Jamestown Canyon virus is transmissible by Aedes aegypti and is only moderately blocked by Wolbachia co-infection.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101291488 Publication Model: eCollection Cited Medium: Internet ISSN: 1935-2735 (Electronic) Linking ISSN: 19352727 NLM ISO Abbreviation: PLoS Negl Trop Dis Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science

Aedes* ; Encephalitis Virus, California* ; Deer* ; Wolbachia* ; Coinfection* ; Zika Virus* ; Zika Virus Infection*; Animals ; Humans ; Mosquito Vectors

Jamestown Canyon virus (JCV), a negative-sense arbovirus, is increasingly common in the upper Midwest of the USA. Transmitted by a range of mosquito genera, JCV's primary amplifying host is white-tailed deer. Aedes aegypti is responsible for transmitting various positive-sense viruses globally including dengue (DENV), Zika, chikungunya, and Yellow Fever. Ae. aegypti's distribution, once confined to the tropics, is expanding, in part due to climate change. Wolbachia, an insect endosymbiont, limits the replication of co-infecting viruses inside insects. The release and spread of the symbiont into Ae. aegypti populations have been effective in reducing transmission of DENV to humans, although the mechanism of Wolbachia-mediated viral blocking is still poorly understood. Here we explored JCV infection potential in Ae. aegypti, the nature of the vector's immune response, and interactions with Wolbachia infection. We show that Ae. aegypti is highly competent for JCV, which grows to high loads and rapidly reaches the saliva after an infectious blood meal. The mosquito immune system responds with strong induction of RNAi and JAK/STAT. Neither the direct effect of viral infection nor the energetic investment in immunity appears to affect mosquito longevity. Wolbachia infection blocked JCV only in the early stages of infection. Wolbachia-induced immunity was small compared to that of JCV, suggesting innate immune priming does not likely explain blocking. We propose two models to explain why Wolbachia's blocking of negative-sense viruses like JCV may be less than that of positive-sense viruses, relating to the slowdown of host protein synthesis and the triggering of interferon-like factors like Vago. In conclusion, we highlight the risk for increased human disease with the predicted future overlap of Ae. aegypti and JCV ranges. We suggest that with moderate Wolbachia-mediated blocking and distinct biology, negative-sense viruses represent a fruitful comparator model to other viruses for understanding blocking mechanisms in mosquitoes.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2023 Lau et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Trends Parasitol. 2016 Mar;32(3):177-186. (PMID: 26626596)
mBio. 2018 May 22;9(3):. (PMID: 29789369)
Elife. 2015 Jun 30;4:e08347. (PMID: 26126267)
Virol J. 2016 Jul 02;13:118. (PMID: 27368371)
Nat Microbiol. 2019 May;4(5):854-863. (PMID: 30833735)
Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17841-6. (PMID: 19805194)
PLoS Pathog. 2008 Jul 04;4(7):e1000098. (PMID: 18604274)
Front Microbiol. 2021 Jul 29;12:711107. (PMID: 34394061)
Exp Hematol. 2002 Jun;30(6):503-12. (PMID: 12063017)
Proc Natl Acad Sci U S A. 2006 Mar 14;103(11):4198-203. (PMID: 16537508)
Parasit Vectors. 2017 Dec 28;10(1):622. (PMID: 29282144)
J Med Entomol. 2006 May;43(3):543-51. (PMID: 16739414)
Viruses. 2018 Mar 21;10(4):. (PMID: 29561780)
Microbes Infect. 2002 Mar;4(3):341-50. (PMID: 11909745)
Curr Biol. 2019 Dec 16;29(24):4241-4248.e5. (PMID: 31761702)
Dev Comp Immunol. 2010 Jun;34(6):625-9. (PMID: 20079370)
PLoS Pathog. 2020 Jun 18;16(6):e1008513. (PMID: 32555677)
Am J Trop Med Hyg. 1996 Apr;54(4):338-42. (PMID: 8615443)
Nat Rev Microbiol. 2018 Aug;16(8):508-518. (PMID: 29777177)
Infect Genet Evol. 2019 Jan;67:191-209. (PMID: 30465912)
PLoS Negl Trop Dis. 2014 Apr 24;8(4):e2823. (PMID: 24762775)
PLoS Negl Trop Dis. 2017 Jan 12;11(1):e0005187. (PMID: 28081143)
Future Microbiol. 2011 Mar;6(3):265-77. (PMID: 21449839)
PLoS One. 2019 Oct 7;14(10):e0223582. (PMID: 31589661)
Insect Biochem Mol Biol. 2018 Jan;92:45-52. (PMID: 29157676)
ISME J. 2018 Jan;12(1):277-288. (PMID: 29099491)
Nat Microbiol. 2019 Nov;4(11):1832-1839. (PMID: 31451771)
Curr Opin Insect Sci. 2022 Apr;50:100874. (PMID: 35051619)
PLoS Pathog. 2018 Nov 13;14(11):e1007445. (PMID: 30422992)
Nat Immunol. 2005 Sep;6(9):946-53. (PMID: 16086017)
Science. 2005 Oct 14;310(5746):326-8. (PMID: 16224027)
Philos Trans R Soc Lond B Biol Sci. 2015 Apr 5;370(1665):. (PMID: 25688023)
Proc Natl Acad Sci U S A. 2012 Nov 13;109(46):18915-20. (PMID: 23027947)
Neurohospitalist. 2021 Jul;11(3):277-278. (PMID: 34163560)
PLoS Negl Trop Dis. 2020 May 18;14(5):e0007754. (PMID: 32421713)
J Virol. 2021 Aug 25;95(18):e0095321. (PMID: 34432527)
Cell. 2009 Dec 24;139(7):1268-78. (PMID: 20064373)
Pathogens. 2019 Jun 13;8(2):. (PMID: 31200426)
PLoS Pathog. 2009 Feb;5(2):e1000299. (PMID: 19214215)
Emerg Microbes Infect. 2020 Dec;9(1):903-912. (PMID: 32302268)
PLoS Negl Trop Dis. 2016 Nov 17;10(11):e0005145. (PMID: 27855218)
Proc Natl Acad Sci U S A. 2010 Nov 9;107(45):19390-5. (PMID: 20978209)
J Gen Virol. 2016 Nov;97(11):3024-3029. (PMID: 27692043)
Cell Host Microbe. 2016 Jun 8;19(6):771-4. (PMID: 27156023)
Health Promot Perspect. 2021 Dec 19;11(4):371-381. (PMID: 35079581)
Parasit Vectors. 2018 Jan 9;11(1):29. (PMID: 29316963)
J Med Entomol. 2005 Sep;42(5):844-9. (PMID: 16363170)
Appl Environ Microbiol. 2012 Oct;78(19):6922-9. (PMID: 22843518)
PLoS One. 2008 Apr 30;3(4):e2032. (PMID: 18446221)
Am J Trop Med Hyg. 2015 Aug;93(2):384-9. (PMID: 26033022)
PLoS Pathog. 2016 Feb 18;12(2):e1005434. (PMID: 26891349)
Parasit Vectors. 2022 Mar 24;15(1):103. (PMID: 35331315)
J Virol. 1988 Jan;62(1):27-32. (PMID: 3334745)
Proc Natl Acad Sci U S A. 2012 Jun 19;109(25):E1638-46. (PMID: 22645363)
PLoS Negl Trop Dis. 2021 Jul 27;15(7):e0009637. (PMID: 34314434)
mSphere. 2017 May 3;2(3):. (PMID: 28497117)
Commun Biol. 2021 Nov 25;4(1):1327. (PMID: 34824354)
Sci Transl Med. 2015 Mar 18;7(279):279ra37. (PMID: 25787763)
Am J Trop Med Hyg. 1982 Nov;31(6):1238-44. (PMID: 7149109)
Proc Natl Acad Sci U S A. 2012 Jan 3;109(1):E23-31. (PMID: 22123956)
N Engl J Med. 2021 Jun 10;384(23):2177-2186. (PMID: 34107180)
PLoS Pathog. 2019 Dec 2;15(12):e1008218. (PMID: 31790509)
Sci Rep. 2017 Mar 06;7:43847. (PMID: 28262718)
J Virol. 2006 May;80(10):5059-64. (PMID: 16641297)
Am J Trop Med Hyg. 1985 May;34(3):586-95. (PMID: 4003669)
PLoS Negl Trop Dis. 2012;6(11):e1892. (PMID: 23133693)

R01 AI143758 United States AI NIAID NIH HHS

Odocoileus virginianus

Date Created: 20230905 Date Completed: 20230918 Latest Revision: 20230930

20231215

PMC10503764

10.1371/journal.pntd.0011616

37669272