Tick saliva enhances powassan virus transmission to the host, influencing its dissemination and the course of disease

Journal of Virology

Volumn 89, Issue 15, 2015, Pages 7852-7860

  Hermance, Meghan E ^a   Thangamani, Saravanan ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEATH; DISEASE COURSE; DISEASE SEVERITY; FEMALE; FLAVIVIRUS INFECTION; GENE EXPRESSION PROFILING; HOST PATHOGEN INTERACTION; INOCULATION; IXODES SCAPULARIS; LYMPH NODE; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PARALYSIS; PATHOPHYSIOLOGY; POWASSAN VIRUS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SALIVA; SALIVARY GLAND; VIRAL CLEARANCE; VIRUS CONCENTRATION; VIRUS LOAD; VIRUS TRANSMISSION; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; HUMAN; IXODES; MORTALITY; PARASITE VECTOR; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; TICK BORNE ENCEPHALITIS; TICK BORNE ENCEPHALITIS VIRUS; TRANSMISSION; UNITED STATES; VIROLOGY; VIRULENCE;

IXODES SCAPULARIS; IXODIDA; MUS; POWASSAN VIRUS; TICK-BORNE FLAVIVIRUS;

ANIMALS; ARACHNID VECTORS; DISEASE PROGRESSION; ENCEPHALITIS VIRUSES, TICK-BORNE; ENCEPHALITIS, TICK-BORNE; FEMALE; HUMANS; IXODES; LYMPH NODES; MICE; MICE, INBRED BALB C; SALIVA; UNITED STATES; VIRULENCE;

EID: 84937694685     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01056-15     Document Type: Article

References (33)

1. McLean DM, Donahue W. 1959. Powassan virus: isolation of virus from a fatal case of encephalitis. Can Med Assoc J 80:708-711.
2. Hinten S, Beckett GA, Gensheimer KF, Pritchard E, Courtney TM, Sears SD, Woytowicz JM, Preston DG, Smith RP, Jr, Rand PW, Lacombe EH, Holman MS, Lubelczyk CB, Kelso PT, Beelen AP, Stobierski MG, Sotir MJ, Wong S, Ebel G, Kosoy O, Piesman J, Campbell GL, Marfin AA. 2008. Increased recognition of Powassan encephalitis in the United States, 1999-2005. Vector Borne Zoonotic Dis 8:733-740. http://dx.doi.org/10.1089/vbz.2008.0022.
3. Holbrook M, Aronson J, Campbell G, Jones J, Feldmann H, Barrett A. 2005. An animal model for the tickborne flavivirus-Omsk hemorrhagic fever virus. J Infect Dis 191:100-108. http://dx.doi.org/10.1086/426397.
4. Ebel GD. 2010. Update on Powassan virus: emergence of a North American tick-borne flavivirus. Annu Rev Entomol 55:95-110. http://dx.doi.org/10.1146/annurev-ento-112408-085446.
5. Hermance ME, Thangamani S. 2014. Proinflammatory cytokines and chemokines at the skin interface during Powassan virus transmission. J Investig Dermatol 134:2280-2283. http://dx.doi.org/10.1038/jid.2014.150.
6. Kazimirova M, Stibraniova I. 2013. Tick salivary compounds: their role in modulation of host defenses and pathogen transmission. Front Cell Infect Microbiol 3:43. http://dx.doi.org/10.3389/fcimb.2013.00043.
7. Schoeler G, Wikel S. 2001. Modulation of host immunity by haematophagous arthropods. Ann Trop Med Parasitol 95:755-771. http://dx.doi.org/10.1080/0003498012011118.
8. Wikel S. 2013 Ticks and tick-borne pathogens at the cutaneous interface: host defenses, tick countermeasures, and a suitable environment for pathogen establishment. Front Microbiol 4:337. http://dx.doi.org/10.3389/fmicb.2013.00337.
9. Brossard M, Wikel S. 2004. Tick immunobiology. Parasitology 129: S161-S176. http://dx.doi.org/10.1017/S0031182004004834.
10. Titus R, Bishop J, Mejia J. 2006. The immunomodulatory factors of arthropod saliva and the potential for these factors to serve as vaccine targets to prevent pathogen transmission. Parasite Immunol 28:131-141. http://dx.doi.org/10.1111/j.1365-3024.2006.00807.x.
11. Labuda M, Jones L, Williams T, Nuttall P. 1993. Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Med Vet Entomol 7:193-196. http://dx.doi.org/10.1111/j.1365-2915.1993.tb00674.x.
12. Jones L, Hodgson E, Nuttall P. 1989. Enhancement of virus transmission by tick salivary glands. J Gen Virol 70:1895-1898. http://dx.doi.org/10.1099/0022-1317-70-7-1895.
13. Krocová Z, Macela A, Hernychová L, Kroca M, Pechová J, Kopeckỳ J. 2003. Tick salivary gland extract accelerates proliferation of Franciscella tularensis in the host. J Parasitol 89:14-20. http://dx.doi.org/10.1645/0022-3395(2003)089[0014:TSGEAP]2.0.CO;2.
14. Horká H, Cerná-Kỳcková K, Skallová A, Kopeckỳ J. 2009. Tick saliva affects both proliferation and distribution of Borrelia burgdorferi spirochetes in mouse organs and increases transmission of spirochetes to ticks. Int J Med Microbiol 299:373-380. http://dx.doi.org/10.1016/j.ijmm.2008.10.009.
15. Heinze DM, Wikel SK, Thangamani S, Alarcon-Chaidez FJ. 2012. Transcriptional profiling of the murine cutaneous response during initial and subsequent infestations with Ixodes scapularis nymphs. Parasit Vectors 5:26. http://dx.doi.org/10.1186/1756-3305-5-26.
16. Anderson JF, Armstrong PM. 2012. Prevalence and genetic characterization of Powassan virus strains infecting Ixodes scapularis in Connecticut. Am J Trop Med Hyg 87:754-759. http://dx.doi.org/10.4269/ajtmh.2012.12-0294.
17. Schneider BS. 2006. Ph.D. dissertation. The University of Texas Graduate School of Biomedical Sciences at Galveston, Galveston, TX.
18. Heinze DM, Carmical JR, Aronson JF, Thangamani S. 2012. Early immunologic events at the tick-host interface. PLoS One 7:e47301. http://dx.doi.org/10.1371/journal.pone.0047301.
19. Zhang J, An J. 2007. Cytokines, inflammation and pain. Int Anesthesiol Clin 45:27-37. http://dx.doi.org/10.1097/AIA.0b013e318034194e.
20. Titus R, Ribeiro J. 1988. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239:1306-1308. http://dx.doi.org/10.1126/science.3344436.
21. Styer LM, Lim PY, Louie KL, Albright RG, Kramer LD, Bernard KA. 2011. Mosquito saliva causes enhancement of West Nile virus infection in mice. J Virol 85:1517-1527. http://dx.doi.org/10.1128/JVI.01112-10.
22. Schneider B, Higgs S. 2008. The enhancement of arbovirus transmission and disease by mosquito saliva is associated with modulation of the host immune response. Trans R Soc Trop Med Hyg 102:400-408. http://dx.doi.org/10.1016/j.trstmh.2008.01.024.
23. Costero A, Grayson M. 1996. Experimental transmission of Powassan virus (Flaviviridae) by Ixodes scapularis ticks (Acari: Ixodidae). Am J Trop Med Hyg 55:536-546.
24. American Committee on Arthropod-Borne Viruses. 2013. Reaction to the introduction of Chikungunya virus in St. Martin. American Society of Tropical Medicine and Hygiene, Deerfield, IL.
25. Ebel G, Kramer L. 2004. Short report: duration of tick attachment required for transmission of Powassan virus by deer ticks. Am J Trop Med Hyg 71:268-271.
26. Hayasaka D, Nagata N, Fujii Y, Hasegawa H, Sata T, Suzuki R, Gould E, Takashima I, Koike S. 2009. Mortality following peripheral infection with Tick-borne encephalitis virus results from a combination of central nervous system pathology, systemic inflammatory and stress responses. Virology 390:139-150. http://dx.doi.org/10.1016/j.virol.2009.04.026.
27. Orandle M, MacLean A, Sasseville V, Alvarez X, Lackner A. 2002. Enhanced expression of proinflammatory cytokines in the central nervous system is associated with neuroinvasion by simian immunodeficiency virus and the development of encephalitis. J Virol 76:5797-5802. http://dx.doi.org/10.1128/JVI.76.11.5797-5802.2002.
28. Wang T, Town T, Alexopoulou L, Anderson J, Fikrig E, Flavell R. 2004. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10:1366-1373. http://dx.doi.org/10.1038/nm1140.
29. Ryman K, Gardner C, Meier K, Biron C, Johnston R, Klimstra W. 2007. Early restriction of alphavirus replication and dissemination contributes to age-dependent attenuation of systemic hyperinflammatory disease. J Gen Virol 88:518-529. http://dx.doi.org/10.1099/vir.0.82359-0.
30. Nuttall P, Labuda M. 2004. Tick-host interactions: saliva-activated transmission. Parasitology 129:S177-S189. http://dx.doi.org/10.1017/S0031182004005633.
31. Kaufman W. 1989. Tick-host interaction: a synthesis of current concepts. Trends Parasitol 5:47-56.
32. McSwain J, Essenber R, Sauer J. 1982. Protein changes in the salivary glands of the female lone star tick, Amblyomma americanum, during feeding. J Parasitol 68:100-106. http://dx.doi.org/10.2307/3281330.
33. Ribeiro JM, Alarcon-Chaidez F, Francischetti IM, Mans BJ, Mather TN, Valenzuela JG, Wikel SK. 2006. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem Mol Biol 36:111-129. http://dx.doi.org/10.1016/j.ibmb.2005.11.005.