The Electrical Properties of Olfactory Receptors in the Development of Biological Smell Sensors

  • Eleonora Alfinito
  • Jeremy Pousset
  • Lino Reggiani
Protocol
First Online:
Part of the Methods in Molecular Biology book series (MIMB, volume 1003)

Abstract

We present here the results of the investigation of the electrical properties of two olfactory receptors (ORs): rat, OR I7, and human, OR 17-40, which are of interest in the creation of smell nanobiosensors. Described here is our investigation comparing the results from experiments using electrochemical impedance spectroscopy with the theoretical predictions obtained from a recently developed impedance network protein analog. The changes in the OR response following excitation correlated with the protein conformational change. The satisfactory agreement between theory and experiment points to a promising development of a new class of nanobiosensors based on the electrical properties of sensing proteins.

Key words

Olfactory receptors Biosensors Protein electrical properties 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This research is carried out within the bioelectronic olfactory neuron device (BOND) project sponsored by the European Community (EC) within the Seventh Program, grant agreement: 228685-2.

Dr V. Akimov and the INRA-MIG laboratory of Paris are gratefully acknowledged for providing the 3D structures of the OR 17-40.

Drs. E. Pajot, J.-F. Millithaler, N. Jaffrezic-Renault, and C. Pennetta are thanked for useful discussions on the subject.

References

  1. 1.
    Bioelectronic Olfactory Neuron Device (BOND) Collaborative project FP7-NMP-2008-SMALL-2, GA number 228685Google Scholar
  2. 2.
    Pardo M, Sberveglieri G (eds) (2009) Olfaction and electronic nose: proceedings of the 13th international symposium on olfaction and electronic nose. American Institute of Physics, Melville, pp 115–118. ISBN 978-0-7354-0674-2/09/S25.00AIPGoogle Scholar
  3. 3.
    Quaranta F, Rella R, Siciliano P, Capone S, Epifani M, Vasanelli L et al (1999) A novel gas sensor based on SnO2/Os thin film for the detection of methane at low temperature. Sens Actuators B 58:350–355CrossRefGoogle Scholar
  4. 4.
    Gardner JW, Bartlett PN (eds) (1991) Sensor and sensory systems of an electronic nose. Nato ASI series, 212. Kluwer, DordrechtGoogle Scholar
  5. 5.
    Göpel W (1998) Chemical imaging: I. Concepts and visions for electronic and bioelectronic noses. Sens Actuators B 52:125–142CrossRefGoogle Scholar
  6. 6.
    Göpel W, Ziegler C, Breer H, Schild D, Apfelbach R, Joerges J, Malaka R (1998) Bioelectronic noses: a status report. Part I. Biosens Bioelectron 13:479–493PubMedCrossRefGoogle Scholar
  7. 7.
    Liu Q, Qu X, Guo H, Chen H, Liu B, Dong S (2006) Olfactory cell-based biosensors: a fist step toward a neurochip of bioelectronic nose. Biosens Bioelectron 22:2195–2201CrossRefGoogle Scholar
  8. 8.
    Marrakchi M, Vidic J, Jaffrezic-Renault N, Martelet C, Pajot-Augy E (2007) A new concept of olfactory biosensor based on interdigitated microelectrodes and immobilized yeasts expressing the human receptor OR17-40/Eur. Biophys J 36:1015–1018Google Scholar
  9. 9.
    Lefkowitz RJ (2000) The superfamily of heptahelical receptors. Nat Cell Biol 2:E133–E136PubMedCrossRefGoogle Scholar
  10. 10.
    Palczewski K, Kumasala T, Hori T, Behnke CA, Motoshima H, Fox BA et al (2000) Crystal structure of rhodopsin: a G-coupled protein receptor. Science 289:739–745PubMedCrossRefGoogle Scholar
  11. 11.
    Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187PubMedCrossRefGoogle Scholar
  12. 12.
    Mombaerts P (2004) Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revised. Curr Opin Neurobiol 14:31–36PubMedCrossRefGoogle Scholar
  13. 13.
    Duchamp-Viret P, Chaput MA, Duchamp A (1999) Odor response properties of rat olfactory receptor neurons. Science 284:2171–2174PubMedCrossRefGoogle Scholar
  14. 14.
    Buck LB (2004) Olfactory receptors and odor coding in mammals. Nutr Rev 62:S184–S188PubMedCrossRefGoogle Scholar
  15. 15.
    Crasto C, Singer SM, Shepherd GM (2001) The olfactory receptor family album. Genome Biol 2:reviews 1027-1–reviews 1027-4CrossRefGoogle Scholar
  16. 16.
    Jones TD, Reed RR (1989) Golf: an olfactory neuron specific-G protein involved in odorant signal. Science 244:790–795PubMedCrossRefGoogle Scholar
  17. 17.
    Hou Y, Helali S, Jaffrezic-Renault N, Martelet C, Zhang A, Minic J et al (2006) Immobilization of rhodopsin on a self-assembled monolayer and its specific detection by electrochemical impedance spettroscopy. Biosens Bioelectron 21:1393–1402PubMedCrossRefGoogle Scholar
  18. 18.
    Hou Y, Jaffrezic-Renault N, Martelet C, Zhang A, Minic J, Gorojankina T et al (2007) A novel detection strategy for odorant molecules based on controlled bioengineering of rat olfactory receptor I7. Biosens Bioelectron 22:1550–1555PubMedCrossRefGoogle Scholar
  19. 19.
    Levasseur G, Persuy M-A, Grebert D, Remy J-J, Salesse R, Pajot-Augy E (2003) Ligand-specific dose-response in heterologously expressed olfactory receptors. Eur J Biochem 270:2905–2912PubMedCrossRefGoogle Scholar
  20. 20.
    Pennetta C, Akimov V, Alfinito E, Reggiani L, Gorojankina T, Minic J et al (2006) Towards the realization of nanobiosensors based on G-protein-coupled receptors. In: Kumar CSSR (ed) Nanotechnologies of the life science, vol 4. Wiley, Weinheim, pp 217–240Google Scholar
  21. 21.
    Benilova IV, Minic-Vidic J, Pajot-Augy E, Soldatkin AP, Martelet C, Jaffrezic-Renault N (2008) Electrochemical study of human olfactory receptor OR 17-40 stimulation by odorant in solution. Mater Sci Eng C 28:633–639CrossRefGoogle Scholar
  22. 22.
    Vidic J, Grosclaude J, Monnerie K, Persuy M-A, Badonnel K, Baly C et al (2008) On a chip demonstration of a functional role for odorant binding protein in the preservation of olfactory receptor activity at high odorant concentration. Lab Chip 8:678–688PubMedCrossRefGoogle Scholar
  23. 23.
    Gaillard I, Rouquier S, Giorgi D (2004) Olfactory receptors. Cell Mol Life Sci 61:456–469PubMedCrossRefGoogle Scholar
  24. 24.
    Vestergaard M, Kerman K, Tamiya E (2007) An overview of label-free electrochemical protein sensors. Sensors 7:3442–3458CrossRefGoogle Scholar
  25. 25.
    Yoon H, Lee SH, Kwon OS, Song HS, Oh EH, Park TH et al (2009) Polypyrrole nanotubes conjugated with human olfactory receptors: high-performance transducers for FET-type bioelectronic noses. Angew Chem Int Ed Engl 48:2755–2758PubMedCrossRefGoogle Scholar
  26. 26.
    Rhodes G (2006) Crystallography made crystal clear: a guide for users of macromolecular models. Academic, New YorkGoogle Scholar
  27. 27.
    Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat HWTN, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242PubMedCrossRefGoogle Scholar
  28. 28.
    Fiser A, Sali A (2003) ModLoop: automated modeling of loops in protein structures. Bioinformatics 19:2500–2501PubMedCrossRefGoogle Scholar
  29. 29.
    Sali A, Blundell TL (1994) Comparative protein modelling by satisfaction of spatial restraints. In: Bohr H, Brunak S (eds) Protein structure by distance analysis., pp 64–86Google Scholar
  30. 30.
    Launay G, Téletchéa S, Wade F, Pajot-Augy E, Gibrat J-F, Sanz G (2012) Automatic modeling of mammalian olfactory receptors and docking of odorants. Protein Eng Des Sel 25:377–386PubMedCrossRefGoogle Scholar
  31. 31.
    Alfinito E, Akimov V, Pennetta C, Reggiani L, Gomila G (2005) Thermal Fluctuations of a GPCR: a two force constant model, AIP Proc. UPON, Conf. Eds. L.Reggiani, C. Pennetta, V. Akimov, E. Alfinito and M. Rosini, 800, pp 381–387Google Scholar
  32. 32.
    Akimov V, Alfinito E, Baussels J, Benilova V, Paramo IC, Errachid A et al (2008) Nanobiosensor based on individual olfactory receptors. Analog Integr Circ Signal Process 57:197–203CrossRefGoogle Scholar
  33. 33.
    Alfinito E, Pennetta C, Reggiani L (2008) A network model to correlate conformational change and the impedance spectrum of single proteins. Nanotechnology 19:065202-1–065202-12CrossRefGoogle Scholar
  34. 34.
    Alfinito E, Millithaler J-F, Pennetta C, Reggiani L (2009) A nanobiosensor based on olfactory receptor. In: IEEE, 25–28, 10.1109/IWASI.2009.5184762Google Scholar
  35. 35.
    Alfinito E, Reggiani L (2009) Charge transport in bacteriorhodopsin monolayers: the contribution of conformational change to current-voltage characteristics. Europhys Lett 85:68002-1–68002-6CrossRefGoogle Scholar
  36. 36.
    Alfinito E, Pennetta C, Reggiani L (2009) Topological change and impedance spectrum of rat olfactory I7: a comparative analysis with bovine rhodopsin and bacteriorhodopsin. J Appl Phys 105:084703-1–084703-6CrossRefGoogle Scholar
  37. 37.
    Weiss TF (1997) Cellular biophysics, 2nd edn. MIT, CambridgeGoogle Scholar
  38. 38.
    Fraufelder H, Wolynes PG, Austin RH (1999) Biological physics. Rev Mod Phys 71:S419–S430CrossRefGoogle Scholar
  39. 39.
    Vaidehi N, Floriano WB, Trabanino R, Hall SE, Freddolino P, Choi EJ et al (2002) Prediction of structure and function of G protein-coupled receptors. Proc Natl Acad Sci USA 99:12622–12627PubMedCrossRefGoogle Scholar
  40. 40.
    Alfinito E, Pennetta C, Reggiani L (2010) Olfactory receptor-based smell nanobiosensors: an overview of theoretical and experimental results. Sens Actuators B 146:554–558CrossRefGoogle Scholar
  41. 41.
    Alfinito E, Reggiani L (2010) The role of topology in electrical properties of bR and rat-olfactory receptor. Phys Rev E 81:032902-1–032902-4CrossRefGoogle Scholar
  42. 42.
    Alfinito E, Pennetta C, Reggiani L (2010) Smell nanobiosensors: hybrid systems based on the electrical response to odorant capture: theory and experiment. AIP Conf Proc 1137:115–118Google Scholar
  43. 43.
    Alfinito E, Millithaler J-F, Pennetta C, Reggiani L (2010) A single protein based nanobiosensor for odorant recognition. Microelectronics J 41:718–722CrossRefGoogle Scholar
  44. 44.
    Alfinito E, Millithaler J-F, Reggiani L, Zine N, Jaffrezic-Renault N (2011) Topological and electrical properties of human 17-40 olfactory receptor for the realization of a nanobiosensor. RCS Adv 1:718–722Google Scholar
  45. 45.
    Alfinito E, Millithaler J-F, Reggiani L (2011) Olfactory receptors for a smell sensor: a comparative study of the electrical responses of rat I7 and human 17-40. Meas Sci Tech 22:124004CrossRefGoogle Scholar
  46. 46.
    Alfinito E, Millithaler J-F, Reggiani L (2011) Charge transport in purple membrane monolayers: a sequential tunneling approach. Phys Rev E 83:1–4CrossRefGoogle Scholar
  47. 47.
    Atilgan AR, Durell SR, Jernigan RL, Demirel MC, Keskin O, Bahar I (2001) Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys J 80:505–515PubMedCrossRefGoogle Scholar
  48. 48.
    Kim MK, Jernigan RL, Chirikjian GS (2002) Efficient generation of feasible pathways for protein conformational transitions. Biophys J 83:1620–1630PubMedCrossRefGoogle Scholar
  49. 49.
    Albert R, Barabasi AL (2002) Statistical mechanics of complex networks. Rev Mod Phys 74:47–97CrossRefGoogle Scholar
  50. 50.
    Micheletti C, Carloni P, Maritan A (2004) Accurate and efficient description of protein vibrational dynamics: comparing molecular dynamics and Gaussian models. Proteins 55:635–645PubMedCrossRefGoogle Scholar
  51. 51.
    Tirion MM (1996) Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 77:1905–1908PubMedCrossRefGoogle Scholar
  52. 52.
    Song X (2002) An inhomogeneous model of protein dielectric properties: intrinsic polarizability of amino acids. J Chem Phys 116:9359–9363CrossRefGoogle Scholar
  53. 53.
    Churg AK, Weiss RM, Warshel A, Takano T (1983) On the action of cytochrome c: correlating geometry changes upon oxidation with activation energy of electron transfer. J Phys Chem 87:1683–1694CrossRefGoogle Scholar
  54. 54.
    Warshel A, Parson WW (2001) Dynamics of biochemical and biophysical reactions: insight from computer simulations. Q RevBiophys 34:563–679Google Scholar
  55. 55.
    Hall SE, Floriano WB, Vaidehi N, Goddard WAIII (2004) Predicted 3-D structures for mouse I7 and rat I7 receptors and comparison of predicted odor recognition profiles with experiment. Chem Senses 29:595–616PubMedCrossRefGoogle Scholar
  56. 56.
    Kolbika BK, Deupi X (2007) Conformational complexity of G-protein-coupled receptors. Trends Pharmacol Sci 28:397–406CrossRefGoogle Scholar
  57. 57.
    Miyashita O, Wolynes PG, Onuchic JN (2005) Simple energy landscape model for the kinetics of functional transitions in proteins. J Phys Chem B 109:1959–1969PubMedCrossRefGoogle Scholar
  58. 58.
    Gardino AK, Villali J, Kivenson A, Lei M, Liu CF, Steindel P et al (2009) Transient non-native hydrogen bonds promote activation of a signaling protein. Cell 139:1109–1118PubMedCrossRefGoogle Scholar
  59. 59.
    Jin Y, Friedman N, Sheves M, He T, Cahen D (2006) Bacteriorhodopsin (bR) as an electronic conduction medium: current transport through bR-containing monolayers. Proc Natl Acad Sic USA 103:8601–8606CrossRefGoogle Scholar
  60. 60.
    Sankaran S, Khot LR, Panigrahi S (2012) Biology and applications of olfactory sensing system: a review. Sens Actuators B 171:1–17CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2013

Authors and Affiliations

  • Eleonora Alfinito
    • 1
    • 2
  • Jeremy Pousset
    • 3
  • Lino Reggiani
    • 2
    • 3
  1. 1.Dipartimento di Ingegneria dell’InnovazioneUniversità del SalentoLecceItaly
  2. 2.Consorzio Nazionale Interuniversitario per le Scienze Fisiche della Materia (CNISM)RomeItaly
  3. 3.Dipartimento di Matematica e Fisica, Ennio de GiorgiUniversità del SalentoLecceItaly

Personalised recommendations