10.1073/pnas.1613422114 PubMed DOI PMC
Karlikow M, Goic B, Saleh MC. RNAi and antiviral defense in Drosophila: setting up a systemic immune response. Dev Comp Immunol (2014) 42:85–92. 10.1016/j.dci.2013.05.004 PubMed DOI
Blair CD. Mosquito RNAi is the major innate immune pathway controlling arbovirus infection and transmission. Future Microbiol (2011) 6:265–77. 10.2217/fmb.11.11 PubMed DOI PMC
Asgari S. Role of microRNAs in arbovirus/vector interactions. Viruses (2014) 6:3514–34. 10.3390/v6093514 PubMed DOI PMC
Schnettler E, Tykalova H, Watson M, Sharma M, Sterken MG, Obbard DJ, et al. . Induction and suppression of tick cell antiviral RNAi responses by tick-borne flaviviruses. Nucleic Acids Res (2014) 42:9436–46. 10.1093/nar/gku657 PubMed DOI PMC
Yuan C, Wu J, Peng Y, Li Y, Shen S, Deng F, et al. . Transcriptome analysis of the innate immune system of Hyalomma asiaticum. J Invertebr Pathol (2020) 177:107481. 10.1016/j.jip.2020.107481 PubMed DOI
Weisheit S, Villar M, Tykalova H, Popara M, Loecherbach J, Watson M, et al. . Ixodes scapularis and Ixodes ricinus tick cell lines respond to infection with tick-borne encephalitis virus: transcriptomic and proteomic analysis. Parasit Vectors (2015) 8:599. 10.1186/s13071-015-1210-x PubMed DOI PMC
Grubaugh ND, Ruckert C, Armstrong PM, Bransfield A, Anderson JF, Ebel GD, et al. . Transmission bottlenecks and RNAi collectively influence tick-borne flavivirus evolution. Virus Evol (2016) 2:vew033. 10.1093/ve/vew033 PubMed DOI PMC
Hermance ME, Widen SG, Wood TG, Thangamani S. Ixodes scapularis salivary gland microRNAs are differentially expressed during Powassan virus transmission. Sci Rep (2019) 9:13110. 10.1038/s41598-019-49572-5 PubMed DOI PMC
Artigas-Jeronimo S, Alberdi P, Villar Rayo M, Cabezas-Cruz A, Prados PJE, Mateos-Hernandez L, et al. . Anaplasma phagocytophilum modifies tick cell microRNA expression and upregulates isc-mir-79 to facilitate infection by targeting the roundabout protein 2 pathway. Sci Rep (2019) 9:9073. 10.1038/s41598-019-45658-2 PubMed DOI PMC
Morazzani EM, Wiley MR, Murreddu MG, Adelman ZN, Myles KM. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PloS Pathog (2012) 8:e1002470. 10.1371/journal.ppat.1002470 PubMed DOI PMC
Vodovar N, Bronkhorst AW, van Cleef KW, Miesen P, Blanc H, van Rij RP, et al. . Arbovirus-derived piRNAs exhibit a ping-pong signature in mosquito cells. PloS One (2012) 7:e30861. 10.1371/journal.pone.0030861 PubMed DOI PMC
Hess AM, Prasad AN, Ptitsyn A, Ebel GD, Olson KE, Barbacioru C, et al. . Small RNA profiling of Dengue virus-mosquito interactions implicates the PIWI RNA pathway in anti-viral defense. BMC Microbiol (2011) 11:45. 10.1186/1471-2180-11-45 PubMed DOI PMC
Tanji T, Hu X, Weber AN, Ip YT. Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol Cell Biol (2007) 27:4578–88. 10.1128/MCB.01814-06 PubMed DOI PMC
Hussain M, Walker T, O’Neill SL, Asgari S. Blood meal induced microRNA regulates development and immune associated genes in the Dengue mosquito vector, Aedes aegypti. Insect Biochem Mol Biol (2013) 43:146–52. 10.1016/j.ibmb.2012.11.005 PubMed DOI
Li Y, Li S, Li R, Xu J, Jin P, Chen L, et al. . Genome-wide miRNA screening reveals miR-310 family members negatively regulate the immune response in Drosophila melanogaster via co-targeting drosomycin. Dev Comp Immunol (2017) 68:34–45. 10.1016/j.dci.2016.11.014 PubMed DOI
Kim LK, Choi UY, Cho HS, Lee JS, Lee WB, Kim J, et al. . Down-regulation of NF-kappaB target genes by the AP-1 and STAT complex during the innate immune response in Drosophila. PloS Biol (2007) 5:e238. 10.1371/journal.pbio.0050238 PubMed DOI PMC
Bulet P, Stocklin R, Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol Rev (2004) 198:169–84. 10.1111/j.0105-2896.2004.0124.x PubMed DOI
Sonenshine DE, Hynes WL. Molecular characterization and related aspects of the innate immune response in ticks. Front Biosci (2008) 13:7046–63. 10.2741/3209 PubMed DOI
Kopacek P, Hajdusek O, Buresova V, Daffre S. Tick innate immunity. Adv Exp Med Biol (2010) 708:137–62. 10.1007/978-1-4419-8059-5_8 PubMed DOI
Sonenshine DE, Macaluso KR. Microbial invasion vs. tick immune regulation. Front Cell Infect Microbiol (2017) 7:390. 10.3389/fcimb.2017.00390 PubMed DOI PMC
Fogaca AC, da Silva PI, Jr, Miranda MT, Bianchi AG, Miranda A, Ribolla PE, et al. . Antimicrobial activity of a bovine hemoglobin fragment in the tick Boophilus microplus. J Biol Chem (1999) 274:25330–4. 10.1074/jbc.274.36.25330 PubMed DOI
Nakajima Y, Ogihara K, Taylor D, Yamakawa M. Antibacterial hemoglobin fragments from the midgut of the soft tick, Ornithodoros moubata (Acari: Argasidae). J Med Entomol (2003) 40:78–81. 10.1603/0022-2585-40.1.78 PubMed DOI
Sonenshine DE, Hynes WL, Ceraul SM, Mitchell R, Benzine T. Host blood proteins and peptides in the midgut of the tick Dermacentor variabilis contribute to bacterial control. Exp Appl Acarol (2005) 36:207–23. 10.1007/s10493-005-2564-0 PubMed DOI
Belmonte R, Cruz CE, Pires JR, Daffre S. Purification and characterization of Hb 98-114: a novel hemoglobin-derived antimicrobial peptide from the midgut of Rhipicephalus (Boophilus) microplus. Peptides (2012) 37:120–7. 10.1016/j.peptides.2012.05.017 PubMed DOI
Dubin A, Mak P, Dubin G, Rzychon M, Stec-Niemczyk J, Wladyka B, et al. . New generation of peptide antibiotics. Acta Biochim Pol (2005) 52:633–8. PubMed
Cruz CE, Fogaca AC, Nakayasu ES, Angeli CB, Belmonte R, Almeida IC, et al. . Characterization of proteinases from the midgut of Rhipicephalus (Boophilus) microplus involved in the generation of antimicrobial peptides. Parasit Vectors (2010) 3:63. 10.1186/1756-3305-3-63 PubMed DOI PMC
Machado A, Sforca ML, Miranda A, Daffre S, Pertinhez TA, Spisni A, et al. . Truncation of amidated fragment 33-61 of bovine alpha-hemoglobin: effects on the structure and anticandidal activity. Biopolymers (2007) 88:413–26. 10.1002/bip.20688 PubMed DOI
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. Dev Comp Immunol (2004) 28:191–200. 10.1016/j.dci.2003.08.001 PubMed DOI
Lai R, Takeuchi H, Lomas LO, Jonczy J, Rigden DJ, Rees HH, et al. . A new type of antimicrobial protein with multiple histidines from the hard tick, Amblyomma hebraeum. FASEB J (2004) 18:1447–9. 10.1096/fj.03-1154fje PubMed DOI
Esteves E, Fogaca AC, Maldonado R, Silva FD, Manso PP, Pelajo-Machado M, et al. . Antimicrobial activity in the tick Rhipicephalus (Boophilus) microplus eggs: Cellular localization and temporal expression of microplusin during oogenesis and embryogenesis. Dev Comp Immunol (2009) 33:913–9. 10.1016/j.dci.2009.02.009 PubMed DOI
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) 284:34735–46. 10.1074/jbc.M109.016410 PubMed DOI PMC
Silva FD, Rossi DC, Martinez LR, Frases S, Fonseca FL, Campos CB, et al. . Effects of microplusin, a copper-chelating antimicrobial peptide, against Cryptococcus neoformans. FEMS Microbiol Lett (2011) 324:64–72. 10.1111/j.1574-6968.2011.02386.x PubMed DOI
Martins LA, Malossi CD, Galletti M, Ribeiro JM, Fujita A, Esteves E, et al. . The transcriptome of the salivary glands of Amblyomma aureolatum reveals the antimicrobial peptide microplusin as an important factor for the tick protection against Rickettsia rickettsii infection. Front Physiol (2019) 10:529. 10.3389/fphys.2019.00529 PubMed DOI PMC
Pelc RS, McClure JC, Sears KT, Chung A, Rahman MS, Ceraul SM. Defending the fort: a role for defensin-2 in limiting Rickettsia montanensis infection of Dermacentor variabilis. Insect Mol Biol (2014) 23:457–65. 10.1111/imb.12094 PubMed DOI PMC
Chou S, Daugherty MD, Peterson SB, Biboy J, Yang Y, Jutras BL, et al. . Transferred interbacterial antagonism genes augment eukaryotic innate immune function. Nature (2015) 518:98–101. 10.1038/nature13965 PubMed DOI PMC
Hayes BM, Radkov AD, Yarza F, Flores S, Kim J, Zhao Z, et al. . Ticks resist skin commensals with immune factor of bacterial origin. Cell (2020) 183:1562–71.e12. 10.1016/j.cell.2020.10.042 PubMed DOI PMC
Gulley MM, Zhang X, Michel K. The roles of serpins in mosquito immunology and physiology. J Insect Physiol (2013) 59:138–47. 10.1016/j.jinsphys.2012.08.015 PubMed DOI PMC
Armstrong PB. The contribution of proteinase inhibitors to immune defense. Trends Immunol (2001) 22:47–52. 10.1016/s1471-4906(00)01803-2 PubMed DOI
Fogaca AC, Almeida IC, Eberlin MN, Tanaka AS, Bulet P, Daffre S. Ixodidin, a novel antimicrobial peptide from the hemocytes of the cattle tick Boophilus microplus with inhibitory activity against serine proteinases. Peptides (2006) 27:667–74. 10.1016/j.peptides.2005.07.013 PubMed DOI
Bania J, Stachowiak D, Polanowski A. Primary structure and properties of the cathepsin G/chymotrypsin inhibitor from the larval hemolymph of Apis mellifera. Eur J Biochem (1999) 262:680–7. 10.1046/j.1432-1327.1999.00406.x PubMed DOI
Ceraul SM, Chung A, Sears KT, Popov VL, Beier-Sexton M, Rahman MS, et al. . A Kunitz protease inhibitor from Dermacentor variabilis, a vector for spotted fever group rickettsiae, limits Rickettsia montanensis invasion. Infect Immun (2011) 79:321–9. 10.1128/IAI.00362-10 PubMed DOI PMC
Ceraul SM, Dreher-Lesnick SM, Mulenga A, Rahman MS, Azad AF. Functional characterization and novel rickettsiostatic effects of a Kunitz-type serine protease inhibitor from the tick Dermacentor variabilis. Infect Immun (2008) 76:5429–35. 10.1128/IAI.00866-08 PubMed DOI PMC
Ha EM, Oh CT, Bae YS, Lee WJ. A direct role for dual oxidase in Drosophila gut immunity. Science (2005) 310:847–50. 10.1126/science.1117311 PubMed DOI
Molina-Cruz A, DeJong RJ, Charles B, Gupta L, Kumar S, Jaramillo-Gutierrez G, et al. . Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chem (2008) 283:3217–23. 10.1074/jbc.M705873200 PubMed DOI
Fang FC. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol (2004) 2:820–32. 10.1038/nrmicro1004 PubMed DOI
Jones DP. Redefining oxidative stress. Antioxid Redox Signal (2006) 8:1865–79. 10.1089/ars.2006.8.1865 PubMed DOI
Pereira LS, Oliveira PL, Barja-Fidalgo C, Daffre S. Production of reactive oxygen species by hemocytes from the cattle tick Boophilus microplus. Exp Parasitol (2001) 99:66–72. 10.1006/expr.2001.4657 PubMed DOI
Bifano TD, Ueti MW, Esteves E, Reif KE, Braz GR, Scoles GA, et al. . Knockdown of the Rhipicephalus microplus cytochrome c oxidase subunit III gene is associated with a failure of Anaplasma marginale transmission. PloS One (2014) 9:e98614. 10.1371/journal.pone.0098614 PubMed DOI PMC
Narasimhan S, Sukumaran B, Bozdogan U, Thomas V, Liang X, DePonte K, et al. . A tick antioxidant facilitates the Lyme disease agent’s successful migration from the mammalian host to the arthropod vector. Cell Host Microbe (2007) 2:7–18. 10.1016/j.chom.2007.06.001 PubMed DOI PMC
Kumar S, Molina-Cruz A, Gupta L, Rodrigues J, Barillas-Mury C. A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science (2010) 327:1644–8. 10.1126/science.1184008 PubMed DOI PMC
Oliveira Gde A, Lieberman J, Barillas-Mury C. Epithelial nitration by a peroxidase/NOX5 system mediates mosquito antiplasmodial immunity. Science (2012) 335:856–9. 10.1126/science.1209678 PubMed DOI PMC
Yang X, Smith AA, Williams MS, Pal U. A dityrosine network mediated by dual oxidase and peroxidase influences the persistence of Lyme disease pathogens within the vector. J Biol Chem (2014) 289:12813–22. 10.1074/jbc.M113.538272 PubMed DOI PMC
Kalil SP, Rosa RDD, Capelli-Peixoto J, Pohl PC, Oliveira PL, Fogaca AC, et al. . Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale. Parasit Vectors (2017) 10:613. 10.1186/s13071-017-2575-9 PubMed DOI PMC
Hillyer JF, Christensen BM. Characterization of hemocytes from the Yellow Fever mosquito, Aedes aegypti. Histochem Cell Biol (2002) 117:431–40. 10.1007/s00418-002-0408-0 PubMed DOI
Kuhn KH, Haug T. Ultrastructural, cytochemical, and immunocytochemical characterization of haemocytes of the hard tick Ixodes ricinus (Acari; Chelicerata). Cell Tissue Res (1994) 277:493–504. 10.1007/BF00300222 DOI
Borovickova B, Hypsa V. Ontogeny of tick hemocytes: a comparative analysis of Ixodes ricinus and Ornithodoros moubata. Exp Appl Acarol (2005) 35:317–33. 10.1007/s10493-004-2209-8 PubMed DOI
Inoue N, Hanada K, Tsuji N, Igarashi I, Nagasawa H, Mikami T, et al. . Characterization of phagocytic hemocytes in Ornithodoros moubata (Acari: Ixodidae). J Med Entomol (2001) 38:514–9. 10.1603/0022-2585-38.4.514 PubMed DOI
Fiorotti J, Menna-Barreto RFS, Golo PS, Coutinho-Rodrigues CJB, Bitencourt ROB, Spadacci-Morena DD, et al. . Ultrastructural and cytotoxic effects of Metarhizium robertsii infection on Rhipicephalus microplus hemocytes. Front Physiol (2019) 10:654. 10.3389/fphys.2019.00654 PubMed DOI PMC
Feitosa AP, Alves LC, Chaves MM, Veras DL, Silva EM, Alianca AS, et al. . Hemocytes of Rhipicephalus sanguineus (Acari: Ixodidae): characterization, population abundance, and ultrastructural changes following challenge with Leishmania infantum. J Med Entomol (2015) 52:1193–202. 10.1093/jme/tjv125 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) 3:623–30. 10.1159/000328851 PubMed DOI
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. Dev Comp Immunol (2015) 48:55–64. 10.1016/j.dci.2014.09.004 PubMed DOI
Urbanova V, Hajdusek O, Honig Mondekova H, Sima R, Kopacek P. Tick thioester-containing proteins and phagocytosis do not affect transmission of Borrelia afzelii from the competent vector Ixodes ricinus. Front Cell Infect Microbiol (2017) 7:73. 10.3389/fcimb.2017.00073 PubMed DOI PMC
Dunham-Ems SM, Caimano MJ, Pal U, Wolgemuth CW, Eggers CH, Balic A, et al. . Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J Clin Invest (2009) 119:3652–65. 10.1172/JCI39401 PubMed DOI PMC
Eggenberger LR, Lamoreaux WJ, Coons LB. Hemocytic encapsulation of implants in the tick Dermacentor variabilis. Exp Appl Acarol (1990) 9:279–87. 10.1007/BF01193434 PubMed DOI
Ceraul SM, Sonenshine DE, Hynes WL. Resistance of the tick Dermacentor variabilis (Acari: Ixodidae) following challenge with the bacterium Escherichia coli (Enterobacteriales: Enterobacteriaceae). J Med Entomol (2002) 39:376–83. 10.1603/0022-2585-39.2.376 PubMed DOI
Cerenius L, Soderhall K. The prophenoloxidase-activating system in invertebrates. Immunol Rev (2004) 198:116–26. 10.1111/j.0105-2896.2004.00116.x PubMed DOI
Nakhleh J, El Moussawi L, Osta MA. The melanization response in insect immunity. Adv Insect Physiol (2017) 52:83–109. 10.1016/bs.aiip.2016.11.002 DOI
Yuan C, Xing L, Wang M, Wang X, Yin M, Wang Q, et al. . Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera. PloS Pathog (2017) 13:e1006645. 10.1371/journal.ppat.1006645 PubMed DOI PMC
Zhioua E, Browning M, Johnson PW, Ginsberg HS, LeBrun RA. Pathogenicity of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycetes) to Ixodes scapularis (Acari: Ixodidae). J Parasitol (1997) 83:815–8. PubMed
Feitosa APS, Chaves MM, Veras DL, de Deus DMV, Portela NCJ, Araujo AR, et al. . Assessing the cellular and humoral immune response in Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) infected with Leishmania infantum (Nicolle, 1908). Ticks Tick Borne Dis (2018) 9:1421–30. 10.1016/j.ttbdis.2018.06.007 PubMed DOI
Kadota K, Satoh E, Ochiai M, Inoue N, Tsuji N, Igarashi I, et al. . Existence of phenol oxidase in the argasid tick Ornithodoros moubata. Parasitol Res (2002) 88:781–4. 10.1007/s00436-002-0664-x PubMed DOI
Jiravanichpaisal P, Lee BL, Soderhall K. Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology (2006) 211:213–36. 10.1016/j.imbio.2005.10.015 PubMed DOI
Iwanaga S, Lee BL. Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol (2005) 38:128–50. 10.5483/bmbrep.2005.38.2.128 PubMed DOI
Osaki T, Okino N, Tokunaga F, Iwanaga S, Kawabata S. Proline-rich cell surface antigens of horseshoe crab hemocytes are substrates for protein cross-linking with a clotting protein coagulin. J Biol Chem (2002) 277:40084–90. 10.1074/jbc.M206773200 PubMed DOI
Nagai T, Kawabata S. A link between blood coagulation and prophenol oxidase activation in arthropod host defense. J Biol Chem (2000) 275:29264–7. 10.1074/jbc.M002556200 PubMed DOI
Theopold U, Krautz R, Dushay MS. The Drosophila clotting system and its messages for mammals. Dev Comp Immunol (2014) 42:42–6. 10.1016/j.dci.2013.03.014 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. Dev Comp Immunol (2014) 46:439–47. 10.1016/j.dci.2014.05.016 PubMed DOI
Hillyer JF, Strand MR. Mosquito hemocyte-mediated immune responses. Curr Opin Insect Sci (2014) 3:14–21. 10.1016/j.cois.2014.07.002 PubMed DOI PMC
Kotsyfakis M, Kopacek P, Franta Z, Pedra JH, Ribeiro JM. Deep sequencing analysis of the Ixodes ricinus haemocytome. PloS Negl Trop Dis (2015) 9:e0003754. 10.1371/journal.pntd.0003754 PubMed DOI PMC
Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol (2010) 11:785–97. 10.1038/ni.1923 PubMed DOI PMC
Zhu Y, Thangamani S, Ho B, Ding JL. The ancient origin of the complement system. EMBO J (2005) 24:382–94. 10.1038/sj.emboj.7600533 PubMed DOI PMC
Sekiguchi R, Nonaka M. Evolution of the complement system in protostomes revealed by de novo transcriptome analysis of six species of Arthropoda. Dev Comp Immunol (2015) 50:58–67. 10.1016/j.dci.2014.12.008 PubMed DOI
Kawabata S. Immunocompetent molecules and their response network in horseshoe crabs. Adv Exp Med Biol (2010) 708:122–36. 10.1007/978-1-4419-8059-5_7 PubMed DOI
Gokudan S, Muta T, Tsuda R, Koori K, Kawahara T, Seki N, et al. . Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc Natl Acad Sci USA (1999) 96:10086–91. 10.1073/pnas.96.18.10086 PubMed DOI PMC
Kawabata S, Tsuda R. Molecular basis of non-self recognition by the horseshoe crab tachylectins. Biochim Biophys Acta (2002) 1572:414–21. 10.1016/s0304-4165(02)00322-7 PubMed DOI
Zhu Y, Ng PM, Wang L, Ho B, Ding JL. Diversity in lectins enables immune recognition and differentiation of wide spectrum of pathogens. Int Immunol (2006) 18:1671–80. 10.1093/intimm/dxl101 PubMed DOI
Matsushita M. Ficolins: complement-activating lectins involved in innate immunity. J Innate Immun (2010) 2:24–32. 10.1159/000228160 PubMed DOI
Kovar V, Kopacek P, Grubhoffer L. Isolation and characterization of Dorin M, a lectin from plasma of the soft tick Ornithodoros moubata. Insect Biochem Mol Biol (2000) 30:195–205. 10.1016/s0965-1748(99)00107-1 PubMed DOI
Rego RO, Kovar V, Kopacek P, Weise C, Man P, Sauman I, et al. . The tick plasma lectin, Dorin M, is a fibrinogen-related molecule. Insect Biochem Mol Biol (2006) 36:291–9. 10.1016/j.ibmb.2006.01.008 PubMed DOI
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) 35:991–1004. 10.1016/j.ibmb.2005.04.001 PubMed DOI
Honig Mondekova H, Sima R, Urbanova V, Kovar V, Rego ROM, Grubhoffer L, et al. . Characterization of Ixodes ricinus fibrinogen-related proteins (ixoderins) discloses their function in the tick innate immunity. Front Cell Infect Microbiol (2017) 7:509. 10.3389/fcimb.2017.00509 PubMed DOI PMC
Urbanova V, Hajdusek O, Sima R, Franta Z, Honig-Mondekova H, Grunclova L, et al. . IrC2/Bf - A yeast and Borrelia responsive component of the complement system from the hard tick Ixodes ricinus. Dev Comp Immunol (2018) 79:86–94. 10.1016/j.dci.2017.10.012 PubMed DOI
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) 27:4745–56. 10.1096/fj.13-232140 PubMed DOI PMC
Perner J, Kropackova S, Kopacek P, Ribeiro JMC. Sialome diversity of ticks revealed by RNAseq of single tick salivary glands. PloS Negl Trop Dis (2018) 12:e0006410. 10.1371/journal.pntd.0006410 PubMed DOI PMC
Blandin SA, Marois E, Levashina EA. Antimalarial responses in Anopheles gambiae: from a complement-like protein to a complement-like pathway. Cell Host Microbe (2008) 3:364–74. 10.1016/j.chom.2008.05.007 PubMed DOI
Shokal U, Eleftherianos I. Evolution and function of thioester-containing proteins and the complement system in the innate immune response. Front Immunol (2017) 8:759. 10.3389/fimmu.2017.00759 PubMed DOI PMC
Stroschein-Stevenson SL, Foley E, O’Farrell PH, Johnson AD. Identification of Drosophila gene products required for phagocytosis of Candida albicans. PloS Biol (2006) 4:e4. 10.1371/journal.pbio.0040004 PubMed DOI PMC
Simpson SD, Ramsdell JS, Watson Iii WH, Chabot CC. The draft genome and transcriptome of the atlantic horseshoe crab, Limulus polyphemus. Int J Genomics (2017) 2017:7636513. 10.1155/2017/7636513 PubMed DOI PMC
Zhou Y, Liang Y, Yan Q, Zhang L, Chen D, Ruan L, et al. . The draft genome of horseshoe crab Tachypleus tridentatus reveals its evolutionary scenario and well-developed innate immunity. BMC Genomics (2020) 21:137. 10.1186/s12864-020-6488-1 PubMed DOI PMC
Saravanan T, Weise C, Sojka D, Kopacek P. Molecular cloning, structure and bait region splice variants of alpha2-macroglobulin from the soft tick Ornithodoros moubata. Insect Biochem Mol Biol (2003) 33:841–51. 10.1016/s0965-1748(03)00083-3 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. Dev Comp Immunol (2009) 33:489–98. 10.1016/j.dci.2008.09.011 PubMed DOI
Tagawa K, Yoshihara T, Shibata T, Kitazaki K, Endo Y, Fujita T, et al. . Microbe-specific C3b deposition in the horseshoe crab complement system in a C2/factor B-dependent or -independent manner. PloS One (2012) 7:e36783. 10.1371/journal.pone.0036783 PubMed DOI PMC
Le Saux A, Ng PM, Koh JJ, Low DH, Leong GE, Ho B, et al. . The macromolecular assembly of pathogen-recognition receptors is impelled by serine proteases, via their complement control protein modules. J Mol Biol (2008) 377:902–13. 10.1016/j.jmb.2008.01.045 PubMed DOI
Buresova V, Franta Z, Kopacek P. A comparison of Chryseobacterium indologenes pathogenicity to the soft tick Ornithodoros moubata and hard tick Ixodes ricinus. J Invertebr Pathol (2006) 93:96–104. 10.1016/j.jip.2006.05.006 PubMed DOI
Pospisilova T, Urbanova V, Hes O, Kopacek P, Hajdusek O, Sima R. Tracking of Borrelia afzelii transmission from infected Ixodes ricinus nymphs to mice. Infect Immun (2019) 87:e00896–18. 10.1128/IAI.00896-18 PubMed DOI PMC
Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, et al. . Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ (2018) 25:486–541. 10.1038/s41418-017-0012-4 PubMed DOI PMC
Ashida H, Mimuro H, Ogawa M, Kobayashi T, Sanada T, Kim M, et al. . Cell death and infection: a double-edged sword for host and pathogen survival. J Cell Biol (2011) 195:931–42. 10.1083/jcb.201108081 PubMed DOI PMC
Steinert S, Levashina EA. Intracellular immune responses of dipteran insects. Immunol Rev (2011) 240:129–40. 10.1111/j.1600-065X.2010.00985.x PubMed DOI
Cooper DM, Mitchell-Foster K. Death for survival: what do we know about innate immunity and cell death in insects? Invertebr Surv J (2011) 8:162–72. 10.1111/j.1600-065X.2011.01040.x DOI
Kuo CJ, Hansen M, Troemel E. Autophagy and innate immunity: insights from invertebrate model organisms. Autophagy (2018) 14:233–42. 10.1080/15548627.2017.1389824 PubMed DOI PMC
Moy RH, Cherry S. Antimicrobial autophagy: a conserved innate immune response in Drosophila. J Innate Immun (2013) 5:444–55. 10.1159/000350326 PubMed DOI PMC
Yano T, Mita S, Ohmori H, Oshima Y, Fujimoto Y, Ueda R, et al. . Autophagic control of Listeria through intracellular innate immune recognition in Drosophila. Nat Immunol (2008) 9:908–16. 10.1038/ni.1634 PubMed DOI PMC
Shelly S, Lukinova N, Bambina S, Berman A, Cherry S. Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity (2009) 30:588–98. 10.1016/j.immuni.2009.02.009 PubMed DOI PMC
Nakamoto M, Moy RH, Xu J, Bambina S, Yasunaga A, Shelly SS, et al. . Virus recognition by Toll-7 activates antiviral autophagy in Drosophila. Immunity (2012) 36:658–67. 10.1016/j.immuni.2012.03.003 PubMed DOI PMC
Echavarria-Consuegra L, Smit JM, Reggiori F. Role of autophagy during the replication and pathogenesis of common mosquito-borne flavi- and alphaviruses. Open Biol (2019) 9:190009. 10.1098/rsob.190009 PubMed DOI PMC
Umemiya R, Matsuo T, Hatta T, Sakakibara S, Boldbaatar D, Fujisaki K. Autophagy-related genes from a tick, Haemaphysalis longicornis. Autophagy (2008) 4:79–81. 10.4161/auto.5143 PubMed DOI
Kawano S, Umemiya-Shirafuji R, Boldbaatar D, Matsuoka K, Tanaka T, Fujisaki K. Cloning and characterization of the autophagy-related gene 6 from the hard tick, Haemaphysalis longicornis. Parasitol Res (2011) 109:1341–9. 10.1007/s00436-011-2429-x PubMed DOI
Wang XR, Kurtti TJ, Oliver JD, Munderloh UG. The identification of tick autophagy-related genes in Ixodes scapularis responding to amino acid starvation. Ticks Tick Borne Dis (2020) 11:101402. 10.1016/j.ttbdis.2020.101402 PubMed DOI PMC
Moura-Martiniano NO, Machado-Ferreira E, Gazeta GS, Soares CAG. Relative transcription of autophagy-related genes in Amblyomma sculptum and Rhipicephalus microplus ticks. Exp Appl Acarol (2017) 73:401–28. 10.1007/s10493-017-0193-z PubMed DOI
Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol (2007) 35:495–516. 10.1080/01926230701320337 PubMed DOI PMC
Nainu F, Tanaka Y, Shiratsuchi A, Nakanishi Y. Protection of insects against viral infection by apoptosis-dependent phagocytosis. J Immunol (2015) 195:5696–706. 10.4049/jimmunol.1500613 PubMed DOI
Ocampo CB, Caicedo PA, Jaramillo G, Ursic Bedoya R, Baron O, Serrato IM, et al. . Differential expression of apoptosis related genes in selected strains of Aedes aegypti with different susceptibilities to Dengue virus. PloS One (2013) 8:e61187. 10.1371/journal.pone.0061187 PubMed DOI PMC
Vaidyanathan R, Scott TW. Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis (2006) 11:1643–51. 10.1007/s10495-006-8783-y PubMed DOI
Alberdi P, Mansfield KL, Manzano-Roman R, Cook C, Ayllon N, Villar M, et al. . Tissue-specific signatures in the transcriptional response to Anaplasma phagocytophilum Infection of Ixodes scapularis and Ixodes ricinus tick cell lines. Front Cell Infect Microbiol (2016) 6:20. 10.3389/fcimb.2016.00020 PubMed DOI PMC
Lamkanfi M, Dixit VM. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe (2010) 8:44–54. 10.1016/j.chom.2010.06.007 PubMed DOI
Slonchak A, Hugo LE, Freney ME, Hall-Mendelin S, Amarilla AA, Torres FJ, et al. . Zika virus noncoding RNA suppresses apoptosis and is required for virus transmission by mosquitoes. Nat Commun (2020) 11:2205. 10.1038/s41467-020-16086-y PubMed DOI PMC
Alberdi P, Ayllon N, Cabezas-Cruz A, Bell-Sakyi L, Zweygarth E, Stuen S, et al. . Infection of Ixodes spp. tick cells with different Anaplasma phagocytophilum isolates induces the inhibition of apoptotic cell death. Ticks Tick Borne Dis (2015) 6:758–67. 10.1016/j.ttbdis.2015.07.001 PubMed DOI
Ayllon N, Villar M, Busby AT, Kocan KM, Blouin EF, Bonzon-Kulichenko E, et al. . Anaplasma phagocytophilum inhibits apoptosis and promotes cytoskeleton rearrangement for infection of tick cells. Infect Immun (2013) 81:2415–25. 10.1128/IAI.00194-13 PubMed DOI PMC
Ayllon N, Villar M, Galindo RC, Kocan KM, Sima R, Lopez JA, et al. . Systems biology of tissue-specific response to Anaplasma phagocytophilum reveals differentiated apoptosis in the tick vector Ixodes scapularis. PloS Genet (2015) 11:e1005120. 10.1371/journal.pgen.1005120 PubMed DOI PMC
Rikihisa Y. Anaplasma phagocytophilum and Ehrlichia chaffeensis: subversive manipulators of host cells. Nat Rev Microbiol (2010) 8:328–39. 10.1038/nrmicro2318 PubMed DOI
Martins LA, Palmisano G, Cortez M, Kawahara R, de Freitas Balanco JM, Fujita A, et al. . The intracellular bacterium Rickettsia rickettsii exerts an inhibitory effect on the apoptosis of tick cells. Parasit Vectors (2020) 13:603. 10.1186/s13071-020-04477-5 PubMed DOI PMC
Berthelet J, Dubrez L. Regulation of apoptosis by inhibitors of apoptosis (IAPs). Cells (2013) 2:163–87. 10.3390/cells2010163 PubMed DOI PMC
Orme M, Meier P. Inhibitor of apoptosis proteins in Drosophila: gatekeepers of death. Apoptosis (2009) 14:950–60. 10.1007/s10495-009-0358-2 PubMed DOI
Gesellchen V, Kuttenkeuler D, Steckel M, Pelte N, Boutros M. An RNA interference screen identifies inhibitor of apoptosis protein 2 as a regulator of innate immune signalling in Drosophila. EMBO Rep (2005) 6:979–84. 10.1038/sj.embor.7400530 PubMed DOI PMC
Huh JR, Foe I, Muro I, Chen CH, Seol JH, Yoo SJ, et al. . The Drosophila inhibitor of apoptosis (IAP) DIAP2 is dispensable for cell survival, required for the innate immune response to gram-negative bacterial infection, and can be negatively regulated by the reaper/hid/grim family of IAP-binding apoptosis inducers. J Biol Chem (2007) 282:2056–68. 10.1074/jbc.M608051200 PubMed DOI
Kleino A, Valanne S, Ulvila J, Kallio J, Myllymaki H, Enwald H, et al. . Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J (2005) 24:3423–34. 10.1038/sj.emboj.7600807 PubMed DOI PMC
Leulier F, Lhocine N, Lemaitre B, Meier P. The Drosophila inhibitor of apoptosis protein DIAP2 functions in innate immunity and is essential to resist gram-negative bacterial infection. Mol Cell Biol (2006) 26:7821–31. 10.1128/MCB.00548-06 PubMed DOI PMC
Severo MS, Choy A, Stephens KD, Sakhon OS, Chen G, Chung DW, et al. . The E3 ubiquitin ligase XIAP restricts Anaplasma phagocytophilum colonization of Ixodes scapularis ticks. J Infect Dis (2013) 11:1830–40. 10.1093/infdis/jit380 PubMed DOI PMC
Bonnet SI, Binetruy F, Hernandez-Jarguin AM, Duron O. The tick microbiome: why non-pathogenic microorganisms matter in tick biology and pathogen transmission. Front Cell Infect Microbiol (2017) 7:236. 10.3389/fcimb.2017.00236 PubMed DOI PMC
Narasimhan S, Schuijt TJ, Abraham NM, Rajeevan N, Coumou J, Graham M, et al. . Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization. Nat Commun (2017) 8:184. 10.1038/s41467-017-00208-0 PubMed DOI PMC
Duron O, Binetruy F, Noel V, Cremaschi J, McCoy KD, Arnathau C, et al. . Evolutionary changes in symbiont community structure in ticks. Mol Ecol (2017) 26:2905–21. 10.1111/mec.14094 PubMed DOI
Pavanelo DB, Schroder NCH, Pin Viso ND, Martins LA, Malossi CD, Galletti M, et al. . Comparative analysis of the midgut microbiota of two natural tick vectors of Rickettsia rickettsii. Dev Comp Immunol (2020) 106:103606. 10.1016/j.dci.2019.103606 PubMed DOI
Barletta A, Nascimento-Silva M, Talyuli O, Oliveira J, Pereira L, Oliveira P, et al. . Microbiota activates IMD pathway and limits Sindbis infection in Aedes aegypti. Parasit Vectors (2017) 10:103. 10.1186/s13071-017-2040-9 PubMed DOI PMC
Xiao X, Yang L, Pang X, Zhang R, Zhu Y, Wang P, et al. . A Mesh-Duox pathway regulates homeostasis in the insect gut. Nat Microbiol (2017) 2:17020. 10.1038/nmicrobiol.2017.20 PubMed DOI PMC
Oliveira JH, Goncalves RL, Lara FA, Dias FA, Gandara AC, Menna-Barreto RF, et al. . Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PloS Pathog (2011) 7:e1001320. 10.1371/journal.ppat.1001320 PubMed DOI PMC
Pang X, Xiao X, Liu Y, Zhang R, Liu J, Liu Q, et al. . Mosquito C-type lectins maintain gut microbiome homeostasis. Nat Microbiol (2016) 1:16023. 10.1038/nmicrobiol.2016.23 PubMed DOI
Caragata E, Tikhe C, Dimopoulos G. Curious entanglements: interactions between mosquitoes, their microbiota, and arboviruses. Curr Opin Virol (2019) 37:26–36. 10.1016/j.coviro.2019.05.005 PubMed DOI PMC
Moreno-García M, Vargas V, Ramírez-Bello I, Hernández-Martínez G, Lanz-Mendoza H. Bacterial exposure at the larval stage induced sexual immune dimorphism and priming in adult Aedes aegypti mosquitoes. PloS One (2015) 10:e0133240. 10.1371/journal.pone.0133240 PubMed DOI PMC
Dickson L, Jiolle D, Minard G, Moltini-Conclois I, Volant S, Ghozlane A, et al. . Carryover effects of larval exposure to different environmental bacteria drive adult trait variation in a mosquito vector. Sci Adv (2017) 3:e1700585. 10.1126/sciadv.1700585 PubMed DOI PMC
Moltini-Conclois I, Stalinski R, Tetreau G, Després L, Lambrechts L. Larval exposure to the bacterial insecticide Bti enhances Dengue virus susceptibility of adult Aedes aegypti mosquitoes. Insects (2018) 9:193. 10.3390/insects9040193 PubMed DOI PMC
Tetreau G, Grizard S, Patil C, Tran F, Tran Van V, Stalinski R, et al. . Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis. Parasit Vectors (2018) 11:121. 10.1186/s13071-018-2741-8 PubMed DOI PMC
Zug R, Hammerstein P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PloS One (2012) 7:e38544. 10.1371/journal.pone.0038544 PubMed DOI PMC
Caragata E, Dutra H, Moreira L. Exploiting intimate relationships: controlling mosquito-transmitted disease with Wolbachia. Trends Parasitol (2016) 32:207–18. 10.1016/j.pt.2015.10.011 PubMed DOI
Bian G, Xu Y, Lu P, Xie Y, Xi Z. The endosymbiotic bacterium Wolbachia induces resistance to Dengue virus in Aedes aegypti. PloS Pathog (2010) 6:e1000833. 10.1371/journal.ppat.1000833 PubMed DOI PMC
Hoffmann A, Montgomery B, Popovici J, Iturbe-Ormaetxe I, Johnson P, Muzzi F, et al. . Successful establishment of Wolbachia in Aedes populations to suppress Dengue transmission. Nature (2011) 476:454–7. 10.1038/nature10356 PubMed DOI
Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, et al. . The wMel Wolbachia strain blocks Dengue and invades caged Aedes aegypti populations. Nature (2011) 476:450–3. 10.1038/nature10355 PubMed DOI
Dutra H, Dos Santos L, Caragata E, Silva J, Villela D, Maciel-de-Freitas R, et al. . From lab to field: the influence of urban landscapes on the invasive potential of Wolbachia in Brazilian Aedes aegypti mosquitoes. PloS Negl Trop Dis (2015) 9:e0003689. 10.1371/journal.pntd.0003689 PubMed DOI PMC
Caragata E, Rocha M, Pereira T, Mansur S, Dutra H, Moreira L. Pathogen blocking in Wolbachia-infected Aedes aegypti is not affected by Zika and Dengue virus co-infection. PloS Negl Trop Dis (2019) 13:e0007443. 10.1371/journal.pntd.0007443 PubMed DOI PMC
Andreotti R, Perez de Leon AA, Dowd SE, Guerrero FD, Bendele KG, Scoles GA. Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol (2011) 11:6. 10.1186/1471-2180-11-6 PubMed DOI PMC
Cerutti F, Modesto P, Rizzo F, Cravero A, Jurman I, Costa S, et al. . The microbiota of hematophagous ectoparasites collected from migratory birds. PloS One (2018) 13:e0202270. 10.1371/journal.pone.0202270 PubMed DOI PMC
Estrada-Peña A, Cabezas-Cruz A, Obregón D. Resistance of tick gut microbiome to anti-tick vaccines, pathogen infection and antimicrobial peptides. Pathogens (2020) 9:309. 10.3390/pathogens9040309 PubMed DOI PMC
Ross BD, Hayes B, Radey MC, Lee X, Josek T, Bjork J, et al. . Ixodes scapularis does not harbor a stable midgut microbiome. ISME J (2018) 12:2596–607. 10.1038/s41396-018-0161-6 PubMed DOI PMC
Kurokawa C, Lynn GE, Pedra JHF, Pal U, Narasimhan S, Fikrig E. Interactions between Borrelia burgdorferi and ticks. Nat Rev Microbiol (2020) 18:1–14. 10.1038/s41579-020-0400-5 PubMed DOI PMC
Guizzo MG, Neupane S, Kucera M, Perner J, Frantova H, da Silva Vaz I, et al. . Poor unstable midgut microbiome of hard ticks contrasts with abundant and stable monospecific microbiome in ovaries. Front Cell Infect Microbiol (2020) 10:211. 10.3389/fcimb.2020.00211 PubMed DOI PMC
Guizzo MG, Parizi LF, Nunes RD, Schama R, Albano RM, Tirloni L, et al. . A Coxiella mutualist symbiont is essential to the development of Rhipicephalus microplus. Sci Rep (2017) 7:17554. 10.1038/s41598-017-17309-x PubMed DOI PMC
Gall CA, Reif KE, Scoles GA, Mason KL, Mousel M, Noh SM, et al. . The bacterial microbiome of Dermacentor andersoni ticks influences pathogen susceptibility. ISME J (2016) 10:1846–55. 10.1038/ismej.2015.266 PubMed DOI PMC
Clayton KA, Gall CA, Mason KL, Scoles GA, Brayton KA. The characterization and manipulation of the bacterial microbiome of the Rocky Mountain wood tick, Dermacentor andersoni. Parasit Vectors (2015) 8:632. 10.1186/s13071-015-1245-z PubMed DOI PMC
Labruna MB, Ogrzewalska M, Martins TF, Pinter A, Horta MC. Comparative susceptibility of larval stages of Amblyomma aureolatum, Amblyomma cajennense, and Rhipicephalus sanguineus to infection by Rickettsia rickettsii. J Med Entomol (2008) 45:1156–9. 10.1603/0022-2585(2008)45[1156:csolso]2.0.co;2 PubMed DOI
Martins LA, Galletti M, Ribeiro JM, Fujita A, Costa FB, Labruna MB, et al. . The distinct transcriptional response of the midgut of Amblyomma sculptum and Amblyomma aureolatum ticks to Rickettsia rickettsii correlates to their differences in susceptibility to infection. Front Cell Infect Microbiol (2017) 7:129. 10.3389/fcimb.2017.00129 PubMed DOI PMC
Cooper D, Eleftherianos I. Memory and specificity in the insect immune system: current perspectives and future challenges. Front Immunol (2017) 8:539. 10.3389/fimmu.2017.00539 PubMed DOI PMC
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