Dengue infection modulates locomotion and host seeking in Aedes aegypti.
Journal
PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
27
03
2020
accepted:
27
06
2020
entrez:
10
9
2020
pubmed:
11
9
2020
medline:
24
10
2020
Statut:
epublish
Résumé
Pathogens may manipulate their human and mosquito hosts to enhance disease transmission. Dengue, caused by four viral serotypes, is the fastest-growing transmissible disease globally resulting in 50-100 million infections annually. Transmission of the disease relies on the interaction between humans and the vector Aedes aegypti and is largely dependent on the odor-mediated host seeking of female mosquitoes. In this study, we use activity monitors to demonstrate that dengue virus-1 affects the locomotion and odor-mediated behavior of Ae. aegypti, reflecting the progression of infection within the mosquito. Mosquitoes 4-6 days post-infection increase locomotion, but do not alter their odor-driven host-seeking response. In contrast, females 14-16 days post-infection are less active, yet more sensitive to human odors as assessed by behavioral and electrophysiological assays. Such an increase in physiological and behavioral sensitivity is reflected by the antennal-specific increase in abundance of neural signaling transcripts in 14 days post-infection females, as determined by transcriptome analysis. This suggests that the sensitivity of the mosquito peripheral olfactory system is altered by the dengue virus by enhancing the overall neural responsiveness of the antenna, rather than the selective regulation of chemosensory-related genes. Our study reveals that dengue virus-1 enhances vector-related behaviors in the early stages post-infection that aid in avoiding predation and increasing spatial exploration. On the other hand, at the later stages of infection, the virus enhances the host-seeking capacity of the vector, thereby increasing the risk of virus transmission. A potential mechanism is discussed.
Identifiants
pubmed: 32911504
doi: 10.1371/journal.pntd.0008531
pii: PNTD-D-20-00502
pmc: PMC7482838
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0008531Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Acta Trop. 2006 Jul;98(3):219-23
pubmed: 16780784
Cell. 2009 Dec 24;139(7):1268-78
pubmed: 20064373
Am J Trop Med Hyg. 1997 Aug;57(2):119-25
pubmed: 9288801
Sci Rep. 2017 Jan 09;7:40297
pubmed: 28067294
Proc Biol Sci. 1998 May 7;265(1398):763-8
pubmed: 9628035
PLoS One. 2011 Mar 08;6(3):e17690
pubmed: 21408119
Proc Biol Sci. 2013 May 22;280(1763):20130711
pubmed: 23698008
Biochem Biophys Res Commun. 2017 Oct 28;492(4):617-623
pubmed: 28161634
J Med Entomol. 2016 Jan;53(1):233-6
pubmed: 26512141
PLoS One. 2013;8(3):e59933
pubmed: 23555838
Med Vet Entomol. 1995 Apr;9(2):176-80
pubmed: 7787226
Cell Rep. 2019 Nov 12;29(7):1946-1960.e5
pubmed: 31722209
Insect Biochem Mol Biol. 2005 Nov;35(11):1293-307
pubmed: 16203210
PLoS One. 2010 May 18;5(5):e10678
pubmed: 20502529
PLoS One. 2012;7(11):e50972
pubmed: 23226436
Annu Rev Entomol. 2008;53:273-91
pubmed: 17803458
J Insect Physiol. 2020 Apr;122:104021
pubmed: 32035953
J Med Entomol. 2001 May;38(3):411-22
pubmed: 11372967
Jpn J Infect Dis. 1999 Oct;52(5):214-6
pubmed: 10680088
Proc Biol Sci. 2005 Oct 22;272(1577):2117-26
pubmed: 16191624
PLoS One. 2013 May 15;8(5):e63602
pubmed: 23691073
Viruses. 2019 Dec 05;11(12):
pubmed: 31817553
Insects. 2018 Oct 23;9(4):
pubmed: 30360532
Front Immunol. 2014 Jun 17;5:290
pubmed: 24987394
PLoS Pathog. 2012;8(3):e1002631
pubmed: 22479185
PLoS Negl Trop Dis. 2017 Jan 12;11(1):e0005187
pubmed: 28081143
Mem Inst Oswaldo Cruz. 2018 Aug 23;113(10):e180290
pubmed: 30156598
Proc Natl Acad Sci U S A. 2014 Jul 29;111(30):11079-84
pubmed: 24982164
Science. 2017 Mar 10;355(6329):1076-1080
pubmed: 28183997
PLoS One. 2012;7(11):e50512
pubmed: 23209765
Annu Rev Entomol. 2003;48:141-61
pubmed: 12414739
Curr Opin Insect Sci. 2017 Apr;20:75-83
pubmed: 28602240
PLoS One. 2014 Aug 19;9(8):e105255
pubmed: 25136800
Med Vet Entomol. 1996 Jul;10(3):269-76
pubmed: 8887339
BMC Microbiol. 2007 Jan 30;7:9
pubmed: 17263893
J Virol. 2015 Sep;89(17):8880-96
pubmed: 26085147
mBio. 2015 Mar 24;6(2):
pubmed: 25805727
Trends Parasitol. 2012 Mar;28(3):114-21
pubmed: 22300806
Sci Rep. 2018 Sep 4;8(1):13179
pubmed: 30181545
Parasit Vectors. 2018 Apr 18;11(1):254
pubmed: 29669591
Sci Rep. 2019 Mar 4;9(1):3396
pubmed: 30833618
Malar J. 2014 Nov 20;13:442
pubmed: 25412797
J Med Entomol. 2007 Nov;44(6):1074-85
pubmed: 18047209
BMC Evol Biol. 2014 Aug 29;14:166
pubmed: 25085339
Am J Trop Med Hyg. 1992 Oct;47(4):484-8
pubmed: 1443347
Proc Natl Acad Sci U S A. 2013 May 28;110(22):9072-7
pubmed: 23674683
Sci Rep. 2019 Jan 10;9(1):43
pubmed: 30631085
Neuron. 2011 Jan 13;69(1):44-60
pubmed: 21220098
Sci Rep. 2016 Nov 30;6:37930
pubmed: 27901056
Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5716-21
pubmed: 18391205
PLoS Pathog. 2008 Jul 04;4(7):e1000098
pubmed: 18604274
Am J Trop Med Hyg. 1997 Aug;57(2):235-9
pubmed: 9288822
J Med Entomol. 1980 Jan 31;17(1):1-7
pubmed: 7365753
Virology. 2017 Jul;507:75-81
pubmed: 28431281
PLoS One. 2009 Sep 15;4(9):e7032
pubmed: 19753115
Trans R Soc Trop Med Hyg. 2011 Aug;105(8):452-8
pubmed: 21700303
Ann Trop Med Parasitol. 1983 Oct;77(5):483-95
pubmed: 6660954
Infect Genet Evol. 2008 Jul;8(4):504-19
pubmed: 17588825
J Exp Biol. 2009 May;212(Pt 10):1436-41
pubmed: 19411536
Proc Natl Acad Sci U S A. 2018 May 29;115(22):5780-5785
pubmed: 29760095
Proc Biol Sci. 1999 Sep 7;266(1430):1729-33
pubmed: 10518321
Int J Parasitol. 2018 Mar;48(3-4):257-264
pubmed: 29170087
Sci Rep. 2019 Jul 4;9(1):9699
pubmed: 31273284
J Exp Biol. 2013 Jan 1;216(Pt 1):134-41
pubmed: 23225876
J Exp Biol. 2017 Oct 1;220(Pt 19):3598-3603
pubmed: 28978641
PLoS Negl Trop Dis. 2017 Dec 19;11(12):e0006152
pubmed: 29261661
PLoS Negl Trop Dis. 2019 May 20;13(5):e0007443
pubmed: 31107912
Brain Behav Evol. 2002;60(6):370-7
pubmed: 12563169
Cell Mol Life Sci. 2018 Feb;75(3):485-508
pubmed: 28828501
J Chem Ecol. 2009 Aug;35(8):933-43
pubmed: 19626371
J Exp Biol. 2013 Jan 1;216(Pt 1):56-66
pubmed: 23225868
Parasit Vectors. 2015 Sep 23;8:485
pubmed: 26395987
Mem Inst Oswaldo Cruz. 2011 Sep;106(6):755-8
pubmed: 22012232
Bioinformatics. 2003 Aug 12;19(12):1477-83
pubmed: 12912827
BMC Genomics. 2016 Jan 06;17:32
pubmed: 26738925
Med Vet Entomol. 1996 Jan;10(1):87-92
pubmed: 8834747
Parasitology. 1986 Jun;92 ( Pt 3):721-36
pubmed: 3737249
Proteomics. 2007 Jun;7(11):1908-15
pubmed: 17464940
PLoS Pathog. 2011 Sep;7(9):e1002189
pubmed: 21909258