Advertisement

Mammalian Genome

, Volume 23, Issue 1–2, pp 132–143 | Cite as

Genetics of canine olfaction and receptor diversity

  • Pascale QuignonEmail author
  • Maud Rimbault
  • Stéphanie Robin
  • Francis Galibert
Article

Abstract

Olfaction is a particularly important sense in the dog. Humans selected for this capacity during the domestication process, and selection has continued to be employed to enhance this ability. In this review we first describe the different olfactory systems that exist and the different odorant receptors that are expressed in those systems. We then focus on the dog olfactory receptors by describing the olfactory receptor gene repertoire and its polymorphisms. Finally, we discuss the different uses of dog olfaction and the questions that still need to be studied.

Keywords

Olfactory Receptor Olfactory Epithelium Vomeronasal Organ Odorant Molecule Copy Number Variation Region 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We deeply thank Dr. Jean-Paul Boidot for providing the schematic drawing of the dog head and Dr. Tyrone C. Spady for careful reading and editing of the manuscript.

References

  1. Asai H, Kasai H, Matsuda Y, Yamasaki N, Nagawa F, Sakano H, Tsuboi A (1996) Genomic structure and transcription of a murine odorant receptor gene: differential initiation of transcription in the olfactory and testicular cells. Biochem Biophys Res Commun 221:240–247PubMedCrossRefGoogle Scholar
  2. Ben-Arie N, Lancet D, Taylor C, Khen M, Walker N, Ledbetter DH, Carrozzo R, Patel K, Sheer D, Lehrach H et al (1994) Olfactory receptor gene cluster on human chromosome 17: possible duplication of an ancestral receptor repertoire. Hum Mol Genet 3:229–235PubMedCrossRefGoogle Scholar
  3. Benbernou N, Tacher S, Robin S, Rakotomanga M, Senger F, Galibert F (2007) Functional analysis of a subset of canine olfactory receptor genes. J Hered 98:500–505PubMedCrossRefGoogle Scholar
  4. Benbernou N, Robin S, Tacher S, Rimbault M, Rakotomanga M, Galibert F (2011) cAMP and IP3 signaling pathways in HEK293 cells transfected with canine olfactory receptor genes. J Hered 102(Suppl 1):S47–S61PubMedCrossRefGoogle Scholar
  5. Bjarnadottir TK, Fredriksson R, Schioth HB (2005) The gene repertoire and the common evolutionary history of glutamate, pheromone (V2R), taste(1) and other related G protein-coupled receptors. Gene 362:70–84PubMedCrossRefGoogle Scholar
  6. Brand-Arpon V, Rouquier S, Massa H, de Jong PJ, Ferraz C, Ioannou PA, Demaille JG, Trask BJ, Giorgi D (1999) A genomic region encompassing a cluster of olfactory receptor genes and a myosin light chain kinase (MYLK) gene is duplicated on human chromosome regions 3q13–q21 and 3p13. Genomics 56:98–110PubMedCrossRefGoogle Scholar
  7. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187PubMedCrossRefGoogle Scholar
  8. Chen WK, Swartz JD, Rush LJ, Alvarez CE (2009) Mapping DNA structural variation in dogs. Genome Res 19:500–509PubMedCrossRefGoogle Scholar
  9. Church J, Williams H (2001) Another sniffer dog for the clinic? Lancet 358:930PubMedCrossRefGoogle Scholar
  10. Cornu JN, Cancel-Tassin G, Ondet V, Girardet C, Cussenot O (2010) Olfactory detection of prostate cancer by dogs sniffing urine: a step forward in early diagnosis. Eur Urol 59:197–201PubMedCrossRefGoogle Scholar
  11. Dennis JC, Allgier JG, Desouza LS, Eward WC, Morrison EE (2003) Immunohistochemistry of the canine vomeronasal organ. J Anat 203:329–338PubMedGoogle Scholar
  12. Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195–206PubMedCrossRefGoogle Scholar
  13. Dulac C, Torello AT (2003) Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 4:551–562PubMedCrossRefGoogle Scholar
  14. Ehlers A, Beck S, Forbes SA, Trowsdale J, Volz A, Younger R, Ziegler A (2000) MHC-linked olfactory receptor loci exhibit polymorphism and contribute to extended HLA/OR-haplotypes. Genome Res 10:1968–1978PubMedCrossRefGoogle Scholar
  15. Feldmesser E, Olender T, Khen M, Yanai I, Ophir R, Lancet D (2006) Widespread ectopic expression of olfactory receptor genes. BMC Genom 7:121CrossRefGoogle Scholar
  16. Fleischer J, Schwarzenbacher K, Breer H (2007) Expression of trace amine-associated receptors in the Grueneberg ganglion. Chem Senses 32:623–631PubMedCrossRefGoogle Scholar
  17. Freitag J, Krieger J, Strotmann J, Breer H (1995) Two classes of olfactory receptors in Xenopus laevis. Neuron 15:1383–1392PubMedCrossRefGoogle Scholar
  18. Freitag J, Ludwig G, Andreini I, Rossler P, Breer H (1998) Olfactory receptors in aquatic and terrestrial vertebrates. J Comp Physiol A 183:635–650PubMedCrossRefGoogle Scholar
  19. Fukuda N, Yomogida K, Okabe M, Touhara K (2004) Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility. J Cell Sci 117:5835–5845PubMedCrossRefGoogle Scholar
  20. Furton KG, Myers LJ (2001) The scientific foundation and efficacy of the use of canines as chemical detectors for explosives. Talanta 54:487–500PubMedCrossRefGoogle Scholar
  21. Gilad Y, Lancet D (2003) Population differences in the human functional olfactory repertoire. Mol Biol Evol 20:307–314PubMedCrossRefGoogle Scholar
  22. Gilad Y, Segre D, Skorecki K, Nachman MW, Lancet D, Sharon D (2000) Dichotomy of single-nucleotide polymorphism haplotypes in olfactory receptor genes and pseudogenes. Nat Genet 26:221–224PubMedCrossRefGoogle Scholar
  23. Gloriam DE, Bjarnadottir TK, Yan YL, Postlethwait JH, Schioth HB, Fredriksson R (2005) The repertoire of trace amine G-protein-coupled receptors: large expansion in zebrafish. Mol Phylogenet Evol 35:470–482PubMedCrossRefGoogle Scholar
  24. Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–702PubMedCrossRefGoogle Scholar
  25. Godfrey PA, Malnic B, Buck LB (2004) The mouse olfactory receptor gene family. Proc Natl Acad Sci USA 101:2156–2161PubMedCrossRefGoogle Scholar
  26. Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M (2007) Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat Neurosci 10:348–354PubMedCrossRefGoogle Scholar
  27. Grus WE, Shi P, Zhang YP, Zhang J (2005) Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. Proc Natl Acad Sci USA 102:5767–5772PubMedCrossRefGoogle Scholar
  28. Hashiguchi Y, Nishida M (2007) Evolution of trace amine associated receptor (TAAR) gene family in vertebrates: lineage-specific expansions and degradations of a second class of vertebrate chemosensory receptors expressed in the olfactory epithelium. Mol Biol Evol 24:2099–2107PubMedCrossRefGoogle Scholar
  29. Hasin Y, Olender T, Khen M, Gonzaga-Jauregui C, Kim PM, Urban AE, Snyder M, Gerstein MB, Lancet D, Korbel JO (2008) High-resolution copy-number variation map reflects human olfactory receptor diversity and evolution. PLoS Genet 4:e1000249PubMedCrossRefGoogle Scholar
  30. Herrada G, Dulac C (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763–773PubMedCrossRefGoogle Scholar
  31. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinform 8:460CrossRefGoogle Scholar
  32. Issel-Tarver L, Rine J (1996) Organization and expression of canine olfactory receptor genes. Proc Natl Acad Sci USA 93:10897–10902PubMedCrossRefGoogle Scholar
  33. Kaluza JF, Gussing F, Bohm S, Breer H, Strotmann J (2004) Olfactory receptors in the mouse septal organ. J Neurosci Res 76:442–452PubMedCrossRefGoogle Scholar
  34. Katada S, Hirokawa T, Oka Y, Suwa M, Touhara K (2005) Structural basis for a broad but selective ligand spectrum of a mouse olfactory receptor: mapping the odorant-binding site. J Neurosci 25:1806–1815PubMedCrossRefGoogle Scholar
  35. Keller A, Zhuang H, Chi Q, Vosshall LB, Matsunami H (2007) Genetic variation in a human odorant receptor alters odour perception. Nature 449:468–472PubMedCrossRefGoogle Scholar
  36. Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645–650PubMedCrossRefGoogle Scholar
  37. Liberles SD, Horowitz LF, Kuang D, Contos JJ, Wilson KL, Siltberg-Liberles J, Liberles DA, Buck LB (2009) Formyl peptide receptors are candidate chemosensory receptors in the vomeronasal organ. Proc Natl Acad Sci USA 106:9842–9847PubMedCrossRefGoogle Scholar
  38. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, Kamal M, Clamp M, Chang JL, Kulbokas EJ 3rd, Zody MC et al (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438:803–819PubMedCrossRefGoogle Scholar
  39. Lindemann L, Ebeling M, Kratochwil NA, Bunzow JR, Grandy DK, Hoener MC (2005) Trace amine-associated receptors form structurally and functionally distinct subfamilies of novel G protein-coupled receptors. Genomics 85:372–385PubMedCrossRefGoogle Scholar
  40. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723PubMedCrossRefGoogle Scholar
  41. Malnic B, Godfrey PA, Buck LB (2004) The human olfactory receptor gene family. Proc Natl Acad Sci USA 101:2584–2589PubMedCrossRefGoogle Scholar
  42. Marshall DA, Maruniak JA (1986) Masera’s organ responds to odorants. Brain Res 366:329–332PubMedCrossRefGoogle Scholar
  43. Matsunami H, Buck LB (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775–784PubMedCrossRefGoogle Scholar
  44. McCulloch M, Jezierski T, Broffman M, Hubbard A, Turner K, Janecki T (2006) Diagnostic accuracy of canine scent detection in early- and late-stage lung and breast cancers. Integr Cancer Ther 5:30–39PubMedCrossRefGoogle Scholar
  45. Menashe I, Man O, Lancet D, Gilad Y (2002) Population differences in haplotype structure within a human olfactory receptor gene cluster. Hum Mol Genet 11:1381–1390PubMedCrossRefGoogle Scholar
  46. Menashe I, Man O, Lancet D, Gilad Y (2003) Different noses for different people. Nat Genet 34:143–144PubMedCrossRefGoogle Scholar
  47. Menashe I, Abaffy T, Hasin Y, Goshen S, Yahalom V, Luetje CW, Lancet D (2007) Genetic elucidation of human hyperosmia to isovaleric acid. PLoS Biol 5:e284PubMedCrossRefGoogle Scholar
  48. Migeotte I, Communi D, Parmentier M (2006) Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev 17:501–519PubMedCrossRefGoogle Scholar
  49. Mombaerts P (2001) How smell develops. Nat Neurosci 4(Suppl):1192–1198PubMedCrossRefGoogle Scholar
  50. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675–686PubMedCrossRefGoogle Scholar
  51. Nakamura T, Gold GH (1987) A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325:442–444PubMedCrossRefGoogle Scholar
  52. Newman T, Trask BJ (2003) Complex evolution of 7E olfactory receptor genes in segmental duplications. Genome Res 13:781–793PubMedCrossRefGoogle Scholar
  53. Nicholas TJ, Cheng Z, Ventura M, Mealey K, Eichler EE, Akey JM (2009) The genomic architecture of segmental duplications and associated copy number variants in dogs. Genome Res 19:491–499PubMedCrossRefGoogle Scholar
  54. Niimura Y, Nei M (2005) Comparative evolutionary analysis of olfactory receptor gene clusters between humans and mice. Gene 346:13–21PubMedCrossRefGoogle Scholar
  55. Nozawa M, Kawahara Y, Nei M (2007) Genomic drift and copy number variation of sensory receptor genes in humans. Proc Natl Acad Sci USA 104:20421–20426PubMedCrossRefGoogle Scholar
  56. Parmentier M, Libert F, Schurmans S, Schiffmann S, Lefort A, Eggerickx D, Ledent C, Mollereau C, Gerard C, Perret J et al (1992) Expression of members of the putative olfactory receptor gene family in mammalian germ cells. Nature 355:453–455PubMedCrossRefGoogle Scholar
  57. Quignon P, Kirkness E, Cadieu E, Touleimat N, Guyon R, Renier C, Hitte C, Andre C, Fraser C, Galibert F (2003) Comparison of the canine and human olfactory receptor gene repertoires. Genome Biol 4:R80PubMedCrossRefGoogle Scholar
  58. Quignon P, Giraud M, Rimbault M, Lavigne P, Tacher S, Morin E, Retout E, Valin AS, Lindblad-Toh K, Nicolas J, Galibert F (2005) The dog and rat olfactory receptor repertoires. Genome Biol 6:R83PubMedCrossRefGoogle Scholar
  59. Quignon P, Tacher S, Rimbault M, Galibert F (2006) The dog olfactory and vomeronasal receptor repertoires. In: Ostrander EA, Giger U, Lindblad-Toh K (eds) The dog and its genome. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 221–231Google Scholar
  60. Rimbault M, Robin S, Vaysse A, Galibert F (2009) RNA profiles of rat olfactory epithelia: individual and age related variations. BMC Genom 10:572CrossRefGoogle Scholar
  61. Riviere S, Challet L, Fluegge D, Spehr M, Rodriguez I (2009) Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature 459:574–577PubMedCrossRefGoogle Scholar
  62. Robin S, Tacher S, Rimbault M, Vaysse A, Dreano S, Andre C, Hitte C, Galibert F (2009) Genetic diversity of canine olfactory receptors. BMC Genom 10:21CrossRefGoogle Scholar
  63. Rodriguez I (2005) Remarkable diversity of mammalian pheromone receptor repertoires. Proc Natl Acad Sci USA 102:6639–6640PubMedCrossRefGoogle Scholar
  64. Rodriguez I, Del Punta K, Rothman A, Ishii T, Mombaerts P (2002) Multiple new and isolated families within the mouse superfamily of V1r vomeronasal receptors. Nat Neurosci 5:134–140PubMedCrossRefGoogle Scholar
  65. Ryba NJ, Tirindelli R (1997) A new multigene family of putative pheromone receptors. Neuron 19:371–379PubMedCrossRefGoogle Scholar
  66. Sharon D, Glusman G, Pilpel Y, Horn-Saban S, Lancet D (1998) Genome dynamics, evolution, and protein modeling in the olfactory receptor gene superfamily. Ann NY Acad Sci 855:182–193PubMedCrossRefGoogle Scholar
  67. Sharon D, Glusman G, Pilpel Y, Khen M, Gruetzner F, Haaf T, Lancet D (1999) Primate evolution of an olfactory receptor cluster: diversification by gene conversion and recent emergence of pseudogenes. Genomics 61:24–36PubMedCrossRefGoogle Scholar
  68. Sharon D, Gilad Y, Glusman G, Khen M, Lancet D, Kalush F (2000) Identification and characterization of coding single-nucleotide polymorphisms within a human olfactory receptor gene cluster. Gene 260:87–94PubMedCrossRefGoogle Scholar
  69. Shi P, Zhang J (2007) Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Res 17:166–174PubMedCrossRefGoogle Scholar
  70. Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, Zimmer RK, Hatt H (2003) Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299:2054–2058PubMedCrossRefGoogle Scholar
  71. Staubert C, Boselt I, Bohnekamp J, Rompler H, Enard W, Schoneberg T (2010) Structural and functional evolution of the trace amine-associated receptors TAAR3, TAAR4 and TAAR5 in primates. PLoS One 5:e11133PubMedCrossRefGoogle Scholar
  72. Tacher S, Quignon P, Rimbault M, Dreano S, Andre C, Galibert F (2005) Olfactory receptor sequence polymorphism within and between breeds of dogs. J Hered 96:812–816PubMedCrossRefGoogle Scholar
  73. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  74. Tian H, Ma M (2004) Molecular organization of the olfactory septal organ. J Neurosci 24:8383–8390PubMedCrossRefGoogle Scholar
  75. Tortora GJ, Grabowski SR (2003) Principles of anatomy and physiology, 10th edn. Wiley, New YorkGoogle Scholar
  76. Vanderhaeghen P, Schurmans S, Vassart G, Parmentier M (1993) Olfactory receptors are displayed on dog mature sperm cells. J Cell Biol 123:1441–1452PubMedCrossRefGoogle Scholar
  77. Vanderhaeghen P, Schurmans S, Vassart G, Parmentier M (1997) Specific repertoire of olfactory receptor genes in the male germ cells of several mammalian species. Genomics 39:239–246PubMedCrossRefGoogle Scholar
  78. Walensky LD, Ruat M, Bakin RE, Blackshaw S, Ronnett GV, Snyder SH (1998) Two novel odorant receptor families expressed in spermatids undergo 5′-splicing. J Biol Chem 16:9378–9387CrossRefGoogle Scholar
  79. Williams H, Pembroke A (1989) Sniffer dogs in the melanoma clinic? Lancet 1:734PubMedCrossRefGoogle Scholar
  80. Willis CM, Church SM, Guest CM, Cook WA, McCarthy N, Bransbury AJ, Church MR, Church JC (2004) Olfactory detection of human bladder cancer by dogs: proof of principle study. BMJ 329:712PubMedCrossRefGoogle Scholar
  81. Xu F, Schaefer M, Kida I, Schafer J, Liu N, Rothman DL, Hyder F, Restrepo D, Shepherd GM (2005) Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J Comp Neurol 489:491–500PubMedCrossRefGoogle Scholar
  82. Yang H, Shi P, Zhang YP, Zhang J (2005) Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics 86:306–315PubMedCrossRefGoogle Scholar
  83. Young JM, Trask BJ (2007) V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet 23:212–215PubMedCrossRefGoogle Scholar
  84. Young JM, Friedman C, Williams EM, Ross JA, Tonnes-Priddy L, Trask BJ (2002) Different evolutionary processes shaped the mouse and human olfactory receptor gene families. Hum Mol Genet 11:535–546PubMedCrossRefGoogle Scholar
  85. Young JM, Shykind BM, Lane RP, Tonnes-Priddy L, Ross JA, Walker M, Williams EM, Trask BJ (2003) Odorant receptor expressed sequence tags demonstrate olfactory expression of over 400 genes, extensive alternate splicing and unequal expression levels. Genome Biol 4:R71PubMedCrossRefGoogle Scholar
  86. Young JM, Kambere M, Trask BJ, Lane RP (2005) Divergent V1R repertoires in five species: Amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs. Genome Res 15:231–240PubMedCrossRefGoogle Scholar
  87. Young JM, Endicott RM, Parghi SS, Walker M, Kidd JM, Trask BJ (2008) Extensive copy-number variation of the human olfactory receptor gene family. Am J Hum Genet 83:228–242PubMedCrossRefGoogle Scholar
  88. Young JM, Massa HF, Hsu L, Trask BJ (2010) Extreme variability among mammalian V1R gene families. Genome Res 20:10–18PubMedCrossRefGoogle Scholar
  89. Zhang X, Firestein S (2002) The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5:124–133PubMedGoogle Scholar
  90. Zhang X, Rodriguez I, Mombaerts P, Firestein S (2004a) Odorant and vomeronasal receptor genes in two mouse genome assemblies. Genomics 83:802–811PubMedCrossRefGoogle Scholar
  91. Zhang X, Rogers M, Tian H, Zhang X, Zou DJ, Liu J, Ma M, Shepherd GM, Firestein SJ (2004b) High-throughput microarray detection of olfactory receptor gene expression in the mouse. Proc Natl Acad Sci USA 101:14168–14173PubMedCrossRefGoogle Scholar
  92. Zhang X, Zhang X, Firestein S (2007) Comparative genomics of odorant and pheromone receptor genes in rodents. Genomics 89:441–450PubMedCrossRefGoogle Scholar
  93. Zucchi R, Chiellini G, Scanlan TS, Grandy DK (2006) Trace amine-associated receptors and their ligands. Br J Pharmacol 149:967–978PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Pascale Quignon
    • 1
    Email author
  • Maud Rimbault
    • 2
  • Stéphanie Robin
    • 1
  • Francis Galibert
    • 1
  1. 1.Institut de Génétique et Développement de RennesUMR6061 CNRS Université de Rennes 1, Faculté de MédecineRennes CedexFrance
  2. 2.NHGRI, NIH, Cancer Genetics BranchBethesdaUSA

Personalised recommendations