Skip to main content
SpringerLink
Log in
Book cover

Bioelectronic Nose pp 97–113Cite as

Neurobiology and Cultivation of Olfactory Receptor Neurons on a Chip

  • Chapter
  • First Online:

  • 1209 Accesses

Abstract

The continued study of the olfactory system is essential, as elucidation of its molecular, cellular, and systems neurobiology will undoubtedly reveal a complex interplay that transduces odorant molecule-induced action potentials into odor information processes in the brain such as the mediation of emotion, memory and behavior. Additionally, interest in the olfactory system and its potential applications in the industrial and engineering fields continue to increase. In this chapter, we describe various aspects of olfactory cells ranging from their cellular structures and functions to the development of olfactory cell cultivation methods and the application of cultivated olfactory cells and bio-engineered cells to various types of bioelectronic devices. These applications may ultimately facilitate the development of biomimetic artificial noses.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Lancet D (1986) Vertebrate olfactory reception. Annu Rev Neurosci 9:329–355. doi:10.1146/annurev.ne.09.030186.001553

    Article  CAS  PubMed  Google Scholar 

  2. Snyder SH, Sklar PB, Pevsner J (1988) Molecular mechanisms of olfaction. J Biol Chem 263(28):13971–13974

    Google Scholar 

  3. Graziadei GA, Graziadei PP (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J Neurocytol 8(2):197–213

    Article  CAS  PubMed  Google Scholar 

  4. Moulton DG, Beidler LM (1967) Structure and function in the peripheral olfactory system. Physiol Rev 47:1–52

    CAS  PubMed  Google Scholar 

  5. Labarca P, Bacigalupo J (1988) Ion channels from chemosensory olfactory neurons. J Bioenerg Biomembr 20:551–569

    Article  CAS  PubMed  Google Scholar 

  6. Getchell TV (1986) Functional properties of vertebrate olfactory receptor neurons. Physiol Rev 66:772–818

    CAS  PubMed  Google Scholar 

  7. Lowe G, Gold GH (1993) Contribution of the ciliary cyclic nucleotide-gated conductance to olfactory transduction in the salamander. J Physiol 462:175–196

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Menco BP, Cunningham AM, Qasba P, Levy N, Reed RR (1997) Putative odour receptors localize in cilia of olfactory receptor cells in rat and mouse: a freeze-substitution ultrastructural study. J Neurocytol 26(10):691–706

    Article  CAS  PubMed  Google Scholar 

  9. Menco BP, Bruch RC, Dau B, Danho W (1992) Ultrastructural localization of olfactory transduction components: the G protein subunit Golf alpha and type III adenylyl cyclase. Neuron 8(3):441–453

    Article  CAS  PubMed  Google Scholar 

  10. Farbman AI (1992) Structure of olfactory mucous membrane. In: Barlow PW, Bray D, Green PB, Slack JMW (eds) Cell biology of olfaction, vol 6. Cambridge University Press, Cambridge, pp 24–74

    Google Scholar 

  11. Roskams AJ, Cai X, Ronnett GV (1998) Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat. Neuroscience 83(1):191–200

    Article  CAS  PubMed  Google Scholar 

  12. Graziadei PP (1973) Cell dynamics in the olfactory mucosa. Tissue Cell 5(1):113–131

    Article  CAS  PubMed  Google Scholar 

  13. Graziadei PP (1971) Topological relations between olfactory neurons. Z Zellforsch Mikrosk Anat 118(4):449–466

    Article  CAS  PubMed  Google Scholar 

  14. Caggiano M, Kauer JS, Hunter DD (1994) Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron 13:339–352

    Article  CAS  PubMed  Google Scholar 

  15. Carr VM, Farbman AI (1993) The dynamics of cell death in the olfactory epithelium. Exp Neurol 124:308–314

    Article  CAS  PubMed  Google Scholar 

  16. Constanzo RM, Morrison EE (1989) Three-dimensional scanning electron microscopic study of the normal hamster olfactory epithelium. J Neurocytol 18:381–391

    Article  Google Scholar 

  17. Hirsch JD, Margolis FL (1980) Influence of unilateral bulbectomy on opiate and other binding sites in the contralateral bulb. Brain Res 199:39–47

    Article  CAS  PubMed  Google Scholar 

  18. Graziadei PP, Graziadei GA (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8(1):1–18

    Article  CAS  PubMed  Google Scholar 

  19. Calof AL, Chikaraishi DM (1989) Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3:115–127

    Article  CAS  PubMed  Google Scholar 

  20. Goldstein BJ, Schwob JE (1996) Analysis of the globose basal cell compartment in rat olfactory epithelium using GBC-1, a new monoclonal antibody against globose basal cells. J Neurosci 16(12):4005–4016

    CAS  PubMed  Google Scholar 

  21. Huard JM, Youngentob SL, Goldstein BJ, Luskin MB, Schwob JE (1998) Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J Comp Neurol 400(4):469–486

    Article  CAS  PubMed  Google Scholar 

  22. Getchell TV, Margolis FL, Getchell ML (1985) Perireceptor and receptor events in vertebrate olfaction. Prog Neurobiol 23:317–345

    Article  Google Scholar 

  23. Okano TM (1974) Secreation and electrogenesis of the supporting cell in the olfactory epithelium. J Physiol (London) 242:353–370

    Google Scholar 

  24. Hansel DE, Eipper BA, Ronnett GV (2001) Neuropeptide Y functions as a neuroproliferative factor. Nature 410(6831):940–944

    Article  CAS  PubMed  Google Scholar 

  25. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65(1):175–187

    Article  CAS  PubMed  Google Scholar 

  26. Taupin P, Gage F (2002) Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 69:745–749

    Article  CAS  PubMed  Google Scholar 

  27. Vaccarino FM, Ganat Y, Zhang Y, Zheng W (2001) Stem cells in neurodevelopment and plasticity. Neuropsychopharmacology 25(6):805–815

    Article  CAS  PubMed  Google Scholar 

  28. Pincus DW, Keyoung HM, Harrison-Restelli C, Goodman RR, Fraser RA, Edgar M, Sakakibara S, Okano H, Nedergaard M, Goldman SA (1998) Fibroblast growth factor-2/brain-derived neurotrophic factor- associated maturation of new neurons generated from adult human subependymal cells. Ann Neurol 43(5):576–585

    Article  CAS  PubMed  Google Scholar 

  29. Carpenter MK, Cui X, Hu ZY, Jackson J, Sherman S, Seiger A, Wahlberg LU (1999) In vitro expansion of a multipotent population of human neural progenitor cells. Exp Neurol 158(2):265–278

    Article  CAS  PubMed  Google Scholar 

  30. Maric D, Maric I, Chang YH, Barker JL (2003) Prospective cell sorting of embryonic rat neural stem cells and neuronal and glial progenitors reveals selective effects of basic fibroblast growth factor and epidermal growth factor on self-renewal and differentiation. J Neurosci 23(1):240–251

    CAS  PubMed  Google Scholar 

  31. Riaz SS, Theofilopoulos S, Jauniaux E, Stern GM, Bradford HF (2004) The differentiation potential of human foetal neuronal progenitor cells in vitro. Brain Res Dev Brain Res 153(1):39–51

    Article  CAS  PubMed  Google Scholar 

  32. Li X-J, Du Z-W, Zarnowska ED, Pankratz M, Hansen LO, Pearce RA, Zhang S-C (2005) Specification of motoneurons from human embryonic stem cells. Nature Biotechnology Advance online publication

    Google Scholar 

  33. Bally-Cuif L, Hammerschmidt M (2003) Induction and patterning of neuronal development, and its connection to cell cycle control. Curr Opin Neurobiol 13:16–25

    Article  CAS  PubMed  Google Scholar 

  34. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurology 124(3):319–335

    Article  CAS  Google Scholar 

  35. Graziadei PPC, Monti-Graziadei GA (1978) Continuous nerve cell renewal in the olfactory system. In: Jacobson M (ed) Handbook of sensory physiology, vol IX. Springer-Verlag, Berlin, pp 55–82

    Google Scholar 

  36. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137(4):433–457

    Article  CAS  PubMed  Google Scholar 

  37. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain ventricular zone. Neuron 11:173–189

    Article  CAS  PubMed  Google Scholar 

  38. Calof AL, Bonnin A, Crocker C, Kawauchi R, Murray RC, Shou J, Wu H-H (2002) Progenitor cells of the olfactory receptor neuron lineage. Micro Res Tech 58:176–188

    Article  CAS  Google Scholar 

  39. Hansel DE, May V, Eipper BA, Ronnett GV (2001) PACAP peptides and a-amidation in olfactory neurogenesis and neuronal survival in vitro. J Neurosci 21(13):4625–4636

    Google Scholar 

  40. Simpson PJ, Miller I, Moon C, Hanlon AL, Liebl DJ, Ronnett GV (2002) Atrial natriuretic peptide type C induces a cell-cycle switch from proliferation to differentiation in brain-derived neurotrophic factor- or nerve growth factor-primed olfactory receptor neurons. J Neurosci 22(13):5536–5551

    CAS  PubMed  Google Scholar 

  41. Simpson PJ, Wang E, Moon C, Matarazzo V, Cohen D, Leibl DJ, Ronnett GV (2003) Neurotrophin-3 signaling maintains maturational homeostasis between neuronal populations in the olfactory system. Mol Cell Neurosci 24:858–874

    Article  CAS  PubMed  Google Scholar 

  42. Uranagase A, Katsunuma S, Doi K, Nibu K (2012) BDNF expression in olfactory bulb and epithelium during regeneration of olfactory epithelium. Neurosci Lett 516(1):45–49. doi:10.1016/j.neulet.2012.03.051

    Google Scholar 

  43. Moon C, Liu BQ, Kim SY, Kim EJ, Park YJ, Yoo JY, Han HS, Bae YC, Ronnett GV (2009) Leukemia inhibitory factor promotes olfactory sensory neuronal survival via phosphoinositide 3-kinase pathway activation and Bcl-2. J Neurosci Res 87(5):1098–1106. doi:10.1002/jnr.21919

    Article  CAS  PubMed  Google Scholar 

  44. Noble M, Mallaburn PS, Klein N (1984) The growth of olfactory neurons in short-term cultures of rat olfactory epithelium. Neurosci Lett 45(2):193–198

    Google Scholar 

  45. Ronnett GV, Hester LD, Snyder SH (1991) Primary culture of neonatal rat olfactory neurons. J Neurosci 11(5):1243–1255

    CAS  PubMed  Google Scholar 

  46. Ash KO, Bransford JE, Koch RB (1966) Studies on dispersion of rabbit olfactory cells. J Cell Biol 29(3):554–561

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Hirsch JD, Margolis FL (1979) Cell suspensions from rat olfactory neuroepithelium: biochemical and histochemical characterization. Brain Res 161(2):277–291

    Article  CAS  PubMed  Google Scholar 

  48. Gonzales F, Farbman AI, Gesteland RC (1985) Cell and explant culture of olfactory chemoreceptor cells. J Neurosci Meth 14(2):77–90

    Article  CAS  Google Scholar 

  49. Largent BL, Sosnowski RG, Reed RR (1993) Directed expression of an oncogene to the olfactory neuronal lineage in transgenic mice. J Neurosci 13(1):300–312

    CAS  PubMed  Google Scholar 

  50. MacDonald KP, Mackay-Sim A, Bushell GR, Bartlett PF (1996) Olfactory neuronal cell lines generated by retroviral insertion of the n-myc oncogene display different developmental phenotypes. J Neurosci Res 45(3):237–247. doi:10.1002/(SICI)1097-4547(19960801)45:3 & lt;237::AID-JNR5 & gt;3.0.CO;2-E

    Google Scholar 

  51. Barber RD, Jaworsky DE, Yau KW, Ronnett GV (2000) Isolation and in vitro differentiation of conditionally immortalized murine olfactory receptor neurons. J Neurosci 20(10):3695–3704

    CAS  PubMed  Google Scholar 

  52. Kim H, Kim SY, Nam S, Ronnett GV, Han HS, Moon C, Kim Y (2012) Direct measurement of extracellular electrical signals from mammalian olfactory sensory neurons in planar triode devices. Analyst 137(9):2047–2053. doi:10.1039/c2an16205a

    Article  CAS  PubMed  Google Scholar 

  53. Thomas CA Jr, Springer PA, Loeb GE, Berwald-Netter Y, Okun LM (1972) A miniature microelectrode array to monitor the bioelectric activity of cultured cells. Exp Cell Res 74(1):61–66

    Article  PubMed  Google Scholar 

  54. Lee SH, Jun SB, Ko HJ, Kim SJ, Park TH (2009) Cell-based olfactory biosensor using microfabricated planar electrode. Biosens Bioelectron 24(8):2659–2664. doi:10.1016/j.bios.2009.01.035

    Article  CAS  PubMed  Google Scholar 

  55. Ling SC, Gao TY, Liu J, Li YQ, Zhou J, Li J, Zhou CC, Tu CL, Han F, Ye XS (2010) The fabrication of an olfactory receptor neuron chip based on planar multi-electrode array and its odor-response analysis. Biosens Bioelectron 26(3):1124–1128. doi: 10.1016/j.bios.2010.08.071

    Article  CAS  PubMed  Google Scholar 

  56. Micholt E, Jans D, Callewaert G, Bartic C, Lammertyn J, Nicolai B (2013) Extracellular recordings from rat olfactory epithelium slices using micro electrode arrays. Sens Actuators B-Chem 184:40–47. doi:10.1016/j.snb.2013.03.134

    Article  CAS  Google Scholar 

  57. Liu QJ, Cai H, Xu Y, Li Y, Li R, Wang P (2006) Olfactory cell-based biosensor: a first step towards a neurochip of bioelectronic nose. Biosens Bioelectron 22(2):318–322. doi: 10.1016/j.bios.2006.01.016

    Article  CAS  PubMed  Google Scholar 

  58. Liu QJ, Ye WW, Hu N, Cai H, Yu H, Wang P (2010) Olfactory receptor cells respond to odors in a tissue and semiconductor hybrid neuron chip. Biosens Bioelectron 26(4):1672–1678. doi:10.1016/j.bios.2010.09.019

    Article  CAS  PubMed  Google Scholar 

  59. Wang P, Liu QJ, Xu Y, Cai H, Li Y (2007) Olfactory and taste cell sensor and its applications in biomedicine. Sens Actuators A-Phys 139(1–2):131–138. doi:10.1016/j.sna.2007.05.018

    Article  CAS  Google Scholar 

  60. Wu CS, Chen PH, Yu H, Liu QJ, Zong XL, Cai H, Wang P (2009) A novel biomimetic olfactory-based biosensor for single olfactory sensory neuron monitoring. Biosens Bioelectron 24(5):1498–1502. doi:10.1016/j.bios.2008.07.065

    Article  CAS  PubMed  Google Scholar 

  61. Schoning MJ, Poghossian A (2002) Recent advances in biologically sensitive field-effect transistors (BioFETs). Analyst 127(9):1137–1151. doi:10.1039/B204444 g

    Article  PubMed  Google Scholar 

  62. Schoning MJ, Poghossian A (2006) Bio FEDs (Field-Effect devices): state-of-the-art and new directions. Electroanalalysis 18 (19–20):1893–1900. doi:10.1002/elan.200603609

    Article  Google Scholar 

  63. Schoning MJ, Schutz S, Schroth P, Weissbecker B, Steffen A, Kordos P, Hummel HE, Luth H (1998) A BioFET on the basis of intact insect antennae. Sens Actuators B-Chem 47(1–3):235–238. doi:10.1016/S0925-4005(98)00029-X

    Article  CAS  Google Scholar 

  64. Chabot V, Cuerrier CM, Escher E, Aimez V, Grandbois M, Charette PG (2009) Biosensing based on surface plasmon resonance and living cells. Biosens Bioelectron 24(6):1667–1673. doi:10.1016/j.bios.2008.08.025

    Article  CAS  PubMed  Google Scholar 

  65. Yotter RA, Lee LA, Wilson DM (2004) Sensor technologies for monitoring metabolic activity in single cells - part I: optical, methods. IEEE Sens J 4(4):395–411. doi:10.1109/Jsen.2004.830952

    Article  CAS  Google Scholar 

  66. Misawa N, Mitsuno H, Kanzaki R, Takeuchi S (2010) Highly sensitive and selective odorant sensor using living cells expressing insect olfactory receptors. Proc Natl Acad Sci U S A 107(35):15340–15344. doi:10.1073/pnas.1004334107

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. 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(7):3103–3109. doi:10.1016/j.bios.2010.07.122

    Article  CAS  PubMed  Google Scholar 

  68. Sankaran S, Panigrahi S, Mallik S (2011) Olfactory receptor based piezoelectric biosensors for detection of alcohols related to food safety applications. Sens Actuators B-Chem 155(1):8–18. doi:10.1016/j.snb.2010.08.003

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Converging Research Center Program through the Ministry of Science, ICT and Future Planning, Korea (2013K000363).

Author information

Authors and Affiliations

  1. Department of Brain Science, Graduate School, Daegu Gyeongbuk Institute of Science and Technology, 711–873, Daegu, Republic of Korea

    Cheil Moon, Samhwan Kim & Jisub Bae

  2. Department of Neuroscience, Biological Chemistry, and Neurology, School of Medicine, Johns Hopkins University, 21205, Baltimore, MD, USA

    Gabriele V. Ronnett

Authors
  1. Cheil Moon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samhwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jisub Bae
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriele V. Ronnett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cheil Moon .

Editor information

Editors and Affiliations

  1. School of Chemical and Biological Engineering, Seoul National University, Seoul, Korea, Republic of (South Korea)

    Tai Hyun Park

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Moon, C., Kim, S., Bae, J., Ronnett, G. (2014). Neurobiology and Cultivation of Olfactory Receptor Neurons on a Chip. In: Park, T. (eds) Bioelectronic Nose. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-8613-3_6

Download citation

Publish with us

Policies and ethics

Search

Navigation