Chemosensory Proteins: A Versatile Binding Family

  • Jiao Zhu
  • Immacolata Iovinella
  • Francesca Romana Dani
  • Paolo PelosiEmail author
  • Guirong WangEmail author


Chemosensory Proteins (CSPs), a family of small soluble polypeptides, own their name to their highly abundant expression in chemosensory organs of insects. However, CSPs are extremely versatile and perform different tasks in chemical communication, but also in unrelated functions, such as development and insecticide resistance. Their multifunction is certainly linked to their simple structure and easy refolding.

In insect chemoreception, they may perform functions similar to OBPs (Odorant-binding Proteins), another class of soluble polypeptides able to bind pheromones and odorants. Both families of proteins are reported to play roles in detecting and releasing semiochemicals with specific tasks according to species. In the first part of this review, after a brief historical introduction on their discovery, we describe structural aspects and binding properties of CSPs and compare such features with those of OBPs. Evolutionary aspects are also discussed with attention on the expansion of the CSP family across insect orders and species. The second part is focused on CSPs expressed in non-sensory organs and their possible physiological functions. Most of these proteins have been reported in pheromone glands, where they likely assist the release of chemical messages in the environment. Other functions have been reported in relation to solubilization of essential nutrients during feeding, embryo development and regeneration of amputated limbs, as well as resistance to insecticides. Finally, given the compact structure and stability of CSPs, their potential uses as biosensing elements, scavengers for noxious compounds and reservoirs for slow release of fragrances and other volatiles are proposed and discussed.


  1. Angeli S, Ceron F, Scaloni A, Monti M, Monteforti G, Minnocci A, Petacchi R, Pelosi P (1999) Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. Eur J Biochem 262:745–754CrossRefPubMedGoogle Scholar
  2. Baer B, Zareie R, Paynter E, Poland V, Millar AH (2012) Seminal fluid proteins differ in abundance between genetic lineages of honeybees. J Proteome 75:5646–5653CrossRefGoogle Scholar
  3. Ban LP, Zhang L, Yan YH, Pelosi P (2002) Binding properties of a locust’s chemosensory protein. Biochem Biophys Res Commun 293:50–54CrossRefGoogle Scholar
  4. Ban LP, Scaloni A, Brandazza A, Angeli S, Zhang L, Yan YH, Pelosi P (2003) Chemosensory proteins of Locusta migratoria. Insect Mol Biol 12:125–134CrossRefPubMedGoogle Scholar
  5. Ban L, Napolitano E, Serra A, Zhou X, Iovinella I, Pelosi P (2013) Identification of pheromone-like compounds in male reproductive organs of the oriental locust Locusta migratoria. Biochem Biophys Res Commun 437:620–624CrossRefPubMedGoogle Scholar
  6. Bautista MA, Bhandary B, Wijeratne AJ, Michel AP, Hoy CW, Mittapalli O (2015) Evidence for trade-offs in detoxification and chemosensation gene signatures in Plutella xylostella. Pest Manag Sci 71:423–432CrossRefPubMedGoogle Scholar
  7. Beynon RJ, Hurst JL (2004) Urinary proteins and the modulation of chemical scents in mice and rats. Peptides 25:1553–1563CrossRefPubMedGoogle Scholar
  8. Briand L, Nespoulous C, Huet JC, Takahashi M, Pernollet JC (2002) Characterization of a chemosensory protein (ASP3c) from honeybee (Apis mellifera L.) as a brood pheromone carrier. Eur J Biochem 269:4586–4596CrossRefPubMedGoogle Scholar
  9. Bruschini C, Dani FR, Pieraccini G, Guarna F, Turillazzi S (2006) Volatiles from the venom of five species of paper wasps (Polistes dominulus, P. gallicus, P. nimphus, P. sulcifer and P. olivaceus). Toxicon 48:473–475CrossRefGoogle Scholar
  10. Bruschini C, Cervo R, Protti I, Turillazzi S (2008) Caste differences in venom volatiles and their effect on alarm behaviour in the paper wasp Polistes dominulus (Christ). J Exp Biol 211:2442–2449CrossRefPubMedGoogle Scholar
  11. Calvello M, Guerra N, Brandazza A, D’Ambrosio C, Scaloni A, Dani FR, Turillazzi S, Pelosi P (2003) Soluble proteins of chemical communication in the social wasp Polistes dominulus. Cell Mol Life Sci 60:1933–1943CrossRefPubMedGoogle Scholar
  12. Campanacci V, Lartigue A, Hallberg 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 29:5069–5074CrossRefGoogle Scholar
  13. Cavaggioni A, Mucignat-Caretta C (2000) Major urinary proteins, r2u-globulins and aphrodisin. Biochim Biophys Acta 1482:218–228CrossRefPubMedGoogle Scholar
  14. Chang H, Liu Y, Yang T, Pelosi P, Dong S, Wang G (2015) Pheromone binding proteins enhance the sensitivity of olfactory receptors to sex pheromones in Chilo suppressalis. Sci Rep 5:13093CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cheng D, Lu Y, Zeng L, Liang G, He X (2015) Si-CSP9 regulates the integument and moulting process of larvae in the red imported fire ant, Solenopsis invicta. Sci Rep 5:9245CrossRefPubMedPubMedCentralGoogle Scholar
  16. Costa-da-Silva AL, Kojin BB, Marinotti O, James AA, Capurro ML (2013) Expression and accumulation of the two-domain odorant-binding protein AaegOBP45 in the ovaries of blood-fed Aedes aegypti. Parasite Vect 6:364CrossRefGoogle Scholar
  17. Damberger F, Nikonova L, Horst R, Peng G, Leal WS, Wuthrich K (2000) NMR characterization of a pH-dependent equilibrium between two folded solution conformations of the pheromone-binding protein from Bombyx mori. Protein Sci 9:1038–1041CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dani FR, Iovinella I, Felicioli A, Niccolini A, Calvello MA, Carucci MG, Qiao H, Pieraccini G, Turillazzi S, Moneti G, Pelosi P (2010) Mapping the expression of soluble olfactory proteins in the honeybee. J Proteome Res 9:1822–1833CrossRefPubMedGoogle Scholar
  19. Dani FR, Michelucci E, Francese S, Mastrobuoni G, Cappellozza S, La Marca G, Niccolini A, Felicioli A, Moneti G, Pelosi P (2011) Odorant-binding proteins and Chemosensory proteins in pheromone detection and release in the silkmoth Bombyx mori. Chem Senses 36:335–344CrossRefGoogle Scholar
  20. Dyanov HM, Dzitoeva SG (1995) Method for attachment of microscopic preparations on glass for in situ hybridization, PRINS and in situ PCR studies. BioTechniques 18:822–826PubMedGoogle Scholar
  21. Eliash N, Singh NK, Thangarajan S, Sela N, Leshkowitz D, Kamer Y, Zaidman I, Rafaeli A, Soroker V (2017) Chemosensing of honeybee parasite, Varroa destructor: transcriptomic analysis. Sci Rep 7:13091CrossRefPubMedPubMedCentralGoogle Scholar
  22. Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318:1–14CrossRefPubMedPubMedCentralGoogle Scholar
  23. Forêt S, Maleszka R (2006) Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res 16:1404–1413CrossRefPubMedPubMedCentralGoogle Scholar
  24. Forêt S, Wanner KW, Maleszka R (2007) Chemosensory proteins in the honey bee: Insights from the annotated genome, comparative analyses and expressional profiling. Insect Biochem Mol Biol 37:19–28CrossRefPubMedGoogle Scholar
  25. Forstner M, Breer H, Krieger J (2009) A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int J Biol Sci 5:745–757CrossRefPubMedPubMedCentralGoogle Scholar
  26. Free JB (1987) Pheromones of social bees. Cornell University Press, Ithaca, p 218Google Scholar
  27. Gomez-Diaz C, Reina JH, Cambillau C, Benton R (2013) Ligands for pheromone-sensing neurons are not conformationally activated odorant binding proteins. PLoS Biol 11:e1001546CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gong DP, Zhang HJ, Zhao P, Lin Y, Xia QY, Xiang ZH (2007) Identification and expression pattern of the chemosensory protein gene family in the silkworm, Bombyx mori. Insect Biochem Mol Biol 37:266–277CrossRefPubMedGoogle Scholar
  29. Gong Y, Pace TC, Castillo C, Bohne C, O’Neill MA, Plettner E (2009a) Ligand-interaction kinetics of the pheromone-binding protein from the gypsy moth, L. dispar: insights into the mechanism of binding and release. Chem Biol 16:162–172CrossRefPubMedGoogle Scholar
  30. Gong DP, Zhang HJ, Zhao P, Xia QY, Xiang ZH (2009b) The odorant binding protein gene family from the genome of silkworm, Bombyx mori. BMC Genomics 10:332CrossRefPubMedPubMedCentralGoogle Scholar
  31. González D, Zhao Q, McMahan C, Velasquez D, Haskins WE, Sponsel V, Cassill A, Renthal R (2009) The major antennal chemosensory protein of red imported fire ant workers. Insect Mol Biol 18:395–404CrossRefPubMedPubMedCentralGoogle Scholar
  32. Grosse-Wilde E, Svatos A, Krieger J (2006) A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem Senses 31:547–555CrossRefPubMedGoogle Scholar
  33. Gu SH, Wu KM, Guo YY, Pickett JA, Field LM, Zhou JJ, Zhang YJ (2013) Identification of genes expressed in the sex pheromone gland of the black cutworm Agrotis ipsilon with putative roles in sex pheromone biosynthesis and transport. BMC Genomics 14:636CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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:e1001291CrossRefPubMedPubMedCentralGoogle Scholar
  35. Heavner ME, Gueguen G, Rajwani R, Pagan PE, Small C, Govind S (2013) Partial venom gland transcriptome of a Drosophila parasitoid wasp, Leptopilina heterotoma, reveals novel and shared bioactive profiles with stinging Hymenoptera. Gene 526:195–204CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hojo MK, Ishii K, Sakura M, Yamaguchi K, Shigenobu S, Ozaki M (2015) Antennal RNA-sequencing analysis reveals evolutionary aspects of chemosensory proteins in the carpenter ant, Camponotus japonicus. Sci Rep 5:13541CrossRefPubMedPubMedCentralGoogle Scholar
  37. Holt RA et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149CrossRefPubMedGoogle Scholar
  38. Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 44:931–949CrossRefGoogle Scholar
  39. Iovinella I, Dani FR, Niccolini A, Sagona S, Michelucci E, Gazzano A, Turillazzi S, Felicioli A, Pelosi P (2011) Differential expression of odorant-binding proteins in the mandibular glands of the honey bee according to caste and age. J Proteome Res 10:3439–3449CrossRefPubMedGoogle Scholar
  40. Iovinella I, McAfee A, Mastrobuoni G, Kempa S, Foster LJ, Pelosi P, Dani FR (2018) Proteomic analysis of chemosensory organs in the honey bee parasite Varroa destructor: a comprehensive examination of the potential carriers for semiochemicals. J Proteome 181:131–141CrossRefGoogle Scholar
  41. Ishida Y, Chiang V, Leal WS (2002) Protein that makes sense in the Argentine ant. Naturwiss 89:505–507CrossRefPubMedGoogle Scholar
  42. Ishida Y, Ishibashi J, Leal WS (2013) Fatty acid solubilizer from the oral disk of the blowfly. PLoS One 8:e51779CrossRefPubMedPubMedCentralGoogle Scholar
  43. Jacquin-Joly E, Vogt RG, François MC, Nagnan-Le Meillour P (2001) Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chem Senses 26:833–844CrossRefGoogle Scholar
  44. Jansen S, Chmelík J, Zídek L, Padrta P, Novák P, Zdráhal Z, Picimbon JF, Löfstedt C, Sklenár V (2007) Structure of Bombyx mori chemosensory protein 1 in solution. Arch Insect Biochem Physiol 66:135–145CrossRefPubMedGoogle Scholar
  45. Jin X, Brandazza A, Navarrini A, Ban L, Zhang S, Steinbrecht RA, Zhang L, Pelosi P (2005) Expression and immunolocalisation of odorant-binding and chemosensory proteins in locusts. Cell Mol Life Sci 62:56–66CrossRefGoogle Scholar
  46. Kitabayashi AN, 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 28:785–790CrossRefPubMedGoogle Scholar
  47. Kulmuni J, Havukainen H (2013) Insights into the evolution of the CSP gene family through the integration of evolutionary analysis and comparative protein modeling. PLoS One 8:e63688CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kulmuni J, Wurm Y, Pamilo P (2013) Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates. Heredity 110:538–547CrossRefPubMedPubMedCentralGoogle Scholar
  49. Larisika M, Kotlowski C, Steininger C, Mastrogiacomo R, Pelosi P, Schutz 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 Chemie Int Ed 54:13245–13248CrossRefGoogle Scholar
  50. Lartigue A, Campanacci V, Roussel A, Larsson AM, Jones TA, Tegoni M, Cambillau C (2002) X-ray structure and ligand binding study of a moth chemosensory protein. J Biol Chem 277:32094–32098CrossRefPubMedGoogle Scholar
  51. Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391CrossRefPubMedGoogle Scholar
  52. Leal WS, Nikonova L, Peng G (1999) Disulfide structure of the pheromone binding protein from the silkworm moth, Bombyx mori. FEBS Lett 464:85–90CrossRefPubMedGoogle Scholar
  53. Leal WS, Chen AM, Ishida Y, Chiang VP, Erickson ML, Morgan TI, Tsuruda JM (2005) Kinetics and molecular properties of pheromone binding and release. Proc Natl Acad Sci U S A 102:5386–5391CrossRefPubMedPubMedCentralGoogle Scholar
  54. Li S, Picimbon JF, Ji SD, Kan YC, Qiao CL, Zhou JJ, Pelosi P (2008) Multiple functions of an odorant-binding protein in the mosquito Aedes aegypti. Biochem Biophys Res Commun 372:464–468CrossRefPubMedGoogle Scholar
  55. Liu GX, Xuan N, Chu D, Xie HY, Fan ZX, Bi YP, Picimbon JF, Qin YC, Zhong ST, Li YF, Gao ZL, Pan WL, Wang GY, Rajashekar B (2014a) Biotype expression and insecticide response of Bemisia tabaci chemosensory protein-1. Arch Insect Biochem Physiol 85:137–151CrossRefPubMedGoogle Scholar
  56. Liu YL, Guo H, Huang LQ, Pelosi P, Wang CZ (2014b) Unique function of a chemosensory protein in the proboscis of two Helicoverpa species. J Exp Biol 217:1821–1826CrossRefPubMedGoogle Scholar
  57. Liu GX, 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:e0154706CrossRefPubMedPubMedCentralGoogle Scholar
  58. Loebel D, Scaloni A, Paolini S, Fini C, Ferrara L, Breer H, Pelosi P (2000) Cloning, post-translational modifications, heterologous expression, ligand-binding and modelling of boar salivary lipocalin. Biochem J 350:369–379CrossRefPubMedPubMedCentralGoogle Scholar
  59. Maleszka R, Stange G (1997) Molecular cloning, by a novel approach, of a cDNA encoding a putative olfactory protein in the labial palps of the moth Cactoblastis cactorum. Gene 202:39–43CrossRefPubMedGoogle Scholar
  60. 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 217:189–196CrossRefPubMedGoogle Scholar
  61. Mameli M, Tuccini A, Mazza M, Petacchi R, Pelosi P (1996) Soluble proteins in chemosensory organs of phasmids. Insect Biochem Mol Biol 26:875–882CrossRefPubMedGoogle Scholar
  62. Marchese S, Pes D, Scaloni A, Carbone V, Pelosi P (1998) Lipocalins of boar salivary glands binding odours and pheromones. Eur J Biochem 252:563–568CrossRefPubMedGoogle Scholar
  63. Marchese S, Angeli S, Andolfo A, Scaloni A, Brandazza A, Mazza M, Picimbon JF, Leal WS, Pelosi P (2000) Soluble proteins from chemosensory organs of Eurycantha calcarata (Insecta, Phasmatodea). Insect Biochem Mol Biol 30:1091–1098CrossRefPubMedGoogle Scholar
  64. Marinotti O, Ngo T, Kojin BB, Chou SP, Nguyen B, Juhn J, Carballar-Lejarazú R, Marinotti PN, Jiang X, Walter MF, Tu Z, Gershon PD, James AA (2014) Integrated proteomic and transcriptomic analysis of the Aedes aegypti eggshell. BMC Dev Biol 14:15CrossRefPubMedPubMedCentralGoogle Scholar
  65. Mastrobuoni G, Qiao H, Iovinella I, Sagona S, Niccolini A, Boscaro F, Caputo B, Orejuela MR, dellaTorre A, Kempa S, Felicioli A, Pelosi P, Moneti G, Dani FR (2013) A proteomic investigation of soluble olfactory proteins in Anopheles gambiae. PLoS One 8:e75162CrossRefPubMedPubMedCentralGoogle Scholar
  66. Mastrogiacomo R, D’Ambrosio C, Niccolini A, Serra A, Gazzano A, Scaloni A, Pelosi P (2014) An odorant-binding protein is abundantly expressed in the nose and in the seminal fluid of the rabbit. PLoS One 9:111932CrossRefGoogle Scholar
  67. Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5:e118CrossRefPubMedPubMedCentralGoogle Scholar
  68. McKenna MP, Hekmat-Scafe DS, Gaines P, Carlson JR (1994) Putative Drosophila pheromone-binding proteins expressed in a sub-region of the olfactory system. J Biol Chem 269:16340–16347PubMedGoogle Scholar
  69. McKenzie SK, Oxley PR, Kronauer DJC (2014) Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins. BMC Genomics 15:718–732CrossRefPubMedPubMedCentralGoogle Scholar
  70. Missbach C, Vogel H, Hansson BS, Groβe-Wilde E (2015) Identification of odorant binding proteins and chemosensory proteins in antennal transcriptomes of the jumping bristletail Lepismachilis y-signata and the firebrat Thermobia domestica: evidence for an independent OBP-OR origin. Chem Senses 40:615–626CrossRefPubMedGoogle Scholar
  71. Monaco HL (2000) The transthyretin-retinol-binding protein complex. Biochim Biophys Acta 1482:65–72CrossRefPubMedGoogle Scholar
  72. Monteforti G, Angeli S, Petacchi R, Minnocci A (2002) Ultrastructural characterization of antennal sensilla and immunocytochemical localization of a chemosensory protein in Carausius morosus Brünner (Phasmida: Phasmatidae). Arthropod Struct Dev 30:195–205CrossRefPubMedGoogle Scholar
  73. 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 6:6010CrossRefPubMedPubMedCentralGoogle Scholar
  74. Nagnan-Le Meillour P, Cain AH, Jacquin-Joly E, François MC, Ramachandran S, Maida R, Steinbrecht RA (2000) Chemosensory proteins from the proboscis of Mamestra brassicae. Chem Sens 25:541–553CrossRefGoogle Scholar
  75. Newcomer ME, Ong DE (2000) Plasma retinol binding protein: structure and function of the prototypic lipocalin. Biochim Biophys Acta 1482:57–64CrossRefPubMedPubMedCentralGoogle Scholar
  76. Nomura A, Kawasaki K, Kubo T, Natori S (1992) Purification and localization of p10, a novel protein that increases in nymphal regenerating legs of Periplaneta americana American cockroach. Int J Dev Biol 36:391–398PubMedGoogle Scholar
  77. Ono M, Terabe H, Hori H, Sasaki M (2003) Insect signalling: components of giant hornet alarm pheromone. Nature 424:637–638CrossRefPubMedGoogle Scholar
  78. Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–314CrossRefPubMedGoogle Scholar
  79. Pelosi P (1994) Odorant-binding proteins. Crit Rev Biochem Mol Biol 29:199–228CrossRefPubMedGoogle Scholar
  80. Pelosi P, Baldaccini NE, Pisanelli AM (1982) Identification of a specific olfactory receptor for 2-isobutyl-3-methoxypyrazine. Biochem J 201:245–248CrossRefPubMedPubMedCentralGoogle Scholar
  81. Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 63:1658–1676CrossRefPubMedGoogle Scholar
  82. Pelosi P, Iovinella I, Felicioli A, Dani FR (2014a) Soluble proteins of chemical communication: an overview across arthropods. Front Physiol 5:320CrossRefPubMedPubMedCentralGoogle Scholar
  83. Pelosi P, Mastrogiacomo R, Iovinella I, Tuccori E, Persaud KC (2014b) Structure and biotechnological applications of odorant-binding proteins. Appl Microbiol Biotechnol 98:61–70CrossRefPubMedGoogle Scholar
  84. Pelosi P, Iovinella I, Zhu J, Wang G, Dani FR (2018a) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biol Rev Camb Philos Soc 93:184–200CrossRefPubMedGoogle Scholar
  85. Pelosi P, Zhu J, Knoll W (2018b) Odorant-binding proteins as sensing elements for odour monitoring. Sensors 18(10):3248CrossRefGoogle Scholar
  86. Picimbon JF (2003) Biochemistry and evolution of CSP and OBP proteins. In: Blomquist GJ, Vogt RG (eds) Insect pheromone biochemistry and molecular biology – the biosynthesis and detection of pheromones and plant volatiles. Elsevier, London/San Diego, pp 539–566CrossRefGoogle Scholar
  87. Picimbon JF, Leal WS (1999) Olfactory soluble proteins of cockroaches. Insect Biochem Mol Biol 30:973–978CrossRefGoogle Scholar
  88. Picimbon JF, Dietrich K, Breer H, Krieger J (2000a) Chemosensory proteins of Locusta migratoria (Orthoptera: Acrididae). Insect Biochem Mol Biol 30:233–241CrossRefPubMedGoogle Scholar
  89. Picimbon JF, Dietrich K, Angeli S, Scaloni A, Krieger J, Breer H, Pelosi P (2000b) Purification and molecular cloning of chemosensory proteins from Bombyx mori. Arch Insect Biochem Physiol 44:120–129CrossRefPubMedGoogle Scholar
  90. Picimbon JF, Dietrich K, Krieger J, Breer H (2001) Identity and expression pattern of chemosensory proteins in Heliothis virescens (Lepidoptera, Noctuidae). Insect Biochem Mol Biol 31:1173–1181CrossRefPubMedGoogle Scholar
  91. Pikielny CW, Hasan G, Rouyer F, Rosbash H (1994) Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12:35–49CrossRefPubMedGoogle Scholar
  92. Qiao H, Tuccori E, He X, Gazzano A, Field L, Zhou JJ, Pelosi P (2009) Discrimination of alarm pheromone (E)-beta-farnesene by aphid odorant-binding proteins. Insect Biochem Mol Biol 39:414–419CrossRefPubMedGoogle Scholar
  93. Renthal R, Manghnani L, Bernal S, Qu Y, Griffith WP, Lohmeyer K, Guerrero FD, Borges LMF, Pérez de León A (2017) The chemosensory appendage proteome of Amblyomma americanum (Acari: Ixodidae) reveals putative odorant-binding and other chemoreception-related proteins. Insect Sci 24:730–742CrossRefPubMedGoogle Scholar
  94. Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 11:1395–1403CrossRefGoogle Scholar
  95. Robertson HM, Gadau J, Wanner KW (2010) The insect chemoreceptor superfamily of the parasitoid jewel wasp Nasonia vitripennis. Insect Mol Biol 19(Suppl 1):121–136CrossRefPubMedGoogle Scholar
  96. Sabatier L, Jouanguy E, Dostert C, Zachary D, Dimarcq JL, Bulet P, Imler JL (2003) Pherokine-2 and -3: two Drosophila molecules related to pheromone/odor-binding proteins induced by viral and bacterial infections. Eur J Biol 270:3398–3407CrossRefGoogle Scholar
  97. Sánchez-Gracia A, Vieira FG, Rozas J (2009) Molecular evolution of the major chemosensory gene families in insects. Hered (Edinb) 103:208–216CrossRefGoogle Scholar
  98. 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 7:143–151CrossRefPubMedGoogle Scholar
  99. Scaloni A, Monti M, Angeli S, Pelosi P (1999) Structural analyses and disulfide-bridge pairing of two odorant-binding proteins from Bombyx mori. Biochem Biophys Res Commun 266:386–391CrossRefPubMedGoogle Scholar
  100. Spinelli S, Vincent F, Pelosi P, Tegoni M, Cambillau C (2002) Boar salivary lipocalin: three-dimensional X-ray structure and androstenol/androstenone docking simulations. Eur J Biochem 269:2449–2456CrossRefPubMedGoogle Scholar
  101. Strandh M, Johansson T, Löfstedt C (2009) Global transcriptional analysis of pheromone biosynthesis-related genes in the female turnip moth, Agrotis segetum (Noctuidae) using a custom-made cDNA microarray. Insect Biochem Mol Biol 39:484–489CrossRefPubMedGoogle Scholar
  102. Sun YF, De Biasio F, Qiao HL, Iovinella I, Yang SX, Ling Y, Riviello L, Battaglia D, Falabella P, Yang XL, Pelosi P (2012a) Two odorant-binding proteins mediate the behavioural response of aphids to the alarm pheromone (E)-ß-farnesene and structural analogues. PLoS One 7:e32759CrossRefPubMedPubMedCentralGoogle Scholar
  103. Sun YL, Huang LQ, Pelosi P, Wang CZ (2012b) Expression in antennae and reproductive organs suggests a dual role of an odorant-binding protein in two sibling Helicoverpa species. PLoS One 7:e30040CrossRefPubMedPubMedCentralGoogle Scholar
  104. Sun M, Liu Y, Walker WB, Liu C, Lin K, Gu S, Zhang Y, Zhou J, Wang G (2013) Identification and characterization of pheromone receptors and interplay between receptors and pheromone binding proteins in the diamondback moth, Plutella xyllostella. PLoS One 8:e62098CrossRefPubMedPubMedCentralGoogle Scholar
  105. Sun H, Guan L, Feng H, Yin J, Cao Y, Xi J, Li K (2014) Functional characterization of chemosensory proteins in the scarab beetle, Holotrichia oblita Faldermann (Coleoptera: Scarabaeida). PLoS One 9:e107059CrossRefPubMedPubMedCentralGoogle Scholar
  106. Swarup S, Williams TI, Anholt RR (2011) Functional dissection of odorant binding protein genes in Drosophila melanogaster. Genes Brain Behav 10:648–657CrossRefPubMedPubMedCentralGoogle Scholar
  107. Tegoni M, Pelosi P, Vincent F, Spinelli S, Campanacci V, Grolli S, Ramoni R, Cambillau C (2000) Mammalian odorant binding proteins. Biochim Biophys Acta 1482:229–240CrossRefPubMedGoogle Scholar
  108. Tegoni M, Campanacci V, Cambillau C (2004) Structural aspects of sexual attraction and chemical communication in insects. Trends Biochem Sci 29:257–264CrossRefPubMedGoogle Scholar
  109. Tomaselli S, Crescenzi O, Sanfelice D, Ab E, Wechselberger R, Angeli S, Scaloni A, Boelens R, Tancredi T, Pelosi P, Picone D (2006) Solution structure of a chemosensory protein from the desert locust Schistocerca gregaria. Biochemistry 45:10606–10613CrossRefPubMedGoogle Scholar
  110. Tuccini A, Maida R, Rovero P, Mazza M, Pelosi P (1996) Putative odorant-binding proteins in antennae and legs of Carausius morosus Insecta, Phasmatodea. Insect Biochem Mol Biol 26:19–24CrossRefPubMedGoogle Scholar
  111. Vieira FG, Rozas J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 3:476–490CrossRefPubMedPubMedCentralGoogle Scholar
  112. Vieira FG, Forêt S, He X, Rozas J, Field LM, Zhou JJ (2012) Unique features of odorant-binding proteins of the parasitoid wasp Nasonia vitripennis revealed by genome annotation and comparative analyses. PLoS One 7:e43034CrossRefPubMedPubMedCentralGoogle Scholar
  113. Vizueta J, Frías-López C, Macías-Hernández N, Arnedo MA, Sánchez-Gracia A, Rozas J (2017) Evolution of chemosensory gene families in arthropods: insight from the first inclusive comparative transcriptome analysis across spider appendages. Genome Biol Evol 9:178–196PubMedGoogle Scholar
  114. Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293:161–163CrossRefGoogle Scholar
  115. Wang T, Zhao M, Rotgans BA, Ni G, Dean JF, Nahrung HF, Cummins SF (2016) Proteomic analysis of the venom and venom sac of the woodwasp, Sirex noctilio – towards understanding its biological impact. J Proteome 146:195–206CrossRefGoogle Scholar
  116. Wanner KW, Willis LG, Theilmann DA, Isman MB, Feng Q, Plettner E (2004) Analysis of the insect OS-D-like gene family. J Chem Ecol 30:889–911CrossRefPubMedGoogle Scholar
  117. Werren JH et al. (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327:343–348Google Scholar
  118. Xia YH, Zhang YN, Hou XQ, Li F, Dong SL (2015) Large number of putative chemoreception and pheromone biosynthesis genes revealed by analyzing transcriptome from ovipositor-pheromone glands of Chilo suppressalis. Sci Rep 5:7888CrossRefPubMedPubMedCentralGoogle Scholar
  119. Xu PX, Zwiebel LJ, Smith DP (2003) Identification of a distinct family of genes encoding atypical odorant-binding proteins in the malaria vector mosquito, Anopheles gambiae. Insect Mol Biol 12:549–560CrossRefPubMedGoogle Scholar
  120. Xu PX, Atkinson R, Jones DN, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45:193–200CrossRefPubMedGoogle Scholar
  121. Xuan N, Bu X, Liu YY, Yang X, Liu GX, Fan ZX, Bi YP, Yang LQ, Lou QN, Rajashekar B, Leppik G, Kasvandik S, Picimbon JF (2014) Molecular evidence of RNA editing in Bombyx chemosensory protein family. PLoS One 9:e86932CrossRefPubMedPubMedCentralGoogle Scholar
  122. Xuan N, Guo X, Xie HY, Lou QN, Lu XB, Liu GX, Picimbon JF (2015) Increased expression of CSP and CYP genes in adult silkworm females exposed to avermectins. Insect Sci 22:203–219CrossRefPubMedGoogle Scholar
  123. Zhang YN, Zhu XY, Fang LP, He P, Wang ZQ, Chen G, Sun L, Ye ZF, Deng DG, Li JB (2015) Identification and expression profiles of sex pheromone biosynthesis and transport related genes in Spodoptera litura. PLoS One 10:e0140019CrossRefPubMedPubMedCentralGoogle Scholar
  124. Zhang R, Wang B, Grossi G, Falabella P, Liu Y, Yan S, Lu J, Xi J, Wang G (2017) Molecular basis of alarm pheromone detection in aphids. Curr Biol 27:55–61CrossRefPubMedGoogle Scholar
  125. Zhou JJ, Huang W, Zhang GA, Pickett JA, Field LM (2004) “Plus-C” odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. Gene 327:117–129CrossRefGoogle Scholar
  126. Zhou XH, Ban LP, Iovinella I, Zhao LJ, Gao Q, Felicioli A, Sagona S, Pieraccini G, Pelosi P, Zhang L, Dani FR (2013) Diversity, abundance and sex-specific expression of chemosensory proteins in the reproductive organs of the locust Locusta migratoria manilensis. Biol Chem 394:43–54CrossRefPubMedGoogle Scholar
  127. Zhu J, Iovinella I, Dani FR, Liu YL, Huang LQ, Liu Y, Wang CZ, Pelosi P, Wang GR (2016) Conserved chemosensory proteins in the proboscis and eyes of Lepidoptera. Int J Biol Sci 12:1394–1404CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.State Key Laboratory for Biology of Plant Diseases and Insect PestsInstitute of Plant Protection, Chinese Academy of Agricultural SciencesBeijingChina
  2. 2.Dipartimento di BiologiaUniversità degli Studi di FirenzeFlorenceItaly
  3. 3.AIT Austrian Institute of Technology GmbHTullnAustria

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