Skip to main content
SpringerLink
Log in

Mechanisms controlling diversification of olfactory sensory neuron classes

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Animals survive in harsh and fluctuating environments using sensory neurons to detect and respond to changes in their surroundings. Olfactory sensory neurons are essential for detecting food, identifying danger, and sensing pheromones. The ability to sense a large repertoire of different types of odors is crucial to distinguish between different situations, and is achieved through neuronal diversity within the olfactory system. Here, we review the developmental mechanisms used to establish diversity of olfactory sensory neurons in various model organisms, including Caenorhabditis elegans, Drosophila, and vertebrate models. Understanding and comparing how different olfactory neurons develop within the nervous system of different animals can provide insight into how the olfactory system is shaped in humans.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Mesholam RI, Moberg PJ, Mahr RN, Doty RL (1998) Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer’s and Parkinson’s diseases. Arch Neurol 55(1):84–90

    Article  CAS  PubMed  Google Scholar 

  2. Tabert MH, Liu X, Doty RL, Serby M, Zamora D, Pelton GH, Marder K, Albers MW, Stern Y, Devanand DP (2005) A 10-item smell identification scale related to risk for Alzheimer’s disease. Ann Neurol 58(1):155–160. doi:10.1002/ana.20533

    Article  PubMed  Google Scholar 

  3. Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78(5):823–834

    Article  CAS  PubMed  Google Scholar 

  4. Mombaerts P (2004) Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol 14(1):31–36. doi:10.1016/j.conb.2004.01.014

    Article  CAS  PubMed  Google Scholar 

  5. Bargmann CI (2006) Chemosensation in C. elegans. WormBook

  6. Bargmann CI, Avery L (1995) Laser killing of cells in Caenorhabditis elegans. Methods Cell Biol 48:225–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bargmann CI, Hartwieg E, Horvitz HR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74(3):515–527

    Article  CAS  PubMed  Google Scholar 

  8. Sengupta P, Chou JH, Bargmann CI (1996) odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84(6):899–909

    Article  CAS  PubMed  Google Scholar 

  9. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83(2):207–218

    Article  CAS  PubMed  Google Scholar 

  10. Troemel ER, Kimmel BE, Bargmann CI (1997) Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell 91(2):161–169

    Article  CAS  PubMed  Google Scholar 

  11. Sulston JE (1983) Neuronal cell lineages in the nematode Caenorhabditis elegans. Cold Spring Harbor Symposia Quant Biol 48 Pt 2:443–452

    Article  Google Scholar 

  12. Hobert O (2010) Neurogenesis in the nematode Caenorhabditis elegans. WormBook:1–24. doi:10.1895/wormbook.1.12.2

    PubMed  PubMed Central  Google Scholar 

  13. Colosimo ME, Tran S, Sengupta P (2003) The divergent orphan nuclear receptor ODR-7 regulates olfactory neuron gene expression via multiple mechanisms in Caenorhabditis elegans. Genetics 165(4):1779–1791

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Sagasti A, Hobert O, Troemel ER, Ruvkun G, Bargmann CI (1999) Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4. Genes Dev 13 (14):1794–1806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Alqadah A, Hsieh YW, Chuang CF (2016) Sox2 goes beyond stem cell biology. Cell Cycle 15(6):777–778. doi:10.1080/15384101.2015.1137714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Alqadah A, Hsieh YW, Vidal B, Chang C, Hobert O, Chuang CF (2015) Postmitotic diversification of olfactory neuron types is mediated by differential activities of the HMG-box transcription factor SOX-2. EMBO J 34(20):2574–2589. doi:10.15252/embj.201592188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Troemel ER, Sagasti A, Bargmann CI (1999) Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell 99(4):387–398

    Article  CAS  PubMed  Google Scholar 

  18. Wes PD, Bargmann CI (2001) C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature 410(6829):698–701. doi:10.1038/35070581

    Article  CAS  PubMed  Google Scholar 

  19. Bauer Huang SL, Saheki Y, VanHoven MK, Torayama I, Ishihara T, Katsura I, van der Linden A, Sengupta P, Bargmann CI (2007) Left-right olfactory asymmetry results from antagonistic functions of voltage-activated calcium channels and the Raw repeat protein OLRN-1 in C. elegans. Neural development 2:24. doi:10.1186/1749-8104-2-24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Sagasti A, Hisamoto N, Hyodo J, Tanaka-Hino M, Matsumoto K, Bargmann CI (2001) The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 105(2):221–232

    Article  CAS  PubMed  Google Scholar 

  21. Chang C, Hsieh YW, Lesch BJ, Bargmann CI, Chuang CF (2011) Microtubule-based localization of a synaptic calcium-signaling complex is required for left-right neuronal asymmetry in C. elegans. Development 138 (16):3509–3518. doi:10.1242/dev.069740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Chuang CF, Bargmann CI (2005) A Toll-interleukin 1 repeat protein at the synapse specifies asymmetric odorant receptor expression via ASK1 MAPKKK signaling. Genes Dev 19 (2):270–281. doi:10.1101/gad.1276505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Chuang CF, Vanhoven MK, Fetter RD, Verselis VK, Bargmann CI (2007) An innexin-dependent cell network establishes left-right neuronal asymmetry in C. elegans. Cell 129(4):787–799. doi:10.1016/j.cell.2007.02.052

    Article  CAS  PubMed  Google Scholar 

  24. Schumacher JA, Hsieh YW, Chen S, Pirri JK, Alkema MJ, Li WH, Chang C, Chuang CF (2012) Intercellular calcium signaling in a gap junction-coupled cell network establishes asymmetric neuronal fates in C. elegans. Development 139 (22):4191–4201. doi:10.1242/dev.083428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Vanhoven MK, Bauer Huang SL, Albin SD, Bargmann CI (2006) The claudin superfamily protein nsy-4 biases lateral signaling to generate left-right asymmetry in C. elegans olfactory neurons. Neuron 51(3):291–302. doi:10.1016/j.neuron.2006.06.029

    Article  CAS  PubMed  Google Scholar 

  26. Alqadah A, Hsieh YW, Schumacher JA, Wang X, Merrill SA, Millington G, Bayne B, Jorgensen EM, Chuang CF (2016) SLO BK potassium channels couple gap junctions to inhibition of calcium signaling in olfactory neuron diversification. PLoS Genet 12(1):e1005654. doi:10.1371/journal.pgen.1005654

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Alqadah A, Hsieh YW, Chuang CF (2013) microRNA function in left-right neuronal asymmetry: perspectives from C. elegans. Front Cell Neurosci 7:158. doi:10.3389/fncel.2013.00158

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Hsieh YW, Chang C, Chuang CF (2012) The microRNA mir-71 inhibits calcium signaling by targeting the TIR-1/Sarm1 adaptor protein to control stochastic L/R neuronal asymmetry in C. elegans. PLoS Genet 8(8):e1002864. doi:10.1371/journal.pgen.1002864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hsieh YW, Alqadah A, Chuang CF (2014) Asymmetric neural development in the Caenorhabditis elegans olfactory system. Genesis 52(6):544–554. doi:10.1002/dvg.22744

    Article  PubMed  PubMed Central  Google Scholar 

  30. Taylor RW, Hsieh YW, Gamse JT, Chuang CF (2010) Making a difference together: reciprocal interactions in C. elegans and zebrafish asymmetric neural development. Development 137 (5):681–691. doi:10.1242/dev.038695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Cochella L, Tursun B, Hsieh YW, Galindo S, Johnston RJ, Chuang CF, Hobert O (2014) Two distinct types of neuronal asymmetries are controlled by the Caenorhabditis elegans zinc finger transcription factor die-1. Genes Dev 28 (1):34–43. doi:10.1101/gad.233643.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lesch BJ, Bargmann CI (2010) The homeodomain protein hmbx-1 maintains asymmetric gene expression in adult C. elegans olfactory neurons. Genes Dev 24 (16):1802–1815. doi:10.1101/gad.1932610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lesch BJ, Gehrke AR, Bulyk ML, Bargmann CI (2009) Transcriptional regulation and stabilization of left-right neuronal identity in C. elegans. Genes Dev 23 (3):345–358. doi:10.1101/gad.1763509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Joseph RM, Carlson JR (2015) Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Trends Genet 31(12):683–695. doi:10.1016/j.tig.2015.09.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Shanbhag SR, Müller B, Steinbrecht RA (1999) Atlas of olfactory organs of Drosophila melanogaster: 1. Types, external organization, innervation and distribution of olfactory sensilla. Int J Insect Morphol Embryol 28(4):377–397. doi:10.1016/S0020-7322(99)00039-2

    Article  Google Scholar 

  36. Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15(17):1535–1547. doi:10.1016/j.cub.2005.07.034

    Article  CAS  PubMed  Google Scholar 

  37. Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452(7190):1007–1011. doi:10.1038/nature06861

    Article  CAS  PubMed  Google Scholar 

  38. Fuss SH, Ray A (2009) Mechanisms of odorant receptor gene choice in Drosophila and vertebrates. Mol Cell Neurosci 41(2):101–112. doi:10.1016/j.mcn.2009.02.014

    Article  CAS  PubMed  Google Scholar 

  39. Barish S, Volkan PC (2015) Mechanisms of olfactory receptor neuron specification in Drosophila. Wiley Interdiscip Rev Dev Biol 4(6):609–621. doi:10.1002/wdev.197

    Article  PubMed  PubMed Central  Google Scholar 

  40. Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15(17):1548–1553. doi:10.1016/j.cub.2005.07.066

    Article  CAS  PubMed  Google Scholar 

  41. Goldman AL, Naters WVDG, Lessing D, Warr CG, Carlson JR (2005) Coexpression of two functional odor receptors in one neuron. Neuron 45 (5):661–666. doi:10.1016/j.neuron.2005.01.025

    Article  CAS  PubMed  Google Scholar 

  42. Bargmann CI (2006) Comparative chemosensation from receptors to ecology. Nature 444(7117):295–301. doi:10.1038/nature05402

    Article  CAS  PubMed  Google Scholar 

  43. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43(5):703–714. doi:10.1016/j.neuron.2004.08.019

    Article  CAS  PubMed  Google Scholar 

  44. Vosshall LB, Hansson BS (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem Senses 36(6):497–498. doi:10.1093/chemse/bjr022

    Article  PubMed  Google Scholar 

  45. Ray A, Naters WVDG, Carlson JR (2008) A regulatory code for neuron-specific odor receptor expression. PLoS Biol 6(5):e125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Ray A, Naters WVDG, Shiraiwa T, Carlson JR (2007) Mechanisms of odor receptor gene choice in Drosophila. Neuron 53(3):353–369. doi:10.1016/j.neuron.2006.12.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96(5):725–736

    Article  CAS  PubMed  Google Scholar 

  48. Marin EC, Jefferis GS, Komiyama T, Zhu H, Luo L (2002) Representation of the glomerular olfactory map in the Drosophila brain. Cell 109(2):243–255

    Article  CAS  PubMed  Google Scholar 

  49. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109(2):229–241

    Article  CAS  PubMed  Google Scholar 

  50. Kumar JP, Moses K (2001) EGF receptor and Notch signaling act upstream of Eyeless/Pax6 to control eye specification. Cell 104(5):687–697

    Article  CAS  PubMed  Google Scholar 

  51. Casares F, Mann RS (1998) Control of antennal versus leg development in Drosophila. Nature 392(6677):723–726. doi:10.1038/33706

    Article  CAS  PubMed  Google Scholar 

  52. Dong PD, Chu J, Panganiban G (2000) Coexpression of the homeobox genes Distal-less and homothorax determines Drosophila antennal identity. Development 127 (2):209–216

    CAS  PubMed  Google Scholar 

  53. Dong PD, Dicks JS, Panganiban G (2002) Distal-less and homothorax regulate multiple targets to pattern the Drosophila antenna. Development 129 (8):1967–1974

    CAS  PubMed  Google Scholar 

  54. Rodrigues V, Hummel T (2008) Development of the Drosophila olfactory system. Adv Exp Med Biol 628:82–101. doi:10.1007/978-0-387-78261-4_6

    Article  PubMed  Google Scholar 

  55. Theisen H, Haerry TE, O’Connor MB, Marsh JL (1996) Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. Development 122 (12):3939–3948

    CAS  PubMed  Google Scholar 

  56. Royet J, Finkelstein R (1997) Establishing primordia in the Drosophila eye-antennal imaginal disc: the roles of decapentaplegic, wingless and hedgehog. Development 124 (23):4793–4800

    CAS  PubMed  Google Scholar 

  57. Hobert O, Carrera I, Stefanakis N (2010) The molecular and gene regulatory signature of a neuron. Trends Neurosci 33(10):435–445. doi:10.1016/j.tins.2010.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Li Q, Barish S, Okuwa S, Maciejewski A, Brandt AT, Reinhold D, Jones CD, Volkan PC (2016) A Functionally conserved gene regulatory network module governing olfactory neuron diversity. PLoS Genet 12(1):e1005780. doi:10.1371/journal.pgen.1005780

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Li Q, Ha TS, Okuwa S, Wang Y, Wang Q, Millard SS, Smith DP, Volkan PC (2013) Combinatorial rules of precursor specification underlying olfactory neuron diversity. Curr Biol 23(24):2481–2490. doi:10.1016/j.cub.2013.10.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Reddy GV, Gupta B, Ray K, Rodrigues V (1997) Development of the Drosophila olfactory sense organs utilizes cell-cell interactions as well as lineage. Development 124 (3):703–712

    CAS  PubMed  Google Scholar 

  61. Guo M, Jan LY, Jan YN (1996) Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17(1):27–41

    Article  PubMed  Google Scholar 

  62. Endo K, Aoki T, Yoda Y, Kimura K, Hama C (2007) Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat Neurosci 10(2):153–160. doi:10.1038/nn1832

    Article  CAS  PubMed  Google Scholar 

  63. Sim CK, Perry S, Tharadra SK, Lipsick JS, Ray A (2012) Epigenetic regulation of olfactory receptor gene expression by the Myb-MuvB/dREAM complex. Genes Dev 26 (22):2483–2498. doi:10.1101/gad.201665.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Magklara A, Yen A, Colquitt BM, Clowney EJ, Allen W, Markenscoff-Papadimitriou E, Evans ZA, Kheradpour P, Mountoufaris G, Carey C, Barnea G, Kellis M, Lomvardas S (2011) An epigenetic signature for monoallelic olfactory receptor expression. Cell 145(4):555–570. doi:10.1016/j.cell.2011.03.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Komiyama T, Carlson JR, Luo L (2004) Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat Neurosci 7(8):819–825. doi:10.1038/nn1284

    Article  CAS  PubMed  Google Scholar 

  66. Hummel T, Vasconcelos ML, Clemens JC, Fishilevich Y, Vosshall LB, Zipursky SL (2003) Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37(2):221–231

    Article  CAS  PubMed  Google Scholar 

  67. Jhaveri D, Saharan S, Sen A, Rodrigues V (2004) Positioning sensory terminals in the olfactory lobe of Drosophila by Robo signaling. Development 131 (9):1903–1912. doi:10.1242/dev.01083

    Article  CAS  PubMed  Google Scholar 

  68. Ang LH, Kim J, Stepensky V, Hing H (2003) Dock and Pak regulate olfactory axon pathfinding in Drosophila. Development 130 (7):1307–1316

    Article  CAS  PubMed  Google Scholar 

  69. Hummel T, Zipursky SL (2004) Afferent induction of olfactory glomeruli requires N-cadherin. Neuron 42(1):77–88

    Article  CAS  PubMed  Google Scholar 

  70. Ward A, Hong W, Favaloro V, Luo L (2015) Toll receptors instruct axon and dendrite targeting and participate in synaptic partner matching in a Drosophila olfactory circuit. Neuron 85(5):1013–1028. doi:10.1016/j.neuron.2015.02.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Hong W, Mosca TJ, Luo L (2012) Teneurins instruct synaptic partner matching in an olfactory map. Nature 484(7393):201–207. doi:10.1038/nature10926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Komiyama T, Sweeney LB, Schuldiner O, Garcia KC, Luo L (2007) Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128(2):399–410. doi:10.1016/j.cell.2006.12.028

    Article  CAS  PubMed  Google Scholar 

  73. Sweeney LB, Chou YH, Wu Z, Joo W, Komiyama T, Potter CJ, Kolodkin AL, Garcia KC, Luo L (2011) Secreted semaphorins from degenerating larval ORN axons direct adult projection neuron dendrite targeting. Neuron 72(5):734–747. doi:10.1016/j.neuron.2011.09.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Hong W, Zhu H, Potter CJ, Barsh G, Kurusu M, Zinn K, Luo L (2009) Leucine-rich repeat transmembrane proteins instruct discrete dendrite targeting in an olfactory map. Nat Neurosci 12(12):1542–1550. doi:10.1038/nn.2442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Gerber B, Stocker RF (2007) The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem Senses 32(1):65–89. doi:10.1093/chemse/bjl030

    Article  CAS  PubMed  Google Scholar 

  76. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121(5):795–807. doi:10.1016/j.cell.2005.04.026

    Article  CAS  PubMed  Google Scholar 

  77. Hueston CE, Olsen D, Li Q, Okuwa S, Peng B, Wu J, Volkan PC (2016) Chromatin modulatory proteins and olfactory receptor signaling in the refinement and maintenance of fruitless expression in olfactory receptor neurons. PLoS Biol 14(4):e1002443. doi:10.1371/journal.pbio.1002443

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Devaud JM, Acebes A, Ferrus A (2001) Odor exposure causes central adaptation and morphological changes in selected olfactory glomeruli in Drosophila. J Neurosci 21(16):6274–6282

    CAS  PubMed  Google Scholar 

  79. Kidd S, Lieber T (2016) Mechanism of Notch Pathway activation and its role in the regulation of olfactory plasticity in Drosophila melanogaster. PLoS One 11(3):e0151279. doi:10.1371/journal.pone.0151279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Kidd S, Struhl G, Lieber T (2015) Notch is required in adult Drosophila sensory neurons for morphological and functional plasticity of the olfactory circuit. PLoS Genet 11(5):e1005244. doi:10.1371/journal.pgen.1005244

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Lieber T, Kidd S, Struhl G (2011) DSL-Notch signaling in the Drosophila brain in response to olfactory stimulation. Neuron 69(3):468–481. doi:10.1016/j.neuron.2010.12.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. 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 

  83. Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100(6):611–618

    Article  CAS  PubMed  Google Scholar 

  84. Donner AL, Episkopou V, Maas RL (2007) Sox2 and Pou2f1 interact to control lens and olfactory placode development. Dev Biol 303(2):784–799. doi:10.1016/j.ydbio.2006.10.047

    Article  CAS  PubMed  Google Scholar 

  85. 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(2):339–352

    Article  CAS  PubMed  Google Scholar 

  86. Guillemot F, Lo LC, Johnson JE, Auerbach A, Anderson DJ, Joyner AL (1993) Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75(3):463–476

    Article  CAS  PubMed  Google Scholar 

  87. Ressler KJ, Sullivan SL, Buck LB (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73(3):597–609

    Article  CAS  PubMed  Google Scholar 

  88. Clowney EJ, LeGros MA, Mosley CP, Clowney FG, Markenskoff-Papadimitriou EC, Myllys M, Barnea G, Larabell CA, Lomvardas S (2012) Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 151(4):724–737. doi:10.1016/j.cell.2012.09.043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Zhang X, Firestein S (2002) The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5(2):124–133. doi:10.1038/nn800

    CAS  PubMed  Google Scholar 

  90. Lyons DB, Allen WE, Goh T, Tsai L, Barnea G, Lomvardas S (2013) An epigenetic trap stabilizes singular olfactory receptor expression. Cell 154(2):325–336. doi:10.1016/j.cell.2013.06.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R (2006) Interchromosomal interactions and olfactory receptor choice. Cell 126(2):403–413. doi:10.1016/j.cell.2006.06.035

    Article  CAS  PubMed  Google Scholar 

  92. Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M, Yoshihara Y, Sakano H (2003) Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302(5653):2088–2094. doi:10.1126/science.1089122

    Article  CAS  PubMed  Google Scholar 

  93. Hanchate NK, Kondoh K, Lu Z, Kuang D, Ye X, Qiu X, Pachter L, Trapnell C, Buck LB (2015) Single-cell transcriptomics reveals receptor transformations during olfactory neurogenesis. Science 350(6265):1251–1255. doi:10.1126/science.aad2456

    Article  CAS  PubMed  Google Scholar 

  94. Tan L, Li Q, Xie XS (2015) Olfactory sensory neurons transiently express multiple olfactory receptors during development. Mol Syst Biol 11(12):844. doi:10.15252/msb.20156639

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Magklara A, Lomvardas S (2013) Stochastic gene expression in mammals: lessons from olfaction. Trends Cell Biol 23(9):449–456. doi:10.1016/j.tcb.2013.04.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Mori K, Sakano H (2011) How is the olfactory map formed and interpreted in the mammalian brain? Annu Rev Neurosci 34:467–499. doi:10.1146/annurev-neuro-112210-112917

    Article  CAS  PubMed  Google Scholar 

  97. Feinstein P, Bozza T, Rodriguez I, Vassalli A, Mombaerts P (2004) Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117(6):833–846. doi:10.1016/j.cell.2004.05.013

    Article  CAS  PubMed  Google Scholar 

  98. Mombaerts P (1996) Targeting olfaction. Curr Opin Neurobiol 6(4):481–486

    Article  CAS  PubMed  Google Scholar 

  99. Wang F, Nemes A, Mendelsohn M, Axel R (1998) Odorant receptors govern the formation of a precise topographic map. Cell 93(1):47–60

    Article  CAS  PubMed  Google Scholar 

  100. Imai T, Suzuki M, Sakano H (2006) Odorant receptor-derived cAMP signals direct axonal targeting. Science 314(5799):657–661. doi:10.1126/science.1131794

    Article  CAS  PubMed  Google Scholar 

  101. Imai T, Yamazaki T, Kobayakawa R, Kobayakawa K, Abe T, Suzuki M, Sakano H (2009) Pre-target axon sorting establishes the neural map topography. Science 325(5940):585–590. doi:10.1126/science.1173596

    Article  CAS  PubMed  Google Scholar 

  102. Dalton RP, Lyons DB, Lomvardas S (2013) Co-opting the unfolded protein response to elicit olfactory receptor feedback. Cell 155(2):321–332. doi:10.1016/j.cell.2013.09.033

    Article  CAS  PubMed  Google Scholar 

  103. Rodriguez I (2013) Singular expression of olfactory receptor genes. Cell 155(2):274–277. doi:10.1016/j.cell.2013.09.032

    Article  CAS  PubMed  Google Scholar 

  104. Miyasaka N, Wanner AA, Li J, Mack-Bucher J, Genoud C, Yoshihara Y, Friedrich RW (2013) Functional development of the olfactory system in zebrafish. Mech Dev 130(6–8):336–346. doi:10.1016/j.mod.2012.09.001

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work is supported by an Alfred P. Sloan Research Fellowship and an NIH grant R01GM098026 to C.-F.C.

Author information

Author notes

    Authors and Affiliations

    1. Department of Biological Sciences, University of Illinois at Chicago, 900 S. Ashland Avenue, MC 567, Chicago, IL, 60607, USA

      Yi-Wen Hsieh, Amel Alqadah & Chiou-Fen Chuang

    Authors
    1. Yi-Wen Hsieh
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Amel Alqadah
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Chiou-Fen Chuang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Chiou-Fen Chuang.

    Additional information

    Yi-Wen Hsieh and Amel Alqadah contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Hsieh, YW., Alqadah, A. & Chuang, CF. Mechanisms controlling diversification of olfactory sensory neuron classes. Cell. Mol. Life Sci. 74, 3263–3274 (2017). https://doi.org/10.1007/s00018-017-2512-2

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00018-017-2512-2

    Keywords

    Search

    Navigation