Abstract
Odorant-binding proteins (OBPs) are small soluble proteins whose biological function is believed to be facilitating olfaction by assisting the transport of volatile chemicals in both vertebrate and insect sensory organs, where they are secreted. Their capability to interact with a broad range of hydrophobic compounds combined with interesting features such as being small, stable, and easy to produce and modify, makes them suitable targets for applied research in various industrial segments, including textile, cosmetic, pesticide, and pharmaceutical, as well as for military, environmental, health, and security field applications. In addition to reviewing already established biotechnological applications of OBPs, this paper also discusses their potential use in prospecting of new technologies. The development of new products for insect population management is currently the most prevailing use for OBPs, followed by biosensor technology, an area that has recently seen a significant increase in studies evaluating their incorporation into sensing devices. Finally, less typical approaches include applications in anchorage systems and analytical tools.
Key points
• Odorant-binding proteins (OBPs) present desired characteristics for applied research.
• OBPs are mainly used for developing new products for insect population control.
• Incorporation of OBPs into chemosensory devices is a growing area of study.
• Less conventional uses for OBPs include anchorage systems and analytical purposes.
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Availability of data and material
Not applicable.
References
Affonso R d S, Guimarães AP, Oliveira AA, GBC S, França TCC (2013) Applications of molecular modeling in the design of new insect repellents targeting the odorant binding protein of Anopheles gambiae. J Braz Chem Soc 24:473–482. https://doi.org/10.1590/s0103-50532013000300015
Antwi FB, Shama LM, Peterson RKD (2008) Risk assessments for the insect repellents DEET and picaridin. Regul Toxicol Pharmacol 51:31–36. https://doi.org/10.1016/j.yrtph.2008.03.002
Barbosa AJM, Oliveira AR, Roque ACA (2018) Protein- and peptide-based biosensors in artificial olfaction. Trends Biotechnol 36:1244–1258. https://doi.org/10.1016/j.tibtech.2018.07.004
Benton R, Vannice KS, Gomez-diaz C, Leslie B (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136:149–162. https://doi.org/10.1016/j.cell.2008.12.001.Variant
Bian X, Liu D, Zeng H, Zhang G, Wei R, Hou R (2013) Exposure to odors of rivals enhances sexual motivation in male giant pandas. PLoS One 8:e69889. https://doi.org/10.1371/journal.pone.0069889
Bianchi F, Basini G, Grolli S, Conti V, Bianchi F, Grasselli F, Careri M, Ramoni R (2013) An innovative bovine odorant binding protein-based filtering cartridge for the removal of triazine herbicides from water. Anal Bioanal Chem 405:1067–1075. https://doi.org/10.1007/s00216-012-6499-0
Bozdogan A, Hageneder S, Dostalek J (2020) Plasmonic biosensors relying on biomolecular conformational changes: Case of odorant binding proteins, 1st edn. Elsevier Inc.
Breer H (2003) Olfactory receptors: molecular basis for recognition and discrimination of odors. Anal Bioanal Chem 377:427–433. https://doi.org/10.1007/s00216-003-2113-9
Briand L, Nespoulous C, Huet JC, Pernollet JC (2001) Disulfide pairing and secondary structure of ASP1, an olfactory-binding protein from honeybee (Apis mellifera L). J Pept Res 58:540–545. https://doi.org/10.1034/j.1399-3011.2001.00949.x
Briand L, Swasdipan N, Nespoulous C, Bézirard V, Blon F, Huet J-C, Ebert P, Pernollet J-C (2002) Characterization of a chemosensory protein (ASP3c) from honeybee (Apis mellifera L.) as a brood pheromone carrier. Eur J Biochem 269:4586–4596. https://doi.org/10.1046/j.1432-1033.2002.03156.x
Brito NF, Moreira MF, Melo ACA (2016) A look inside odorant-binding proteins in insect chemoreception. J Insect Physiol 95:51–65. https://doi.org/10.1016/j.jinsphys.2016.09.008
Broschard TH, Bohlmann AM, Konietzny S, Schauer UMD, Dekant W (2013) Biotransformation and toxicokinetics of the insect repellent IR3535(R) in male and female human subjects after dermal exposure. Toxicol Lett 218:246–252. https://doi.org/10.1016/j.toxlet.2013.02.002
Cali K, Persaud KC (2020) Modification of an Anopheles gambiae odorant binding protein to create an array of chemical sensors for detection of drugs. Sci Rep 10:1–13. https://doi.org/10.1038/s41598-020-60824-7
Campanacci V, Lartigue A, Hällberg BM, Jones TA, Giudici-Orticoni MT, Tegoni M, Cambillau C (2003) Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding. Proc Natl Acad Sci U S A 100:5069–5074. https://doi.org/10.1073/pnas.0836654100
Capo A, Pennacchio A, Varriale A, D’Auria S, Staiano M (2018) The porcine odorant-binding protein as molecular probe for benzene detection. PLoS One 13:1–24. https://doi.org/10.1371/journal.pone.0202630
Carraher C, Dalziel J, Jordan MD, Christie DL, Newcomb RD, Kralicek AV (2015) Towards an understanding of the structural basis for insect olfaction by odorant receptors. Insect Biochem Mol Biol 66:31–41. https://doi.org/10.1016/j.ibmb.2015.09.010
Cave JW, Wickiser JK, Mitropoulos AN (2019) Progress in the development of olfactory-based bioelectronic chemosensors. Biosens Bioelectron 123:211–222. https://doi.org/10.1016/j.bios.2018.08.063
Cennamo N, Di Giovanni S, Varriale A, Staiano M, Di Pietrantonio F, Notargiacomo A, Zeni L, D’Auria S (2015) Easy to use plastic optical fiber-based biosensor for detection of butanal. PLoS One 10:1–12. https://doi.org/10.1371/journal.pone.0116770
Chahda JS, Soni N, Sun JS, Ebrahim SAM, Weiss BL, Carlson JR (2019) The molecular and cellular basis of olfactory response to tsetse fly attractants. PLoS Genet 15:1–22. https://doi.org/10.1371/journal.pgen.1008005
Coleman RE, Robert LL, Roberts LW, Glass JA, Seeley DC, Laughinghouse A, Perkins PV, Wirtz RA (1993) Laboratory evaluation of repellents against four anopheline mosquitoes (Diptera: Culicidae) and two phlebotomine sand flies (Diptera: Psychodidae). J Med Entomol 30:499–502. https://doi.org/10.1093/jmedent/30.3.499
Corcoran JA, Jordan MD, Carraher C, Newcomb RD (2014) A novel method to study insect olfactory receptor function using HEK293 cells. Insect Biochem Mol Biol 54:22–32. https://doi.org/10.1016/j.ibmb.2014.08.005
D’Onofrio C, Zaremska V, Zhu J, Knoll W, Pelosi P (2020) Ligand-binding assays with OBPs and CSPs. In: Ligand-binding assays with OBPs and CSPs, 1st edn. Elsevier Inc.
Da Costa KS, Galúcio JM, Da Costa CHS, Santana AR, Dos Santos CV, Do Nascimento LD, Lima E, Lima AH, Neves Cruz J, Alves CN, Lameira J (2019) Exploring the potentiality of natural products from essential oils as inhibitors of odorant-binding proteins: a structure- and ligand-based virtual screening approach to find novel mosquito repellents. ACS Omega 4:22475–22486. https://doi.org/10.1021/acsomega.9b03157
Dahanukar A, Hallem EA, Carlson JR (2005) Insect chemoreception. Curr Opin Neurobiol 15:423–430. https://doi.org/10.1016/j.conb.2005.06.001
Devillers J (2018) 2D and 3D structure–activity modelling of mosquito repellents: a review. SAR QSAR Environ Res 29:693–723. https://doi.org/10.1080/1062936X.2018.1513218
Di Pietrantonio F, Benetti M, Cannatà D, Verona E, Palla-Papavlu A, Fernández-Pradas JM, Serra P, Staiano M, Varriale A, D’Auria S (2015) A surface acoustic wave bio-electronic nose for detection of volatile odorant molecules. Biosens Bioelectron 67:516–523. https://doi.org/10.1016/j.bios.2014.09.027
Di Pietrantonio F, Cannatà D, Benetti M, Verona E, Varriale A, Staiano M, D’Auria S (2013) Detection of odorant molecules via surface acoustic wave biosensor array based on odorant-binding proteins. Biosens Bioelectron 41:328–334. https://doi.org/10.1016/j.bios.2012.08.046
Diaz JH (2016) Chemical and plant-based insect repellents: efficacy, safety, and toxicity. Wilderness Environ Med 27:153–163. https://doi.org/10.1016/j.wem.2015.11.007
Dimitratos SD, Hommel AS, Konrad KD, Simpson LM, Wu-Woods JJ, Woods DF (2019) Biosensors to monitor water quality utilizing insect odorant-binding proteins as detector elements. Biosensors 9:1–15. https://doi.org/10.3390/bios9020062
Dobritsa AA, Van Der Goes Van Naters W, Warr CG, Steinbrecht RA, Carlson JR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827–841. https://doi.org/10.1016/S0896-6273(03)00094-1
Drakou CE, Tsitsanou KE, Potamitis C, Fessas D, Zervou M, Zographos SE (2016) The crystal structure of the AgamOBP1•Icaridin complex reveals alternative binding modes and stereo-selective repellent recognition. Cell Mol Life Sci 74:319–338. https://doi.org/10.1007/s00018-016-2335-6
Du L, Zou L, Wang Q, Zhao L, Huang L, Wang P, Wu C (2015) A novel biomimetic olfactory cell-based biosensor with DNA-directed site-specific immobilization of cells on a microelectrode array. Sensors Actuators B Chem 217:186–192. https://doi.org/10.1016/j.snb.2014.08.054
Du S, Yang Z, Qin Y, Wang S, Duan H, Yang X (2018) Computational investigation of the molecular conformation-dependent binding mode of (E)-β-farnesene analogs with a heterocycle to aphid odorant-binding proteins. J Mol Model 24:70. https://doi.org/10.1007/s00894-018-3612-0
Duan SG, Li DZ, Wang MQ (2019) Chemosensory proteins used as target for screening behaviourally active compounds in the rice pest Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Insect Mol Biol 28:123–135. https://doi.org/10.1111/imb.12532
Ferrari E, Lodi T, Sorbi RT, Tirindelli R, Cavaggioni A, Spisni A (1997) Expression of a lipocalin in Pichia pastoris: secretion, purification and binding activity of a recombinant mouse major urinary protein. FEBS Lett 401:73–77. https://doi.org/10.1016/S0014-5793(96)01436-6
Firestein S (2001) How the olfactory system makes sense of scents. Nature 413:211–218
Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318:1–14. https://doi.org/10.1042/bj3180001
Flower DR, North ACT, Sansom CE (2000) The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta Protein Struct Mol Enzymol 1482:9–24. https://doi.org/10.1016/S0167-4838(00)00148-5
Franco TA, Oliveira DS, Moreira MF, Leal WS, Melo ACAA (2016) Silencing the odorant receptor co-receptor RproOrco affects the physiology and behavior of the Chagas disease vector Rhodnius prolixus. Insect Biochem Mol Biol 69:82–90. https://doi.org/10.1016/j.ibmb.2015.02.012
Franco TA, Xu P, Brito NF, Oliveira DS, Wen X, Moreira MF, Unelius CR, Leal WS, Melo ACA (2018) Reverse chemical ecology-based approach leading to the accidental discovery of repellents for Rhodnius prolixus, a vector of Chagas diseases refractory to DEET. Insect Biochem Mol Biol 103:46–52. https://doi.org/10.1016/j.ibmb.2018.10.004
Gao A, Wang Y, Zhang D, He Y, Zhang L, Liu Y, Wang Y, Song H, Li T (2020) Highly sensitive and selective detection of human-derived volatile organic compounds based on odorant binding proteins functionalized silicon nanowire array. Sensors Actuators B Chem 309:127762. https://doi.org/10.1016/j.snb.2020.127762
Gardner JW, Bartlett PN (1994) A brief history of electronic materials. Sensors Actuators B Chem 18:210–211
Gonçalves F, Castro TG, Nogueira E, Pires R, Silva C, Ribeiro A, Cavaco-Paulo A (2018a) OBP fused with cell-penetrating peptides promotes liposomal transduction. Colloids Surf B: Biointerfaces 161:645–653. https://doi.org/10.1016/j.colsurfb.2017.11.026
Goncalves F, Ribeiro A, Silva C, Cavaco-Paulo A (2019) Release of fragrances from cotton functionalized with carbohydrate-binding module proteins. ACS Appl Mater Interfaces 11:28499–28506. https://doi.org/10.1021/acsami.9b08191
Gonçalves F, Silva C, Ribeiro A, Cavaco-Paulo A (2018b) 1-Aminoanthracene transduction into liposomes driven by odorant-binding protein proximity. ACS Appl Mater Interfaces 10:27531–27539. https://doi.org/10.1021/acsami.8b10158
Grabe V, Sachse S (2018) Fundamental principles of the olfactory code. BioSystems 164:94–101. https://doi.org/10.1016/j.biosystems.2017.10.010
Guo W, Wang X, Ma Z, Xue L, Han J, Yu D, Kang L (2011) CSP and takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust. PLoS Genet 7:e1001291. https://doi.org/10.1371/journal.pgen.1001291
Hamana H, Shou-xin L, Breuils L, Hirono J, Sato T (2010) Heterologous functional expression system for odorant receptors. J Neurosci Methods 185:213–220. https://doi.org/10.1016/j.jneumeth.2009.09.024
Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711. https://doi.org/10.1016/j.neuron.2011.11.003
Heng S, Sluydts V, Durnez L, Mean V, Polo K, Tho S, Coosemans M, Van Griensven J (2017) Safety of a topical insect repellent (picaridin) during community mass use for malaria control in rural Cambodia. PLoS One 12:1–16. https://doi.org/10.1371/journal.pone.0172566
Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across Phyla. Annu Rev Neurosci 20:595–631. https://doi.org/10.1146/annurev.neuro.20.1.595
Hou X, Zhang DD, Yuvaraj JK, Corcoran JA, Andersson MN, Löfstedt C (2020) Functional characterization of odorant receptors from the moth Eriocrania semipurpurella: a comparison of results in the Xenopus oocyte and HEK cell systems. Insect Biochem Mol Biol 117:103289. https://doi.org/10.1016/j.ibmb.2019.103289
Hou Y, Jaffrezic-Renault N, Martelet C, Tlili C, Zhang A, Pernollet JC, Briand L, Gomila G, Errachid A, Samitier J, Salvagnac L, Torbiéro B, Temple-Boyer P (2005) Study of Langmuir and Langmuir-Blodgett films of odorant-binding protein/amphiphile for odorant biosensors. Langmuir 21:4058–4065. https://doi.org/10.1021/la0471801
Hurot C, Brenet S, Buhot A, Barou E, Belloir C, Briand L, Hou Y (2019) Highly sensitive olfactory biosensors for the detection of volatile organic compounds by surface plasmon resonance imaging. Biosens Bioelectron 123:230–236. https://doi.org/10.1016/j.bios.2018.08.072
Ibarra-Soria X, Nakahara TS, Lilue J, Jiang Y, Trimmer C, Souza MAA, Netto PHM, Ikegami K, Murphy NR, Kusma M, Kirton A, Saraiva LR, Keane TM, Matsunami H, Mainland J, Papes F, Logan DW (2017) Variation in olfactory neuron repertoires is genetically controlled and environmentally modulated. Elife 6:1–29. https://doi.org/10.7554/eLife.21476
Ju Q, Li X, Guo XQ, Du L, Shi CR, Qu MJ (2018) Two odorant-binding proteins of the dark black chafer (Holotrichia parallela) display preferential binding to biologically active host plant volatiles. Front Physiol 9:1–14. https://doi.org/10.3389/fphys.2018.00769
Kaiser L, Graveland-Bikker J, Steuerwald D, Vanberghem M, Herlihy K, Zhang S (2008) Efficient cell-free production of olfactory receptors: detergent optimization, structure, and ligand binding analyses. Proc Natl Acad Sci U S A 105:15726–15731. https://doi.org/10.1073/pnas.0804766105
Khadka R, Aydemir N, Carraher C, Hamiaux C, Colbert D, Cheema J, Malmström J, Kralicek A, Travas-Sejdic J (2019) An ultrasensitive electrochemical impedance-based biosensor using insect odorant receptors to detect odorants. Biosens Bioelectron 126:207–213. https://doi.org/10.1016/j.bios.2018.10.043
Klint JK, Senff S, Saez NJ, Seshadri R, Lau HY, Bende NS, Undheim EAB, Rash LD, Mobli M, King GF (2013) Production of recombinant disulfide-rich venom peptides for structural and functional analysis via expression in the periplasm of E. coli. PLoS One 8:e63865. https://doi.org/10.1371/journal.pone.0063865
Ko HJ, Park TH (2005) Piezoelectric olfactory biosensor: ligand specificity and dose-dependence of an olfactory receptor expressed in a heterologous cell system. Biosens Bioelectron 20:1327–1332. https://doi.org/10.1016/j.bios.2004.05.002
Korsching S (2002) Olfactory maps and odor images. Curr Opin Neurobiol 12:387–392
Kotlowski C, Larisika M, Guerin PM, Kleber C, Kröber T, Mastrogiacomo R, Nowak C, Pelosi P, Schütz S, Schwaighofer A, Knoll W (2018) Fine discrimination of volatile compounds by graphene-immobilized odorant-binding proteins. Sensors Actuators B Chem 256:564–572. https://doi.org/10.1016/j.snb.2017.10.093
Kröber T, Koussis K, Bourquin M, Tsitoura P, Konstantopoulou M, Awolola TS, Dani FR, Qiao H, Pelosi P, Iatrou K, Guerin PM (2018) Odorant-binding protein-based identification of natural spatial repellents for the African malaria mosquito Anopheles gambiae. Insect Biochem Mol Biol 96:36–50. https://doi.org/10.1016/j.ibmb.2018.03.008
Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446:542–546. https://doi.org/10.1038/nature05672
Larisika M, Kotlowski C, Steininger C, Mastrogiacomo R, Pelosi P, Schütz S, Peteu SF, Kleber C, Reiner-Rozman C, Nowak C, Knoll W (2015) Electronic olfactory sensor based on A. mellifera odorant-binding protein 14 on a reduced graphene oxide field-effect transistor. Angew Chem Int Ed 54:13245–13248. https://doi.org/10.1002/anie.201505712
Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714. https://doi.org/10.1016/j.neuron.2004.08.019
Lartigue A, Gruez A, Briand L, Blon F, Bézirard V, Walsh M, Pernollet JC, Tegoni M, Cambillau C (2004) Sulfur single-wavelength anomalous diffraction crystal structure of a pheromone-binding protein from the honeybee Apis mellifera L. J Biol Chem 279:4459–4464. https://doi.org/10.1074/jbc.M311212200
Leal WS (2011) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:120928130709004–120928130709391. https://doi.org/10.1146/annurev-ento-120811-153635
Leal WS (2017) Reverse chemical ecology at the service of conservation biology. Proc Natl Acad Sci U S A 114:12094–12096. https://doi.org/10.1073/pnas.1717375114
Leal WS, Barbosa RMR, Xu W, Ishida Y, Syed Z, Latte N, Chen AM, Morgan TI, Cornel AJ, Furtado A (2008) Reverse and conventional chemical ecology approaches for the development of oviposition attractants for Culex mosquitoes. PLoS One 3:e3045. https://doi.org/10.1371/journal.pone.0003045
Leal WS, Parra-Pedrazzoli AL, Kaissling K-EE, Morgan TI, Zalom FG, Pesak DJ, Dundulis EA, Burks CS, Higbee BS (2005) Unusual pheromone chemistry in the navel orangeworm: Novel sex attractants and a behavioral antagonist. Naturwissenschaften 92:139–146. https://doi.org/10.1007/s00114-004-0598-5
Lee KM, Son M, Kang JH, Kim D, Hong S, Park TH, Chun HS, Choi SS (2018) A triangle study of human, instrument and bioelectronic nose for non-destructive sensing of seafood freshness. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-017-19033-y
Lee SH, Jun SB, Ko HJ, Kim SJ, Park TH (2009) Cell-based olfactory biosensor using microfabricated planar electrode. Biosens Bioelectron 24:2659–2664. https://doi.org/10.1016/j.bios.2009.01.035
Li HL, Zhang LY, Zhuang SL, Ni CX, Shang HW (2013) Fluorescence investigation on the interaction of a prevalent competitive fluorescent probe with entomic odorant binding protein. Spectrosc Lett 46:527–534. https://doi.org/10.1080/00387010.2013.763830
Li QL, Yi SC, Li DZ, Nie XP, Li SQ, Wang MQ, Zhou AM (2018) Optimization of reverse chemical ecology method: false positive binding of Aenasius bambawalei odorant binding protein 1 caused by uncertain binding mechanism. Insect Mol Biol 27:305–318. https://doi.org/10.1111/imb.12372
Lim CM, Kwon JY, Cho WJ (2017) Field-effect transistor biosensor platform fused with Drosophila odorant-binding proteins for instant ethanol detection. ACS Appl Mater Interfaces 9:14051–14057. https://doi.org/10.1021/acsami.6b15539
Liu G, Arnaud P, Offmann B, Picimbon JF (2017) Genotyping and bio-sensing chemosensory proteins in insects. Sensors (Switzerland) 17. https://doi.org/10.3390/s17081801
Liu G, Ma H, Xie H, Xuan N, Guo X, Fan Z, Rajashekar B, Arnaud P, Offmann B, Picimbon JF (2016) Biotype characterization, developmental profiling, insecticide response and binding property of Bemisia tabaci chemosensory proteins: role of CSP in insect defense. PLoS One 11:1–29. https://doi.org/10.1371/journal.pone.0154706
Liu Q, Wang H, Li H, Zhang J, Zhuang S, Zhang F, Jimmy Hsia K, Wang P (2013) Impedance sensing and molecular modeling of an olfactory biosensor based on chemosensory proteins of honeybee. Biosens Bioelectron 40:174–179. https://doi.org/10.1016/j.bios.2012.07.011
Liu Y, Cui Z, Wang G, Zhou Q, Liu Y (2020) Cloning and functional characterization of three odorant receptors from the Chinese citrus fly Bactrocera minax (Diptera: Tephritidae). Front Physiol 11:1–9. https://doi.org/10.3389/fphys.2020.00246
Lu Y, Li H, Zhuang S, Zhang D, Zhang Q, Zhou J, Dong S, Liu Q, Wang P (2014) Olfactory biosensor using odorant-binding proteins from honeybee: ligands of floral odors and pheromones detection by electrochemical impedance. Sensors Actuators B Chem 193:420–427. https://doi.org/10.1016/j.snb.2013.11.045
Lu Y, Yao Y, Zhang Q, Zhang D, Zhuang S, Li H, Liu Q (2015) Olfactory biosensor for insect semiochemicals analysis by impedance sensing of odorant-binding proteins on interdigitated electrodes. Biosens Bioelectron 67:662–669. https://doi.org/10.1016/j.bios.2014.09.098
Maleszka J, Forêt S, Saint R, Maleszka R (2007) RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honeybee (Apis mellifera). Dev Genes Evol 217:189–196. https://doi.org/10.1007/s00427-006-0127-y
Manai R, Scorsone E, Rousseau L, Ghassemi F, Possas Abreu M, Lissorgues G, Tremillon N, Ginisty H, Arnault JC, Tuccori E, Bernabei M, Cali K, Persaud KC, Bergonzo P (2014) Grafting odorant binding proteins on diamond bio-MEMS. Biosens Bioelectron 60:311–317. https://doi.org/10.1016/j.bios.2014.04.020
Manoharan M, Ng Fuk Chong M, Vaïtinadapoulé A, Frumence E, Sowdhamini R, Offmann B, Chong MNF, Vätinadapoulé A, Frumence E, Sowdhamini R, Offmann B (2013) Comparative genomics of odorant binding proteins in Anopheles gambiae, Aedes aegypti, and Culex quinquefasciatus. Genome Biol Evol 5:163–180. https://doi.org/10.1093/gbe/evs131
Margaryan A, Moaddel R, Aldrich JR, Tsuruda JM, Chen AM, Leal WS, Wainer IW (2006) Synthesis of an immobilized Bombyx mori pheromone-binding protein liquid chromatography stationary phase. Talanta 70:752–755. https://doi.org/10.1016/j.talanta.2006.01.046
McQueen RH, Vaezafshar S (2020) Odor in textiles: A review of evaluation methods, fabric characteristics, and odor control technologies. Text Res J 90:1157–1173. https://doi.org/10.1177/0040517519883952
Miazzi F, Schulze HC, Zhang L, Kaltofen S, Hansson BS, Wicher D (2019) Low Ca2+ levels in the culture media support the heterologous expression of insect odorant receptor proteins in HEK cells. J Neurosci Methods 312:122–125. https://doi.org/10.1016/j.jneumeth.2018.11.021
Mombaerts P (1999) Molecular Biology of Odorant Receptors in Vertebrates. Annu Rev Neurosci 22:487–509. https://doi.org/10.1146/annurev.neuro.22.1.487
Mulla MY, Tuccori E, Magliulo M, Lattanzi G, Palazzo G, Persaud K, Torsi L (2015) Capacitance-modulated transistor detects odorant binding protein chiral interactions. Nat Commun 6:1–9. https://doi.org/10.1038/ncomms7010
Murphy EJ, Booth JC, Davrazou F, Port AM, Jones DNM (2013) Interactions of Anopheles gambiae odorant-binding proteins with a human-derived repellent: Implications for the mode of action of N,N-diethyl-3-methylbenzamide (DEET). J Biol Chem 288:4475–4485. https://doi.org/10.1074/jbc.M112.436386
Nichols AS, Luetje CW (2010) Transmembrane segment 3 of Drosophila melanogaster odorant receptor subunit 85b contributes to ligand-receptor interactions. J Biol Chem 285:11854–11862. https://doi.org/10.1074/jbc.M109.058321
Nomura Kitabayashi A, Arai T, Kubo T, Natori S (1998) Molecular cloning of cDNA for p10, a novel protein that increases in the regenerating legs of Periplaneta americana (American cockroach). Insect Biochem Mol Biol 28:785–790. https://doi.org/10.1016/S0965-1748(98)00058-7
Oliferenko PV, Oliferenko AA, Poda GI, Osolodkin DI, Pillai GG, Bernier UR, Tsikolia M, Agramonte NM, Clark GG, Linthicum KJ, Katritzky AR (2013) Promising Aedes aegypti repellent chemotypes identified through integrated QSAR, virtual screening, synthesis, and bioassay. PLoS One 8:1–13. https://doi.org/10.1371/journal.pone.0064547
Pagadala Damdaram KJ, Kempraj V, Aurade RM, Kumar Roy T, Shivashankara KS, Verghese A (2014) Computational reverse chemical ecology: virtual screening and predicting behaviorally active semiochemicals for Bactrocera dorsalis. BMC Genomics 15:209. https://doi.org/10.1186/1471-2164-15-209
Palla-Papavlu A, Patrascioiu A, Di Pietrantonio F, Fernández-Pradas JM, Cannatà D, Benetti M, D’Auria S, Verona E, Serra P (2014) Preparation of surface acoustic wave odor sensors by laser-induced forward transfer. Sensors Actuators B Chem 192:369–377. https://doi.org/10.1016/j.snb.2013.10.082
Paolini S, Tanfani F, Fini C, Bertoli E, Pelosi P (1999) Porcine odorant-binding protein: structural stability and ligand affinities measured by Fourier-transform infrared spectroscopy and fluorescence spectroscopy. Biochim Biophys Acta Protein Struct Mol Enzymol 1431:179–188. https://doi.org/10.1016/S0167-4838(99)00037-0
Pelosi P, Iovinella I, Zhu J, Wang G, Dani FR (2017) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biol Rev 93:184–200. https://doi.org/10.1111/brv.12339
Pelosi P, Mastrogiacomo R, Iovinella I, Tuccori E, Persaud KC (2014) Structure and biotechnological applications of odorant-binding proteins. Appl Microbiol Biotechnol 98:61–70. https://doi.org/10.1007/s00253-013-5383-y
Pelosi P, Zhu J, Knoll W (2018) Odorant-binding proteins as sensing elements for odour monitoring. Sensors (Switzerland) 18. https://doi.org/10.3390/s18103248
Plettner E, Lazar J, Prestwich EG, Prestwich GD (2000) Discrimination of pheromone enantiomers by two pheromone binding proteins from the gypsy moth Lymantria dispar. Biochemistry 39:8953–8962
Possas-Abreu M, Rousseau L, Ghassemi F, Lissorgues G, Habchi M, Scorsone E, Cal K, Persaud K (2017) Biomimetic diamond MEMS sensors based on odorant-binding proteins: sensors validation through an autonomous electronic system. ISOEN 2017 - ISOCS/IEEE Int Symp Olfaction Electron Nose, Proc 9–11. https://doi.org/10.1109/ISOEN.2017.7968909
Ramoni R, Bellucci S, Grycznyski I, Grycznyski Z, Grolli S, Staiano M, De Bellis G, Micciulla F, Pastore R, Tiberia A, Conti V, Merli E, Varriale A, Rossi M, D’Auria S (2007) The protein scaffold of the lipocalin odorant-binding protein is suitable for the design of new biosensors for the detection of explosive components. J Phys Condens Matter 19:395012. https://doi.org/10.1088/0953-8984/19/39/395012
Reiner-Rozman C, Kotlowski C, Knoll W (2016) Electronic biosensing with functionalized rGO FETs. Biosensors 6:1–12. https://doi.org/10.3390/bios6020017
Ricatti J, Acquasaliente L, Ribaudo G, De Filippis V, Bellini M, Llovera RE, Barollo S, Pezzani R, Zagotto G, Persaud KC, Mucignat-Caretta C (2019) Effects of point mutations in the binding pocket of the mouse major urinary protein MUP20 on ligand affinity and specificity. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-018-36391-3
Sandler BH, Nikonova L, Leal WS, Clardy J (2000) Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chem Biol 7:143–151. https://doi.org/10.1016/S1074-5521(00)00078-8
Sankaran S, Khot LR, Panigrahi S (2012) Biology and applications of olfactory sensing system: a review. Sensors Actuators B Chem 171–172:1–17. https://doi.org/10.1016/j.snb.2012.03.029, 1
Sankaran S, Panigrahi S, Mallik S (2011) Odorant binding protein based biomimetic sensors for detection of alcohols associated with Salmonella contamination in packaged beef. Biosens Bioelectron 26:3103–3109. https://doi.org/10.1016/j.bios.2010.07.122
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. https://doi.org/10.1038/nature06850
Shiao MS, Chang AYF, Liao BY, Ching YH, Lu MYJ, Chen SM, Li WH (2012) Transcriptomes of mouse olfactory epithelium reveal sexual differences in odorant detection. Genome Biol Evol 4:703–712. https://doi.org/10.1093/gbe/evs039
Siciliano P, He XLL, Woodcock C, Pickett JAA, Field LMM, Birkett MAA, Kalinova B, Gomulski LMM, Scolari F, Gasperi G, Malacrida ARR, Zhou JJJ (2014) Identification of pheromone components and their binding affinity to the odorant binding protein CcapOBP83a-2 of the Mediterranean fruit fly, Ceratitis capitata. Insect Biochem Mol Biol 48:51–62. https://doi.org/10.1016/j.ibmb.2014.02.005
Silva C, Matamá T, Azoia NG, Mansilha C, Casal M, Cavaco-Paulo A (2014) Odorant binding proteins: a biotechnological tool for odour control. Appl Microbiol Biotechnol 98:3629–3638. https://doi.org/10.1007/s00253-013-5243-9
Son M, Kim D, Kang J, Lim JH, Lee SH, Ko HJ, Hong S, Park TH (2016) Bioelectronic nose using odorant binding protein-derived peptide and carbon nanotube field-effect transistor for the assessment of Salmonella contamination in food. Anal Chem 88:11283–11287. https://doi.org/10.1021/acs.analchem.6b03284
Stanczyk NM, Brookfield JFY, Field LM, Logan JG (2013) Aedes aegypti mosquitoes exhibit decreased repellency by DEET following previous exposure. PLoS One:8. https://doi.org/10.1371/journal.pone.0054438
Strauch M, Lüdke A, Münch D, Laudes T, Giovanni Galizia C, Martinelli E, Lavra L, Paolesse R, Ulivieri A, Catini A, Capuano R, Di Natale C (2014) More than apples and oranges - detecting cancer with a fruit fly’s antenna. Sci Rep 4:1–9. https://doi.org/10.1038/srep03576
Suh E, Bohbot JD, Zwiebel LJ (2014) Peripheral olfactory signaling in insects. Curr Opin Insect Sci 6:86–92. https://doi.org/10.1016/j.cois.2014.10.006
Sun S, Zeng F, Yi S, Wang M (2019) Molecular screening of behaviorally active compounds with CmedOBP14 from the rice leaf folder Cnaphalocrocis medinalis
Sun SF, Zhou B, Hou HN, Liu Y, Xiang GY (2006) Studies on the interaction between oxaprozin-E and bovine serum albumin by spectroscopic methods. Int J Biol Macromol 39:197–200. https://doi.org/10.1016/j.ijbiomac.2006.03.020
Swale DR, Sun B, Tong F, Bloomquist JR (2014) Neurotoxicity and mode of action of N,N-diethyl-meta-toluamide (DEET). PLoS One 9. https://doi.org/10.1371/journal.pone.0103713
Szunerits S, Boukherroub R, Vasilescu A (2020) Electrochemical biosensing with odorant binding proteins. In: Electrochemical biosensing with odorant binding proteins, 1st edn. Elsevier Inc.
Tan J, Zaremska V, Lim S, Knoll W, Pelosi P (2019) Probe-dependence of competitive fluorescent ligand binding assays to odorant-binding proteins. Anal Bioanal Chem 412:547–554. https://doi.org/10.1007/s00216-019-02309-9
Tegoni M, Campanacci V, Cambillau C (2004) Structural aspects of sexual attraction and chemical communication in insects. Trends Biochem Sci 29:257–264. https://doi.org/10.1016/j.tibs.2004.03.003
Thireou T, Kythreoti G, Tsitsanou KE, Koussis K, Drakou CE, Kinnersley J, Kröber T, Guerin PM, Zhou JJ, Iatrou K, Eliopoulos E, Zographos SE (2018) Identification of novel bioinspired synthetic mosquito repellents by combined ligand-based screening and OBP-structure-based molecular docking. Insect Biochem Mol Biol 98:48–61. https://doi.org/10.1016/j.ibmb.2018.05.001
Tian Z, Liu J, Zhang Y (2016) Structural insights into Cydia pomonella pheromone binding protein 2 mediated prediction of potentially active semiochemicals. Sci Rep 6:1–11. https://doi.org/10.1038/srep22336
Tsitsanou KE, Thireou T, Drakou CE, Koussis K, Keramioti MV, Leonidas DD, Eliopoulos E, Iatrou K, Zographos SE (2012) Anopheles gambiae odorant binding protein crystal complex with the synthetic repellent DEET: implications for structure-based design of novel mosquito repellents. Cell Mol Life Sci 69:283–297. https://doi.org/10.1007/s00018-011-0745-z
Tzotzos G, Iley JN, Moore EA (2018) New insights on repellent recognition by Anopheles gambiae odorant-binding protein 1. PLoS One 13:1–23. https://doi.org/10.1371/journal.pone.0194724
Vanhove E, De Sanoit J, Arnault JC, Saada S, Mer C, Mailley P, Bergonzo P, Nesladek M (2007) Stability of H-terminated BDD electrodes: an insight into the influence of the surface preparation. Phys Status Solidi Appl Mater Sci 204:2931–2939
Venthur H, Zhou JJ (2018) Odorant receptors and odorant-binding proteins as insect pest control targets: a comparative analysis. Front Physiol 9:1–16. https://doi.org/10.3389/fphys.2018.01163
Vosshall LB, Hansson BS (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem Senses 36:497–498. https://doi.org/10.1093/chemse/bjr022
Wang B, Liu Y, He K, Wang G (2016) Comparison of research methods for functional characterization of insect olfactory receptors. Sci Rep 6:1–10. https://doi.org/10.1038/srep32806
Wasilewski T, Gębicki J, Kamysz W (2018) Advances in olfaction-inspired biomaterials applied to bioelectronic noses. Sensors Actuators B Chem 257:511–537. https://doi.org/10.1016/j.snb.2017.10.086
Wasilewski T, Szulczyński B, Wojciechowski M, Kamysz W, Gębicki J (2019) A highly selective biosensor based on peptide directly derived from the HarmOBP7 aldehyde binding site. Sensors (Switzerland) 19. https://doi.org/10.3390/s19194284
Wiles D, Yee J, Castillo U, Russell J, Spiller H, Casavant M (2014) A lethal case of DEET toxicity due to intentional ingestion. J Anal Toxicol 38:696–698. https://doi.org/10.1093/jat/bku082
Wojtasek H, Leal WS (1999) Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes. J Biol Chem 274:30950–30956. https://doi.org/10.1074/jbc.274.43.30950
Yabuki M, Portman KL, Scott DJ, Briand L, Taylor AJ (2010) DyBOBS: A dynamic biomimetic assay for odorant-binding to odor-binding protein. Chemosens Percept 3:108–117. https://doi.org/10.1007/s12078-010-9070-4
Yang G, Winberg G, Ren H, Zhang S (2011) Expression, purification and functional analysis of an odorant binding protein AaegOBP22 from Aedes aegypti. Protein Expr Purif 75:165–171. https://doi.org/10.1016/j.pep.2010.09.004
Yang H, Kim D, Kim J, Moon D, Song HS, Lee M, Hong S, Park TH (2017a) Nanodisc-based bioelectronic nose using olfactory receptor produced in Escherichia coli for the assessment of the death-associated odor cadaverine. ACS Nano 11:11847–11855. https://doi.org/10.1021/acsnano.7b04992
Yang RN, Li DZ, Yu G, Yi SC, Zhang Y, Kong DX, Wang MQ (2017b) Structural transformation detection contributes to screening of behaviorally active compounds: dynamic binding process analysis of DhelOBP21 from Dastarcus helophoroides. J Chem Ecol 43:1033–1045. https://doi.org/10.1007/s10886-017-0897-x
Yi SY, Li DZ, Zhou CX, Tang YL, Abdelnabby HE, Wang MQ (2018) Screening behaviorally active compounds based on fluorescence quenching in combination with binding mechanism analyses of SspOBP7, an odorant binding protein from Sclerodermus sp. Int J Biol Macromol 107:2667–2678. https://doi.org/10.1016/j.ijbiomac.2017.10.149
Yin J, Choo Y-M, Duan H, Leal WS (2015) Selectivity of odorant-binding proteins from the southern house mosquito tested against physiologically relevant ligands. Front Physiol 6:56. https://doi.org/10.3389/fphys.2015.00056
Zarzo M (2007) The sense of smell: Molecular basis of odorant recognition. Biol Rev 82:455–479. https://doi.org/10.1111/j.1469-185X.2007.00019.x
Zhang D, Lu Y, Zhang Q, Yao Y, Li S, Li H, Zhuang S, Jiang J, Liu GL, Liu Q (2015) Nanoplasmonic monitoring of odorants binding to olfactory proteins from honeybee as biosensor for chemical detection. Sensors Actuators B Chem 221:341–349. https://doi.org/10.1016/j.snb.2015.06.091
Zhou YL, Zhu XQ, Gu SH, Cui H, Guo YY, Zhou JJ, Zhang YJ (2014) Silencing in Apolygus lucorum of the olfactory coreceptor Orco gene by RNA interference induces EAG response declining to two putative semiochemicals. J Insect Physiol 60:31–39. https://doi.org/10.1016/j.jinsphys.2013.10.006
Zhou XH, Zhang L, Ban LP, Iovinella I, Zhao LJ, Gao Q, Felicioli A, Sagona S, Pieraccini G, Pelosi P, Dani FR (2013) Diversity, abundance, and sex-specific expression of chemosensory proteins in the reproductive organs of the locust Locusta migratoria manilensis. Biol Chem 394:43–54. https://doi.org/10.1515/hsz-2012-0114
Zhou YT, Li L, Zhou XR, Tan Y, Pang BP (2020) Three chemosensory proteins involved in chemoreception of Oedaleus asiaticus (Orthopera: Acridoidea). J Chem Ecol 46:138–149. https://doi.org/10.1007/s10886-019-01138-5
Zhu J, Arena S, Spinelli S, Liu D, Zhang G, Wei R, Cambillau C, Scaloni A, Wang G, Pelosi P (2017) Reverse chemical ecology: olfactory proteins from the giant panda and their interactions with putative pheromones and bamboo volatiles. Proc Natl Acad Sci U S A 114:E9802–E9810. https://doi.org/10.1073/pnas.1711437114
Zographos SE, Eliopoulos E, Thireou T, Tsitsanou KE (2018) OBP Structure-aided repellent discovery. In: Computational design of chemicals for the control of mosquitoes and their diseases. CRC Press, pp 65–106
Zohora SE, Khan AM, Hundewale N (2013) Chemical sensors employed in electronic noses: a review. Adv Intell Syst Comput 178:177–184. https://doi.org/10.1007/978-3-642-31600-5_18
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This study was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM/CNPq), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. No additional external funding was received for this study.
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A.C.A.M. and N.F.B. conceived the presented concept for a review article. N.F.B. was responsible for bibliographic search, critical discussion, article design, illustrations and writing of the manuscript. D.S.O. and T.C.S. contributed to article design, writing and bibliographic enrichment. A.C.A.M. and M.F.M. contributed with critical discussion and provided writing support. All authors provided input, read and approved the final version of the manuscript.
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Brito, N.F., Oliveira, D.S., Santos, T.C. et al. Current and potential biotechnological applications of odorant-binding proteins. Appl Microbiol Biotechnol 104, 8631–8648 (2020). https://doi.org/10.1007/s00253-020-10860-0
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DOI: https://doi.org/10.1007/s00253-020-10860-0