Early transcriptomic changes at the skin interface during Powassan virus transmission by ticks.

Dakota N Paine, Meghan Hermance, Saravanan Thangamani
Author Information
  1. Dakota N Paine: Department of Microbiology and Immunology, State University of New York Upstate Medical University, Syracuse, NY, United States.
  2. Meghan Hermance: Department of Microbiology and Immunology, University of South Alabama, Mobile, AL, United States.
  3. Saravanan Thangamani: Department of Microbiology and Immunology, State University of New York Upstate Medical University, Syracuse, NY, United States.

Abstract

Introduction: Powassan virus (POWV), a vector-borne pathogen transmitted by ticks in North America, is the causative agent of Powassan encephalitis. As obligate hematophagous organisms, ticks transmit pathogens like POWV at the tick bite site, specifically during the initial stages of feeding. Tick feeding and salivary factors modulate the host's immunological responses, facilitating blood feeding and pathogen transmission. However, the mechanisms of immunomodulation during POWV transmission remain inadequately understood. In this study, we investigated the global cutaneous transcriptomic changes associated with tick bites during POWV transmission.
Methods: We collected skin biopsies from the tick attachment sites at 1, 3, and 6 h after feeding by POWV-infected and uninfected ticks, followed by RNA sequencing of these samples. Differentially expressed genes were analyzed for pathway enrichment using gene ontology and pathway enrichment analyses.
Results: Our findings reveal that tick feeding alone significantly impacts the skin transcriptome within the first 1 to 3 h of tick attachment. Although early POWV transmission induces minimal changes in the local environment, a pronounced shift toward a proinflammatory state is observed 6 h after tick attachment, characterized by neutrophil recruitment and interleukin signaling.
Discussion: These transcriptomic data elucidate the dynamic changes at the tick bite site, transitioning from changes that assist blood meal acquisition to a proinflammatory phase that may facilitate viral dissemination.

Keywords

References

  1. PLoS Negl Trop Dis. 2020 Oct 29;14(10):e0008788 [PMID: 33119599]
  2. Cells. 2019 Dec 23;9(1): [PMID: 31877982]
  3. Ticks Tick Borne Dis. 2021 Nov;12(6):101819 [PMID: 34520993]
  4. Mol Cell Biol. 1999 Jul;19(7):4980-8 [PMID: 10373548]
  5. Arch Dermatol Res. 2013 Jul;305(5):397-406 [PMID: 23463292]
  6. Vector Borne Zoonotic Dis. 2017 Jul;17(7):453-462 [PMID: 28498740]
  7. Nat Rev Immunol. 2007 Apr;7(4):255-66 [PMID: 17380156]
  8. Front Cell Infect Microbiol. 2020 Apr 28;10:172 [PMID: 32411615]
  9. Front Microbiol. 2018 Jul 31;9:1722 [PMID: 30108573]
  10. Front Immunol. 2020 Mar 10;11:352 [PMID: 32210961]
  11. PLoS One. 2012;7(10):e47301 [PMID: 23077588]
  12. Med Vet Entomol. 1993 Apr;7(2):193-6 [PMID: 8481537]
  13. Sci Rep. 2021 Oct 22;11(1):20873 [PMID: 34686683]
  14. Exp Cell Res. 1991 Jan;192(1):93-101 [PMID: 1898594]
  15. Front Microbiol. 2018 Jan 15;8:2686 [PMID: 29379481]
  16. Insect Biochem Mol Biol. 2006 Feb;36(2):111-29 [PMID: 16431279]
  17. J Virol. 2019 Oct 15;93(21): [PMID: 31413130]
  18. Front Microbiol. 2013 Nov 19;4:337 [PMID: 24312085]
  19. J Immunother Cancer. 2022 May;10(5): [PMID: 35613826]
  20. PLoS One. 2016 May 20;11(5):e0155889 [PMID: 27203436]
  21. Parasit Vectors. 2011 Sep 28;4:187 [PMID: 21951834]
  22. J Infect Dis. 1997 Apr;175(4):996-9 [PMID: 9086168]
  23. Sci Rep. 2019 Sep 11;9(1):13110 [PMID: 31511580]
  24. J Gen Virol. 1989 Jul;70 ( Pt 7):1895-8 [PMID: 2544668]
  25. Elife. 2020 Sep 02;9: [PMID: 32876567]
  26. PLOS Glob Public Health. 2022 Jun 27;2(6):e0000215 [PMID: 36962313]
  27. Int J Mol Sci. 2019 Sep 19;20(18): [PMID: 31546972]
  28. Trends Biochem Sci. 2016 Dec;41(12):1012-1021 [PMID: 27669650]
  29. Sci Rep. 2021 Jul 1;11(1):13626 [PMID: 34211002]
  30. Front Immunol. 2021 Feb 23;12:595140 [PMID: 33708197]
  31. Science. 2013 Aug 2;341(6145):514-9 [PMID: 23908230]
  32. Virology. 2012 Feb 5;423(1):58-67 [PMID: 22178263]
  33. Immune Netw. 2019 Dec 23;19(6):e40 [PMID: 31921470]
  34. Front Biosci (Landmark Ed). 2009 Jan 01;14(6):2051-88 [PMID: 19273185]
  35. Can Med Assoc J. 1959 May 1;80(9):708-11 [PMID: 13652010]
  36. Nat Rev Immunol. 2023 Sep;23(9):580-594 [PMID: 36750615]
  37. Ticks Tick Borne Dis. 2021 May;12(3):101649 [PMID: 33549976]
  38. J Proteomics. 2012 Jul 16;75(13):3842-54 [PMID: 22564820]
  39. PLoS One. 2009;4(1):e4261 [PMID: 19156204]
  40. Cell. 1984 Oct;38(3):745-55 [PMID: 6548414]
  41. Am J Physiol Lung Cell Mol Physiol. 2015 Jun 1;308(11):L1178-88 [PMID: 26033355]
  42. Am J Trop Med Hyg. 1996 Nov;55(5):536-46 [PMID: 8940987]
  43. J Med Entomol. 2017 Sep 1;54(5):1360-1364 [PMID: 28874016]
  44. Clin Exp Immunol. 2003 Jan;131(1):148-54 [PMID: 12519399]
  45. PLoS Pathog. 2019 Jun 18;15(6):e1007880 [PMID: 31211814]
  46. J Invest Dermatol. 2014 Aug;134(8):2280-2283 [PMID: 24658509]
  47. J Leukoc Biol. 2021 Apr;109(4):777-791 [PMID: 32881070]
  48. Am J Trop Med Hyg. 2004 Sep;71(3):268-71 [PMID: 15381804]
  49. Ticks Tick Borne Dis. 2017 Aug;8(5):677-681 [PMID: 28501504]
  50. J Med Entomol. 2002 May;39(3):509-12 [PMID: 12061448]
  51. J Virol. 2019 Jun 14;93(13): [PMID: 30971475]
  52. Front Immunol. 2020 Jul 09;11:1259 [PMID: 32733442]
  53. Can Fam Physician. 1990 Jul;36:1289-90 [PMID: 21233909]
  54. J Virol. 2015 Aug;89(15):7852-60 [PMID: 25995246]
  55. J Infect Dis. 2001 Mar 1;183(5):773-8 [PMID: 11181154]
  56. Vaccines (Basel). 2023 Mar 08;11(3): [PMID: 36992196]

Grants

  1. R01 AI127771/NIAID NIH HHS

MeSH Term

Ixodes
Animals
Transcriptome
Encephalitis Viruses, Tick-Borne
Skin
Encephalitis, Tick-Borne
Tick Bites
Female
Gene Expression Profiling
Mice

Word Cloud

Created with Highcharts 10.0.0ticktransmissionPOWVfeedingchangesPowassanticksvirustranscriptomicskinattachmenthpathogenbitesitebloodimmunomodulation136pathwayenrichmentproinflammatoryIntroduction:vector-bornetransmittedNorthAmericacausativeagentencephalitisobligatehematophagousorganismstransmitpathogenslikespecificallyinitialstagesTicksalivaryfactorsmodulatehost'simmunologicalresponsesfacilitatingHowevermechanismsremaininadequatelyunderstoodstudyinvestigatedglobalcutaneousassociatedbitesMethods:collectedbiopsiessitesPOWV-infecteduninfectedfollowedRNAsequencingsamplesDifferentiallyexpressedgenesanalyzedusinggeneontologyanalysesResults:findingsrevealalonesignificantlyimpactstranscriptomewithinfirstAlthoughearlyinducesminimallocalenvironmentpronouncedshifttowardstateobservedcharacterizedneutrophilrecruitmentinterleukinsignalingDiscussion:dataelucidatedynamictransitioningassistmealacquisitionphasemayfacilitateviraldisseminationEarlyinterfaceIxodesarbovirus

Similar Articles

Cited By

No available data.