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Neuronal Responses of Antennal Olfactory Sensilla to Insect Chemical Repellents in the Yellow Fever Mosquito, Aedes aegypti

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Abstract

The yellow fever mosquito, Aedes aegypti, is a vector of many human diseases such as yellow fever, dengue fever, and Zika. As insecticide resistance has been widely reported, chemical repellents have been adopted as alternative options for mosquito and mosquito-borne disease control. This study characterized the responses of olfactory receptor neurons (ORNs) in different types of antennal olfactory sensilla in Ae. aegypti to 48 chemicals that exhibited repellent activity in various insect species. Both excitatory and inhibitory responses were observed from ORNs in response to these chemicals and differential tuning properties were also observed among ORNs. Remarkable excitatory responses were recorded from the ORNs in sensilla SST1, SST2, SBTI, SBTII, and LST2, while inhibitory activities were detected from a neuron in sensillum SST2 in response to several terpene/terpenoid compounds. Moreover, the temporal dynamics of neuronal responses were found to be compound-specific and concentration-dependent. Hierarchical cluster analysis and principal component analysis of the response to each compound across ORNs in seven types of olfactory sensilla in Ae. aegypti revealed that odor reception depended not only on chemical class but also specific chemical structure. Results of this study give new insights into the sensory physiology of Aedes mosquitoes to the chemical repellents and should contribute to the development of new repellent reagents for human protection.

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References

  • Ansari MA, Vasudevan P, Tandon M, Razdan RK (2000) Larvicidal and mosquito repellent action of peppermint (Mentha piperita) oil. Bioresour Technol 71:267–271

    Article  CAS  Google Scholar 

  • Boeckh J, Kaissling KE, Schneider D (1965) Insect olfactory receptors. Cold Spring Harb Symp Quant Biol 30:263–280

    Article  CAS  Google Scholar 

  • Campbell C, Gries R, Gries G (2011) Forty-two compounds in eleven essential oils elicit antennal responses from Aedes aegypti. Entomol Exp Appl 138:21–32

    Article  CAS  Google Scholar 

  • Cao LH, Yang D, Wu W, Zeng X, Jing BY, Li MT, Qin SS, Tang C, Tu YH, Luo DG (2017) Odor-evoked inhibition of olfactory sensory neurons drives olfactory perception in Drosophila. Nat Commun 8:1–13

    Article  Google Scholar 

  • Carey AF, Wang G, Su CY, Laurence JZ, Carlson JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464:66–71

    Article  CAS  Google Scholar 

  • De Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552

    Article  Google Scholar 

  • DeGennaro M, McBride CS, Seeholzer L, Nakagawa T, Dennis EJ, Goldman C, Jasinskiene N, James AA, Vosshall LB (2013) Orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature 498:487–491

    Article  CAS  Google Scholar 

  • Den Otter CJ, Behan M, Maes FW (1980) Single cell responses in female Pieris brassicae (Lepidoptera: Pieridae) to plant volatiles and conspecific egg odours. J Insect Physiol 26:465–472

    Article  Google Scholar 

  • Fradin MS, Day JF (2002) Comparative efficacy of insect repellents against mosquito bites. N Engl J Med 347:13–18

    Article  CAS  Google Scholar 

  • Gertler S (1946) Nu, nu-diethylbenzamide as an insect repelle. US Pat 2,408,389. Washington DC: U.S. Patent and Trademark Office

  • Ghaninia M, Ignell R, Hansson BS (2007) Functional classification and central nervous projections of olfactory receptor neurons housed in antennal trichoid sensilla of female yellow fever mosquitoes, Aedes aegypti. Eur J Neurosci 26:1611–1623

    Article  Google Scholar 

  • Gubler DJ (2004) The changing epidemiology of yellow fever and dengue, 1900 to 2003: full circle? Comp Immunol Microbiol Infect Dis 27:319–330

    Article  CAS  Google Scholar 

  • Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160

    Article  CAS  Google Scholar 

  • Hill S, Hansson BS, Ignell R (2009) Characterization of antennal trichoid sensilla from female southern house mosquito, Culex quinquefasciatus say. Chem Senses 34:231–252

    Article  Google Scholar 

  • Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66

    Article  CAS  Google Scholar 

  • Joseph RM, Carlson JR (2015) Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Trends Genet 31:683–695

    Article  CAS  Google Scholar 

  • Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J Neurosci 16:3837–3847

    Article  CAS  Google Scholar 

  • Lei H, Christensen TA, Hildebrand JG (2004) Spatial and temporal organization of ensemble representations for different odor classes in the moth antennal lobe. J Neurosci 24:11108–11119

    Article  CAS  Google Scholar 

  • Liu N (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol 60:537–559

    Article  CAS  Google Scholar 

  • Liu F, Liu N (2015) Human odorant reception in the common bed bug, Cimex lectularius. Sci Rep 5:15558

    Article  CAS  Google Scholar 

  • Liu F, Chen L, Appel AG, Liu N (2013) Olfactory responses of the antennal trichoid sensilla to chemical repellents in the mosquito, Culex quinquefasciatus. J Insect Physiol 59:1169–1177

    Article  CAS  Google Scholar 

  • Liu F, Haynes KF, Appel AG, Liu N (2014) Antennal olfactory sensilla responses to insect chemical repellents in the common bed bug, Cimex lectularius. J Chem Ecol 40:522–533

    Article  Google Scholar 

  • Liu F, Xiong C, Liu N (2017) Chemoreception to aggregation pheromones in the common bed bug, Cimex lectularius. Insect Biochem Mol Biol 82:62–73

    Article  CAS  Google Scholar 

  • Marchette N, Garcia R, Rudnick A (1969) Isolation of Zika virus from Aedes aegypti mosquitoes in Malaysia. Am J Trop Med Hyg 18:411–415

    Article  CAS  Google Scholar 

  • Matthews BJ, McBride CS, DeGennaro M, Despo O, Vosshall LB (2016) The neurotranscriptome of the Aedes aegypti mosquito. BMC Genomics 17:32

    Article  Google Scholar 

  • McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J, Sang R, Ignell R, Vosshall LB (2014) Evolution of mosquito preference for humans linked to an odorant receptor. Nature 515:222–227

    Article  CAS  Google Scholar 

  • McIver S (1978) Structure of sensilla trichodea of female Aedes aegypti with comments on innervation of antennal sensilla. J Insect Physiol 24:383–390

    Article  Google Scholar 

  • Monath TP (2001) Yellow fever: an update. Lancet Infect Dis 1:11–20

    Article  CAS  Google Scholar 

  • Nakagawa T, Sakurai T, Nishioka T (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638–1642

    Article  CAS  Google Scholar 

  • Qiu Y, Van Loon JJ, Takken W, Meijerink J, Smid HM (2006) Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem Senses 31:845–863

    Article  CAS  Google Scholar 

  • Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006

    Article  CAS  Google Scholar 

  • Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odor discrimination on desynchronization of odor–encoding neural assemblies. Nature 390:70–74

    Article  CAS  Google Scholar 

  • Trongtokit Y, Rongsriyam Y, Komalamisra N, Apiwathnasorn C (2005) Comparative repellency of 38 essential oils against mosquito bites. Phytother Res 19:303–309

    Article  CAS  Google Scholar 

  • Ufkes LL, Grams GW (2007) The isolation and identification of volatile insect repellents from the fruit of the Osage orange (Maclura pomifera). J Essent Oil Res 19:167–170

    Article  CAS  Google Scholar 

  • von Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den Sexual-Lockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch 14b:283–284

    Google Scholar 

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Acknowledgements

This project was supported by Award Alabama Agricultural Experiment Station (AAES) Multistate/Hatch Grants ALA08-045 and ALA015-1-10026 to N.L. The Orlando strain used in this study was a generous gift from Dr. James Becnel (USDA, ARS, Mosquito and Fly Research Unit). The authors thank two anonymous reviewers for their valuable comments on the manuscript.

Funding

This project was supported by Award Alabama Agricultural Experiment Station (AAES) Multistate/Hatch Grants ALA08–045 and ALA015–1-10026 to N.L.

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Authors and Affiliations

  1. Department of Entomology & Plant Pathology, Auburn University, 301 Funchess Hall, Auburn, AL, 36849-5413, USA

    Zhou Chen, Feng Liu & Nannan Liu

Authors
  1. Zhou Chen
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  2. Feng Liu
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  3. Nannan Liu
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Contributions

Conceived and designed the study: NL, ZC, and F.L. Performed the experiments: ZC. Prepared the materials: NL. Wrote the paper: NL, ZC, and FL.

Corresponding author

Correspondence to Nannan Liu.

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The authors declare that they have no conflict of interests.

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Chen, Z., Liu, F. & Liu, N. Neuronal Responses of Antennal Olfactory Sensilla to Insect Chemical Repellents in the Yellow Fever Mosquito, Aedes aegypti. J Chem Ecol 44, 1120–1126 (2018). https://doi.org/10.1007/s10886-018-1022-5

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  • DOI: https://doi.org/10.1007/s10886-018-1022-5

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