Skip to main content
SpringerLink
Log in

Reconstructing smell

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Odorant signal transduction and neurogenesis are fundamental properties of the olfactory epithelium. Many preparations have been used to elucidate some of the mechanisms underlying these properties. In this article, we briefly review these research areas and describe some of the techniques used to obtain the data. We focus specifically on the cell-culture paradigm and the data obtained from various immortal cell lines in their attempts to reconstruct the olfactory epithelium in vitro.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

    PubMed  CAS  Google Scholar 

  2. Jones D. T. and Reed, R. R. (1989) Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244, 790–795.

    PubMed  CAS  Google Scholar 

  3. Bakalyar H. A. and Reed R. R. (1990) Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250, 1403–1406.

    PubMed  CAS  Google Scholar 

  4. Dhallan R. S., Yau K. W., Schrader K. A., and Reed, R. R. (1990) Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347, 184–187.

    PubMed  CAS  Google Scholar 

  5. Liman E. R. and Buck, L. B. (1994) A second subunit of the olfactory cyclic nucleotidegated channel confers high sensitivity to cAMP. Neuron 13, 611–621.

    PubMed  CAS  Google Scholar 

  6. Bonigk W., Bradley, J., Muller F., Sesti F., Boehoff I., Ronnett G. V., et al. (1999) The native rat olfactory cyclic nucleotide-gated channel is composed of three distinct subunits. J. Neurosci. 19, 5332–5347.

    PubMed  CAS  Google Scholar 

  7. Bradley J., Li J., Davidson N., Lester H. S., and Zinn K. (1994) Heteromeric olfactory cyclic nucleotide-gated channels: a subunit that confers increased sensitivity to cAMP. PNAS 91, 8890–8894.

    PubMed  CAS  Google Scholar 

  8. Malnic B., Hirono J., Sato T., and Buck L. B. (1999) Combinatorial receptor codes for odors. Cell 96, 713–723.

    PubMed  CAS  Google Scholar 

  9. Reed R. R. (1992) Signaling pathways in odorant detection. Neuron 8, 205–209.

    PubMed  CAS  Google Scholar 

  10. Shepherd G. M. (1994) Discrimination of molecular signals by the olfactory receptor neuron. Neuron 13, 771–790.

    PubMed  CAS  Google Scholar 

  11. Buck L. B. (1996) Information coding in the vertebrate olfactory system Ann. Rev. Neurosci. 19, 517–544.

    PubMed  CAS  Google Scholar 

  12. Ressler K. J., Sullivan S. L., and Buck L. B. (1994) Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245–1255.

    PubMed  CAS  Google Scholar 

  13. Mombaerts P., Wang F., Dulac C., Chao S. K., Nemes A., Mendelsohn M., et al. (1996) Visualizing an olfactory sensory map. Cell 15, 675–686.

    Google Scholar 

  14. Dulac C. and Axel R. (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83, 195–206.

    PubMed  CAS  Google Scholar 

  15. Herrada G. and Dulac C. (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90, 763–773.

    PubMed  CAS  Google Scholar 

  16. Matsunami H. and Buck L. B. (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90, 775–784.

    PubMed  CAS  Google Scholar 

  17. Rodriquez I., Feinstein P., and Mombaerts P. (1999) Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97, 199–208.

    Google Scholar 

  18. Belluscio L., and Kolfactory epitheliumntges G., Axel R., and Dulac C. (1999) A map of pheromone receptor activation in the mammalian brain. Cell 97, 209–220.

    PubMed  CAS  Google Scholar 

  19. Buck L. B. (2000) The molecular architecture of odor and pheromone sensing in mammals, Cell 100, 611–618.

    PubMed  CAS  Google Scholar 

  20. Leinders-Zufall T., Lane A. P., Puche A. C., Ma W., Novotny M. V., Shipley M. T., and Zufall F. (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405, 792–796.

    PubMed  CAS  Google Scholar 

  21. Ngai J., Dowling M. M., Buck L., Axel R., and Chess A. (1993) The family of genes encoding odorant receptors in the channel catfish. Cell 72, 657–666.

    PubMed  CAS  Google Scholar 

  22. Mombaerts P. (1999) Seven-transmembrane proteins as odorant and chemosensory receptors. Science 286, 707–711.

    PubMed  CAS  Google Scholar 

  23. Sengupta P., Chou J. H., and Bargmann C. I. (1996) odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899–909.

    PubMed  CAS  Google Scholar 

  24. Zhao H., Ivic L., Otaki J. M., Hashimoto M., Mikoshiba K., and Firestein S. (1998) Functional expression of a mammalian odorant receptor. Science 279, 237–242.

    PubMed  CAS  Google Scholar 

  25. Krautwurst D., Yau K.-W., and Reed R. R. (1998) Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95, 917–926.

    PubMed  CAS  Google Scholar 

  26. Speca D. J., Lin D. M., Sorensen P. W., Isacoff E. Y., Ngai J., and Dittman A. H. (1999) Functional identification of a goldfish odorant receptor. Neuron 23, 487–498.

    PubMed  CAS  Google Scholar 

  27. Touhara K., Sengoku S., Inaki K., Tsuboi A., Hirono J., Sato T., et al. (1999) Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl. Acad. Sci. USA 96, 4040–4045.

    PubMed  CAS  Google Scholar 

  28. McClintock T. S., Landers T. M., Gimelbrant A. A., Fuller L. Z., Jackson B. A., Jayawickreme C. K., and Lerner M. R. (1997) Functional expression of olfactory-adrenergic receptor chimeras and intracellular retention of heterologously expressed olfactory receptors. Brain. Res. Mol. Brain Res. 48, 270–278.

    PubMed  CAS  Google Scholar 

  29. Wellerdieck C., Oles M., Pott L., Korsching S., Gisselmann G., and Hatt H. (1997) Functional expression of odorant receptors of the zebrafish Danio rerio and of the nematode C. elegans in HEK293 cells. Chem. Senses 22, 467–476.

    PubMed  CAS  Google Scholar 

  30. Murrell J. R. and Hunter D. D. (1999) An olfactory sensory neuron line, odora, properly targets olfactory proteins and responds to odorants. J. Neurosci. 19, 8260–8270.

    PubMed  CAS  Google Scholar 

  31. Dahl A. R., (1988) Metabolism and olfaction, in Molecular Neurobiology of the Olfactory System, Margolis F. L. and Getchell, T. V., eds., Plenum Press, New York, pp. 51–70.

    Google Scholar 

  32. Getchell M. V., Zielinski B., and Getchell T. V. (1988) Odorant and autonomic regulation of secretion in the olfactory mucosa, in Molecular Neurobiology of the Olfactory System, Margolis F. L. and Getchell, T. V. eds., Plenum Press, New York, pp 71–98.

    Google Scholar 

  33. Calof A. L. and Chikaraishi D. M. (1989) Analysis of neurogenesis in a mammalian neurolfactory epitheliumpithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3, 115–127.

    PubMed  CAS  Google Scholar 

  34. Schwartz Levey M., Chikaraishi D. M., and Kauer J. S. (1991) Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J. Neurosci. 11, 3556–3564.

    PubMed  CAS  Google Scholar 

  35. Hinds J. W., Hinds P. L., and McNelly N. A. (1984) An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors. Anat. Rec. 210, 375–383.

    PubMed  CAS  Google Scholar 

  36. Camara C. G. and Harding J. W. (1984) Thymidine incorporation in the olfactory epithelium of mice: early exponential response induced by olfactory neurectomy. Brain Res. 308, 63–68.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  38. Monti Graziadei G. A. and Graziadei P. P. (1979) Studies on neuronal plasticity and regeneration in the olfactory system: morphologic and functional characteristics of the olfactory sensory neuron, in Neural Growth and Differentiation, Meisami E. and Brazier M. A. B., eds., Raven Press, New York, pp. 373–396.

    Google Scholar 

  39. Graziadei P. P. and Monti Graziadei G. A. (1980) Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria in rat. J. Neurocytol. 2, 145–162.

    Google Scholar 

  40. Miwa T., Uramoto N., Ishimaru T., Furukawa M., Shiba K., and Morjizumi T. (1998) Retrograde transport of nerve growth factor from olfactory bulb to olfactory epithelium. Neuroreport 9, 153–155.

    PubMed  CAS  Google Scholar 

  41. Balboni G. C., Zonefrati R., Repice F., Barni T., and Vannelli G. B. (1991) Immunohistochemical detection of EGF and NGF receptors in human olfactory epithelium. Boll. Soc. Ital. Biol. Sper. 67, 901–906.

    PubMed  CAS  Google Scholar 

  42. Aiba T., Mori J., and Nakai Y. (1993) Nerve growth factor (NGF) and its receptor in rat olfactory epithelium. Acta. Otolaryngol. Suppl. (Stockh) 506, 37–40.

    CAS  Google Scholar 

  43. Ronnett G. V., Hester L. D., and Snyder S. H. (1991) Primary culture of neonatal rat olfactory neurons. J. Neurosci. 11, 1243–1255.

    PubMed  CAS  Google Scholar 

  44. Mahanthappa N. K. and Schwarting G. A. (1993) Peptide growth factor control of olfactory neurogenesis and neuron survival in vitro: roles of EGF and TGF-beta s. Neuron 10, 293–305.

    PubMed  CAS  Google Scholar 

  45. Farbman A. I. and Buchholz J. A. (1996) Transforming growth factor-alpha and other growth factors stimulate cell division in olfactory epithelium in vitro. J. Neurobiol. 30, 267–280.

    PubMed  CAS  Google Scholar 

  46. Buckland M. E. and Cunningham A. M. (1998) Alterations in the neurotrophic factors BDNF, GDNF and CNTF in the regenerating olfactory system. Ann. NY Acad. Sci. 855, 260–265.

    PubMed  CAS  Google Scholar 

  47. Holcomb J. D., Mumm J. S., and Calof A. L. (1995) Apoptosis in the neuronal lineage of the mouse olfactory epithelium: regulation in vivo and in vitro. Dev. Biol. 172, 307–323.

    PubMed  CAS  Google Scholar 

  48. Deckner M. L., Frisen J., Verge V. M., Hokfelt T., and Risling M. (1993) Localization of neurotrophin receptors in olfactory epithelium and bulb. Neuroreport 5, 301–304.

    PubMed  CAS  Google Scholar 

  49. Roskams A. J., Bethel M. A., Hurt K. J., and Ronnett G. V. (1996) Sequential expression of Trks A, B, and C in the regenerating olfactory neurolfactory epitheliumpithelium. J. Neurosci. 16, 1294–1307.

    PubMed  CAS  Google Scholar 

  50. DeHamer M. K., Guevara J. L., Hannon K., Olwin B. B., and Calof A. L. (1994) Genesis of olfactory receptor neurons in vitro: regulation of progenitor cell divisions by fibroblast growth factors. Neuron 13, 1083–1097.

    PubMed  CAS  Google Scholar 

  51. Goldstein B. J., Wolozin B. L., and Schwob J. E. (1997) FGF2 suppresses neuronogenesis of a cell line derived from rat olfactory epithelium. J. Neurobiol. 33, 411–428.

    PubMed  CAS  Google Scholar 

  52. MacDonald K. P., Murrell W. G., Bartlett P. F., Bushell G. R., and Mackay-Sim A. (1996) FGF2 promotes neuronal differentiation in explant cultures of adult and embryonic mouse olfactory epithelium. J. Neurosci. Res. 44, 27–39.

    PubMed  CAS  Google Scholar 

  53. Farbman A. I. (1994) Developmental biology of olfactory sensory neurons. Semin. Cell. Biol. 5, 3–10.

    PubMed  CAS  Google Scholar 

  54. Plendl J., Stierstorfer B., and Sinowatz F. (1999) Growth factors and their receptors in the olfactory system. Anat. Histol. Embryol. 28, 73–79.

    PubMed  CAS  Google Scholar 

  55. Murray R. C. and Calof A. L. (1999) Neuronal regeneration: lessons from the olfactory system. Semin. Cell Dev. Biol. 10, 421–431.

    PubMed  CAS  Google Scholar 

  56. Costanzo R. M. and Graziadei P. P. C. (1983) A quantitative analysis of changes in the olfactory epithelium following bulbectomy in hamster. J. Comp. Neurol. 215, 370–381.

    PubMed  CAS  Google Scholar 

  57. Carr VMcM and Farbmann A. I. (1992) Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp. Neurol. 115, 55–59.

    PubMed  CAS  Google Scholar 

  58. Liu N., Shields C. B., and Roisen F. J. (1998) Primary culture of adult mouse olfactory recepotr neurons. Exp. Neurol. 151, 173–183.

    PubMed  CAS  Google Scholar 

  59. Harding J. W., Getchell T. V., and Margolis F. L. (1978) Denervation of the primary olfactory pathway in mice. V. Long-term effect of intranasal ZnSO4 irrigation on behavior, biochemistry and morphology. Brain. Res. 140, 271–285.

    PubMed  CAS  Google Scholar 

  60. Burd G. D. (1993) Morphological study of the effects of intranasal zinc sulfate irrigation on the mouse olfactory epithelium and olfactory bulb. Microsc. Res. Tech. 24, 195–213.

    PubMed  CAS  Google Scholar 

  61. Miwa T., Moriizumi T., Sakashita H., Kimura Y., Donjo T., and Furukawa M. (1993) Transection of the olfactory nerves induces expression of nerve growth factor receptor in mouse olfactory epithelium. Neurosci. Lett. 155, 96–98.

    PubMed  CAS  Google Scholar 

  62. Burd G. D. and Sein V. (1998) Influence of olfactory innervation on neurogenesis in the developing olfactory bulb of the frog, Xenopus laevis. Ann. NY Acad. Sci. 855, 270–273.

    PubMed  CAS  Google Scholar 

  63. Brunjes P. C. (1994) Unilateral naris closure and olfactory system development. Brain Res. Brain Res. Rev. 19, 146–160.

    PubMed  CAS  Google Scholar 

  64. Kleene S. J. and Gesteland R. C. (1983) Dissociation of frog olfactory epithelium. J. Neurosci. Methods 9, 173–183.

    PubMed  CAS  Google Scholar 

  65. Ivanova T. T. and Caprio J. (1993) Odorant receptors activated by amino acids in sensory neurons of the channel catfish Ictalurus punctatus. J. Gen. Physiol. 102, 1085–1105.

    PubMed  CAS  Google Scholar 

  66. Firestein S., Picco C., and Menini A. (1993) The relation between stimulus and response in olfactory receptor cells of the tiger salamander. J. Physiol. (Lond) 468, 1–10.

    CAS  Google Scholar 

  67. Leinders-Zufall T., Greer C. A., Shepherd G. M., and Zufall F. (1998) Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J. Neurosci. 18, 5630–5639.

    PubMed  CAS  Google Scholar 

  68. Kleene S. J. and Gesteland R. C. (1981) Dissociation of frog olfactory epithelium with N-ethylmaleimide. Brain Res. 229, 536–540.

    PubMed  CAS  Google Scholar 

  69. Maue R. A. and Dionne V. E. (1987) Preparation of isolated mouse olfactory receptor neurons. Pflugers Arch. 409, 244–250.

    PubMed  CAS  Google Scholar 

  70. Nakamura T. and Gold G. H. (1987) A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325, 442–444.

    PubMed  CAS  Google Scholar 

  71. Sato T., Hirono J., Tonoike M., and Takebayashi M. (1991) Two types of increases in free Ca2+ evoked by odor in isolated frog olfactory receptor neurons. Neuroreport 2, 229–232.

    PubMed  CAS  Google Scholar 

  72. Rawson N. E., Gomez G., Cowart B., Brand J. G., Lowry L. D., Pribitkin E. A., and Restrepo D. (1997) Selectivity and response characteristics of human olfactory neurons. J. Neurophysiol. 77, 1606–1613.

    PubMed  CAS  Google Scholar 

  73. Tareilus E., Noe J., and Breer H. (1995) Calcium signals in olfactory neurons. Biochim. Biophys. Acta 1269, 129–138.

    PubMed  Google Scholar 

  74. Vargas G. and Lucero M. T. (1999) A method for maintaining odor-responsive adult rat olfactory receptor neurons in short-term culture. Chem. Senses. 24, 211–216.

    PubMed  CAS  Google Scholar 

  75. Gilbert S. F., Oster-Granite M. L., Kirby W., Durie D., Lyons D., and Greene E. (1986) Selective culture medium enhances survival of neuroblasts from postnatal rodent brain. Brain Res. Bull. 16, 853–860.

    PubMed  CAS  Google Scholar 

  76. Chuah M. I., David S., and Blaschuk O. (1991) Differentiation and survival of rat olfactory epithelial neurons in dissociated culture. Dev. Brain Res. 60, 123–132.

    CAS  Google Scholar 

  77. Pixley S. K. (1992) CNS Glial cells support in vitro survival, division, and differentiation of olfactory neuronal progenitor cells. Neuron 8, 1191–1204.

    PubMed  CAS  Google Scholar 

  78. Mumm J. S., Shou J., and Calof A. L. (1996) Colony-forming progenitors from mouse olfactory epithelium:Evidence for feedback regulation of neuron production. Proc. Natl. Acad. Sci. USA 93, 11,166–11,172.

    Google Scholar 

  79. Moon C., Sung Y. K., Reddy R., and Ronnett G. V. (1999) Odorants induce the phosphorylation of the cAMP response element binding protein in olfactory receptor neurons. Proc. Natl. Acad. Sci. USA 96, 14,605–14,610.

    CAS  Google Scholar 

  80. Moon C, Jaberi P., Otto-Bruc A., Baehr W., Palczewski K., and Ronnett G. V. (1998) Calciumsensitive particulate guanylyl cyclase as a modulator of cAMP in olfactory receptor neurons. J. Neurosci. 18, 3195–3205.

    PubMed  CAS  Google Scholar 

  81. Cunningham A. M., Manis P. B., Reed R. R., and Ronnett G. V. (1999) Olfactory receptor neurons exist as distinct subclasses of immature and mature cells in primary culture. Neuroscience 93, 1301–1312.

    PubMed  CAS  Google Scholar 

  82. Largent B. L., Sosnowski R. G., and Reed R. R. (1993) Directed expression of an oncogene to the olfactory neuronal lineage in transgenic mice. J. Neurosci. 13, 300–312.

    PubMed  CAS  Google Scholar 

  83. MacDonald K. P., Mackay-Sim A., Bushell G. R., and Bartlett PF (1996) Olfactory neuronal cell lines generated by retroviral insertion of the n-myc oncogene display different developmental phenotypes. J. Neurosci. Res. 45, 237–247.

    PubMed  CAS  Google Scholar 

  84. Barber R. D., Jaworsky D. E., Yau K. W., and Ronnett G. V. (2000) Isolation and in vitro differentiation of conditionally immortalized murine olfactory receptor neurons. J. Neurosci. 20, 3695–3704.

    PubMed  CAS  Google Scholar 

  85. Coon H. G., Curcio F, Sakaguchi K., Brandi M. L., and Swerdlow R. D. (1988) Cell cultures of neuroblasts from rat olfactory epithelium that show odorant responses. Proc. Natl. Acad. Sci. USA 86, 1703–1707.

    Google Scholar 

  86. Wolozin B., Sunderland T., Zheng B. B., Resau J., Dufy B., Barker J., Swerdlow R., and Coon H. (1992) Continuous culture of neuronal cells from adult human olfactory epithelium. J. Mol. Neurosci. 3, 137–146.

    Article  PubMed  CAS  Google Scholar 

  87. Vannelli G. B., Ensoli F., Zonefrati R., Kubota Y., Arcangeli A., Becchetti A., et al. (1995) Neuroblast long-term cell cultures from human fetal olfactory epithelium respond to odors. J. Neurosci. 15, 4382–4394.

    PubMed  CAS  Google Scholar 

  88. Gomez G., Restrepo D., Rawson N., Lowry L. D., Keane W. M., and Rothstein J. L. (1996) Induction of differentiation of human olfactory neuroblastoma cells into odorant-responsive cells. Neuroscience 74, 567–577.

    PubMed  CAS  Google Scholar 

  89. Barni T., Maggi M., Fantoni G., Granchi S., Mancina R., Gulisano M., et al. (1999) Sex steroids and odorants modulate gonadotropin-releasing hormone secretion in primary cultures of human olfactory cells. J. Clin. Endocrinol. Metab. 84, 4266–4273.

    PubMed  CAS  Google Scholar 

  90. Kubota Y., Sakano H., Ensoli F., Thiele C., and Vannelli G. B. (1994) Odorant receptor genes expressed in a human olfactory neuroblast cell line. J. Cell. Biochem. 18B(Suppl.), 182.

    Google Scholar 

  91. Ensoli F., Fiorelli V., Vannelli B., Barni T., De Cristofaro M., Ensoli B., and Thiele C. J. (1998) Basic fibroblast growth factor supports human olfactory neurogenesis by autocrine/paracrine mechanisms. Neuroscience 86, 881–993.

    PubMed  CAS  Google Scholar 

  92. Margolis F. L. (1988) Molecular cloning of olfactory-specific gene products, in Molecular Neurobiology of the Olfactory System, Margolis F. L. and Getchell T. V., eds., Plenum Press, New York, pp. 237–265.

    Google Scholar 

  93. Buiakova O. I., Baker H., Scott J. W., Farbman A., Kream R., Grillo M., et al. (1996) Olfactory marker protein (OMP) gene deletion causes altered physiological activity of olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 93, 9858–9863.

    PubMed  CAS  Google Scholar 

  94. Youngentob S. L. and Margolis F. L. (1999) OMP gene deletion causes an elevation in behavioral threshold sensitivity. Neuroreport 10, 15–19.

    PubMed  CAS  Google Scholar 

  95. Jat P. S., Cepko C. L., Mulligan R. C., and Sharp P. A. (1986) Recombinant retroviruses encoding simian virus 40 large T antigen and polyomavirus large and middle T antigens. Mol. Cell. Biol. 6, 1204–1217.

    PubMed  CAS  Google Scholar 

  96. Jat P. S., Noble M. D., Ataliotis P., Tanaka Y., Yannoutsos N., Larsen L., and Koussis D. (1991) Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc. Natl. Acad. Sci. USA 88, 5096–5100.

    PubMed  CAS  Google Scholar 

  97. Chambers T. J., Owens J. M., Hattersley G., Jat P. S., and Noble M. D. (1993) Generation of osteoclast-inductive and osteoclastogenic cell lines from the H-2Kb-tsA58 transgenic mouse. Proc. Natl. Acad. Sci. USA 90, 5578–5582.

    PubMed  CAS  Google Scholar 

  98. Whitehead R. H., Van Eeden P. E., Noble M. D., Ataliotis P., and Jat P. S. (1993) Establishment of conditionally immortalized epithelial cell lines from both colon and small intestine of adult H-2Kb-tsA58 transgenic mice. Proc. Natl. Acad. Sci. USA 90, 587–591.

    PubMed  CAS  Google Scholar 

  99. Barber R. D., Woolf A. S., and Henderson R. M. (1997) Potassium conductances and proliferation in conditionally immortalized renal glomerular mesangial cells from the H-2Kb-tsA58 transgenic mouse. Biochim. Biophys. Acta 1355, 191–203.

    PubMed  CAS  Google Scholar 

  100. Noble M., Groves A. K., Ataliotis P., Ikram Z., and Jat P. S. (1995) The H-2Kb-tsA58 transgenic mouse: a new tool for the rapid generation of novel cell lines. Transgenic Res. 4, 215–225.

    PubMed  CAS  Google Scholar 

  101. Goldstein B. J. and Schwob J. E. (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, 4005–4016.

    PubMed  CAS  Google Scholar 

  102. Gong Q., Liu W. L., Srodon M., Foster T. D., and Shipley M. T. (1996) Olfactory epithelial organotypic slice cultures: a useful tool for investigating olfactory neural development. Int. J. Dev. Neurosci. 14, 841–852.

    PubMed  CAS  Google Scholar 

  103. Puche A. C. and Shipley M. T. (1999) Odor-induced, activity-dependent transneuronal gene induction in vitro: mediation by NMDA receptors. J. Neurosci. 19, 1359–1370.

    PubMed  CAS  Google Scholar 

  104. Kanaki K, Sato K., and Kashiwayanagi M. (2000) Functional synapse formation between rat olfactory receptor neurons and olfactory bulb neurons in vitro. Neurosci. Lett. 285, 76–78.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, 725 North Wolfe Street, 21205, Baltimore, MD

    Robert D. Barber

  2. Department of Neuroscience, Johns Hopkins University School of Medicine, 725 North Wolfe Street, 21205, Baltimore, MD

    Robert D. Barber & Gabriele V. Ronnett

  3. Department of Neurology, Johns Hopkins University School of Medicine, 725 North Wolfe Street, 21205, Baltimore, MD

    Gabriele V. Ronnett

Authors
  1. Robert D. Barber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gabriele V. Ronnett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriele V. Ronnett.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barber, R.D., Ronnett, G.V. Reconstructing smell. Mol Neurobiol 21, 161–173 (2000). https://doi.org/10.1385/MN:21:3:161

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/MN:21:3:161

Index Entries

Search

Navigation