Large-scale transcriptional profiling of chemosensory neurons identifies receptor-ligand pairs in vivo

Nature Neuroscience

Volumn 18, Issue 10, 2015, Pages 1455-1463

  Von Der Weid, Benoît ^a   Rossier, Daniel ^a   Lindup, Matti ^a   Tuberosa, Joël ^a   Widmer, Alexandre ^a   Col, Julien Dal ^a   Kan, Chenda ^a   Carleton, Alan ^a   Rodriguez, Ivan ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACETOPHENONE; ETHYL ISOBUTYRATE; ISOBUTYRIC ACID DERIVATIVE; LIGAND; RECEPTOR; UNCLASSIFIED DRUG; OLFACTORY RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CHEMOSENSORY NEURON; CONTROLLED STUDY; DRUG EXPOSURE; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; IN VIVO STUDY; MALE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; ODOR; OLFACTORY RECEPTOR; PRIORITY JOURNAL; RAT; RECEPTOR BINDING ASSAY; SENSORY NERVE CELL; SMELLING; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS; ANIMAL; C57BL MOUSE; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LEWIS RAT; METABOLISM; PHYSIOLOGY; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICE; MICE, INBRED C57BL; OLFACTORY RECEPTOR NEURONS; RATS; RATS, INBRED LEW; RECEPTORS, ODORANT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SMELL;

EID: 84942456919     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4100     Document Type: Article

References (48)

1. Buck, L. &Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175-187 (1991)
2. Niimura, Y., Matsui, A. &Touhara, K. Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res. 24, 1485-1496 (2014)
3. Zhang, X. &Firestein, S. Genomics of olfactory receptors. Results Probl. Cell Differ. 47, 25-36 (2009)
4. Malnic, B., Hirono, J., Sato, T. &Buck, L.B. Combinatorial receptor codes for odors. Cell 96, 713-723 (1999)
5. Peterlin, Z., Firestein, S. &Rogers, M.E. The state of the art of odorant receptor deorphanization: a report from the orphanage. J. Gen. Physiol. 143, 527-542 (2014)
6. Katada, S., Nakagawa, T., Kataoka, H. &Touhara, K. Odorant response assays for a heterologously expressed olfactory receptor. Biochem. Biophys. Res. Commun. 305, 964-969 (2003)
7. Abaffy, T., Matsunami, H. &Luetje, C.W. Functional analysis of a mammalian odorant receptor subfamily. J. Neurochem. 97, 1506-1518 (2006)
8. Matarazzo, V. et al. Functional characterization of two human olfactory receptors expressed in the baculovirus Sf9 insect cell system. Chem. Senses 30, 195-207 (2005)
9. Mitsui, K. et al. Functional reconstitution of olfactory receptor complex on baculovirus. Chem. Senses 37, 837-847 (2012)
10. Kajiya, K. et al. Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci. 21, 6018-6025 (2001)
11. Oka, Y., Omura, M., Kataoka, H. &Touhara, K. Olfactory receptor antagonism between odorants. EMBO J. 23, 120-126 (2004)
12. Baud, O. et al. The mouse eugenol odorant receptor: structural and functional plasticity of a broadly tuned odorant binding pocket. Biochemistry 50, 843-853 (2011)
13. Spehr, M. et al. Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299, 2054-2058 (2003)
14. Wetzel, C.H. et al. Specificity and sensitivity of a human olfactory receptor functionally expressed in human embryonic kidney 293 cells and Xenopus laevis oocytes. J. Neurosci. 19, 7426-7433 (1999)
15. Krautwurst, D., Yau, K.W. &Reed, R.R. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95, 917-926 (1998)
16. Saito, H., Chi, Q., Zhuang, H., Matsunami, H. &Mainland, J.D. Odor coding by a mammalian receptor repertoire. Sci. Signal. 2, ra9 (2009)
17. Saito, H., Kubota, M., Roberts, R.W., Chi, Q. &Matsunami, H. RTP family members induce functional expression of mammalian odorant receptors. Cell 119, 679-691 (2004)
18. Shepard, B.D., Natarajan, N., Protzko, R.J., Acres, O.W. &Pluznick, J.L. A cleavable N-terminal signal peptide promotes widespread olfactory receptor surface expression in HEK293T cells. PLoS ONE 8, e68758 (2013)
19. Mainland, J.D. et al. The missense of smell: functional variability in the human odorant receptor repertoire. Nat. Neurosci. 17, 114-120 (2014)
20. Katada, S., Hirokawa, T., Oka, Y., Suwa, M. &Touhara, K. Structural basis for a broad but selective ligand spectrum of a mouse olfactory receptor: mapping the odorant-binding site. J. Neurosci. 25, 1806-1815 (2005)
21. Nagashima, A. &Touhara, K. Enzymatic conversion of odorants in nasal mucus affects olfactory glomerular activation patterns and odor perception. J. Neurosci. 30, 16391-16398 (2010)
22. Araneda, R.C., Kini, A.D. &Firestein, S. The molecular receptive range of an odorant receptor. Nat. Neurosci. 3, 1248-1255 (2000)
23. Oka, Y. et al. Odorant receptor map in the mouse olfactory bulb: in vivo sensitivity and specificity of receptor-defined glomeruli. Neuron 52, 857-869 (2006)
24. Bautze, V. et al. Mammalian-specific OR37 receptors are differentially activated by distinct odorous fatty aldehydes. Chem. Senses 37, 479-493 (2012)
25. Bozza, T., Feinstein, P., Zheng, C. &Mombaerts, P. Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22, 3033-3043 (2002)
26. Feinstein, P., Bozza, T., Rodriguez, I., Vassalli, A. &Mombaerts, P. Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117, 833-846 (2004)
27. Touhara, K. et al. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl. Acad. Sci. USA 96, 4040-4045 (1999)
28. Tsuboi, A. et al. Two highly homologous mouse odorant receptors encoded by tandemly-linked MOR29A and MOR29B genes respond differently to phenyl ethers. Eur. J. Neurosci. 33, 205-213 (2011)
29. Zhao, H. et al. Functional expression of a mammalian odorant receptor. Science 279, 237-242 (1998)
30. Shirasu, M. et al. Olfactory receptor and neural pathway responsible for highly selective sensing of musk odors. Neuron 81, 165-178 (2014)
31. McClintock, T.S. et al. In vivo identification of eugenol-responsive and muscone-responsive mouse odorant receptors. J. Neurosci. 34, 15669-15678 (2014)
32. Vassalli, A., Rothman, A., Feinstein, P., Zapotocky, M. &Mombaerts, P. Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 35, 681-696 (2002)
33. Potter, S.M. et al. Structure and emergence of specific olfactory glomeruli in the mouse. J. Neurosci. 21, 9713-9723 (2001)
34. Zhang, J., Pacifico, R., Cawley, D., Feinstein, P. &Bozza, T. Ultrasensitive detection of amines by a trace amine-associated receptor. J. Neurosci. 33, 3228-3239 (2013)
35. Ibarra-Soria, X., Levitin, M.O., Saraiva, L.R. &Logan, D.W. The olfactory transcriptomes of mice. PLoS Genet. 10, e1004593 (2014)
36. Plessy, C. et al. Promoter architecture of mouse olfactory receptor genes. Genome Res. 22, 486-497 (2012)
37. Knight, Z.A. et al. Molecular profiling of activated neurons by phosphorylated ribosome capture. Cell 151, 1126-1137 (2012)
38. Adipietro, K.A., Mainland, J.D. &Matsunami, H. Functional evolution of mammalian odorant receptors. PLoS Genet. 8, e1002821 (2012)
39. Benton, R., Sachse, S., Michnick, S.W. &Vosshall, L.B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4, e20 (2006)
40. Hansson, B.S. &Stensmyr, M.C. Evolution of insect olfaction. Neuron 72, 698-711 (2011)
41. Buck, L.B. Olfactory receptors and odor coding in mammals. Nutr. Rev. 62, S184-S188; discussion S224-S241 (2004)
42. Jiang, Y. et al. Molecular profiling of activated olfactory neurons identifies odorant receptors responding to odors in vivo. Nat. Neurosci. doi:10.1038/nn.4104 (31 August 2015)
43. Niimura, Y. &Nei, M. Extensive gains and losses of olfactory receptor genes in mammalian evolution. PLoS ONE 2, e708 (2007)
44. Zufall, F. &Leinders-Zufall, T. The cellular and molecular basis of odor adaptation. Chem. Senses 25, 473-481 (2000)
45. Kato, A. &Touhara, K. Mammalian olfactory receptors: pharmacology, G protein coupling and desensitization. Cell. Mol. Life Sci. 66, 3743-3753 (2009)
46. Kobayakawa, K. et al. Innate versus learned odor processing in the mouse olfactory bulb. Nature 450, 503-508 (2007)
47. Hallem, E.A. &Carlson, J.R. Coding of odors by a receptor repertoire. Cell 125, 143-160 (2006)
48. David, F.P. et al. HTSstation: a web application and open-access libraries for high-throughput sequencing data analysis. PLoS ONE 9, e85879 (2014)