Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy, práce podpořená grantem
PubMed
28439499
PubMed Central
PMC5383669
DOI
10.3389/fcimb.2017.00114
Knihovny.cz E-zdroje
- Klíčová slova
- Anaplasma, Babesia, Borrelia, flavivirus, immunology, microbiome, tick, vaccine,
- MeSH
- arachnida jako vektory mikrobiologie parazitologie virologie MeSH
- interakce hostitele a patogenu * MeSH
- klíšťata mikrobiologie parazitologie fyziologie virologie MeSH
- lidé MeSH
- nemoci přenášené klíšťaty epidemiologie MeSH
- přenos infekční nemoci * MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
Ticks and the pathogens they transmit constitute a growing burden for human and animal health worldwide. Vector competence is a component of vectorial capacity and depends on genetic determinants affecting the ability of a vector to transmit a pathogen. These determinants affect traits such as tick-host-pathogen and susceptibility to pathogen infection. Therefore, the elucidation of the mechanisms involved in tick-pathogen interactions that affect vector competence is essential for the identification of molecular drivers for tick-borne diseases. In this review, we provide a comprehensive overview of tick-pathogen molecular interactions for bacteria, viruses, and protozoa affecting human and animal health. Additionally, the impact of tick microbiome on these interactions was considered. Results show that different pathogens evolved similar strategies such as manipulation of the immune response to infect vectors and facilitate multiplication and transmission. Furthermore, some of these strategies may be used by pathogens to infect both tick and mammalian hosts. Identification of interactions that promote tick survival, spread, and pathogen transmission provides the opportunity to disrupt these interactions and lead to a reduction in tick burden and the prevalence of tick-borne diseases. Targeting some of the similar mechanisms used by the pathogens for infection and transmission by ticks may assist in development of preventative strategies against multiple tick-borne diseases.
Animal and Plant Health AgencySurrey UK
Biology Centre Czech Academy of Sciences Institute of ParasitologyCeske Budejovice Czechia
Department of Microbiology Medical School Aristotle University of ThessalonikiThessaloniki Greece
Facultad de Veterinaria Universidad de ZaragozaZaragoza Spain
Faculty of Health and Medicine University of SurreyGuildford UK
Faculty of Science University of South BohemiaČeské Budějovice Czechia
Institute for Parasitology and Tropical Veterinary Medicine Freie Universität BerlinBerlin Germany
Institute of Infection and Global Health University of LiverpoolLiverpool UK
SaBio Instituto de Investigación en Recursos Cinegéticos CSIC UCLM JCCMCiudad Real Spain
Zobrazit více v PubMed
Abraham N. M., Liu L., Jutras B. L., Yadav A. K., Narasimhan S., Gopalakrishnan V., et al. (2017). Pathogen-mediated manipulation of arthropod microbiota to promote infection. Proc. Natl. Acad. Sci. U.S.A. 114, E781–E790. 10.1073/pnas.1613422114 PubMed DOI PMC
Ahantarig A., Trinachartvanit W., Baimai V., Grubhoffer L. (2013). Hard ticks and their bacterial endosymbionts (or would be pathogens). Folia. Microbiol. 58, 419–428. 10.1007/s12223-013-0222-1 PubMed DOI
Alberdi P., Mansfield K. L., Manzano-Román R., Cook C., Ayllón N., Villar M., et al. (2016). Tissue-specific signatures in the transcriptional response to PubMed DOI PMC
Almazán C., Kocan K. M., Blouin E. F., de la Fuente J. (2005). Vaccination with recombinant tick antigens for the control of PubMed DOI
Andreotti R., Perez de Leon A. A., Dowd S. E., Guerrero F. D., Bendele K. G., Scoles G. A. (2011). Assessment of bacterial diversity in the cattle tick PubMed DOI PMC
Antunes S., Galindo R. C., Almazán C., Rudenko N., Golovchenko M., Grubhoffer L., et al. (2012). Functional genomics studies of PubMed DOI
Ashida H., Mimuro H., Ogawa M., Kobayashi T., Sanada T., Kim M., et al. (2011). Host-pathogen interactions cell death and infection: a double-edged sword for host and pathogen survival. J. Cell. Biol. 195, 931–942. 10.1083/jcb.201108081 PubMed DOI PMC
Ayllón N., Naranjo V., Hajdušek O., Villar M., Galindo R. C., Kocan K. M., et al. (2015b). Nuclease Tudor-SN is involved in tick dsRNA-mediated RNA interference and feeding but not in defense against flaviviral or PubMed DOI PMC
Ayllón N., Villar M., Busby A. T., Kocan K. M., Blouin E., Bonzón-Kulichenko E. F., et al. (2013). PubMed DOI PMC
Ayllón N., Villar M., Galindo R. C., Kocan K. M., Šíma R., López J. A., et al. (2015a). Systems biology of tissue-specific response to PubMed DOI PMC
Baldridge G. D., Burkhardt N. Y., Simser J. A., Kurtti T. J., Munderloh U. G. (2004). Sequence and expression analysis of the ompA gene of PubMed DOI PMC
Baxter R. H., Contet A., Krueger K. (2017). Arthropod innate immune systems and vector-borne diseases. Biochemistry. 56, 907–918. 10.1021/acs.biochem.6b00870 PubMed DOI PMC
Beerntsen B. T., James A. A., Christensen B. M. (2000). Genetics of mosquito vector competence. Microbiol. Mol. Biol. Rev. 64, 115–137. 10.1128/MMBR.64.1.115-137.2000 PubMed DOI PMC
Bell-Sakyi L., Zweygarth E., Blouin E. F., Gould E. A., Jongejan F. (2007). Tick cell lines: tools for tick and tick-borne disease research. Trends. Parasitol. 23, 450–457. 10.1016/j.pt.2007.07.009 PubMed DOI
Bernasconi M. V., Casati S., Peter O., Piffaretti J. C. (2002). PubMed DOI
Bohacsova M., Mediannikov O., Kazimirova M., Raoult D., Sekeyova Z. (2016). PubMed DOI PMC
Bonnet S., de la Fuente J., Nicollet P., Liu X., Madani N., Blanchard B., et al. (2013). Prevalence of tick-borne pathogens in adult PubMed DOI
Burgdorfer W., Hayes S., Mavros A. (1981). Non-pathogenic rickettsiae in
Busby A. T., Ayllón N., Kocan K. M., Blouin E. F., de la Fuente G., Galindo R. C., et al. (2012). Expression of heat-shock proteins and subolesin affects stress responses, PubMed DOI
Cabezas-Cruz A., Alberdi P., Ayllón N., Valdés J. J., Pierce R., Villar M., et al. (2016). PubMed DOI PMC
Cabezas-Cruz A., Estrada-Peña A., Rego R. O. M., De la Fuente J. (2017). Tick-pathogen ensembles: do molecular interactions lead ecological innovation? Front. Cell. Infect. Microbiol. 7:74. 10.3389/fcimb.2017.00074 PubMed DOI PMC
Chauvin A., Moreau E., Bonnet S., Plantard O., Malandrin L. (2009). Babesia and its hosts: adaptation to long-lasting interactions as a way to achieve efficient transmission. Vet. Res. 40, 37. 10.1051/vetres/2009020 PubMed DOI PMC
Clay K., Klyachko O., Grindle N., Civitello D., Oleske D., Fuqua C. (2008). Microbial communities and interactions in the lone star tick, PubMed DOI
Cooper A., Stephens J., Ketheesan N., Govan B. (2013). Detection of PubMed DOI
Cotté V., Sabatier L., Schnell G., Carmi-Leroy A., Rousselle J. C., Arsène-Ploetze F., et al. (2014). Differential expression of PubMed DOI
Coumou J., Narasimhan S., Trentelman J. J., Wagemakers A., Koetsveld J., Ersoz J. I., et al. (2016). PubMed DOI PMC
Cramaro W. J., Revets D., Hunewald O. E., Sinner R., Reye A. L., Muller C. P. (2015). Integration of PubMed DOI PMC
Dai J., Narasimhan S., Zhang L., Liu L., Wang P., Fikrig E. (2010). Tick histamine release factor is critical for PubMed DOI PMC
de Castro M. H., de Klerk D., Pienaar R., Latif A. A., Rees D. J., Mans B. J. (2016). PubMed DOI
de la Fuente J., Blouin E. F., Kocan K. M. (2003). Infection exclusion of the rickettsial pathogen PubMed DOI PMC
de la Fuente J., Contreras M. (2015). Tick vaccines: current status and future directions. Expert Rev. Vaccines 14, 1367–1376. 10.1586/14760584.2015.1076339 PubMed DOI
de la Fuente J., Estrada-Peña A., Cabezas-Cruz A., Brey R. (2015). Flying ticks: anciently evolved associations that constitute a risk of infectious disease spread. Parasit Vectors 8, 538. 10.1186/s13071-015-1154-1 PubMed DOI PMC
de la Fuente J., Estrada-Peña A., Cabezas-Cruz A., Kocan K. M. (2016). PubMed DOI
de la Fuente J., Estrada-Peña A., Venzal J. M., Kocan K. M., Sonenshine D. E. (2008). Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front. Biosci. 13, 6938–6946. 10.2741/3200 PubMed DOI
de la Fuente J., Garcia-Garcia J. C., Blouin E. F., McEwen B. R., Clawson D., Kocan K. M. (2001). Major surface protein 1a effects tick infection and transmission of PubMed DOI
de la Fuente J., Kocan K. M. (2014). Development of vaccines for control of tick infestations and interruption of pathogen transmission, in Biology of Ticks, 2nd Edn., ed Sonenshine D., Roe M. (New York, NY: Oxford University Press; ), 333–352.
de la Fuente J., Kocan K. M., Almazán C., Blouin E. F. (2007). RNA interference for the study and genetic manipulation of ticks. Trends Parasitol. 23, 427–433. 10.1016/j.pt.2007.07.002 PubMed DOI
Dergousoff S. J., Chilton N. B. (2010). Detection of a new Arsenophonus-type bacterium in Canadian populations of the Rocky Mountain wood tick, PubMed DOI
Dickson D. L., Turell M. J. (1992). Replication and tissue tropisms of Crimean-Congo hemorrhagic fever virus in experimentally infected adult PubMed DOI
Doherty P. C., Reid H. W. (1971). Experimental louping ill in the sheep. II, Neuropathology. J. Comp. Pathol. 81, 331–337. 10.1016/0021-9975(71)90020-X PubMed DOI
Eng M. W., van Zuylen M. N., Severson D. W. (2016). Apoptosis-related genes control autophagy and influence DENV-2 infection in the mosquito vector, PubMed DOI PMC
Engelstadter J., Hurst G. D. (2007). The impact of male-killing bacteria on host evolutionary processes. Genetics 175, 245–254. 10.1534/genetics.106.060921 PubMed DOI PMC
Estrada-Peña A., de la Fuente J., Ostfeld R. S., Cabezas-Cruz A. (2015). Interactions between tick and transmitted pathogens evolved to minimise competition through nested and coherent networks. Sci. Rep. 5:10361. 10.1038/srep10361 PubMed DOI PMC
Estrada-Peña A., Ortega C., Sánchez N., Desimone L., Sudre B., Suk J. E., et al. (2011). Correlation of PubMed DOI PMC
Florin-Christensen M., Schnittger L. (2009). Piroplasmids and ticks: a long-lasting intimate relationship. Front. Biosci. 14, 3064–3073. 10.2741/3435 PubMed DOI
Garcia-Garcia J. C., Barat N. C., Trembley S. J., Dumler J. S. (2009a). Epigenetic silencing of host cell defense genes enhances intracellular survival of the rickettsial pathogen PubMed DOI PMC
Garcia-Garcia J. C., Rennoll-Bankert K. E., Pelly S., Milstone A. M., Dumler J. S. (2009b). Silencing of host cell CYBB gene expression by the nuclear effector AnkA of the intracellular pathogen PubMed DOI PMC
Garg R., Juncadella I. J., Ramamoorthi N., Ananthanarayanan S. K., Thomas V., Rincón M., et al. (2006). Cutting edge: CD4 is the receptor for the tick saliva immunosuppressor, Salp15. J. Immunol. 177, 6579–6583. 10.4049/jimmunol.177.10.6579 PubMed DOI PMC
Garrison A. R., Radoshitzky S. R., Kota K. P., Pegoraro G., Ruthel G., et al. (2013). Crimean-Congo hemorrhagic fever virus utilizes a clathrin- and early endosome-dependent entry pathway. Virology 444, 45–54. 10.1016/j.virol.2013.05.030 PubMed DOI
Gerold G., Bruening J., Weigel B., Pietschmann T. (2017). Protein interactions during the flavivirus and hepacivirus life cycle. Mol. Cell. Proteomics 16(4 Suppl. 1), S75–S91. 10.1074/mcp.r116.065649 PubMed DOI PMC
Gomes-Solecki M. (2014). Blocking pathogen transmission at the source: reservoir targeted OspA-based vaccines against PubMed DOI PMC
Gómez-Díaz E., Jordà M., Peinado M. A., Rivero A. (2012). Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog. 8:e1003007. 10.1371/journal.ppat.1003007 PubMed DOI PMC
Gulia-Nuss M., Nuss A. B., Meyer J. M., Sonenshine D. E., Roe R. M., Waterhouse R. M., et al. (2016). Genomic insights into the PubMed DOI PMC
Hajdušek O., Síma R., Ayllón N., Jalovecká M., Perner J., de la Fuente J., et al. (2013). Interaction of the tick immune system with transmitted pathogens. Front. Cell Infect Microbiol. 3:26. 10.3389/fcimb.2013.00026 PubMed DOI PMC
Harrus S., Perlman-Avrahami A., Mumcuoglu K. Y., Morick D., Eyal O., Baneth G. (2011). Molecular detection of PubMed DOI
Heekin A. M., Guerrero F. D., Bendele K. G., Saldivar L., Scoles G. A., Dowd S. E., et al. (2013). The ovarian transcriptome of the cattle tick, PubMed DOI PMC
Heekin A. M., Guerrero F. D., Bendele K. G., Saldivar L., Scoles G. A., Gondro C., et al. (2012). Analysis of PubMed DOI PMC
Hermann C., Gern L. (2010). Survival of PubMed DOI
Herrmann C., Gern L. (2012). Do the level of energy reserves, hydration status and Borrelia infection influence walking by Ixodes ricinus (Acari: Ixodidae) ticks? Parasitology 139, 330–337. 10.1017/S0031182011002095 PubMed DOI
Hourcade D. E., Akk A. M., Mitchell L. M., Zhou H. F., Hauhart R., et al. (2016). Anti-complement activity of the PubMed DOI PMC
Ireton K. (2013). Molecular mechanisms of cell-cell spread of intracellular bacterial pathogens. Open Biol. 3:130079. 10.1098/rsob.130079 PubMed DOI PMC
Ivanov I. N., Mitkova N., Reye A. L., Hübschen J. M., Vatcheva-Dobrevska R. S., Dobreva E. G., et al. (2011). Detection of new Francisella-like tick endosymbionts in PubMed DOI PMC
Johnson N., Voller K., Phipps L. P., Mansfield K. L., Fooks A. R. (2012). Rapid molecular detection methods for arboviruses of livestock of importance to Northern Europe. J. Biomed. Biotechnol. 2012:719402. 10.1155/2012/719402 PubMed DOI PMC
Jongejan F., Uilenberg G. (2004). The global importance of ticks. Parasitology 129(Suppl.), S3–S14. 10.1017/S0031182004005967 PubMed DOI
Kagemann J., Clay K. (2013). Effects of infection by Arsenophonus and Rickettsia bacteria on the locomotive ability of the ticks PubMed DOI
Kleiboeker S., Scoles G. A., Burrage T. G., Sur J. (1999). African swine fever virus replication in the midgut epithelium is required for infection of Ornithodoros ticks. J. Virol. 73, 8587–8598. PubMed PMC
Klyachko O., Stein B. D., Grindle N., Clay K., Fuqua C. (2007). Localization and visualization of a coxiella-type symbiont within the lone star tick, PubMed DOI PMC
Kotsyfakis M., Schwarz A., Erhart J., Ribeiro J. M. (2015). Tissue-and time-dependent transcription in PubMed DOI PMC
Kung F., Anguita J., Pal U. (2013). PubMed DOI PMC
Labuda M., Nuttall P. A. (2003). Tick-borne viruses. Parasitology 129, S221–S245. 10.1017/S0031182004005220 PubMed DOI
Lee J. H., Park H. S., Jang W. J., Koh S. E., Park T. K., Kang S. S., et al. (2004). Identification of the PubMed DOI
Liu L. M., Liu J. N., Liu Z., Yu Z. J., Xu S. Q., Yang X. H., et al. (2013). Microbial communities and symbionts in the hard tick PubMed DOI PMC
Lo N., Beninati T., Sassera D., Bouman E. A., Santagati S., Gern L., et al. (2006). Widespread distribution and high prevalence of an alpha-proteobacterial symbiont in the tick PubMed DOI
Lu P., Zhou Y., Yu Y., Cao J., Zhang H., Gong H., et al. (2016). RNA interference and the vaccine effect of a subolesin homolog from the tick PubMed DOI
Macaluso K. R., Sonenshine D. E., Ceraul S. M., Azad A. F. (2002). Rickettsial infection in PubMed DOI
Mansfield K. L., Cook C., Ellis R., Bell-Sakyi L., Johnson N., Alberdi P., et al. (2017). Tick-borne pathogens induce differential expression of genes promoting cell survival and host resistence in PubMed DOI PMC
Mansfield K. L., Johnson N., Banyard A. C., Núñez A., Baylis M., Solomon T., et al. (2016). Innate and adaptive immune responses to tick-borne flavivirus infection in sheep. Vet. Microbiol. 185, 20–28. 10.1016/j.vetmic.2016.01.015 PubMed DOI
Martinez J., Longdon B., Bauer S., Chan Y. S., Miller W. J., Bourtzis K., et al. (2014). Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS Pathog. 10:e1004369. 10.1371/journal.ppat.1004369 PubMed DOI PMC
Mather T. N., Ribeiro J. M., Spielman A. (1987). Lyme disease and babesiosis: acaricide focused on potentially infected ticks. Am. J. Trop. Med. Hyg. 36, 609–614. PubMed
Merino O., Antunes S., Mosqueda J., Moreno-Cid J. A., Pérez de la Lastra J. M., et al. (2013). Vaccination with proteins involved in tick-pathogen interactions reduces vector infestations and pathogen infection. Vaccine 31, 5889–5896. 10.1016/j.vaccine.2013.09.037 PubMed DOI
Michelet L., Bonnet S., Madani N., Moutailler S. (2013). Discriminating PubMed DOI
Montagna M., Sassera D., Epis S., Bazzocchi C., Vannini C., Lo N., et al. (2013). PubMed DOI PMC
Naranjo V., Ayllón N., Pérez de la Lastra J. M., Galindo R. C., Kocan K. M., Blouin E. F., et al. (2013). Reciprocal regulation of NF-kB (Relish) and Subolesin in the tick vector, PubMed DOI PMC
Narasimhan S., Rajeevan N., Liu L., Zhao Y. O., Heisig J., Pan J., et al. (2014). Gut microbiota of the tick vector PubMed DOI PMC
Neelakanta G., Sultana H., Fish D., Anderson J. F., Fikrig E. (2010). PubMed DOI PMC
Nene V., Lee D., Kang'a S., Skilton R., Shah T., de Villiers E., et al. (2004). Genes transcribed in the salivary glands of female PubMed DOI
Nuttall P. A. (2014). Tick-borne viruses, in Biology of Ticks, ed Sonenshine D. E., Roe R. M. (Oxford: Oxford University Press; ), 180–210.
Pal U., Li X., Wang T., Montgomery R. R., Ramamoorthi N., Desilva A. M., et al. (2004). TROSPA, an Ixodes scapularis receptor for PubMed DOI
Papa A. (2010). Crimean-Congo hemorrhagic fever and hantavirus infections, in Tropical and Emerging Infectious Diseases, ed Maltezou H., Gikas A. (Kerala: Research Signpost; ), 49–73.
Plantard O., Bouju-Albert A., Malard M. A., Hermouet A., Capron G., Verheyden H. (2012). Detection of Wolbachia in the tick PubMed DOI PMC
Qiu Y., Nakao R., Ohnuma A., Kawamori F., Sugimoto C. (2014). Microbial population analysis of the salivary glands of ticks; a possible strategy for the surveillance of bacterial pathogens. PLoS ONE 9:e103961. 10.1371/journal.pone.0103961 PubMed DOI PMC
Rachinsky A., Guerrero F. D., Scoles G. A. (2007). Differential protein expression in ovaries of uninfected and Babesia-infected southern cattle ticks PubMed DOI
Radolf J. D., Caimano M. J., Stevenson B., Hu L. T. (2012). Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat. Rev. Microbiol. 10, 87–99. 10.1038/nrmicro2714 PubMed DOI PMC
Ramamoorthi N., Narasimhan S., Pal U., Bao F., Yang X. F., Fish D., et al. (2005). The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436, 573–577. 10.1038/nature03812 PubMed DOI PMC
Ramphul U. N., Garver L. S., Molina-Cruz A., Canepa G. E., Barillas-Mury C. (2015). PubMed DOI PMC
Reis C., Cote M., Paul R. E., Bonnet S. (2011). Questing ticks in suburban forest are infected by at least six tick-borne pathogens. Vector Borne Zoonotic Dis. 11, 907–916. 10.1089/vbz.2010.0103 PubMed DOI
Rennoll-Bankert K. E., Garcia-Garcia J. C., Sinclair S. H., Dumler J. S. (2015). Chromatin-bound bacterial effector ankyrin A recruits histone deacetylase 1 and modifies host gene expression. Cell Microbiol. 17, 1640–1652. 10.1111/cmi.12461 PubMed DOI PMC
Rollend L., Fish D., Childs J. E. (2013). Transovarial transmission of Borrelia spirochetes by PubMed DOI
Rosa P. A., Tilly K., Stewart P. E. (2005). The burgeoning molecular genetics of the Lyme disease spirochaete. Nat. Rev. Microbiol. 3, 129–143. 10.1038/nrmicro1086 PubMed DOI
Rudenko N., Golovchenko M., Edwards M. J., Grubhoffer L. (2005). Differential expression of PubMed DOI
Rynkiewicz E. C., Hemmerich C., Rusch D. B., Fuqua C., Clay K. (2015). Concordance of bacterial communities of two tick species and blood of their shared rodent host. Mol. Ecol. 24, 2566–2579. 10.1111/mec.13187 PubMed DOI
Sabin L. R., Zheng Q., Thekkat P., Yang J., Hannon G. J., Gregory B. D., et al. (2013). Dicer-2 processes diverse viral RNA species. PLoS ONE 8:e55458. 10.1371/journal.pone.0055458 PubMed DOI PMC
Sassera D., Beninati T., Bandi C., Bouman E. A., Sacchi L., Fabbi M., et al. (2006). PubMed DOI
Schnittger L., Rodriguez A. E., Florin-Christensen M., Morrison D. A. (2012). Babesia: a world emerging. Infect Genet. Evol. 12, 1788–1809. 10.1016/j.meegid.2012.07.004 PubMed DOI
Schuijt T. J., Coumou J., Narasimhan S., Dai J., Deponte K., Wouters D., et al. (2011b). A tick mannose-binding lectin inhibitor interferes with the vertebrate complement cascade to enhance transmission of the Lyme disease agent. Cell Host Microbe. 10, 136–146. 10.1016/j.chom.2011.06.010 PubMed DOI PMC
Schuijt T. J., Narasimhan S., Daffre S., DePonte K., Hovius J. W., Van't Veer C., et al. (2011a). Identification and characterization of PubMed DOI PMC
Severo M. S., Choy A., Stephens K. D., Sakhon O. S., Chen G., Chung D. W., et al. (2013). The E3 ubiquitin ligase XIAP restricts PubMed DOI PMC
Severo M. S., Pedra J. H. F., Ayllón N., Kocan K. M., de la Fuente J. (2015). Anaplasma, in Molecular Medical Microbiology, 2nd Edn., ed Tang Y. W., Sussman M., Liu D., Poxton I., Schwartzman J. (New York, NY: Academic Press; Elsevier; ), 2033–2042.
Shaw D. K., Wang X., Brown L. J., Oliva C. A. S., Reif K. E., Smith A. A., et al. (2017). Infection-derived lipids elicit an immune deficiency circuit in arthropods. Nat. Commun. 8:14401. 10.1038/ncomms14401 PubMed DOI PMC
Shih C. M., Telford S. R., III., Spielman A. (1995). Effect of ambient temperature on competence of deer ticks as hosts for Lyme disease spirochetes. J. Clin. Microbiol. 33, 958–961. PubMed PMC
Shtanko O., Nikitina R. A., Altuntas C. Z., Chepurnov A. A., Davey R. A. (2014). Crimean-Congo hemorrhagic fever virus entry into host cells occurs through the multivesicular body and requires ESCRT regulators. PLoS Pathog. 10:e1004390. 10.1371/journal.ppat.1004390 PubMed DOI PMC
Simon M., Johansson C., Mirazimi A. (2009). Crimean-Congo hemorrhagic fever virus entry and replication is clathrin-, pH- and cholesterol-dependent. J. Gen. Virol. 90(Pt 1), 210–215. 10.1099/vir.0.006387-0 PubMed DOI
Smith A. A., Navasa N., Yang X., Wilder C. N., Buyuktanir O., Marques A., et al. (2016). Cross-Species Interferon signaling boosts microbicidal activity within the tick vector. Cell Host Microbe 20, 91–98. 10.1016/j.chom.2016.06.001 PubMed DOI PMC
Steiner F. E., Pinger R. R., Vann C. N., Grindle N., Civitello D., Clay K., et al. (2008). Infection and co-infection rates of PubMed DOI
Suda Y., Fukushi S., Tani H., Murakami S., Saijo M., Horimoto T., et al. (2016). Analysis of the entry mechanism of Crimean-Congo hemorrhagic fever virus, using a vesicular stomatitis virus pseudotyping system. Arch. Virol. 161, 1447–1454. 10.1007/s00705-016-2803-1 PubMed DOI PMC
Sultana H., Neelakanta G., Kantor F. S., Malawista S. E., Fish D., Montgomery R. R., et al. (2010). PubMed DOI PMC
Tabata J., Hattori Y., Sakamoto H., Yukuhiro F., Fujii T., Kugimiya S., et al. (2011). Male killing and incomplete inheritance of a novel spiroplasma in the moth PubMed DOI
Taylor M., Mediannikov O., Raoult D., Greub G. (2012). Endosymbiotic bacteria associated with nematodes, ticks and amoebae. FEMS Immunol. Med. Microbiol. 64, 21–31. 10.1111/j.1574-695X.2011.00916.x PubMed DOI
Tully J. G., Rose D. L., Yunker C. E., Carle P., Bové J. M., Williamson D. L., et al. (1995). PubMed DOI
Turell M. J. (2007). Role of ticks in the transmission of Crimean-Congo hemorrhagic fever virus, in Crimean-Congo Hemorrhagic Fever: A Global Perspective, ed Ergonul O., Whitehouse C. A. (Dordrecht: Springer Press; ), 143–154.
Uilenberg G. (2006). Babesia-a historical overview. Vet. Parasitol. 138, 3–10. 10.1016/j.vetpar.2006.01.035 PubMed DOI
Vayssier-Taussat M., Kazimirova M., Hubalek Z., Hornok S., Farkas R., Cosson J. F., et al. (2015). Emerging horizons for tick-borne pathogens: from the “one pathogen-one disease” vision to the pathobiome paradigm. Future Microbiol. 10, 2033–2043. 10.2217/fmb.15.114 PubMed DOI PMC
Venzal J. M., Estrada-Peña A., Castro O., de Souza C. G., Félix M. L., Nava S., et al. (2008). PubMed DOI
Villar M., Ayllón N., Alberdi P., Moreno A., Moreno M., Tobes R., et al. (2015a). Integrated metabolomics, transcriptomics and proteomics identifies metabolic pathways affected by PubMed DOI PMC
Villar M., Ayllón N., Kocan K. M., Bonzón-Kulichenko E., Alberdi P., et al. (2015b). Identification and characterization of PubMed DOI PMC
Vlachou D., Schlegelmilch T., Christophides G. K., Kafatos F. C. (2005). Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr. Biol. 15, 1185–1195. 10.1016/j.cub.2005.06.044 PubMed DOI
Wagemakers A., Coumou J., Schuijt T. J., Oei A., Nijhof A. M., van 't Veer C., et al. (2016). An PubMed DOI
Wang J. L., Zhang J. L., Chen W., Xu X. F., Gao N., Fan D. Y., et al. (2010). Roles of small GTPase Rac1 in the regulation of actin cytoskeleton during dengue virus infection. PLoS Negl. Trop. Dis. 4:e809. 10.1371/journal.pntd.0000809 PubMed DOI PMC
Weisheit S., Villar M., Tykalová H., Popara M., Loecherbach J., Watson M., et al. (2015). PubMed DOI PMC
Williams-Newkirk A. J., Rowe L. A., Mixson-Hayden T. R., Dasch G. A. (2012). Presence, genetic variability, and potential significance of “ PubMed DOI PMC
Yokoyama N., Okamura M., Igarashi I. (2006). Erythrocyte invasion by Babesia parasites: current advances in the elucidation of the molecular interactions between the protozoan ligands and host receptors in the invasion stage. Vet. Parasitol. 138, 22–32. 10.1016/j.vetpar.2006.01.037 PubMed DOI
Zchori-Fein E., Bourtzis K. (2011). Manipulative Tenants: Bacteria Associated with Arthropods. New York, NY: CRC Press.
Zhang L., Zhang Y., Adusumilli S., Liu L., Narasimhan S., Dai J., et al. (2011). Molecular interactions that enable movement of the Lyme disease agent from the tick gut into the hemolymph. PLoS Pathog. 7:e1002079. 10.1371/journal.ppat.1002079 PubMed DOI PMC
Zhang X., Norris D. E., Rasgon J. L. (2011). Distribution and molecular characterization of Wolbachia endosymbionts and filarial nematodes in Maryland populations of the lone star tick ( PubMed DOI PMC
Zhong J., Jasinskas A., Barbour A. G. (2007). Antibiotic treatment of the tick vector PubMed DOI PMC
Experimental Infection of Mice and Ticks with the Human Isolate of Anaplasma phagocytophilum NY-18
The bacterial community of the lone star tick (Amblyomma americanum)
Editorial: Biological Drivers of Vector-Pathogen Interactions
Environmental and Molecular Drivers of the α-Gal Syndrome
A bite so sweet: the glycobiology interface of tick-host-pathogen interactions
Functional Evolution of Subolesin/Akirin
The Complexity of Piroplasms Life Cycles
Functional Redundancy and Ecological Innovation Shape the Circulation of Tick-Transmitted Pathogens