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The Role of the Peripheral Environment of Neuronal Receptors in Stimuli Perception by Insects’ Sense Organs: Facts and Hypotheses

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Abstract—

The role of intermediate substrates represented by morphological structures or chemical compounds located between the information carrier (stimulus) and the dendrite receptor membrane of insect sense organs is considered an example of olfactory, visual, mechanical, hygro-, and thermoreceptors. Intermediate substrates in olfactory sensillae are represented by their cuticular regions, pores or pore-tubular system, sensillum lymph, and pheromone-binding proteins. Intermediate structures also imply articular membrane (mechanoreceptor hairs), tympanic membrane (hearing organs), mineral statoliths (gravity receptors), iron oxide nanoparticles (magnetic field receptors), matrix surrounding the dendrites (hygroreceptors), microparticles associated with the dendrite membrane (thermoreceptors), and nonsclerotized mesocuticle (infrared receptors). There are two stages in propagation of a signal that is perceived by sense organs of most modalities: (1) before a signal contacts the peripheral environment (substance or structure) and (2) after a signal contacts the peripheral environment. Besides, a signal of one modality on the first stage of its propagation can be replaced by a signal of another modality at the second stage of propagation, as, for example, in hygro- or thermoreceptors, since the primary stimulus (moisture, heat/cold, or infrared radiation) is replaced by a mechanical effect on the dendrite membrane of its peripheral environment. The mechanisms of signal modality substitution in many sense organs, as well as the role of odorant-binding proteins and pore tubules in olfactory sensillae, have not been fully elucidated and require further investigation.

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REFERENCES

  1. Vinnikov, Y.A., Sensory Reception: Cytology, Molecular Mechanisms and Evolution, Berlin–Heidelberg: Springer-Verlag, 1974.

    Google Scholar 

  2. Clyne, P.J., Warr, C.G., Freeman, M.R., Lessing, D., Kim, J., and Carlson, J.R., A novel family of divergent seven-transmembrane proteins: Candidate odorant receptors in drosophila, Neuron, 1999, vol. 22, no. 2, pp. 327–338.

    CAS  PubMed  Google Scholar 

  3. Gao, Q. and Chess, A., Identification of candidate Drosophila olfactory receptors from genomic DNA sequence, Genomic, 1999, vol. 60, no. 1, pp. 31–39.

    CAS  Google Scholar 

  4. Vosshall, L.B., Amrein, H., Morozov, P.S., Rzhetsky, A., and Axel, R., A spatial map of olfactory receptor expression in the Drosophila antenna, Cell, 1999, vol. 96, no. 5, pp. 725–736.

    CAS  PubMed  Google Scholar 

  5. Leal, W.S., Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes, Ann. Rev. Entomol., 2013, vol. 58, pp. 373–391.

    CAS  Google Scholar 

  6. Andersson, M.N., Lofstedt, C., and Newcomb, R.D., Insect olfaction and the evolution of receptor tuning, Front. Ecol. Evol., 2015, vol. 3, p. 53.

    Google Scholar 

  7. Brito, N.F., Moreira, M.F., and Melo, A.C.A., A look inside odorant-binding protein in insect chemoreception, J. Insect Physiol., 2016, vol. 95, pp. 51–65.

    CAS  PubMed  Google Scholar 

  8. Chaika, S.Yu., Gistologiya nasekomykh: Uchebnoe posobie (Insect Histology: A Study Guide), Moscow: Mosk. Univ., 2017.

  9. Hallem, E.A., Dahanukar, A., and Carlson, J.R., Insect odor and taste receptors, Ann. Rev. Entomol., 2006, vol. 51, pp. 113–135.

    CAS  Google Scholar 

  10. Clyne, P., Warr, C., and Carlson, J., Candidate taste receptors in Drosophila, Science, 2000, vol. 287, no. 5459, pp. 1830–1834.

    CAS  PubMed  Google Scholar 

  11. Dunipace, L., Meister, S., McNealy, C., and Amrein, H., Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system, Curr. Biol., 2001, vol. 11, no. 11, pp. 822–835.

    CAS  PubMed  Google Scholar 

  12. Galindo, K. and Smith, D.P., A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla, Genetics, 2001, vol. 159, no. 3, pp. 1059–1072.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Koganezawa, M. and Shimada, I., Novel odorant-binding proteins expressed in the taste tissue of the fly, Chem. Senses, 2002, vol. 27, no. 4, pp. 319–332.

    CAS  PubMed  Google Scholar 

  14. Buck, L. and Axel, R., A novel multigene family may encode odorant receptors: A molecular basis for odor recognition, Cell, 1991, vol. 65, no. 1, pp. 175–187.

    CAS  PubMed  Google Scholar 

  15. Fan, J., Francis, F., Liu, Y., Chen, J.L., and Cheng, D.F., An overview of odorant-binding protein functions in insect peripheral olfactory reception, Genet. Mol. Res., 2011, vol. 10, no. 4, pp. 3056–3069.

    CAS  PubMed  Google Scholar 

  16. Benton, R., Vannice, K.S., Gomez-Diaz, C., and Vosshall, L.B., Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila, Cell, 2009, vol. 136, no. 1, pp. 149–162.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Rogers, M.E., Sun, M., Lerner, M.R., and Vogt, R.G., Snmp-1, a novel membrane protein of olfactory neurons of the silk moth Antheraea polyphemus with homology to the CD36 family of membrane proteins, J. Biol. Chem., 1997, vol. 272, no. 23, pp. 14792–14799.

    CAS  PubMed  Google Scholar 

  18. Vogt, R.G. and Riddiford, L.M., Pheromone binding and inactivation by moth antennae, Nature, 1981, vol. 293, no. 5828, pp. 161–163.

    CAS  PubMed  Google Scholar 

  19. Ishida, Y. and Leal, W.S., Chiral discrimination of the Japanese beetle sex pheromone and a behavioral antagonist by a pheromone-degrading enzyme, Proc. Nat. Acad. Sci. U.S.A., 2008, vol. 105, no. 26, pp. 9076–9080.

    CAS  Google Scholar 

  20. Larter, N.K., Sun, J.S., and Carlson, J.R., Organization and function of Drosophila odorant binding proteins, eLife, 2016, vol. 5, e20242.

    PubMed  PubMed Central  Google Scholar 

  21. Benton, R., Sachse, S., Stephen, W., Milnick, S.W., and Vosshall, L.B., Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo, PLoS Biol., 2006, vol. 4, no. 2, e20.

    PubMed  PubMed Central  Google Scholar 

  22. Rimal, S. and Lee, Y., The multidimensional ionotropic receptors of Drosophila melanogaster, Insect Mol. Biol., 2018, vol. 27, no. 1, pp. 1–7.

    CAS  PubMed  Google Scholar 

  23. Steinbrecht, R.A., Pore structures in insect olfactory sensilla: A review of data and concepts, Int. J. Insect Morphol. Embryol., 1997, vol. 26, nos. 3–4, pp. 229–245.

    Google Scholar 

  24. Klein, U., Sensillum-lymph proteins from antennal olfactory hairs of the moth Antheraea polyphemus (Saturniidae), Insect Biochem., 1987, vol. 17, no. 8, pp. 1193–1204.

    Google Scholar 

  25. Zhukovskaya, M.I., Odorant-dependent changes in surface cuticular secretions on the antenna of Pereplaneta americana, Sens. Sist., 2011, vol. 25, no. 1, pp. 78–86.

    Google Scholar 

  26. Maitani, M.M., Allara, D.L., Park, K.C., Lee, S.G., and Baker, T.C., Moth olfactory trichoid sensilla exhibit nanoscale-level heterogeneity in surface lipid properties, Arthropod Struct. Dev., 2010, vol. 39, no. 1, pp. 1–16.

    CAS  PubMed  Google Scholar 

  27. Chaika, S.Yu., Insect olfaction: A hypothesis about the role of liquid-crystalline pore tubules in olfactory sensilla as conductors of information on the nature of signaling molecules, Aktual. Probl. Sovrem. Nauki, 2013, vol. 2, no. 3, pp. 3–6.

    Google Scholar 

  28. Leal, W.S., Pheromone reception, in The Chemistry of Pheromones and Other Semiochemicals II. Topics in Current Chemistry, Schulz, S., Ed., Berlin–Heidelberg: Springer, 2005, vol. 240, pp. 1–36.

    Google Scholar 

  29. Pelosi, P., Iovinella, I., Zhu, J., Wang, G.R., and Dani, F.R., Beyond chemoreception: Diverse tasks of soluble olfactory proteins in insects, Biol. Rev., 2018, vol. 93, no. 1, pp. 184–200.

    PubMed  Google Scholar 

  30. Sun, J.S., Larter, N.K., Chahda, J.S., Rioux, D., Gumaste, A., and Carlson, J.R., Humidity response depends on the small soluble proteins Obp59a in Drosophila, eLife, 2018, vol. 7, e39249.

    PubMed  PubMed Central  Google Scholar 

  31. Jacquin-July, E., Francois, M.C., and Nagnan-Le, M.P., Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromone gland of Mamestra brassicae, Chem. Senses, 2001, vol. 26, no. 7, pp. 833–844.

    Google Scholar 

  32. Li, S., Picimbon, J.F., Li, S., Kan, Y., Chuanling, Q., Zhou, J.J., and Pelosi, P., Multiple functions of an odorant-binding protein in the mosquito Aedes aegypti, Biochem. Biophys. Res. Commun., 2008, vol. 372, no. 3, pp. 464–468.

    CAS  PubMed  Google Scholar 

  33. Sun, Y.L., Huang, L.Q., Pelosi, P., and Wang, C.Z., Expression in antennae and reproductive organs suggests a dual role of an odorant-binding protein in two sibling Helicoverpa species, PloS One, 2012, vol. 7, e30040.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Pitts, J.R., Liu, C., Zhou, X., Malpartida, J.C., and Zwiebel, L.J., Odorant receptor-mediated sperm activation in disease vector mosquitoes, Proc. Nat. Acad. Sci. U.S.A., 2014, vol. 111, no. 7, pp. 2566–2571.

    CAS  Google Scholar 

  35. Benoit, J.B., Vigneron, A., Broderick, N.A., Aksoy, S., and Weiss, B.L., Symbiont-induced odorant binding proteins mediate insect host hematopoiesis, eLife, 2017, vol. 6, e19535.

    PubMed  PubMed Central  Google Scholar 

  36. Kiely, A., Authier, A., Ktalicek, A.V., Warr, C.G., and Newcomb, R.D., Functional analysis of a Drosophila melanogaster olfactory receptor expressed in Sf9 cells, J. Neurosci. Methods, 2007, vol. 159, no. 2, pp. 189–194.

    CAS  PubMed  Google Scholar 

  37. Ai, M., Blais, S., Park, J-Y., Min, S., Neubert, T.A., and Suh, G.S.B., Ionotropic glutamate receptors IR64a and IR8a form a functional odorant receptor complex in vivo in Drosophila, J. Neurosci., 2013, vol. 33, no. 26, pp. 10741–10749.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Xu, P.X., Atkinson, R., Jones, D.N.M., and Smith, D.P., Drosophila OBP LUSH report is required for activity of pheromone-sensitive neurons, Neuron, 2005, vol. 45, no. 2, pp. 193–200.

    CAS  PubMed  Google Scholar 

  39. Gomez-Diaz, C., Reina, J.H., Cambillau, C., and Benton, R., Ligands for pheromone-sensing neurons are not conformationally activated odorant binding proteins, PLoS Biol., 2013, vol. 11, no. 4, e1001546.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Steinbrecht, R.A., Stimulus transport and inactivation in insect olfactory sensilla: Functional morphology, tracer experiments, and immunocytochemistry, in Nervous Systems: Principles of Design and Function, Singh, R.N., Ed., New Delhi: Wiley Eastern, 1992, pp. 417–435.

    Google Scholar 

  41. Ando, T., Sekine, S., Inagaki, S., Misaki, K., Badel, L., Moriya, H., Sami, M.M., Itakura, Y., Chihara, T., Kazama, H., Yonemura, S., and Hayashi, S., Nanopore formation in the cuticle of an insect olfactory sensillum, Curr. Biol., 2019, vol. 29, no. 9, pp. 1512–1520.

    CAS  PubMed  Google Scholar 

  42. Locke, M., Permeability of insect cuticle to water and lipids, Science, 1965, vol. 147, no. 3655, pp. 295–298.

    PubMed  Google Scholar 

  43. Brown, G.H. and Wolken, J.J., Liquid Crystals and Biological Structures, New York: Academic, 1979.

    Google Scholar 

  44. Leonovich, S.A., Sensornye sistemy paraziticheskikh kleshchei (Sensory Systems of Parasitic Mites), St. Petersburg: Nauka, 2005.

  45. Chandrasekhar, S., Liquid Crystals, London–New York: Cambridge Univ. Press, 1992, 2nd ed.

    Google Scholar 

  46. Woltman, S.J., Jay, D.G., and Crawford, G.P., Liquid-crystal materials find a new order in biomedical applications, Nat. Mater., 2007, vol. 6, no. 12, pp. 929–938.

    CAS  PubMed  Google Scholar 

  47. Smalyukh, I.I., Liquid crystals enable chemoresponsive reconfigurable colloidal self-assembly, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 9, pp. 3945–3946.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Roling, L.T., Scaranto, J., Herron, J.A., Yu, H., Choi, S., Abbott, N.L., and Mavrikakis, M., Towards first-principles molecular design of liquid crystal-based chemoresponsive systems, Nat. Commun., 2016, vol. 7, 13338.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Ostrovsky, M.A., Molecular physiology of visual pigment rhodopsin, Biochem. (Moscow) Suppl. Ser. A: Membr. Cell Biol., 2012, vol. 6, no. 2, pp. 128–138.

    Google Scholar 

  50. Popov, A.V., Akusticheskoe povedenie i slukh nasekomykh (Acoustic Behavior and Hearing of Insects), Leningrad: Nauka, 1985.

  51. Zhantiev, R.D., Bioakustika nasekomykh (Bioacoustics of Insects), Moscow: Mosk. Univ., 1981.

  52. Ishay, J.S., Shimony, T.(B.), and Arcan, L., The presence of statocysts and statoliths in social wasps (Hymenoptera, Vespinae), Life Sci., 1983, vol. 32, no. 15, pp. 1711–1719.

    CAS  PubMed  Google Scholar 

  53. Hsu, C.Y. and Li, C.W., Magnetoreception in honeybees, Science, 1994, vol. 265, no. 5, pp. 95–97.

    CAS  PubMed  Google Scholar 

  54. Altner, H. and Loftus, R., Ultrastructure and function of insect thermo- and hygroreceptors, Ann. Rev. Entomol., 1985, vol. 30, pp. 273–295.

    Google Scholar 

  55. Steinbrecht, R.A. and Muller, B., The thermo-hygrosensitive sensilla of the silkmoth, Bombyx mori: Morphological changes after dry- and moist-adaptation, Cell Tissue Res., 1991, vol. 266, no. 3, pp. 441–456.

    Google Scholar 

  56. Yokohari, F., Hygroreceptor mechanism in the antenna of the cockroach Periplaneta, J. Comp. Physiol., 1978, vol. 124, pp. 53–60.

    Google Scholar 

  57. Altner, H., Tichy, H., and Altner, I., Lamellated outer dendritic segments of a sensory cell within a poreless thermo- and hygroreceptive sensillum of the insect Carausius morosus, Cell Tissue Res., 1978, vol. 191, no. 2, pp. 287–304.

    CAS  PubMed  Google Scholar 

  58. Steinbrecht, R.A., The fine structure of thermo-/hygrosensitive sensilla in the silkmoth Bombyx mori: Receptor membrane substructure and sensory cell contacts, Cell Tissue Res., 1989, vol. 255, no. 1, pp. 49–57.

    Google Scholar 

  59. Vondran, T., Apel, K.-H., and Schmitz, H., The infrared receptor of Melanophila acuminata De Geer (Coleoptera: Buprestidae): Ultrastructural study of a unique insect thermoreceptor and its possible descent from a hair mechanoreceptor, Tissue Cell, 1995, vol. 27, no. 6, pp. 645–658.

    CAS  PubMed  Google Scholar 

  60. Schmitz, A. and Schmitz, H., Cuticle as functional interface in insect infrared receptors, in Functional Surface in Biology. III. Biologically-Inspired Systems, Gorb, S.N. and Gorb, E.V., Eds., Berlin: Springer, 2018, vol. 10, pp. 3–25.

    Google Scholar 

  61. Schneider, E.S., Schmitz, A., and Schmitz, H., Concept of an active amplification mechanism in the infrared organ of pyrophilous Melanophila beetles, Front. Physiol., 2015, vol. 6, p. 391.

    PubMed  PubMed Central  Google Scholar 

  62. Chen, C., Buhl, E., Xu, M., Croset, V., Rees, J.S., Lilley, K.S., Benton, R., Hodge, J.J., and Stanewsky, R., Drosophila ionotropic receptor 25a mediates circadian clock resetting by temperature, Nature, 2015, vol. 527, no. 7579, pp. 516–520.

    CAS  PubMed  Google Scholar 

  63. Knecht, Z.A., Silbering, A.F., Ni, L., Klein, M., Budelli, G., Bell, R., Abuin, L., Ferrer, A.J., Samuel, A.D., Benton, R., and Garrity, P.A., Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila, eLife, 2016, vol. 5, e17879.

    PubMed  PubMed Central  Google Scholar 

  64. Ni, L., Klein, M., Svec, K.V., Budelli, G., Chang, E.C., Ferrer, A.J., Benton, R., Samuel, A.D.T., and Garrity, P.A., The ionotropic receptors IR21a and IR 25a mediate cool sensing in Drosophila, eLife, 2016, vol. 5, e13254.

    PubMed  PubMed Central  Google Scholar 

  65. Nishino, H., Yamashita, S., Yamazaki, Y., Nishikawa, M., Yokohari, P., and Mizunami, M., Projection neurons originating from thermo- and hygrosensory glomeruli in the antennal lobe of the cockroach, J. Comp. Neurol., 2003, vol. 455, no. 1, pp. 40–55.

    PubMed  Google Scholar 

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ACKNOWLEDGMENTS

I thank Prof. J.R. Carlson of Yale University (United States) for kindly providing the figure.

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The study was financially supported by the State Assignment of Moscow State University (fundamental research, AAAA–A16–116021660101–5).

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  1. Department of Biology, Moscow State University, 119234, Moscow, Russia

    S. Yu. Chaika

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Chaika, S.Y. The Role of the Peripheral Environment of Neuronal Receptors in Stimuli Perception by Insects’ Sense Organs: Facts and Hypotheses. Moscow Univ. Biol.Sci. Bull. 75, 164–172 (2020). https://doi.org/10.3103/S0096392520040033

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