Research progress on odor binding proteins and odor receptors of mosquitoes

doi:10.12140/j.issn.1000-7423.2020.06.013

Abstract

Abstract:

Prevention and control of mosquitoes is the main measure to control mosquito-borne diseases, and chemical control remains the primary approach for mosquito control. However, with the increasing occurrences of resistance to insecticides in mosquitoes, there is an imperative need for a novel, efficient and environmentally friendly method for mosquito control. Olfaction plays an important role in the life activities of mosquitoes. Many physiological behaviors of mosquitoes depend on olfaction, such as mating, blood-sucking and oviposition. This paper summarizes research progress on the olfaction-related odor-binding proteins and odor receptors of mosquitoes and discusses the related mechanisms and targets in mosquito repellence and attraction behaviors, in order to provide theoretical references for the application and improvement of mosquito vector control measures.

Key words: Mosquito, Odor binding protein, Odor receptor, Repellence, Attraction

CLC Number:

R384.11

GU Zhen-yu, ZHAO Teng, LI Chun-xiao. Research progress on odor binding proteins and odor receptors of mosquitoes[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2020, 38(6): 753-757.

Figures/Tables 1

References 51

[1]	Picollo MI, Vassena C, Orihuela PS, et al. High resistance to pyrethroid insecticides associated with ineffective field treatments in triatomainfestans (Hemiptera:Reduviidae) from northern argentina[J]. J Med Entomol, 2005,42(4):637-642. pmid: 16119553
[2]	Cueto GM, Zerba E, Picollo MI. Permethrin-resistant head lice (Anoplura:Pediculidae) in argentina are susceptible to spinosad[J]. J Med Entomol, 2006,43(3):634-635. doi: 10.1603/0022-2585(2006)43[634:phlapi]2.0.co;2 pmid: 16739427
[3]	Cabrera M, Jaffe K. An aggregation pheromone modulates lekking behavior in the vector mosquito Aedes aegypti (Diptera:Culicidae)[J]. J Am Mosq Control Assoc, 2007,23(1):1-10. doi: 10.2987/8756-971X(2007)23[1:AAPMLB]2.0.CO;2 pmid: 17536361
[4]	Breer H, Raming K, Krieger J. Signal recognition and transduction in olfactory neurons[J]. Biochim Biophys Acta, 1994,1224(2):277-287. pmid: 7981243
[5]	Bowen MF. The sensory physiology of host-seeking behavior in mosquitoes[J]. Annu Rev Entomol, 1991,36(1):139-158.
[6]	Montell C. Mosquito sensory systems[J]. Adv Insect Physiol, 2016(51):293-328.
[7]	Syed Z, Ishida Y, Taylor K, et al. Pheromone reception in fruit flies expressing a moth’s odorant receptor[J]. Proc Natl AcadSci USA, 2006,103(44):16538-16543.
[8]	Zhang J, Zhang JJ, Shi ZP, et al. Observation of antennal sensilla of the malaria vector Anopheles sinensis(Diptera:Culicidae) under scanning electron microscope[J]. Acta Ento Sin, 2019,62(3):312-322. (in Chinese)
	( 张静, 张晶晶, 史宗畔, 等. 疟疾媒介中华按蚊触角感器的扫描电镜观察[J]. 昆虫学报, 2019,62(3):312-322.)
[9]	Xu W, Cornel AJ, Leal WS. Odorant-binding proteins of the malaria mosquito anopheles funestus sensu stricto[J]. PLoS One, 2010,5(10):e15403. doi: 10.1371/journal.pone.0015403 pmid: 21042539
[10]	Vogt RG, Riddiford LM. Pheromone binding and inactivation by moth antennae[J]. Nature, 1981,293(5828):161-163. doi: 10.1038/293161a0 pmid: 18074618
[11]	Ishida Y, Cornel AJ, Leal WS. Identification and cloning of a female antenna-specific odorant-binding protein in the mosquito Culex quinquefasciatus[J]. J Chem Ecol, 2002,28(4):867-871. doi: 10.1023/a:1015253214273 pmid: 12035932
[12]	Vieira FG, Rozas J. Comparative genomics of the odorant-binding and chemosensory protein gene families across the arthropoda: Origin and evolutionary history of the chemosensory system[J]. Genome Biol Evol, 2011,3(3):476-490. doi: 10.1093/gbe/evr033
[13]	Manoharan M, Chong MNF, Vaitinadapoule A, et al. Comparative genomics of odorant binding proteins in anopheles gambiae, Aedes aegypti and Culex quinquefasciatus[J]. Genome BiolEvol, 2013,5(1):163-180.
[14]	Biessmann H, Nguyen QK, Le D, et al. Microarray-based survey of a subset of putative olfactory genes in the mosquito Anopheles gambiae[J]. Insect Mol Biol, 2005,14(6):575-589. doi: 10.1111/j.1365-2583.2005.00590.x pmid: 16313558
[15]	Zhou J, He X, Pickett JA, et al. Identification of odorant-binding proteins of the yellow fever mosquito Aedes aegypti: genome annotation and comparative analyses[J]. Insect MolBiol, 2008,17(2):147-163.
[16]	Pelletier J, Leal WS. Genome analysis and expression patterns of odorant-binding proteins from the southern house mosquito Culex pipiens quinquefasciatus[J]. PLoS One, 2009,4(7):e6237. doi: 10.1371/journal.pone.0006237 pmid: 19606229
[17]	Lombardo F, Salvemini M, Fiorillo C, et al. Deciphering the olfactory repertoire of the tiger mosquito Aedes albopictus[J]. BMC Genomics, 2017,18(1):1-23. doi: 10.1186/s12864-016-3406-7 pmid: 28049423
[18]	Kreher SA, Mathew D, Kim J, et al. Translation of sensory input into behavioral output via an olfactory system[J]. Neuron, 2008,59(1):110-124. doi: 10.1016/j.neuron.2008.06.010 pmid: 18614033
[19]	Li Z, Pickett JA, Field LM, et al. Identification and expression of odorant-binding proteins of the malaria-carrying mosquitoes Anopheles gambiae and Anopheles arabiensis[J]. Arch Insect Biochem Physiol, 2005,58(3):175-189. doi: 10.1002/arch.20047 pmid: 15717318
[20]	Biessmann H, Andronopoulou E, Biessmann MR, et al. The Anopheles gambiae odorant binding protein 1 (agamobp1) mediates indole recognition in the antennae of female mosquitoes[J]. PLoS One, 2010,5(3):1-8.
[21]	Sim S, Ramirez JL, Dimopoulos G. Dengue virus infection of the Aedes aegyptis alivary gland and chemosensory apparatus induces genes that modulate infection and blood-feeding behavior[J]. PLoS Pathog, 2012,8(3):e1002631. doi: 10.1371/journal.ppat.1002631 pmid: 22479185
[22]	Pelletier J, Guidolin AS, Syed Z, et al. Knockdown of a mosquito odorant-binding protein involved in the sensitive detection of oviposition attractants[J]. J Chem Ecol, 2010,36(3):245-248. doi: 10.1007/s10886-010-9762-x pmid: 20191395
[23]	Deng Y, Yan H, Gu J, et al. Molecular and functional characterization of odorant-binding protein genes in an invasive vector mosquito, Aedes albopictus[J]. PLoS One, 2013,8(7):e68836. doi: 10.1371/journal.pone.0068836 pmid: 23935894
[24]	Tsitsanou KE, Thireou T, Drakou CE, et al. Anopheles gambiae odorant binding protein crystal complex with the synthetic repellent deet: implications for structure-based design of novel mosquito repellents[J]. Cell Mol Life Sci, 2012,69(2):283-297. doi: 10.1007/s00018-011-0745-z
[25]	Ditzen M, Pellegrino M, Vosshall LB. Insect odorant receptors are molecular targets of the insect repellent deet[J]. Science, 2008,319(5871):1838-1842. doi: 10.1126/science.1153121 pmid: 18339904
[26]	Hallem EA, Carlson JR. Coding of odors by a receptor repertoire[J]. Cell, 2006,125(1):143-160. doi: 10.1016/j.cell.2006.01.050 pmid: 16615896
[27]	Jones PL, Pask GM, Rinker DC, et al. Functional agonism of insect odorant receptor ion channels[J]. Proc Natl AcadSci USA, 2011,108(21):8821-8825. doi: 10.1073/pnas.1102425108
[28]	Liu C, Pitts RJ, Bohbot JD, et al. Distinct olfactory signaling mechanisms in the malaria vector mosquito Anopheles gambiae[J]. PLoS Biol, 2010,8(8):365-377.
[29]	Hill CA, Fox AN, Pitts RJ, et al. G protein-coupled receptors in Anopheles gambiae[J]. Science, 2002,298(5591):176-178. pmid: 12364795
[30]	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
[31]	Bohbot JD, Pitts RJ, Kwon H, 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
[32]	Gimonneau G, Bouyer J, Morand S, et al. A behavioral mechanism underlying ecological divergence in the malaria mosquito Anopheles gambiae[J]. Behav Ecol, 2010,21(5):1087-1092. doi: 10.1093/beheco/arq114 pmid: 22476108
[33]	Fox AN, Pitts RJ, Robertson HM, et al. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiaeand evidence of down-regulation in response to blood feeding[J]. Proc Natl AcadSci USA, 2001,98(25):14693-14697.
[34]	Wang G, Carey AF, Carlson JR, et al. Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae[J]. Proc Natl Acad Sci USA, 2010,107(9):4418-4423. doi: 10.1073/pnas.0913392107 pmid: 20160092
[35]	Afify A, Betz JF, Riabinina O, et al. Commonly used insect repellents hide human odors from anopheles mosquitoes[J]. CurrBiol, 2019,29(21):3669.
[36]	Grant GG, Estrera RR, Pathak N, et al. Interactions of deet. Interactions of deet and novel repellents with mosquito odorant receptors[J]. J Med Entomol, 2020, 57: tjaa010. pmid: 32614052
[37]	Carey AF, Wang G, Su C, et al. Odorant reception in the malaria mosquito anopheles gambiae[J]. Nature, 2010,464(7285):66-71. doi: 10.1038/nature08834 pmid: 20130575
[38]	Schymura D, Forstner M, Schultze A, et al. Antennal expression pattern of two olfactory receptors and an odorant binding protein implicated in host odor detection by the malaria vector anopheles gambiae[J]. Int J Biol Sci, 2010,6(7):614-626.
[39]	Jung JW, Baeck S, Perumalsamy H, et al. A novel olfactory pathway is essential for fast and efficient blood-feeding in mosquitoes[J]. Sci Rep, 2015,5(1):13444.
[40]	Riffell JA. Olfaction: Repellents that congest the mosquito nose[J]. Curr Biol, 2019,29(21):R1124-R1126. doi: 10.1016/j.cub.2019.09.053 pmid: 31689395
[41]	Bernier UR, Kline DL, Schreck CE, et al. Chemical analysis of human skin emanations: comparison of volatiles from humans that differ in attraction of Aedes aegypti (Diptera:Culicidae)[J]. J Am Mosq Control Assoc, 2002,18(3):186-195.
[42]	Bohbot JD, Dickens JC. Insect repellents: modulators of mosquito odorant receptor activity[J]. PLoS One, 2010,5(8):e12138. doi: 10.1371/journal.pone.0012138 pmid: 20725637
[43]	Katritzky AR, Wang Z, Slavov SH, et al. Synjournal and bioassay of improved mosquito repellents predicted from chemical structure[J]. Proc Natl AcadSci USA, 2008,105(21):7359-7364.
[44]	Su CY, Menuz K, Carlson JR. Olfactory perception: Receptors, cells, and circuits[J]. Cell, 2009,139(1):45-59. doi: 10.1016/j.cell.2009.09.015 pmid: 19804753
[45]	Shang X, Xie G, Kong XY, , et al. An artificial co2-driven ionic gate inspired by olfactory sensory neurons in mosquitoes [J]. Adv Mater. An artificial co2-driven ionic gate inspired by olfactory sensory neurons in mosquitoes [J]. Adv Mater, 2017, 29(3). https://doi.org/10.1002/adma.201603884
[46]	Leal WS, Barbosa RMR, Xu W, et al. Reverse and conventional chemical ecology approaches for the development of oviposition attractants for Culex mosquitoes[J]. PLoS One, 2008,3(8):e3045. doi: 10.1371/journal.pone.0003045 pmid: 18725946
[47]	Choo Y, Xu P, Hwang JK, et al. Reverse chemical ecology approach for the identification of an oviposition attractant for Culex quinquefasciatus[J]. Proc Natl Acad Sci USA, 2018,115(4):714-719. pmid: 29311316
[48]	Pei D. The transcipt expression research ofanopheles sinensis antennae[D]. Changsha: Nati Univ of Defe Tech, 2016. (in Chinese)
	( 裴迪. 中华按蚊触角转录本表达的研究[D]. 长沙: 国防科学技术大学, 2016.)
[49]	Luo SH. Genome-wide identification and tissue expression analysis of odorant receptor genes in Anopheles sinensis[D]. Chongqing: Chongqing Normal Univ, 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.)
[50]	Cai Z, Yu X, Cheng G. Progress towards mosquito microbiome on regulating the transmission of mosquito-borne diseases[J]. Chin J Parasitol Parasit Dis, 2019,37(5):603-608. (in Chinese)
	( 蔡珍, 余茜, 程功. 蚊肠道微生物调节蚊媒传染病传播的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2019,37(5):603-608.)
[51]	Zhou J, Li CX, Lan CJ, et al. Comparative analysis of antennal olfactory gene expression between Culex pipienspallens and Culex pipiensmolestus[J]. Chin J Parasitol Parasit Dis, 2019,15(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, 2019,15(4):453-457.)

蚊虫种类	气味结合蛋白	气味受体
冈比亚按蚊An. gambiae	69^[14]	79^[29]
埃及伊蚊Ae. aegypti	111^[15]	131^[31]
白纹伊蚊Ae. albopictus	77^[17]	82^[17]
中华按蚊An. sinensis	58 ^[48]	58^[49]
致倦库蚊Cx. quinquefasciatus	109 ^[16]	180^[30]