Odorant-Binding Proteins as Sensing Elements for Odour Monitoring

Odour perception has been the object of fast growing research interest in the last three decades. Parallel to the study of the corresponding biological systems, attempts are being made to model the olfactory system with electronic devices. Such projects range from the fabrication of individual sensors, tuned to specific chemicals of interest, to the design of multipurpose smell detectors using arrays of sensors assembled in a sort of artificial nose. Recently, proteins have attracted increasing interest as sensing elements. In particular, soluble olfaction proteins, including odorant-binding proteins (OBPs) of vertebrates and insects, chemosensory proteins (CSPs) and Niemann-Pick type C2 (NPC2) proteins possess interesting characteristics for their use in sensing devices for odours. In fact, thanks to their compact structure, their soluble nature and small size, they are extremely stable to high temperature, refractory to proteolysis and resistant to organic solvents. Moreover, thanks to the availability of many structures solved both as apo-proteins and in complexes with some ligands, it is feasible to design mutants by replacing residues in the binding sites with the aim of synthesising proteins with better selectivity and improved physical properties, as demonstrated in a number of cases.

[1]  R. Steinbrecht Structure and function of insect olfactory sensilla. , 2007, Ciba Foundation symposium.

[2]  K. Persaud,et al.  Gas sensors: towards an artificial nose , 1988 .

[3]  J. Storch,et al.  Niemann-Pick C2 (NPC2) and intracellular cholesterol trafficking. , 2009, Biochimica et biophysica acta.

[4]  S. Arena,et al.  Reverse chemical ecology: Olfactory proteins from the giant panda and their interactions with putative pheromones and bamboo volatiles , 2017, Proceedings of the National Academy of Sciences.

[5]  C. Cambillau,et al.  Crystal structure of Apis mellifera OBP14, a C-minus odorant-binding protein, and its complexes with odorant molecules. , 2012, Insect biochemistry and molecular biology.

[6]  J. Rozas,et al.  Evolution of Chemosensory Gene Families in Arthropods: Insight from the First Inclusive Comparative Transcriptome Analysis across Spider Appendages , 2016, Genome biology and evolution.

[7]  P. Pelosi,et al.  Proteomic analysis of castor bean tick Ixodes ricinus: a focus on chemosensory organs. , 2016, Insect biochemistry and molecular biology.

[8]  A. Scaloni,et al.  Biochemical characterization and bacterial expression of an odorant-binding protein from Locusta migratoria , 2003, Cellular and Molecular Life Sciences CMLS.

[9]  R. Axel,et al.  A novel multigene family may encode odorant receptors: A molecular basis for odor recognition , 1991, Cell.

[10]  K. Wüthrich,et al.  NMR characterization of a pH‐dependent equilibrium between two folded solution conformations of the pheromone‐binding protein from Bombyx mori , 2000, Protein science : a publication of the Protein Society.

[11]  C Cambillau,et al.  Mammalian odorant binding proteins. , 2000, Biochimica et biophysica acta.

[12]  T. Yamazaki,et al.  Niemann–Pick type C2 protein mediating chemical communication in the worker ant , 2014, Proceedings of the National Academy of Sciences.

[13]  D R Flower,et al.  The lipocalin protein family: structural and sequence overview. , 2000, Biochimica et biophysica acta.

[14]  G. Blobel,et al.  Clues to the mechanism of cholesterol transfer from the structure of NPC1 middle lumenal domain bound to NPC2 , 2016, Proceedings of the National Academy of Sciences.

[15]  L. Foster,et al.  Proteomic analysis of chemosensory organs in the honey bee parasite Varroa destructor: A comprehensive examination of the potential carriers for semiochemicals. , 2018, Journal of proteomics.

[16]  P. Pelosi,et al.  Conserved chemosensory proteins in the proboscis and eyes of Lepidoptera , 2016, International journal of biological sciences.

[17]  A. Pisanelli,et al.  Binding of [3H]-2-isobutyl-3-methoxypyrazine to cow olfactory mucosa , 1981 .

[18]  C. Löfstedt,et al.  Structure of Bombyx mori chemosensory protein 1 in solution. , 2007, Archives of insect biochemistry and physiology.

[19]  Paolo Dario,et al.  Sensors and Sensory Systems for Advanced Robots , 1988, NATO ASI Series.

[20]  C. Tokarski,et al.  Identification of Post-translational Modifications on Odorant-Binding Protein Isoforms from Pig Olfactory Secretome by High-Resolution Mass Spectrometry: O-β-N-acetylglucosaminylation and Phosphorylation , 2017, Front. Ecol. Evol..

[21]  F. Guerrero,et al.  The chemosensory appendage proteome of Amblyomma americanum (Acari: Ixodidae) reveals putative odorant‐binding and other chemoreception‐related proteins , 2017, Insect science.

[22]  Jing Zhang,et al.  Impedance sensing and molecular modeling of an olfactory biosensor based on chemosensory proteins of honeybee. , 2013, Biosensors & bioelectronics.

[23]  A. Scaloni,et al.  Structural analysis and disulfide-bridge pairing of two odorant-binding proteins from Bombyx mori. , 1999, Biochemical and biophysical research communications.

[24]  P. Pelosi,et al.  Binding of polycyclic aromatic hydrocarbons to mutants of odorant-binding protein: a first step towards biosensors for environmental monitoring. , 2008, Biochimica et biophysica acta.

[25]  A. North,et al.  Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography , 1992, Nature.

[26]  P. Grote,et al.  Crystal structure of aphrodisin, a sex pheromone from female hamster. , 2001, Journal of molecular biology.

[27]  J. Rozas,et al.  Comparative Genomics Reveals Thousands of Novel Chemosensory Genes and Massive Changes in Chemoreceptor Repertories across Chelicerates , 2018, Genome biology and evolution.

[28]  Alain Roussel,et al.  X-ray Structure and Ligand Binding Study of a Moth Chemosensory Protein* , 2002, The Journal of Biological Chemistry.

[29]  K. Persaud,et al.  An approach to an artificial nose. , 1985, Transactions - American Society for Artificial Internal Organs.

[30]  S. d'Auria,et al.  Mutant bovine odorant‐binding protein: Temperature affects the protein stability and dynamics as revealed by infrared spectroscopy and molecular dynamics simulations , 2008, Proteins.

[31]  C. Cambillau,et al.  Boar salivary lipocalin , 2002 .

[32]  F. Hilliou,et al.  Proteomic Analysis of Pig (Sus scrofa) Olfactory Soluble Proteome Reveals O-Linked-N-Acetylglucosaminylation of Secreted Odorant-Binding Proteins , 2014, Front. Endocrinol..

[33]  S. Snyder,et al.  Odorant-binding protein. Characterization of ligand binding. , 1990, The Journal of biological chemistry.

[34]  Mariella Tegoni,et al.  Structural aspects of sexual attraction and chemical communication in insects. , 2004, Trends in biochemical sciences.

[35]  Tomasz Wasilewski,et al.  Bioelectronic nose: Current status and perspectives. , 2017, Biosensors & bioelectronics.

[36]  P. Pelosi,et al.  Cooperative interactions between odorant-binding proteins of Anopheles gambiae , 2011, Cellular and Molecular Life Sciences.

[37]  M. Jordan,et al.  Towards an understanding of the structural basis for insect olfaction by odorant receptors. , 2015, Insect biochemistry and molecular biology.

[38]  C. Cambillau,et al.  Domain swapping creates a third putative combining site in bovine odorant binding protein dimer , 1996, Nature Structural Biology.

[39]  A. Scaloni,et al.  Soluble proteins of chemical communication in the social wasp Polistes dominulus , 2003, Cellular and Molecular Life Sciences CMLS.

[40]  Stefan Schütz,et al.  Electronic Olfactory Sensor Based on A. mellifera Odorant‐Binding Protein 14 on a Reduced Graphene Oxide Field‐Effect Transistor , 2015, Angewandte Chemie.

[41]  P. Pelosi,et al.  Soluble proteins of chemical communication: an overview across arthropods , 2014, Front. Physiol..

[42]  W. Leal,et al.  Disulfide structure of the pheromone binding protein from the silkworm moth, Bombyx mori , 1999, FEBS letters.

[43]  Selena Sironi,et al.  Electronic Noses for Environmental Monitoring Applications , 2014, Sensors.

[44]  S. Korsching Olfactory maps and odor images , 2002, Current Opinion in Neurobiology.

[45]  R. Tirindelli,et al.  Expression of a lipocalin in Pichia pastoris: secretion, purification and binding activity of a recombinant mouse major urinary protein , 1997, FEBS letters.

[46]  P. Mombaerts,et al.  Molecular biology of odorant receptors in vertebrates. , 1999, Annual review of neuroscience.

[47]  F. Tanfani,et al.  Porcine odorant-binding protein: structural stability and ligand affinities measured by fourier-transform infrared spectroscopy and fluorescence spectroscopy. , 1999, Biochimica et biophysica acta.

[48]  P. Pelosi,et al.  Niemann-Pick C2 Proteins: A New Function for an Old Family , 2018, Front. Physiol..

[49]  Shannon E. Stitzel,et al.  Artificial noses. , 2011, Annual review of biomedical engineering.

[50]  C. Cambillau,et al.  The Crystal Structure of a Cockroach Pheromone-binding Protein Suggests a New Ligand Binding and Release Mechanism* , 2003, Journal of Biological Chemistry.

[51]  R. Steinbrecht,et al.  Insects as model systems in cell biology. , 2010, Methods in cell biology.

[52]  W. Leal,et al.  Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. , 2013, Annual review of entomology.

[53]  Jonathan Pevsner,et al.  The three-dimensional structure of bovine odorant binding protein and its mechanism of odor recognition , 1996, Nature Structural Biology.

[54]  V. Ruta,et al.  Cryo-EM structure of the insect olfactory receptor Orco , 2018, Nature.

[55]  T. Getchell,et al.  Perireceptor and receptor events in vertebrate olfaction , 1984, Progress in Neurobiology.

[56]  Mohammad Yusuf Mulla,et al.  Capacitance-modulated transistor detects odorant binding protein chiral interactions , 2015, Nature Communications.

[57]  A. Scaloni,et al.  Soluble proteins from chemosensory organs of Eurycantha calcarata (Insects, Phasmatodea). , 2000, Insect biochemistry and molecular biology.

[58]  Ping Wang,et al.  Olfactory biosensor using odorant-binding proteins from honeybee: Ligands of floral odors and pheromones detection by electrochemical impedance , 2014 .

[59]  F. Zufall,et al.  Virus-Mediated Overexpression of Vomeronasal Receptors and Functional Assessment by Live-Cell Calcium Imaging. , 2018, Methods in molecular biology.

[60]  P. Pelosi,et al.  Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects , 2018, Biological reviews of the Cambridge Philosophical Society.

[61]  A. Scaloni,et al.  Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. , 1999, European journal of biochemistry.

[62]  P. Pelosi,et al.  General odorant-binding proteins and sex pheromone guide larvae of Plutella xylostella to better food. , 2016, Insect biochemistry and molecular biology.

[63]  Kurt Wüthrich,et al.  NMR structure of the unliganded Bombyx mori pheromone‐binding protein at physiological pH , 2002, FEBS letters.

[64]  Qingjun Liu,et al.  Impedance spectroscopy analysis of human odorant binding proteins immobilized on nanopore arrays for biochemical detection. , 2016, Biosensors & bioelectronics.

[65]  C. Cambillau,et al.  Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[66]  A. Pisanelli,et al.  Identification of a specific olfactory receptor for 2-isobutyl-3-methoxypyrazine. , 1982, The Biochemical journal.

[67]  M. Benetti,et al.  Detection of odorant molecules via surface acoustic wave biosensor array based on odorant-binding proteins. , 2013, Biosensors & bioelectronics.

[68]  P. Pelosi,et al.  Putative odorant-binding protein in antennae and legs of Carausius morosus (Insecta, Phasmatodea). , 1996, Insect biochemistry and molecular biology.

[69]  D R Flower,et al.  The lipocalin protein family: structure and function. , 1996, The Biochemical journal.

[70]  W. Knoll,et al.  Honey bee odorant-binding protein 14: effects on thermal stability upon odorant binding revealed by FT-IR spectroscopy and CD measurements , 2013, European Biophysics Journal.

[71]  J. Michalski,et al.  Phosphorylation of Native Porcine Olfactory Binding Proteins , 2009, Journal of Chemical Ecology.

[72]  O. Gladysheva,et al.  Glycoprotein composition of olfactory mucus in vertebrates. , 1986, Acta Histochemica.

[73]  Hitoshi Sakano,et al.  How is the olfactory map formed and interpreted in the mammalian brain? , 2011, Annual review of neuroscience.

[74]  C. Cambillau,et al.  Complexes of porcine odorant binding protein with odorant molecules belonging to different chemical classes. , 2000, Journal of molecular biology.

[75]  Paolo Pelosi,et al.  From Gas Sensors to Biomimetic Artificial Noses , 2018, Chemosensors.

[76]  D. Leshkowitz,et al.  Chemosensing of honeybee parasite, Varroa destructor: Transcriptomic analysis , 2017, Scientific Reports.

[77]  K. Persaud,et al.  Analysis of discrimination mechanisms in the mammalian olfactory system using a model nose , 1982, Nature.

[78]  F. Zufall,et al.  Functional Overexpression of Vomeronasal Receptors Using a Herpes Simplex Virus Type 1 (HSV-1)-Derived Amplicon , 2016, PloS one.

[79]  Jing-Jiang Zhou,et al.  "Plus-C" odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. , 2004, Gene.

[80]  M. Jordan,et al.  A novel method to study insect olfactory receptor function using HEK293 cells. , 2014, Insect biochemistry and molecular biology.

[81]  W. Knoll,et al.  Insights into structural features determining odorant affinities to honey bee odorant binding protein 14. , 2014, Biochemical and biophysical research communications.

[82]  Stefan Schütz,et al.  Fine discrimination of volatile compounds by graphene-immobilized odorant-binding proteins , 2018 .

[83]  P. Xu,et al.  Identification of a distinct family of genes encoding atypical odorant‐binding proteins in the malaria vector mosquito, Anopheles gambiae , 2003, Insect molecular biology.

[84]  Qingjun Liu,et al.  Olfactory biosensor for insect semiochemicals analysis by impedance sensing of odorant-binding proteins on interdigitated electrodes. , 2015, Biosensors & bioelectronics.

[85]  J. Clardy,et al.  Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. , 2000, Chemistry & biology.

[86]  L. Buck,et al.  Combinatorial Receptor Codes for Odors , 1999, Cell.

[87]  W. Knoll,et al.  From radioactive ligands to biosensors: binding methods with olfactory proteins , 2018, Applied Microbiology and Biotechnology.

[88]  A. Scaloni,et al.  Solution structure of a chemosensory protein from the desert locust Schistocerca gregaria. , 2006, Biochemistry.

[89]  L. Riddiford,et al.  Pheromone binding and inactivation by moth antennae , 1981, Nature.

[90]  G. Vergoten,et al.  Binding Specificity of Recombinant Odorant-Binding Protein Isoforms is Driven by Phosphorylation , 2010, Journal of Chemical Ecology.