Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-17T16:14:26.557Z Has data issue: false hasContentIssue false
  • English
  • Français

Arbovirus lifecycle in mosquito: acquisition, propagation and transmission

Published online by Cambridge University Press:  13 March 2019

Pa Wu ,
Xi Yu ,
Penghua Wang  and
Gong Cheng Open the ORCID record for Gong Cheng [Opens in a new window]
Pa Wu
Affiliation:
Tsinghua-Peking Center for Life Sciences, School of Medicine, Tsinghua University, Beijing, 100084, China SZCDC-SUSTech Joint Key Laboratory for Tropical Diseases, Shenzhen Center for Disease Control and Prevention, Shenzhen, Guangdong, 518055, China
Xi Yu
Affiliation:
Tsinghua-Peking Center for Life Sciences, School of Medicine, Tsinghua University, Beijing, 100084, China SZCDC-SUSTech Joint Key Laboratory for Tropical Diseases, Shenzhen Center for Disease Control and Prevention, Shenzhen, Guangdong, 518055, China
Penghua Wang
Affiliation:
Department of Immunology, School of Medicine, the University of Connecticut Health Center, Farmington, CT, 06030, USA
Gong Cheng*
Affiliation:
Tsinghua-Peking Center for Life Sciences, School of Medicine, Tsinghua University, Beijing, 100084, China SZCDC-SUSTech Joint Key Laboratory for Tropical Diseases, Shenzhen Center for Disease Control and Prevention, Shenzhen, Guangdong, 518055, China
*
Author for correspondence: Gong Cheng, E-mail: gongcheng@mail.tsinghua.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Mosquitoes are haematophagous vectors for hundreds of pathogenic viruses that are aetiological agents of human diseases. In nature, mosquito-borne viruses maintain a lifecycle between mosquitoes and vertebrate animals. Viruses are acquired by a naive mosquito from an infected host by blood meals and then propagate extensively in the mosquito's tissues. This mosquito then becomes a virus reservoir and is competent to transmit the viruses to a naive vertebrate host through the next blood meal. To survive in and efficiently cycle between two distinct host environments, mosquito-borne viruses have evolved delicate and smart strategies to comprehensively exploit host and vector factors. Here, we provide an update on recent studies of the mechanisms of virus survival in, acquisition and transmission by mosquitoes.

Keywords

Arbovirusesmosquitoestransmission
Type
Invited Review
Information
Expert Reviews in Molecular Medicine , Volume 21 , 2019 , e1
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Cheng, G et al. (2016) Mosquito defense strategies against viral infection. Trends in Parasitology 32, 177–186.Google Scholar
2.Gaunt, MW et al. (2001) Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. The Journal of General Virology 82, 1867–1876.Google Scholar
3.Weaver, SC and Reisen, WK (2010) Present and future arboviral threats. Antiviral Research 85, 328.Google Scholar
4.Gubler, DJ (1998) Resurgent vector-borne diseases as a global health problem. Emerging Infectious Diseases 4, 442–450.Google Scholar
5.Leta, S et al. (2018) Global risk mapping for major diseases transmitted by Aedes aegypti and Aedes albopictus. International Journal of Infectious Diseases 67, 25–35.Google Scholar
6.Bhatt, S et al. (2013) The global distribution and burden of dengue. Nature 496, 504–507.Google Scholar
7.The Pan American Health Organization [PAHO]/World Health Organization [WHO] (2017) Zika cases and congenital syndrome associated with Zika virus reported by countries and territories in the Americas, 2015–2017 Cumulative cases.Google Scholar
8.Gao, GF (2018) From ‘A'IV to ‘Z'IKV: attacks from emerging and re-emerging pathogens. Cell 172, 1157–1159.Google Scholar
9.Parra, B et al. (2016) Guillain-Barre syndrome associated with Zika virus infection in Colombia. New England Journal of Medicine 375, 1513–1523.Google Scholar
10.Iranpour, M et al. (2016) Apoptosis, autophagy and unfolded protein response pathways in arbovirus replication and pathogenesis. Expert Reviews in Molecular Medicine 18, e1.Google Scholar
11.Lessler, J et al. (2016) Assessing the global threat from Zika virus. Science 353, aaf8160.Google Scholar
12.Grinev, A et al. (2015) The global ecology and epidemiology of West Nile virus. BioMed Research International 2015, 376230.Google Scholar
13.Ruckert, C et al. (2017) Impact of simultaneous exposure to arboviruses on infection and transmission by Aedes aegypti mosquitoes. Nature Communications 8, 15412.Google Scholar
14.Nguyen, NM et al. (2013) Host and viral features of human dengue cases shape the population of infected and infectious Aedes aegypti mosquitoes. Proceedings of the National Academy of Sciences, USA 110, 9072–9077.Google Scholar
15.Wagar, ZL et al. (2017) Low density lipopolyprotein inhibits flavivirus acquisition in Aedes aegypti. Insect Molecular Biology 26, 734–742.Google Scholar
16.Bottino-Rojas, V et al. (2015) Heme signaling impacts global gene expression, immunity and dengue virus infectivity in Aedes aegypti. PLoS One 10, e0135985.Google Scholar
17.Zhu, Y et al. (2017) Blood meal acquisition enhances arbovirus replication in mosquitoes through activation of the GABAergic system. Nature Communications 8, 1262.Google Scholar
18.Liu, J et al. (2016) Flavivirus NS1 protein in infected host sera enhances viral acquisition by mosquitoes. Nature Microbiology 1, 16087.Google Scholar
19.Liu, Y et al. (2017) Evolutionary enhancement of Zika virus infectivity in Aedes aegypti mosquitoes. Nature 545, 482–486.Google Scholar
20.Merkling, SH and van Rij, RP (2013) Beyond RNAi: antiviral defense strategies in Drosophila and mosquito. Journal of Insect Physiology 59, 159–170.Google Scholar
21.Blair, CD and Olson, KE (2015) The role of RNA interference (RNAi) in arbovirus-vector interactions. Viruses 7, 820–843.Google Scholar
22.Franz, AW et al. (2014) Fitness impact and stability of a transgene conferring resistance to dengue-2 virus following introgression into a genetically diverse Aedes aegypti strain. PLoS Neglected Tropical Diseases 8, e2833.Google Scholar
23.Sanchez-Vargas, I et al. (2009) Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito's RNA interference pathway. PLoS Pathogens 5, e1000299.Google Scholar
24.Carissimo, G et al. (2015) Antiviral immunity of Anopheles gambiae is highly compartmentalized, with distinct roles for RNA interference and gut microbiota. Proceedings of the National Academy of Sciences of the United States of America 112, E176–E185.Google Scholar
25.Xi, Z et al. (2008) The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathogens 4, e1000098.Google Scholar
26.Souza-Neto, JA et al. (2009) An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proceedings of the National Academy of Sciences, USA 106, 17841–17846.Google Scholar
27.Ramirez, JL et al. (2014) Chromobacterium Csp_P reduces malaria and dengue infection in vector mosquitoes and has entomopathogenic and in vitro anti-pathogen activities. PLoS Pathogens 10, e1004398.Google Scholar
28.Saraiva, RG et al. (2018) Aminopeptidase secreted by Chromobacterium sp. Panama inhibits dengue virus infection by degrading the E protein. PLoS Neglected Tropical Diseases 12, e0006443.Google Scholar
29.Ramirez, JL et al. (2012) Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Neglected Tropical Diseases 6, e1561.Google Scholar
30.Dong, Y et al. (2012) The entomopathogenic fungus Beauveria bassiana activate toll and JAK-STAT pathway-controlled effector genes and anti-dengue activity in Aedes aegypti. Insect Biochemistry and Molecular Biology 42, 126–132.Google Scholar
31.Apte-Deshpande, A et al. (2012) Serratia odorifera a midgut inhabitant of Aedes aegypti mosquito enhances its susceptibility to dengue-2 virus. PLoS One 7, e40401.Google Scholar
32.Anglero-Rodriguez, YI et al. (2017) An Aedes aegypti-associated fungus increases susceptibility to dengue virus by modulating gut trypsin activity. Elife 6, e28844.Google Scholar
33.Franz, AW et al. (2015) Tissue barriers to arbovirus infection in mosquitoes. Viruses 7, 3741–3767.Google Scholar
34.Barrows, NJ et al. (2018) Biochemistry and molecular biology of Flaviviruses. Chemical Reviews 118, 4448–4482.Google Scholar
35.Cheng, G et al. (2010) A C-type lectin collaborates with a CD45 phosphatase homolog to facilitate West Nile virus infection of mosquitoes. Cell 142, 714–725.Google Scholar
36.Liu, Y et al. (2014) Transmission-blocking antibodies against mosquito C-type lectins for dengue prevention. PLoS Pathogens 10, e1003931.Google Scholar
37.Kuadkitkan, A et al. (2010) Identification and characterization of prohibitin as a receptor protein mediating DENV-2 entry into insect cells. Virology 406, 149–161.Google Scholar
38.Salas-Benito, J et al. (2007) Evidence that the 45-kD glycoprotein, part of a putative dengue virus receptor complex in the mosquito cell line C6/36, is a heat-shock related protein. The American Journal of Tropical Medicine and Hygiene 77, 283–290.Google Scholar
39.Sakoonwatanyoo, P et al. (2006) Growth and production of the dengue virus in C6/36 cells and identification of a laminin-binding protein as a candidate serotype 3 and 4 receptor protein. Intervirology 49, 161–172.Google Scholar
40.Londono-Renteria, B et al. (2015) Dengue virus infection of Aedes aegypti requires a putative cysteine rich venom protein. PLoS Pathogens 11, e1005202.Google Scholar
41.Rose, PP et al. (2011) Natural resistance-associated macrophage protein (NRAMP) is a cellular receptor for Sindbis virus in both insect and mammalian hosts. Cell Host & Microbe 10, 97–104.Google Scholar
42.Samuel, GH et al. (2018) Antiviral immunity and virus-mediated antagonism in disease vector mosquitoes. Trends in Microbiology 26, 447–461.Google Scholar
43.Kakumani, PK et al. (2013) Role of RNA interference (RNAi) in dengue virus replication and identification of NS4B as an RNAi suppressor. Journal of Virology 87, 8870–8883.Google Scholar
44.Mathur, K et al. (2016) Analysis of chikungunya virus proteins reveals that non-structural proteins nsP2 and nsP3 exhibit RNA interference (RNAi) suppressor activity. Scientific Reports 6, 38065.Google Scholar
45.Göertz, GP et al. (2016) Noncoding subgenomic flavivirus RNA is processed by the mosquito RNA interference machinery and determines west Nile virus transmission by Culex pipiens mosquitoes. Journal of Virology 90, 10145–10159.Google Scholar
46.Moon, SL et al. (2015) Flavivirus sfRNA suppresses antiviral RNA interference in cultured cells and mosquitoes and directly interacts with the RNAi machinery. Virology 485, 322–329.Google Scholar
47.Pompon, J et al. (2017) Dengue subgenomic flaviviral RNA disrupts immunity in mosquito salivary glands to increase virus transmission. PLoS Pathogens 13, e1006535.Google Scholar
48.Parikh, GR et al. (2009) A haemocyte tropism for an arbovirus. The Journal of General Virology 90, 292–296.Google Scholar
49.Goic, B et al. (2016) Virus-derived DNA drives mosquito vector tolerance to arboviral infection. Nature Communications 7, 12410.Google Scholar
50.Christensen, BM et al. (2005) Melanization immune responses in mosquito vectors. Trends in Parasitology 21, 192–199.Google Scholar
51.Cerenius, L and Soderhall, K (2004) The prophenoloxidase-activating system in invertebrates. Immunological Reviews 198, 116–126.Google Scholar
52.Rodriguez-Andres, J et al. (2012) Phenoloxidase activity acts as a mosquito innate immune response against infection with Semliki Forest virus. PLoS Pathogens 8, e1002977.Google Scholar
53.Xiao, X et al. (2015) A neuron-specific antiviral mechanism prevents lethal flaviviral infection of mosquitoes. PLoS Pathogens 11, e1004848.Google Scholar
54.Xiao, X et al. (2014) Complement-related proteins control the flavivirus infection of Aedes aegypti by inducing antimicrobial peptides. PLoS Pathogens 10, e1004027.Google Scholar
55.Blandin, S et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116, 661–670.Google Scholar
56.Shokal, U and Eleftherianos, I (2017) Evolution and function of thioester-containing proteins and the complement system in the innate immune response. Frontiers in Immunology 8, 759.Google Scholar
57.Kingsolver, MB et al. (2013) Insect antiviral innate immunity: pathways, effectors, and connections. Journal of Molecular Biology 425, 4921–4936.Google Scholar
58.Tassetto, M et al. (2017) Circulating immune cells mediate a systemic RNAi-based adaptive antiviral response in drosophila. Cell 169, 314–325, e313.Google Scholar
59.Goic, B et al. (2013) RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila. Nature Immunology 14, 396–403.Google Scholar
60.Cerny, D et al. (2014) Selective susceptibility of human skin antigen presenting cells to productive dengue virus infection. PLoS Pathogens 10, e1004548.Google Scholar
61.Schmid, MA and Harris, E (2014) Monocyte recruitment to the dermis and differentiation to dendritic cells increases the targets for dengue virus replication. PLoS Pathogens 10, e1004541.Google Scholar
62.Hamel, R et al. (2015) Biology of Zika virus infection in human skin cells. Journal of Virology 89, 8880–8896.Google Scholar
63.Blackley, S et al. (2007) Primary human splenic macrophages, but not T or B cells, are the principal target cells for dengue virus infection in vitro. Journal of Virology 81, 13325–13334.Google Scholar
64.Styer, LM et al. (2011) Mosquito saliva causes enhancement of West Nile virus infection in mice. Journal of Virology 85, 1517–1527.Google Scholar
65.Cox, J et al. (2012) Mosquito bite delivery of dengue virus enhances immunogenicity and pathogenesis in humanized mice. Journal of Virology 86, 7637–7649.Google Scholar
66.Surasombatpattana, P et al. (2014) Aedes aegypti saliva contains a prominent 34-kDa protein that strongly enhances dengue virus replication in human keratinocytes. The Journal of Investigative Dermatology 134, 281–284.Google Scholar
67.Schneider, BS et al. (2004) Aedes aegypti salivary gland extracts modulate anti-viral and TH1/TH2 cytokine responses to sindbis virus infection. Viral Immunology 17, 565–573.Google Scholar
68.Jin, L et al. (2018) Salivary factor LTRIN from Aedes aegypti facilitates the transmission of Zika virus by interfering with the lymphotoxin-beta receptor. Nature Immunology 19, 342–353.Google Scholar
69.Conway, MJ et al. (2014) Mosquito saliva serine protease enhances dissemination of dengue virus into the mammalian host. Journal of Virology 88, 164–175.Google Scholar
70.Pingen, M et al. (2016) Host inflammatory response to mosquito bites enhances the severity of arbovirus infection. Immunity 44, 1455–1469.Google Scholar
71.Schneider, BS et al. (2010) Aedes aegypti saliva alters leukocyte recruitment and cytokine signaling by antigen-presenting cells during west Nile virus infection. PLoS One 5, e11704.Google Scholar