A Microfluidic Platform for Highly Parallel Bite by Bite Profiling of Mosquito-borne Pathogen Transmission

Overview

Journal Nat Commun

Specialty Biology

Date 2021 Oct 15

PMID 34650045

Citations 8

Authors

Shailabh Kumar

Felix J H Hol

Sujit Pujhari

Clayton Ellington

Haripriya Vaidehi Narayanan

Hongquan Li

Jason L Rasgon

Manu Prakash

Affiliations

Soon will be listed here.

Abstract

Mosquito bites transmit a number of pathogens via salivary droplets deposited during blood-feeding, resulting in potentially fatal diseases. Little is known about the genomic content of these nanodroplets, including the transmission dynamics of live pathogens. Here we introduce Vectorchip, a low-cost, scalable microfluidic platform enabling high-throughput molecular interrogation of individual mosquito bites. We introduce an ultra-thin PDMS membrane which acts as a biting interface to arrays of micro-wells. Freely-behaving mosquitoes deposit saliva droplets by biting into these micro-wells. By modulating membrane thickness, we observe species-dependent differences in mosquito biting capacity, utilizable for selective sample collection. We demonstrate RT-PCR and focus-forming assays on-chip to detect mosquito DNA, Zika virus RNA, as well as quantify infectious Mayaro virus particles transmitted from single mosquito bites. The Vectorchip presents a promising approach for single-bite-resolution laboratory and field characterization of vector-pathogen communities, and could serve as a powerful early warning sentinel for mosquito-borne diseases.

Citing Articles

A mosquito salivary protein-driven influx of myeloid cells facilitates flavivirus transmission.

Wang Z, Nie K, Liang Y, Niu J, Yu X, Zhang O EMBO J. 2024; 43(9):1690-1721.

PMID: 38378891 PMC: 11066113. DOI: 10.1038/s44318-024-00056-x.

Ultra-low volume intradermal administration of radiation-attenuated sporozoites with the glycolipid adjuvant 7DW8-5 completely protects mice against malaria.

Watson F, Shears M, Kalata A, Duncombe C, Seilie A, Chavtur C Sci Rep. 2024; 14(1):2881.

PMID: 38311678 PMC: 10838921. DOI: 10.1038/s41598-024-53118-9.

Automated analysis of feeding behaviors of females of the mosquito Aedes aegypti using a modified flyPAD system.

Henriques-Santos B, Xiong C, Pietrantonio P Sci Rep. 2023; 13(1):20188.

PMID: 37980438 PMC: 10657447. DOI: 10.1038/s41598-023-47277-4.

Engineered Human Tissue as A New Platform for Mosquito Bite-Site Biology Investigations.

Seavey C, Doshi M, Panarello A, Felice M, Dickerson A, Jewett M Insects. 2023; 14(6).

PMID: 37367330 PMC: 10299109. DOI: 10.3390/insects14060514.

SPIM-Flow: An Integrated Light Sheet and Microfluidics Platform for Hydrodynamic Studies of .

Hedde P, Le B, Gomez E, Duong L, Steele R, Ahrar S Biology (Basel). 2023; 12(1).

PMID: 36671808 PMC: 9856110. DOI: 10.3390/biology12010116.

References

Johnson B, Mitchell S, Paton C, Stevenson J, Staunton K, Snoad N . Use of rhodamine B to mark the body and seminal fluid of male Aedes aegypti for mark-release-recapture experiments and estimating efficacy of sterile male releases. PLoS Negl Trop Dis. 2017; 11(9):e0005902. PMC: 5634656. DOI: 10.1371/journal.pntd.0005902. View

Long K, Ziegler S, Thangamani S, Hausser N, Kochel T, Higgs S . Experimental transmission of Mayaro virus by Aedes aegypti. Am J Trop Med Hyg. 2011; 85(4):750-7. PMC: 3183788. DOI: 10.4269/ajtmh.2011.11-0359. View

Ramirez A, Hall-Mendelin S, Doggett S, Hewitson G, McMahon J, Ritchie S . Mosquito excreta: A sample type with many potential applications for the investigation of Ross River virus and West Nile virus ecology. PLoS Negl Trop Dis. 2018; 12(8):e0006771. PMC: 6136815. DOI: 10.1371/journal.pntd.0006771. View

Vogt M, Lahon A, Arya R, Kneubehl A, Clinton J, Paust S . Mosquito saliva alone has profound effects on the human immune system. PLoS Negl Trop Dis. 2018; 12(5):e0006439. PMC: 5957326. DOI: 10.1371/journal.pntd.0006439. View

Achee N, Youngblood L, Bangs M, Lavery J, James S . Considerations for the use of human participants in vector biology research: a tool for investigators and regulators. Vector Borne Zoonotic Dis. 2015; 15(2):89-102. PMC: 4340630. DOI: 10.1089/vbz.2014.1628. View

Gantz V, Jasinskiene N, Tatarenkova O, Fazekas A, Macias V, Bier E . Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc Natl Acad Sci U S A. 2015; 112(49):E6736-43. PMC: 4679060. DOI: 10.1073/pnas.1521077112. View

Caputo B, Manica M . Mosquito surveillance and disease outbreak risk models to inform mosquito-control operations in Europe. Curr Opin Insect Sci. 2020; 39:101-108. DOI: 10.1016/j.cois.2020.03.009. View

Takahashi M . The effects of environmental and physiological conditions of Culex tritaeniorhynchus on the pattern of transmission of Japanese encephalitis virus. J Med Entomol. 1976; 13(3):275-84. DOI: 10.1093/jmedent/13.3.275. View

Fontaine A, Jiolle D, Moltini-Conclois I, Lequime S, Lambrechts L . Excretion of dengue virus RNA by Aedes aegypti allows non-destructive monitoring of viral dissemination in individual mosquitoes. Sci Rep. 2016; 6:24885. PMC: 4846815. DOI: 10.1038/srep24885. View

10.

Jove V, Gong Z, Hol F, Zhao Z, Sorrells T, Carroll T . Sensory Discrimination of Blood and Floral Nectar by Aedes aegypti Mosquitoes. Neuron. 2020; 108(6):1163-1180.e12. PMC: 9831381. DOI: 10.1016/j.neuron.2020.09.019. View

11.

Pilotte N, Cook D, Pryce J, Zulch M, Minetti C, Reimer L . Laboratory evaluation of molecular xenomonitoring using mosquito and tsetse fly excreta/feces to amplify , , and DNA. Gates Open Res. 2020; 3:1734. PMC: 7308644. DOI: 10.12688/gatesopenres.13093.2. View

12.

Kenea O, Balkew M, Tekie H, Gebre-Michael T, Deressa W, Loha E . Comparison of two adult mosquito sampling methods with human landing catches in south-central Ethiopia. Malar J. 2017; 16(1):30. PMC: 5237125. DOI: 10.1186/s12936-016-1668-9. View

13.

Sanchez-Vargas I, Harrington L, Black 4th W, Olson K . Analysis of Salivary Glands and Saliva from and Infected with Chikungunya Viruses. Insects. 2019; 10(2). PMC: 6410068. DOI: 10.3390/insects10020039. View

14.

Gomard Y, Lebon C, Mavingui P, Atyame C . Contrasted transmission efficiency of Zika virus strains by mosquito species Aedes aegypti, Aedes albopictus and Culex quinquefasciatus from Reunion Island. Parasit Vectors. 2020; 13(1):398. PMC: 7412802. DOI: 10.1186/s13071-020-04267-z. View

15.

DEVINE T, VENARD C, MYSER W . MEASUREMENT OF SALIVATION BY AEDES AEGYPTI (L.) FEEDING ON A LIVING HOST. J Insect Physiol. 1965; 11:347-53. DOI: 10.1016/0022-1910(65)90082-x. View

16.

Li R, Xu L, Bjornstad O, Liu K, Song T, Chen A . Climate-driven variation in mosquito density predicts the spatiotemporal dynamics of dengue. Proc Natl Acad Sci U S A. 2019; 116(9):3624-3629. PMC: 6397594. DOI: 10.1073/pnas.1806094116. View

17.

Kraemer M, Reiner Jr R, Brady O, Messina J, Gilbert M, Pigott D . Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat Microbiol. 2019; 4(5):854-863. PMC: 6522366. DOI: 10.1038/s41564-019-0376-y. View

18.

Hol F, Lambrechts L, Prakash M . BiteOscope, an open platform to study mosquito biting behavior. Elife. 2020; 9. PMC: 7535929. DOI: 10.7554/eLife.56829. View

19.

Ye Y, Carrasco A, Frentiu F, Chenoweth S, Beebe N, van den Hurk A . Wolbachia Reduces the Transmission Potential of Dengue-Infected Aedes aegypti. PLoS Negl Trop Dis. 2015; 9(6):e0003894. PMC: 4482661. DOI: 10.1371/journal.pntd.0003894. View

20.

Tangena J, Thammavong P, Hiscox A, Lindsay S, Brey P . The Human-Baited Double Net Trap: An Alternative to Human Landing Catches for Collecting Outdoor Biting Mosquitoes in Lao PDR. PLoS One. 2015; 10(9):e0138735. PMC: 4575072. DOI: 10.1371/journal.pone.0138735. View