Skip to main content

Pheromone reception in mammals

Part of the Reviews of Physiology, Biochemistry and Pharmacology book series (REVIEWS,volume 154)

Abstract

Pheromonal communication is the most convenient way to transfer information regarding gender and social status in animals of the same species with the holistic goal of sustaining reproduction. This type of information exchange is based on pheromones, molecules often chemically unrelated, that are contained in body fluids like urine, sweat, specialized exocrine glands, and mucous secretions of genitals. So profound is the relevance of pheromones over the evolutionary process that a specific peripheral organ devoted to their recognition, namely the vomeronasal organ of Jacobson, and a related central pathway arose in most vertebrate species. Although the vomeronasal system is well developed in reptiles and amphibians, most mammals strongly rely on pheromonal communication. Humans use pheromones too; evidence on the existence of a specialized organ for their detection, however, is very elusive indeed. In the present review, we will focus our attention on the behavioral, physiological, and molecular aspects of pheromone detection in mammals. We will discuss the responses to pheromonal stimulation in different animal species, emphasizing the complicacy of this type of communication. In the light of the most recent results, we will also discuss the complex organization of the transduction molecules that underlie pheromone detection and signal transmission from vomeronasal neurons to the higher centers of the brain. Communication is a primary feature of living organisms, allowing the coordination of different behavioral paradigms among individuals. Communication has evolved through a variety of different strategies, and each species refined its own preferred communication medium. From a phylogenetic point of view, the most widespread and ancient way of communication is through chemical signals named pheromones: it occurs in all taxa, from prokaryotes to eukaryotes. The release of specific pheromones into the environment is a sensitive and definite way to send messages to other members of the same species. Therefore, the action of an organism can alter the behavior of another organism, thereby increasing the fitness of either or both. Albeit slow in transmission and not easily modulated, pheromones can travel around objects in the dark and over long distances. In addition, they are emitted when necessary and their biosynthesis is usually economic. In essence, they represent the most efficient tool to refine the pattern of social behaviors and reproductive strategies.

Keywords

  • Mitral Cell
  • Olfactory Neuron
  • TRPC2 Channel
  • Main Olfactory Bulb
  • Accessory Olfactory Bulb

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.

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
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

  • Abel EL (1991) Alarm substance emitted by rats in the forced-swim test is a low volatile pheromone. Physiol Behav 50:723–727

    PubMed  CAS  Google Scholar 

  • Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS (2000) A novel family of mammalian taste receptors. Cell 100:693–702

    PubMed  CAS  Google Scholar 

  • Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, Szabo G, Shipley MT (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426:623–629

    PubMed  CAS  Google Scholar 

  • Bacchini A, Gaetani E, Cavaggioni A (1992) Pheromone binding proteins of the mouse, Mus musculus. Experientia 48:419–421

    PubMed  CAS  Google Scholar 

  • Belluscio L, Koentges G, Axel R, Dulac C (1999) A map of pheromone receptor activation in the mammalian brain. Cell 97:209–220

    PubMed  CAS  Google Scholar 

  • Benton D (1982) The influence of androstenol—a putative human pheromone—on mood throughout the menstrual cycle. Biol Psychol 15:249–256

    PubMed  CAS  Google Scholar 

  • Berghard A, Buck LB (1996) Sensory transduction in vomeronasal neurons: evidence for G alpha o, G alpha i2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J Neurosci 16:909–918

    PubMed  CAS  Google Scholar 

  • Berghard A, Buck LB, Liman ER (1996) Evidence for distinct signaling mechanisms in two mammalian olfactory sense organs. Proc Natl Acad Sci U S A 93:2365–2369

    PubMed  CAS  Google Scholar 

  • Bertmar G (1981) Evolution of vomeronasal organs in vertebrates. Evolution 35:359–366

    Google Scholar 

  • Bhatnagar KP, Smith TD (2003) The human vomeronasal organ. V. An interpretation of its discovery by Ruysch, Jacobson, or Kolliker, with an English translation of Kolliker (1877). Anat Rec 270B:4–15

    Google Scholar 

  • Bocskei Z, Groom CR, Flower DR, Wright CE, Phillips SE, Cavaggioni A, Findlay JB, North AC (1992) Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography. Nature 360:186–188

    PubMed  CAS  Google Scholar 

  • Booth KK, Katz LS (2000) Role of the vomeronasal organ in neonatal offspring recognition in sheep. Biol Reprod 63:953–958

    PubMed  CAS  Google Scholar 

  • Boschat C, Pelofi C, Randin O, Roppolo D, Luscher C, Broillet MC, Rodriguez I (2002) Pheromone detection mediated by a V1r vomeronasal receptor. Nat Neurosci 5:1261–1262

    PubMed  CAS  Google Scholar 

  • Brann JH, Dennis JC, Morrison EE, Fadool DA (2002) Type-specific inositol 1,4,5-trisphosphate receptor localization in the vomeronasal organ and its interaction with a transient receptor potential channel, TRPC2. J Neurochem 83:1452–1460

    PubMed  CAS  Google Scholar 

  • Brennan PA, Schellinck HM, Keverne EB (1999) Patterns of expression of the immediate-early gene egr-1 in the accessory olfactory bulb of female mice exposed to pheromonal constituents of male urine. Neuroscience 90:1463–1470

    PubMed  CAS  Google Scholar 

  • Brouette-Lahlou I, Godinot F, Vernet-Maury E (1999) The mother rat’s vomeronasal organ is involved in detection of dodecyl propionate, the pup’s preputial gland pheromone. Physiol Behav 66:427–436

    PubMed  CAS  Google Scholar 

  • Brown EM, Gamba G, Riccardi D, Lombardi M, Butters R, Kifor O, Sun A, Hediger MA, Lytton J, Hebert SC (1993) Cloning and characterization of an extracellular Ca(2+)-sensing receptor from bovine parathyroid. Nature 366:575–580

    PubMed  CAS  Google Scholar 

  • Brown W, Eisner T, Whittaker R (1970) Allomones and kairomones: transspecific chemical messengers. BioScience 20:21–22

    CAS  Google Scholar 

  • Bruce HM (1960) A block to pregnancy in the mouse caused by proximity of strange males. J Reprod Fertil 1:96–103

    PubMed  CAS  Google Scholar 

  • Buck L, 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 

  • Buck LB (1996) Information coding in the vertebrate olfactory system. Annu Rev Neurosci 19:517–544

    PubMed  CAS  Google Scholar 

  • Cao Y, Oh BC, Stryer L (1998) Cloning and localization of two multigene receptor families in goldfish olfactory epithelium. Proc Natl Acad Sci U S A 95:11987–11992

    PubMed  CAS  Google Scholar 

  • Cavaggioni A, Mucignat-Caretta C (2000) Major urinary proteins, alpha(2U)-globulins and aphrodisin. Biochim Biophys Acta 1482:218–228

    PubMed  CAS  Google Scholar 

  • Cavaggioni A, Findlay JB, Tirindelli R (1990) Ligand binding characteristics of homologous rat and mouse urinary proteins and pyrazine-binding protein of calf. Comp Biochem Physiol B 96:513–520

    PubMed  CAS  Google Scholar 

  • Cavaggioni A, Mucignat C, Tirindelli R (1999) Pheromone signalling in the mouse: role of urinary proteins and vomeronasal organ. Arch Ital Biol 137:193–200

    PubMed  CAS  Google Scholar 

  • Cavaggioni A, Mucignat-Caretta C, Zagotto G (2003) Absolute configuration of 2-sec-butyl-4,5-dihydrothiazole in male mouse urine. Chem Senses 28:791–797

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Clark AJ, Ghazal P, Bingham RW, Barrett D, Bishop JO (1985) Sequence structures of a mouse major urinary protein gene and pseudogene compared. Embo J 4:3159–3165

    PubMed  CAS  Google Scholar 

  • Comfort A (1971) Likelihood of human pheromones. Nature 230:432–3 passim

    PubMed  CAS  Google Scholar 

  • Conigrave AD, Quinn SJ, Brown EM (2000) L-amino acid sensing by the extracellular Ca2+-sensing receptor. Proc Natl Acad Sci U S A 97:4814–4819

    PubMed  CAS  Google Scholar 

  • Cowan CM, Roskams AJ (2002) Apoptosis in the mature and developing olfactory neuroepithelium. Microsc Res Tech 58:204–215

    PubMed  CAS  Google Scholar 

  • Darwish Marie A, Veggerby C, Robertson DH, Gaskell SJ, Hubbard SJ, Martinsen L, Hurst JL, Beynon RJ (2001) Effect of polymorphisms on ligand binding by mouse major urinary proteins. Protein Sci 10:411–417

    Google Scholar 

  • Dean DM, Mazzatenta A, Menini A (2004) Voltage-activated current properties of male and female mouse vomeronasal sensory neurons: sexually dichotomous? J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:491–499

    PubMed  CAS  Google Scholar 

  • Del Punta K, Rothman A, Rodriguez I, Mombaerts P (2000) Sequence diversity and genomic organization of vomeronasal receptor genes in the mouse. Genome Res 10:1958–1967

    Google Scholar 

  • Del Punta K, Leinders-Zufall T, Rodriguez I, Jukam D, Wysocki CJ, Ogawa S, Zufall F, Mombaerts P (2002a) Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419:70–74

    Google Scholar 

  • Del Punta K, Puche A, Adams NC, Rodriguez I, Mombaerts P (2002b) A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron 35:1057–1066

    Google Scholar 

  • Destexhe A, Neubig M, Ulrich D, Huguenard J (1998) Dendritic low-threshold calcium currents in thalamic relay cells. J Neurosci 18:3574–3588

    PubMed  CAS  Google Scholar 

  • Dolphin AC (2003) G protein modulation of voltage-gated calcium channels. Pharmacol Rev 55:607–627

    PubMed  CAS  Google Scholar 

  • Dorries KM, Adkins-Regan E, Halpern BP (1997) Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs. Brain Behav Evol 49:53–62

    PubMed  CAS  Google Scholar 

  • Doty RL, Dunbar I (1974) Attraction of beagles to conspecific urine, vaginal and anal sac secretion odors. Physiol Behav 12:825–833

    PubMed  CAS  Google Scholar 

  • Doving KB, Trotier D (1998) Structure and function of the vomeronasal organ. J Exp Biol 201:2913–2925

    PubMed  CAS  Google Scholar 

  • Duchamp-Viret P, Chaput MA, Duchamp A (1999) Odor response properties of rat olfactory receptor neurons. Science 284:2171–2174

    PubMed  CAS  Google Scholar 

  • Dudley CA, Moss RL (1999) Activation of an anatomically distinct subpopulation of accessory olfactory bulb neurons by chemosensory stimulation. Neuroscience 91:1549–1556

    PubMed  CAS  Google Scholar 

  • Dulac C (2000) Sensory coding of pheromone signals in mammals. Curr Opin Neurobiol 10:511–518

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Emes RD, Beatson SA, Ponting CP, Goodstadt L (2004) Evolution and comparative genomics of odorant- and pheromone-associated genes in rodents. Genome Res 14:591–602

    PubMed  CAS  Google Scholar 

  • Fadem BH (1987) Activation of estrus by pheromones in a marsupial: stimulus control and endocrine factors. Biol Reprod 36:328–332

    PubMed  CAS  Google Scholar 

  • Fadool DA, Wachowiak M, Brann JH (2001) Patch-clamp analysis of voltage-activated and chemically activated currents in the vomeronasal organ of Sternotherus odoratus (stinkpot/musk turtle). J Exp Biol 204:4199–4212

    PubMed  CAS  Google Scholar 

  • Feinstein P, Mombaerts P (2004) A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117:817–831

    PubMed  CAS  Google Scholar 

  • 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 117:833–846

    PubMed  CAS  Google Scholar 

  • Fernandez-Fewell GD, Meredith M (1994) c-fos expression in vomeronasal pathways of mated or pheromone-stimulated male golden hamsters: contributions from vomeronasal sensory input and expression related to mating performance. J Neurosci 14:3643–3654

    PubMed  CAS  Google Scholar 

  • Fieni F, Ghiaroni V, Tirindelli R, Pietra P, Bigiani A (2003) Apical and basal neurones isolated from the mouse vomeronasal organ differ for voltage-dependent currents. J Physiol 552:425–436

    PubMed  CAS  Google Scholar 

  • Firestein S (2001) How the olfactory system makes sense of scents. Nature 413:211–218

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ghiaroni V, Fieni F, Tirindelli R, Pietra P, Bigiani A (2003) Ion conductances in supporting cells isolated from the mouse vomeronasal organ. J Neurophysiol 89:118–127

    PubMed  CAS  Google Scholar 

  • Giorgi D, Friedman C, Trask BJ, Rouquier S (2000) Characterization of nonfunctional V1R-like pheromone receptor sequences in human. Genome Res 10:1979–1985

    PubMed  CAS  Google Scholar 

  • Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–702

    PubMed  CAS  Google Scholar 

  • Goodwin M, Gooding KM, Regnier F (1979) Sex pheromone in the dog. Science 203:559–561

    PubMed  CAS  Google Scholar 

  • Guillamon A, Segovia S (1997) Sex differences in the vomeronasal system. Brain Res Bull 44:377–382

    PubMed  CAS  Google Scholar 

  • Gulyas B, Keri S, O’Sullivan BT, Decety J, Roland PE (2004) The putative pheromone androstadienone activates cortical fields in the human brain related to social cognition. Neurochem Int 44:595–600

    PubMed  CAS  Google Scholar 

  • Halem HA, Cherry JA, Baum MJ (1999) Vomeronasal neuroepithelium and forebrain Fos responses to male pheromones in male and female mice. J Neurobiol 39:249–263

    PubMed  CAS  Google Scholar 

  • Halpern M (1987) The organization and function of the vomeronasal system. Annu Rev Neurosci 10:325–362

    PubMed  CAS  Google Scholar 

  • Halpern M, Martinez-Marcos A (2003) Structure and function of the vomeronasal system: an update. Prog Neurobiol 70:245–318

    PubMed  CAS  Google Scholar 

  • Halpern M, Jia C, Shapiro LS (1998) Segregated pathways in the vomeronasal system. Microsc Res Tech 41:519–529

    PubMed  CAS  Google Scholar 

  • Hegde AN (2003) MHC molecules in the vomeronasal organ: contributors to pheromonal discrimination? Trends Neurosci 26:646–650

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hildebrand JG (1995) Analysis of chemical signals by nervous systems. Proc Natl Acad Sci U S A 92:67–74

    PubMed  CAS  Google Scholar 

  • Holy TE, Dulac C, Meister M (2000) Responses of vomeronasal neurons to natural stimuli. Science 289:1569–1572

    PubMed  CAS  Google Scholar 

  • Hoon MA, Adler E, Lindemeier J, Battey JF, Ryba NJ, Zuker CS (1999) Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96:541–551

    PubMed  CAS  Google Scholar 

  • Hudson R, Distel H (1986) Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol Behav 37:123–128

    PubMed  CAS  Google Scholar 

  • Hurley JH (1999) Structure, mechanism, and regulation of mammalian adenylyl cyclase. J Biol Chem 274:7599–7602

    PubMed  CAS  Google Scholar 

  • Hurst JL, Payne CE, Nevison CM, Marie AD, Humphries RE, Robertson DH, Cavaggioni A, Beynon RJ (2001) Individual recognition in mice mediated by major urinary proteins. Nature 414:631–634

    PubMed  CAS  Google Scholar 

  • Inamura K, Kashiwayanagi M, Kurihara K (1997a) Blockage of urinary responses by inhibitors for IP3-mediated pathway in rat vomeronasal sensory neurons. Neurosci Lett 233:129–132

    PubMed  CAS  Google Scholar 

  • Inamura K, Kashiwayanagi M, Kurihara K (1997b) Inositol-1,4,5-trisphosphate induces responses in receptor neurons in rat vomeronasal sensory slices. Chem Senses 22:93–103

    PubMed  CAS  Google Scholar 

  • Inamura K, Matsumoto Y, Kashiwayanagi M, Kurihara K (1999) Laminar distribution of pheromone-receptive neurons in rat vomeronasal epithelium. J Physiol 517:731–739

    PubMed  CAS  Google Scholar 

  • Ishii T, Hirota J, Mombaerts P (2003) Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Curr Biol 13:394–400

    PubMed  CAS  Google Scholar 

  • Isles AR, Baum MJ, Ma D, Keverne EB, Allen ND (2001) Urinary odour preferences in mice. Nature 409:783–784

    PubMed  CAS  Google Scholar 

  • Jacobson L, Trotier D, Doving KB (1998) Anatomical description of a new organ in the nose of domesticated animals by Ludvig Jacobson (1813). Chem Senses 23:743–754

    PubMed  CAS  Google Scholar 

  • Jahnke V, Merker HJ (2000) Electron microscopic and functional aspects of the human vomeronasal organ. Am J Rhinol 14:63–67

    PubMed  CAS  Google Scholar 

  • Jia C, Halpern M (1996) Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G(o alpha)) and segregated projections to the accessory olfactory bulb. Brain Res 719:117–128

    PubMed  CAS  Google Scholar 

  • Jingami H, Nakanishi S, Morikawa K (2003) Structure of the metabotropic glutamate receptor. Curr Opin Neurobiol 13:271–278

    PubMed  CAS  Google Scholar 

  • Johns MA, Feder HH, Komisaruk BR, Mayer AD (1978) Urine-induced reflex ovulation in anovulatory rats may be a vomeronasal effect. Nature 272:446–448

    PubMed  CAS  Google Scholar 

  • Johnston RE (1998) Pheromones, the vomeronasal system, and communication. From hormonal responses to individual recognition. Ann N Y Acad Sci 855:333–348

    PubMed  CAS  Google Scholar 

  • Johnston RE, Peng M (2000) The vomeronasal organ is involved in discrimination of individual odors by males but not by females in golden hamsters. Physiol Behav 70:537–549

    PubMed  CAS  Google Scholar 

  • Jones DT, Reed RR (1989) Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244:790–795

    PubMed  CAS  Google Scholar 

  • Karlson P, Lüscher M (1959) “Pheromones”: a new term for a class of biologically active substances. Nature 183:55–56

    PubMed  CAS  Google Scholar 

  • Kaupmann K, Huggel K, Heid J, Flor PJ, Bischoff S, Mickel SJ, McMaster G, Angst C, Bittiger H, Froestl W, Bettler B (1997) Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors. Nature 386:239–246

    PubMed  CAS  Google Scholar 

  • Keverne EB (1999) The vomeronasal organ. Science 286:716–720

    PubMed  CAS  Google Scholar 

  • Keverne EB (2002) Pheromones, vomeronasal function, and gender-specific behavior. Cell 108:735–738

    PubMed  CAS  Google Scholar 

  • Krautwurst D, Yau KW, Reed RR (1998) Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95:917–926

    PubMed  CAS  Google Scholar 

  • Krieger J, Schmitt A, Lobel D, Gudermann T, Schultz G, Breer H, Boekhoff I (1999) Selective activation of G protein subtypes in the vomeronasal organ upon stimulation with urine-derived compounds. J Biol Chem 274:4655–4662

    PubMed  CAS  Google Scholar 

  • Kroner C, Breer H, Singer AG, O’Connell RJ (1996) Pheromone-induced second messenger signaling in the hamster vomeronasal organ. Neuroreport 7:2989–2992

    PubMed  CAS  Google Scholar 

  • Kuang D, Yao Y, Wang M, Pattabiraman N, Kotra LP, Hampson DR (2003) Molecular similarities in the ligand binding pockets of an odorant receptor and the metabotropic glutamate receptors. J Biol Chem 278:42551–42559

    PubMed  CAS  Google Scholar 

  • Kunishima N, Shimada Y, Tsuji Y, Sato T, Yamamoto M, Kumasaka T, Nakanishi S, Jingami H, Morikawa K (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407:971–977

    PubMed  CAS  Google Scholar 

  • Lane RP, Cutforth T, Axel R, Hood L, Trask BJ (2002) Sequence analysis of mouse vomeronasal receptor gene clusters reveals common promoter motifs and a history of recent expansion. Proc Natl Acad Sci U S A 99:291–296

    PubMed  CAS  Google Scholar 

  • Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792–796

    PubMed  CAS  Google Scholar 

  • Leon M, Moltz H (1973) Endocrine control of the maternal pheromone in the postpartum female rat. Physiol Behav 10:65–67

    PubMed  CAS  Google Scholar 

  • Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R (2002) Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci U S A 99:6376–6381

    PubMed  CAS  Google Scholar 

  • Liman ER (2003) Regulation by voltage and adenine nucleotides of a Ca2+-activated cation channel from hamster vomeronasal sensory neurons. J Physiol 548:777–787

    PubMed  CAS  Google Scholar 

  • Liman ER, Corey DP (1996) Electrophysiological characterization of chemosensory neurons from the mouse vomeronasal organ. J Neurosci 16:4625–4637

    PubMed  CAS  Google Scholar 

  • Liman ER, Innan H (2003) Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci U S A 100:3328–3332

    PubMed  CAS  Google Scholar 

  • Liman ER, Corey DP, Dulac C (1999) TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc Natl Acad Sci U S A 96:5791–5796

    PubMed  CAS  Google Scholar 

  • Loconto J, Papes F, Chang E, Stowers L, Jones EP, Takada T, Kumanovics A, Fischer Lindahl K, Dulac C (2003) Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112:607–618

    PubMed  CAS  Google Scholar 

  • Lucas P, Ukhanov K, Leinders-Zufall T, Zufall F (2003) A diacylglycerol-gated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: mechanism of pheromone transduction. Neuron 40:551–561

    PubMed  CAS  Google Scholar 

  • Luo M, Katz LC (2004) Encoding pheromonal signals in the mammalian vomeronasal system. Curr Opin Neurobiol 14:428–434

    PubMed  CAS  Google Scholar 

  • Luo M, Fee MS, Katz LC (2003) Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299:1196–1201

    PubMed  CAS  Google Scholar 

  • Lynch JW, Barry PH (1989) Action potentials initiated by single channels opening in a small neuron (rat olfactory receptor). Biophys J 55:755–768

    PubMed  CAS  Google Scholar 

  • Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268:301–304

    PubMed  CAS  Google Scholar 

  • Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723

    PubMed  CAS  Google Scholar 

  • Markram H, Sakmann B (1994) Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. Proc Natl Acad Sci U S A 91:5207–5211

    PubMed  CAS  Google Scholar 

  • Martini S, Silvotti L, Shirazi A, Ryba NJ, Tirindelli R (2001) Co-expression of putative pheromone receptors in the sensory neurons of the vomeronasal organ. J Neurosci 21:843–848

    PubMed  CAS  Google Scholar 

  • Masera T (1943) Su l’esistenza di un particolare organo olfattivo nel setto nasale della cavia e di altri roditori. Arch Ital Anat Embriol 48:157–212

    Google Scholar 

  • Matsunami H, Buck LB (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775–784

    PubMed  CAS  Google Scholar 

  • Matsunami H, Montmayeur JP, Buck LB (2000) A family of candidate taste receptors in human and mouse. Nature 404:601–604

    PubMed  CAS  Google Scholar 

  • Maue RA, Dionne VE (1987) Patch-clamp studies of isolated mouse olfactory receptor neurons. J Gen Physiol 90:95–125

    PubMed  CAS  Google Scholar 

  • Max M, Shanker YG, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF (2001) Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet 28:58–63

    PubMed  CAS  Google Scholar 

  • McClintock MK (1984) Estrous synchrony: modulation of ovarian cycle length by female pheromones. Physiol Behav 32:701–705

    PubMed  CAS  Google Scholar 

  • McGlone JJ (1985) Olfactory cues and pig agonistic behavior: evidence for a submissive pheromone. Physiol Behav 34:195–198

    PubMed  CAS  Google Scholar 

  • Menco BP, Carr VM, Ezeh PI, Liman ER, Yankova MP (2001) Ultrastructural localization of G-proteins and the channel protein TRP2 to microvilli of rat vomeronasal receptor cells. J Comp Neurol 438:468–489

    PubMed  CAS  Google Scholar 

  • Meredith M (1998) Vomeronasal function. Chem Senses 23:463–466

    PubMed  CAS  Google Scholar 

  • Meredith M, Westberry JM (2004) Distinctive responses in the medial amygdala to same-species and different-species pheromones. J Neurosci 24:5719–5725

    PubMed  CAS  Google Scholar 

  • Michael RP, Keverne EB (1970) A male sex-attractant pheromone in rhesus monkey vaginal secretions. J Endocrinol 46:xx–xxi

    PubMed  CAS  Google Scholar 

  • Minke B, Cook B (2002) TRP channel proteins and signal transduction. Physiol Rev 82:429–472

    PubMed  CAS  Google Scholar 

  • Miyawaki A, Matsushita F, Ryo Y, Mikoshiba K (1994) Possible pheromone-carrier function of two lipocalin proteins in the vomeronasal organ. Embo J 13:5835–5842

    PubMed  CAS  Google Scholar 

  • Moltz H, Lee TM (1981) The maternal pheromone of the rat: identity and functional significance. Physiol Behav 26:301–306

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675–686

    PubMed  CAS  Google Scholar 

  • Monti-Bloch L, Jennings-White C, Berliner DL (1998) The human vomeronasal system. A review. Ann N Y Acad Sci 855:373–389

    PubMed  CAS  Google Scholar 

  • Montmayeur JP, Liberles SD, Matsunami H, Buck LB (2001) A candidate taste receptor gene near a sweet taste locus. Nat Neurosci 4:492–498

    PubMed  CAS  Google Scholar 

  • Mori K, Nagao H, Yoshihara Y (1999) The olfactory bulb: coding and processing of odor molecule information. Science 286:711–715

    PubMed  CAS  Google Scholar 

  • Mucignat-Caretta C (2002) Modulation of exploratory behavior in female mice by protein-borne male urinary molecules. J Chem Ecol 28:1853–1863

    PubMed  CAS  Google Scholar 

  • Mucignat-Caretta C, Caretta A (1999a) Chemical signals in male house mice urine: protein-bound molecules modulate interaction between sexes. Behaviour 136:331–343

    Google Scholar 

  • Mucignat-Caretta C, Caretta A (1999b) Urinary chemical cues affect light avoidance behaviour in male laboratory mice, Mus musculus. Anim Behav 57:765–769

    PubMed  Google Scholar 

  • Mucignat-Caretta C, Caretta A, Cavaggioni A (1995) Acceleration of puberty onset in female mice by male urinary proteins. J Physiol 486:517–522

    PubMed  CAS  Google Scholar 

  • Mucignat-Caretta C, Caretta A, Baldini E (1998) Protein-bound male urinary pheromones: differential responses according to age and gender. Chem Senses 23:67–70

    PubMed  CAS  Google Scholar 

  • Mucignat-Caretta C, Cavaggioni A, Caretta A (2004) Male urinary chemosignals differentially affect aggressive behavior in male mice. J Chem Ecol 30:777–791

    PubMed  CAS  Google Scholar 

  • Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS (2001) Mammalian sweet taste receptors. Cell 106:381–390

    PubMed  CAS  Google Scholar 

  • Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS (2002) An amino-acid taste receptor. Nature 416:199–202

    PubMed  CAS  Google Scholar 

  • Niimura Y, Nei M (2003) Evolution of olfactory receptor genes in the human genome. Proc Natl Acad Sci U S A 100:12235–12240

    PubMed  CAS  Google Scholar 

  • Novotny M, Harvey S, Jemiolo B, Alberts J (1985) Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci U S A 82:2059–2061

    PubMed  CAS  Google Scholar 

  • Novotny M, Jemiolo B, Harvey S, Wiesler D, Marchlewska-Koj A (1986) Adrenal-mediated endogenous metabolites inhibit puberty in female mice. Science 231:722–725

    PubMed  CAS  Google Scholar 

  • Novotny M, Harvey S, Jemiolo B (1990) Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 46:109–113

    PubMed  CAS  Google Scholar 

  • Novotny MV, Jemiolo B, Wiesler D, Ma W, Harvey S, Xu F, Xie TM, Carmack M (1999) A unique urinary constituent, 6-hydroxy-6-methyl-3-heptanone, is a pheromone that accelerates puberty in female mice. Chem Biol 6:377–383

    PubMed  CAS  Google Scholar 

  • Okamoto T, Sekiyama N, Otsu M, Shimada Y, Sato A, Nakanishi S, Jingami H (1998) Expression and purification of the extracellular ligand binding region of metabotropic glutamate receptor subtype 1. J Biol Chem 273:13089–13096

    PubMed  CAS  Google Scholar 

  • Okere CO, Kaba H (2000) Increased expression of neuronal nitric oxide synthase mRNA in the accessory olfactory bulb during the formation of olfactory recognition memory in mice. Eur J Neurosci 12:4552–4556

    PubMed  CAS  Google Scholar 

  • Pantages E, Dulac C (2000) A novel family of candidate pheromone receptors in mammals. Neuron 28:835–845

    PubMed  CAS  Google Scholar 

  • Pearse-Pratt R, Schellinck H, Brown R, Singh PB, Roser B (1998) Soluble MHC antigens and olfactory recognition of genetic individuality: the mechanism. Genetica 104:223–230

    PubMed  CAS  Google Scholar 

  • Peleg S, Varon D, Ivanina T, Dessauer CW, Dascal N (2002) G(alpha)(i) controls the gating of the G protein-activated K(+) channel, GIRK. Neuron 33:87–99

    PubMed  CAS  Google Scholar 

  • Perez-Reyes E (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83:117–161

    PubMed  CAS  Google Scholar 

  • Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1–26

    PubMed  CAS  Google Scholar 

  • Poran NS, Vandoros A, Halpern M (1993) Nuzzling in the gray short-tailed opossum. I: Delivery of odors to vomeronasal organ. Physiol Behav 53:959–967

    PubMed  CAS  Google Scholar 

  • Pouille F, Cavelier P, Desplantez T, Beekenkamp H, Craig PJ, Beattie RE, Volsen SG, Bossu JL (2000) Dendro-somatic distribution of calcium-mediated electrogenesis in purkinje cells from rat cerebellar slice cultures. J Physiol 527:265–282

    PubMed  CAS  Google Scholar 

  • Preti G, Wysocki CJ, Barnhart KT, Sondheimer SJ, Leyden JJ (2003) Male axillary extracts contain pheromones that affect pulsatile secretion of luteinizing hormone and mood in women recipients. Biol Reprod 68:2107–2113

    PubMed  CAS  Google Scholar 

  • Rasband MN, Shrager P (2000) Ion channel sequestration in central nervous system axons. J Physiol 525:63–73

    PubMed  CAS  Google Scholar 

  • Ressler KJ, Sullivan SL, Buck LB (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 

  • Richards DB, Stevens DA (1974) Evidence for marking with urine by rats. Behav Biol 12:517–523

    PubMed  CAS  Google Scholar 

  • Rodriguez I (2004) Pheromone receptors in mammals. Horm Behav 46:219–230

    PubMed  CAS  Google Scholar 

  • Rodriguez I, Mombaerts P (2002) Novel human vomeronasal receptor-like genes reveal species-specific families. Curr Biol 12:R409–R411

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rodriguez I, Greer CA, Mok MY, Mombaerts P (2000) A putative pheromone receptor gene expressed in human olfactory mucosa. Nat Genet 26:18–19

    PubMed  CAS  Google Scholar 

  • 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 5:134–140

    PubMed  CAS  Google Scholar 

  • Rossler P, Kroner C, Krieger J, Lobel D, Breer H, Boekhoff I (2000) Cyclic adenosine monophosphate signaling in the rat vomeronasal organ: role of an adenylyl cyclase type VI. Chem Senses 25:313–322

    PubMed  CAS  Google Scholar 

  • Runnenburger K, Breer H, Boekhoff I (2002) Selective G protein beta gamma-subunit compositions mediate phospholipase C activation in the vomeronasal organ. Eur J Cell Biol 81:539–547

    PubMed  Google Scholar 

  • Ryba NJ, Tirindelli R (1997) A new multigene family of putative pheromone receptors. Neuron 19:371–379

    PubMed  CAS  Google Scholar 

  • Saito TR, Moltz H (1986) Copulatory behavior of sexually naive and sexually experienced male rats following removal of the vomeronasal organ. Physiol Behav 37:507–510

    PubMed  CAS  Google Scholar 

  • Sasaki K, Okamoto K, Inamura K, Tokumitsu Y, Kashiwayanagi M (1999) Inositol-1,4,5-trisphosphate accumulation induced by urinary pheromones in female rat vomeronasal epithelium. Brain Res 823:161–168

    PubMed  CAS  Google Scholar 

  • Sato T, Shimada Y, Nagasawa N, Nakanishi S, Jingami H (2003) Amino acid mutagenesis of the ligand binding site and the dimer interface of the metabotropic glutamate receptor 1. Identification of crucial residues for setting the activated state. J Biol Chem 278:4314–4321

    PubMed  CAS  Google Scholar 

  • Savic I, Berglund H, Gulyas B, Roland P (2001) Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron 31:661–668

    PubMed  CAS  Google Scholar 

  • Schild D, Restrepo D (1998) Transduction mechanisms in vertebrate olfactory receptor cells. Physiol Rev 78:429–466

    PubMed  CAS  Google Scholar 

  • Schwende FJ, Wiesler D, Jorgenson JW, Carmack M, Novotny M (1986) Urinary volatile constituents of the house mouse, Mus musculus, and their endocrine dependency. J Chem Ecol 12:277–296

    CAS  Google Scholar 

  • Serizawa S, Ishii T, Nakatani H, Tsuboi A, Nagawa F, Asano M, Sudo K, Sakagami J, Sakano H, Ijiri T, Matsuda Y, Suzuki M, Yamamori T, Iwakura Y (2000) Mutually exclusive expression of odorant receptor transgenes. Nat Neurosci 3:687–693

    PubMed  CAS  Google Scholar 

  • 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 302:2088–2094

    PubMed  CAS  Google Scholar 

  • Shahan K, Gilmartin M, Derman E (1987) Nucleotide sequences of liver, lachrymal, and submaxillary gland mouse major urinary protein mRNAs: mosaic structure and construction of panels of gene-specific synthetic oligonucleotide probes. Mol Cell Biol 7:1938–1946

    PubMed  CAS  Google Scholar 

  • Shapiro LS, Roland RM, Li CS, Halpern M (1996) Vomeronasal system involvement in response to conspecific odors in adult male opossums, Monodelphis domestica. Behav Brain Res 77:101–113

    PubMed  CAS  Google Scholar 

  • Silvotti L, Giannini G, Tirindelli R (2005) The vomeronasal receptor V2R2 does not require escort molecules for heterologous expression. Chem Senses (in press)

    Google Scholar 

  • Simerly RB (1990) Hormonal control of neuropeptide gene expression in sexually dimorphic olfactory pathways. Trends Neurosci 13:104–110

    PubMed  CAS  Google Scholar 

  • Singer AG, Agosta WC, Clancy AN, Macrides F (1987) The chemistry of vomeronasally detected pheromones: characterization of an aphrodisiac protein. Ann N Y Acad Sci 519:287–298

    PubMed  CAS  Google Scholar 

  • Singer AG, Beauchamp GK, Yamazaki K (1997) Volatile signals of the major histocompatibility complex in male mouse urine. Proc Natl Acad Sci U S A 94:2210–2214

    PubMed  CAS  Google Scholar 

  • Speca DJ, Lin DM, Sorensen PW, Isacoff EY, Ngai J, Dittman AH (1999) Functional identification of a goldfish odorant receptor. Neuron 23:487–498

    PubMed  CAS  Google Scholar 

  • Spehr M, Hatt H, Wetzel CH (2002) Arachidonic acid plays a role in rat vomeronasal signal transduction. J Neurosci 22:8429–8437

    PubMed  CAS  Google Scholar 

  • Stephan H, Baron G, Frahm HD (1982) Comparison of brain structure volumes in insectivora and primates. II. Accessory olfactory bulb (AOB). J Hirnforsch 23:575–591

    PubMed  CAS  Google Scholar 

  • Stern K, McClintock MK (1998) Regulation of ovulation by human pheromones. Nature 392:177–179

    PubMed  CAS  Google Scholar 

  • Stowers L, Holy TE, Meister M, Dulac C, Koentges G (2002) Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295:1493–1500

    PubMed  CAS  Google Scholar 

  • Swann JM (1997) Gonadal steroids regulate behavioral responses to pheromones by actions on a subdivision of the medial preoptic nucleus. Brain Res 750:189–194

    PubMed  CAS  Google Scholar 

  • Tirindelli R, Ryba NJ (1996) The G-protein gamma-subunit G gamma 8 is expressed in the developing axons of olfactory and vomeronasal neurons. Eur J Neurosci 8:2388–2398

    PubMed  CAS  Google Scholar 

  • Tirindelli R, Mucignat-Caretta C, Ryba NJ (1998) Molecular aspects of pheromonal communication via the vomeronasal organ of mammals. Trends Neurosci 21:482–486

    PubMed  CAS  Google Scholar 

  • Trinh K, Storm DR (2003) Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat Neurosci 6:519–525

    PubMed  CAS  Google Scholar 

  • Trombley PQ, Westbrook GL (1991) Voltage-gated currents in identified rat olfactory receptor neurons. J Neurosci 11:435–444

    PubMed  CAS  Google Scholar 

  • Trotier D, Doving KB, Ore K, Shalchian-Tabrizi C (1998) Scanning electron microscopy and gramicidin patch clamp recordings of microvillous receptor neurons dissociated from the rat vomeronasal organ. Chem Senses 23:49–57

    PubMed  CAS  Google Scholar 

  • Tsuji Y, Shimada Y, Takeshita T, Kajimura N, Nomura S, Sekiyama N, Otomo J, Usukura J, Nakanishi S, Jingami H (2000) Cryptic dimer interface and domain organization of the extracellular region of metabotropic glutamate receptor subtype 1. J Biol Chem 275:28144–28151

    PubMed  CAS  Google Scholar 

  • Van Der Lee S, Boot LM (1955) Spontaneous pseudopregnancy in mice. Acta Physiol Pharmacol Neerl 4:442–444

    Google Scholar 

  • Vandenbergh JG (1969) Male odor accelerates female sexual maturation in mice. Endocrinology 84:658–660

    PubMed  CAS  Google Scholar 

  • Vassalli A, Rothman A, Feinstein P, Zapotocky M, Mombaerts P (2002) Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 35:681–696

    PubMed  CAS  Google Scholar 

  • Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79:981–991

    PubMed  CAS  Google Scholar 

  • Verberne G (1976) Chemocommunication among domestic cats, mediated by the olfactory and vomeronasal senses. II. The relation between the function of Jacobson’s organ (vomeronasal organ) and Flehmen behaviour. Z Tierpsychol 42:113–128

    PubMed  CAS  Google Scholar 

  • von Campenhausen H, Mori K (2000) Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur J Neurosci 12:33–46

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562

    PubMed  CAS  Google Scholar 

  • Wekesa KS, Anholt RR (1997) Pheromone regulated production of inositol-(1, 4, 5)-trisphosphate in the mammalian vomeronasal organ. Endocrinology 138:3497–3504

    PubMed  CAS  Google Scholar 

  • Wekesa KS, Anholt RR (1999) Differential expression of G proteins in the mouse olfactory system. Brain Res 837:117–126

    PubMed  CAS  Google Scholar 

  • Wekesa KS, Miller S, Napier A (2003) Involvement of G(q/11) in signal transduction in the mammalian vomeronasal organ. J Exp Biol 206:827–832

    PubMed  CAS  Google Scholar 

  • Westberry JM, Meredith M (2003) Pre-exposure to female chemosignals or intracerebral GnRH restores mating behavior in naive male hamsters with vomeronasal organ lesions. Chem Senses 28:191–196

    PubMed  CAS  Google Scholar 

  • White JH, Wise A, Main MJ, Green A, Fraser NJ, Disney GH, Barnes AA, Emson P, Foord SM, Marshall FH (1998) Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 396:679–682

    PubMed  CAS  Google Scholar 

  • Whitten WK (1956) Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J Endocrinol 13:399–404

    PubMed  CAS  Google Scholar 

  • Winberg J, Porter RH (1998) Olfaction and human neonatal behaviour: clinical implications. Acta Paediatr 87:6–10

    PubMed  CAS  Google Scholar 

  • Wirsig-Wiechmann CR, Wiechmann AF, Eisthen HL (2002) What defines the nervus terminalis? Neurochemical, developmental, and anatomical criteria. Prog Brain Res 141:45–58

    PubMed  CAS  Google Scholar 

  • Wu Y, Tirindelli R, Ryba NJ (1996) Evidence for different chemosensory signal transduction pathways in olfactory and vomeronasal neurons. Biochem Biophys Res Commun 220:900–904

    PubMed  CAS  Google Scholar 

  • Wysocki CJ, Lepri JJ (1991) Consequences of removing the vomeronasal organ. J Steroid Biochem Mol Biol 39:661–669

    PubMed  CAS  Google Scholar 

  • Wysocki CJ, Wellington JL, Beauchamp GK (1980) Access of urinary nonvolatiles to the mammalian vomeronasal organ. Science 207:781–783

    PubMed  CAS  Google Scholar 

  • Wysocki CJ, Nyby J, Whitney G, Beauchamp GK, Katz Y (1982) The vomeronasal organ: primary role in mouse chemosensory gender recognition. Physiol Behav 29:315–327

    PubMed  CAS  Google Scholar 

  • Yamazaki K, Boyse EA, Mike V, Thaler HT, Mathieson BJ, Abbott J, Boyse J, Zayas ZA, Thomas L (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med 144:1324–1335

    PubMed  CAS  Google Scholar 

  • 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:R71

    PubMed  Google Scholar 

  • Zhang X, Firestein S (2002) The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5:124–133

    PubMed  CAS  Google Scholar 

  • Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293–301

    PubMed  CAS  Google Scholar 

  • Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS (2003) The receptors for mammalian sweet and umami taste. Cell 115:255–266

    PubMed  CAS  Google Scholar 

  • Zhou A, Moss RL (1997) Effect of urine-derived compounds on cAMP accumulation in mouse vomeronasal cells. Neuroreport 8:2173–2177

    PubMed  CAS  Google Scholar 

  • Zou DJ, Feinstein P, Rivers AL, Mathews GA, Kim A, Greer CA, Mombaerts P, Firestein S (2004) Postnatal refinement of peripheral olfactory projections. Science 304:1976–1979

    PubMed  CAS  Google Scholar 

  • Zou Z, Horowitz LF, Montmayeur JP, Snapper S, Buck LB (2001) Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414:173–179

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Italian Board of Education and University (COFIN and FIRB).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Tirindelli .

Rights and permissions

Reprints and Permissions

Copyright information

© 2005 Springer-Verlag

About this chapter

Cite this chapter

Bigiani, A., Mucignat-Caretta, C., Montani, G., Tirindelli, R. (2005). Pheromone reception in mammals. In: Reviews of Physiology, Biochemistry and Pharmacology. Reviews of Physiology, Biochemistry and Pharmacology, vol 154. Springer, Berlin, Heidelberg. https://doi.org/10.1007/s10254-004-0038-0

Download citation