Advances in research on olfactory receptors of mosquitoes

doi:10.12140/j.issn.1000-7423.2020.05.019

Abstract

Abstract:

Many behaviors of mosquitoes rely on the olfactory system, such as feeding, mating, seeking host and blood-sucking through odors released by the host or natural environment. Therefore, the olfactory system is crucial for mosquitoes in adaptation of to the external environment and population reproduction. Mosquito olfactory receptors(ORs), which serve as a hub for transmitting odor information, play a key role in odor-evoked behaviors. Therefore, based on understanding of mosquito odor-evoked behaviors, to elucidate the characteristics of OR gene expression, and the mechanisms of OR-mediated olfactory signal transductionin association with the design of repellents, can further advance the knowledge of mosquito olfaction, thereby providing scientific basis for development of new measures for mosquito control.

Key words: Mosquito, Olfactory receptors, Repellents

CLC Number:

R384.11

WANG Yang, LI Ting-ting, GONG Mao-qing. Advances in research on olfactory receptors of mosquitoes[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2020, 38(5): 647-652.

Figures/Tables 1

References 54

[1]	Zhu GH, Xiao JP, Liu T, et al. Spatiotemporal analysis of the dengue outbreak in Guangdong Province, China[J]. BMC Infect Dis, 2019,19(1):493. doi: 10.1186/s12879-019-4015-2 pmid: 31164093
[2]	Hennessey M, Fischer M, Staples JE. Zika virus spreads to new areas-region of the Americas, May 2015-January 2016[J]. MMWR, 2016,65(3):55-58. doi: 10.15585/mmwr.mm6503e1 pmid: 26820163
[3]	World Health Organization. World malaria report 2019[R]. Geneva: WHO, 2019.
[4]	Fleischer J, Pregitzer P, Breer H, et al. Access to the odor world: olfactory receptors and their role for signal transduction in insects[J]. Cell Mol Life Sci, 2018,75(3):485-508. doi: 10.1007/s00018-017-2627-5 pmid: 28828501
[5]	Chertemps T, Younus F, Steiner C, et al. An antennal carboxylesterase from Drosophila melanogaster, esterase 6, is a candidate odorant-degrading enzyme toward food odorants[J]. Front Physiol, 2015,6:315. doi: 10.3389/fphys.2015.00315 pmid: 26594178
[6]	Tsitoura P, Andronopoulou E, Tsikou D, et al. Expression and membrane topology of Anopheles gambiae odorant receptors in lepidopteran insect cells[J]. PLoS One, 2010,5(11):e15428. doi: 10.1371/journal.pone.0015428 pmid: 21082026
[7]	Nichols AS, Chen SS, Luetje CW. Subunit contributions to insect olfactory receptor function: channel block and odorant recognition[J]. Chem Senses, 2011,36(9):781-790. pmid: 21677030
[8]	Gomez-Diaz C, Martin F, Garcia-Fernandez JM, et al. The two main olfactory receptor families in Drosophila, ORs and IRs: a comparative approach[J]. Front Cell Neurosci, 2018,12:253. doi: 10.3389/fncel.2018.00253 pmid: 30214396
[9]	Butterwick JA, Del Mármol J, Kim KH, et al. Cryo-EM structure of the insect olfactory receptor Orco[J]. Nature, 2018,560(7719):447-452. doi: 10.1038/s41586-018-0420-8 pmid: 30111839
[10]	Soffan A, Subandiyah S, Makino H, et al. Evolutionary analysis of the highly conserved insect odorant coreceptor (Orco) revealed a positive selection mode, implying functional flexibility[J]. J Insect Sci, 2018,18(6):1-8.
[11]	Carraher C, Dalziel J, Jordan MD, et al. Towards an understanding of the structural basis for insect olfaction by odorant receptors[J]. Insect Biochem Mol Biol, 2015,66:31-41. doi: 10.1016/j.ibmb.2015.09.010 pmid: 26416146
[12]	Clyne PJ, Warr CG, Freeman MR, et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila[J]. Neuron, 1999,22(2):327-338. doi: 10.1016/s0896-6273(00)81093-4 pmid: 10069338
[13]	Benton R, Sachse S, Michnick SW, et al. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo[J]. PLoS Biol, 2006,4(2):e20. doi: 10.1371/journal.pbio.0040020 pmid: 16402857
[14]	Hill CA, Fox AN, Pitts RJ, et al. G protein-coupled receptors in Anopheles gambiae[J]. Science, 2002,298(5591):176-178. doi: 10.1126/science.1076196 pmid: 12364795
[15]	Bohbot J, Pitts RJ, Kwon HW, et al. Molecular characterization of the Aedes aegypti odorant receptor gene family[J]. Insect Mol Biol, 2007,16(5):525-537. doi: 10.1111/j.1365-2583.2007.00748.x pmid: 17635615
[16]	Arensburger P, Megy K, Waterhouse RM, et al. Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics[J]. Science, 2010,330(6000):86-88. doi: 10.1126/science.1191864 pmid: 20929810
[17]	Chen XG, Jiang XT, Gu JB, et al. Genome sequence of the Asian Tiger mosquito, Aedes albopictus, reveals insights into its biology, genetics, and evolution[J]. Proc Natl Acad Sci USA, 2015,112(44):E5907-E5915. doi: 10.1073/pnas.1516410112 pmid: 26483478
[18]	Luo SH. Genome-wide identification and tissue expression analysis of odorant receptor genes in Anopheles sinensis[D]. Chongqing: Chongqing Normal University, 2017. (in Chinese)
	( 罗世惠. 中华按蚊气味受体基因的全基因组鉴定及组织表达分析[D]. 重庆: 重庆师范大学, 2017.)
[19]	Potter CJ. Stop the biting: targeting a mosquito’s sense of smell[J]. Cell, 2014,156(5):878-881. doi: 10.1016/j.cell.2014.02.003 pmid: 24581489
[20]	Choo YM, Buss GK, Tan KM, et al. Multitasking roles of mosquito labrum in oviposition and blood feeding[J]. Front Physiol, 2015,6:306. doi: 10.3389/fphys.2015.00306 pmid: 26578978
[21]	Takken W, Knols BG. Odor-mediated behavior of Afrotropical malaria mosquitoes[J]. Annu Rev Entomol, 1999,44:131-157. doi: 10.1146/annurev.ento.44.1.131 pmid: 9990718
[22]	Gao Q, Su F, Zhou YB, et al. Autogeny, fecundity, and other life history traits of Culex pipiens molestus (Diptera : Culicidae) in Shanghai, China[J]. J Med Entomol, 2019,56(3):656-664. pmid: 30605531
[23]	Iatrou K, Biessmann H. Sex-biased expression of odorant receptors in antennae and palps of the African malaria vector Anopheles gambiae[J]. Insect Biochem Mol Biol, 2008,38(2):268-274. doi: 10.1016/j.ibmb.2007.11.008 pmid: 18207086
[24]	Cork A, Park KC. Identification of electrophysiologically-active compounds for the malaria mosquito, Anopheles gambiae, in human sweat extracts[J]. Med Vet Entomol, 1996,10(3):269-276. doi: 10.1111/j.1365-2915.1996.tb00742.x pmid: 8887339
[25]	Zwiebel LJ, Takken W. Olfactory regulation of mosquito-host interactions[J]. Insect Biochem Mol Biol, 2004,34(7):645-652. doi: 10.1016/j.ibmb.2004.03.017 pmid: 15242705
[26]	Scialò F, Hansson BS, Giordano E, et al. Molecular and functional characterization of the odorant receptor 2 (OR2) in the tiger mosquito Aedes albopictus[J]. PLoS One, 2012,7(5):e36538. doi: 10.1371/journal.pone.0036538 pmid: 22606270
[27]	Rinker DC, Pitts RJ, Zhou XF, et al. Blood meal-induced changes to antennal transcriptome profiles reveal shifts in odor sensitivities in Anopheles gambiae[J]. Proc Natl Acad Sci USA, 2013,110(20):8260-8265. doi: 10.1073/pnas.1302562110 pmid: 23630291
[28]	Taparia T, Ignell R, Hill SR. Blood meal induced regulation of the chemosensory gene repertoire in the southern house mosquito[J]. BMC Genomics, 2017,18(1):393. doi: 10.1186/s12864-017-3779-2 pmid: 28525982
[29]	Das De T, Thomas T, Verma S, et al. A synergistic transcriptional regulation of olfactory genes drives blood-feeding associated complex behavioral responses in the mosquito Anopheles culicifacies[J]. Front Physiol, 2018,9:577. doi: 10.3389/fphys.2018.00577 pmid: 29875685
[30]	Zhang JJ. Transcriptome profiling of chemosensory genes in different chemosensory organs of the malaria vector Anopheles sinensis[D]. Chongqing: Chongqing Normal University, 2019. (in Chinese)
	( 张晶晶. 中华按蚊化感组织的转录组测序及化感基因的表达谱分析[D]. 重庆: 重庆师范大学, 2019.)
[31]	Lombardo F, Salvemini M, Fiorillo C, et al. Deciphering the olfactory repertoire of the tiger mosquito Aedes albopictus[J]. BMC Genomics, 2017,18(1):770-793. doi: 10.1186/s12864-017-4144-1 pmid: 29020917
[32]	McBride CS, Baier F, Omondi AB, et al. Evolution of mosquito preference for humans linked to an odorant receptor[J]. Nature, 2014,515(7526):222-227. doi: 10.1038/nature13964 pmid: 25391959
[33]	DeGennaro M, McBride CS, Seeholzer L, et al. Orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET[J]. Nature, 2013,498(7455):487-491. doi: 10.1038/nature12206 pmid: 23719379
[34]	Liu HM, Liu T, Xie LH, et al. Functional analysis of Orco and odorant receptors in odor recognition in Aedes albopictus[J]. Parasit Vectors, 2016,9(1):363. doi: 10.1186/s13071-016-1644-9 pmid: 27350348
[35]	Ye Z, Liu F, Liu NN. Olfactory responses of southern house mosquito, Culex quinquefasciatus, to human odorants[J]. Chem Senses, 2016,41(5):441-447. doi: 10.1093/chemse/bjv089 pmid: 26969630
[36]	Li CX, Yan T, Dong YD, Evaluation of 1-octen-3-ol as attractant to collect vector mosquito in paddy field areas[J]. Acta Parasitol Med Entomologica Sinica, 2019,26(2):88-91. (in Chinese)
	( 李春晓, 阎婷, 董言德, 等. 1-辛烯-3-醇对我国稻田区主要媒介蚊种的引诱作用研究[J]. 寄生虫与医学昆虫学报, 2019,26(2):88-91.)
[37]	Liu HM, Liu LH, Cheng P, et al. An odorant receptor from Anopheles sinensis in China is sensitive to oviposition attractants[J]. Malar J, 2018,17(1):348. doi: 10.1186/s12936-018-2501-4 pmid: 30290802
[38]	Zhou J, Li CX, Lan CJ, et al. Comparative analysis of antennal olfactory gene expression between Culex pipiens pallens and Culex pipiens molestus[J]. Chin J Parasitol Parasit Dis, 2019,37(4):453-457. (in Chinese)
	( 周洁, 李春晓, 兰策介, 等. 淡色库蚊与骚扰库蚊触角嗅觉基因表达分析[J]. 中国寄生虫学与寄生虫病杂志, 2019,37(4):453-457.)
[39]	Yan T. The function of differential expression of odorant receptors in Culex pipiens quinquefasciatus and Culex pipiens molestus[D]. Beijing: Academy of Military Medical Sciences, 2014. (in Chinese)
	( 阎婷. 致倦库蚊和骚扰库蚊差异表达的气味受体(OR)基因的功能研究[D]. 北京: 中国人民解放军军事医学科学院, 2014.)
[40]	Liu HM, Wang LL, Cheng P, et al. Cloning and tissue expression profiling of the olfactory receptor gene Orco from Culex pipiens pallens[J]. J Parasit Biol, 2017,12(9):868-871, 882. (in Chinese)
	( 刘宏美, 王利磊, 程鹏, 等. 淡色库蚊嗅觉受体基因orco的克隆及组织表达谱分析[J]. 中国病原生物学杂志, 2017,12(9):868-871, 882.)
[41]	Nakagawa T, Vosshall LB. Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system[J]. Curr Opin Neurobiol, 2009,19(3):284-292. doi: 10.1016/j.conb.2009.07.015 pmid: 19660933
[42]	Wicher D, Schäfer R, Bauernfeind R, et al. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels[J]. Nature, 2008,452(7190):1007-1011. doi: 10.1038/nature06861 pmid: 18408711
[43]	Sato K, Pellegrino M, Nakagawa T, et al. Insect olfactory receptors are heteromeric ligand-gated ion channels[J]. Nature, 2008,452(7190):1002-1006. doi: 10.1038/nature06850 pmid: 18408712
[44]	Ray A. Reception of odors and repellents in mosquitoes[J]. Curr Opin Neurobiol, 2015,34:158-164. doi: 10.1016/j.conb.2015.06.014 pmid: 26202080
[45]	Dennis EJ, Dobosiewicz M, Jin X, et al. A natural variant and engineered mutation in a GPCR promote DEET resistance in C. elegans[J]. Nature, 2018,562(7725):119-123. doi: 10.1038/s41586-018-0546-8 pmid: 30258230
[46]	DeGennaro M. The mysterious multi-modal repellency of DEET[J]. Fly (Austin), 2015,9(1):45-51.
[47]	Afify A, Betz JF, Riabinina O, et al. Commonly used insect repellents hide human odors from Anopheles mosquitoes[J]. Curr Biol, 2019,29(21):3669-3680. doi: 10.1016/j.cub.2019.09.007 pmid: 31630950
[48]	Dennis EJ, Goldman OV, Vosshall LB. Aedes aegypti mosquitoes use their legs to sense DEET on contact[J]. Curr Biol, 2019, 29(9):1551-1556.e5. doi: 10.1016/j.cub.2019.04.004 pmid: 31031114
[49]	Xu PX, Choo YM, De La Rosa A, et al. Mosquito odorant receptor for DEET and methyl jasmonate[J]. Proc Natl Acad Sci USA, 2014,111(46):16592-16597. doi: 10.1073/pnas.1417244111 pmid: 25349401
[50]	Xu PX, Zeng FF, Bedoukian RH, et al. DEET and other repellents are inhibitors of mosquito odorant receptors for oviposition attractants[J]. Insect Biochem Mol Biol, 2019,113:103224. doi: 10.1016/j.ibmb.2019.103224 pmid: 31446031
[51]	Turner RM, Derryberry SL, Kumar BN, et al. Mutational analysis of cysteine residues of the insect odorant co-receptor (Orco) from Drosophila melanogaster reveals differential effects on agonist-and odorant-tuning receptor-dependent activation[J]. J Biol Chem, 2014,289(46):31837-31845. doi: 10.1074/jbc.M114.603993 pmid: 25271160
[52]	Jones PL, Pask GM, Rinker DC, et al. Functional agonism of insect odorant receptor ion channels[J]. Proc Natl Acad Sci USA, 2011,108(21):8821-8825. doi: 10.1073/pnas.1102425108 pmid: 21555561
[53]	Tsitoura P, Iatrou K. Positive allosteric modulation of insect olfactory receptor function by Orco agonists[J]. Front Cell Neurosci, 2016,10:275. doi: 10.3389/fncel.2016.00275 pmid: 28018173
[54]	Jones PL, Pask GM, Romaine IM, et al. Allosteric antagonism of insect odorant receptor ion channels[J]. PLoS One, 2012,7(1):e30304. doi: 10.1371/journal.pone.0030304 pmid: 22272331