The genomic basis of vomeronasal-mediated behaviour

Mammalian Genome

Volumn 25, Issue 1-2, 2014, Pages 75-86

  Ibarra Soria, Ximena ^a   Levitin, Maria O ^a,b   Logan, Darren W ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCRINE SECRETED PEPTIDE; FORMYLPEPTIDE RECEPTOR; MAJOR URINARY PROTEIN; PEPTIDE; PHEROMONE; PROTEIN; RECEPTOR; UNCLASSIFIED DRUG; VOMERONASAL RECEPTOR;

AGGRESSION; ANIMAL BEHAVIOR; AVOIDANCE BEHAVIOR; DEFENSIVE BEHAVIOR; GENE MUTATION; GENETIC CODE; GENOMICS; MULTIGENE FAMILY; NEUROEPITHELIUM; NONHUMAN; OLFACTORY RECEPTOR; PREGNANCY TERMINATION; PROTEIN URINE LEVEL; RECEPTOR GENE; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; VOMERONASAL ORGAN;

MAMMALIA; PRIMATES; RODENTIA;

ANIMALS; GENETICS, BEHAVIORAL; HUMANS; PHEROMONES; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION; VOMERONASAL ORGAN;

EID: 84895868439     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-013-9463-1     Document Type: Review

References (105)

1. Ben-Shaul Y, Katz LC, Mooney R, Dulac C (2010) In vivo vomeronasal stimulation reveals sensory encoding of conspecific and allospecific cues by the mouse accessory olfactory bulb. Proc Natl Acad Sci USA 107:5172-5177
2. 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 (Pubitemid 26140846)
3. Berghard A, Buck LB, Liman ER (1996) Evidence for distinct signaling mechanisms in two mammalian olfactory sense organs. Proc Natl Acad Sci USA 93:2365-2369 (Pubitemid 26104356)
4. Blass EM, Teicher MH (1980) Suckling. Science 210:15-22
5. 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 (Pubitemid 35422711)
6. Brechbuhl J, Moine F, Klaey M, Nenniger-Tosato M, Hurni N, Sporkert F, Giroud C, Broillet MC (2013) Mouse alarm pheromone shares structural similarity with predator scents. Proc Natl Acad Sci USA 110:4762-4767
7. Bruce HM (1959) An exteroceptive block to pregnancy in the mouse. Nature 184:105
8. Bufe B, Schumann T, Zufall F (2012) Formyl peptide receptors from immune and vomeronasal system exhibit distinct agonist properties. J Biol Chem 287:33644-33655
9. Bult CJ, Kadin JA, Richardson JE, Blake JA, Eppig JT (2010) The mouse genome database: enhancements and updates. Nucleic Acids Res 38:D586-D592
10. Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, Saghatelian A, Cravatt BF, Stowers L (2007) Identification of protein pheromones that promote aggressive behaviour. Nature 450:899-902 (Pubitemid 350231315)
11. Chamero P, Katsoulidou V, Hendrix P, Bufe B, Roberts R, Matsunami H, Abramowitz J, Birnbaumer L, Zufall F, Leinders-Zufall T (2011) G protein G(alpha)o is essential for vomeronasal function and aggressive behavior in mice. Proc Natl Acad Sci USA 108:12898-12903
12. Cheetham SA, Smith AL, Armstrong SD, Beynon RJ, Hurst JL (2009) Limited variation in the major urinary proteins of laboratory mice. Physiol Behav 96:253-261
13. Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823-834 (Pubitemid 24294457)
14. Clissold PM, Hainey S, Bishop JO (1984) Messenger RNAs coding for mouse major urinary proteins are differentially induced by testosterone. Biochem Genet 22:379-387 (Pubitemid 14149707)
15. Del Punta K, Leinders-Zufall T, Rodriguez I, Jukam D, Wysocki CJ, Ogawa S, Zufall F, Mombaerts P (2002) Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419:70-74 (Pubitemid 34987871)
16. Dewan A, Pacifico R, Zhan R, Rinberg D, Bozza T (2013) Nonredundant coding of aversive odours in the main olfactory pathway. Nature 497:486-489
17. Dey S, Matsunami H (2011) Calreticulin chaperones regulate functional expression of vomeronasal type 2 pheromone receptors. Proc Natl Acad Sci USA 108:16651-16656
18. Doty RL (2010) The great pheromone myth. Johns Hopkins University Press, Baltimore
19. Doving KB, Trotier D (1998) Structure and function of the vomeronasal organ. J Exp Biol 201:2913-2925 (Pubitemid 28560357)
20. Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195-206
21. 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 (Pubitemid 38500230)
22. Ferrero DM, Lemon JK, Fluegge D, Pashkovski SL, Korzan WJ, Datta SR, Spehr M, Fendt M, Liberles SD (2011) Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci USA 108:11235-11240
23. Gelstein S, Yeshurun Y, Rozenkrantz L, Shushan S, Frumin I, Roth Y, Sobel N (2011) Human tears contain a chemosignal. Science 331:226-230
24. 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 102:5767-5772 (Pubitemid 40559634)
25. Grus WE, Shi P, Zhang J (2007) Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol Biol Evol 24:2153-2157 (Pubitemid 47574727)
26. Haga S, Hattori T, Sato T, Sato K, Matsuda S, Kobayakawa R, Sakano H, Yoshihara Y, Kikusui T, Touhara K (2010) The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 466:118-122
27. Hasen NS, Gammie SC (2009) Trpc2 gene impacts on maternal aggression, accessory olfactory bulb anatomy and brain activity. Genes Brain Behav 8:639-649
28. Hasen NS, Gammie SC (2011) Trpc2-deficient lactating mice exhibit altered brain and behavioral responses to bedding stimuli. Behav Brain Res 217:347-353
29. Hastie ND, Held WA, Toole JJ (1979) Multiple genes coding for the androgen-regulated major urinary proteins of the mouse. Cell 17:449-457 (Pubitemid 9230325)
30. Herrada G, Dulac C (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763-773 (Pubitemid 27357967)
31. Huckins LM, Logan DW, Sanchez-Andrade G (2013) Olfaction and olfactory-mediated behaviour in psychiatric disease models. Cell Tissue Res. doi:10.1007/s00441-013-1617-7
32. 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 (Pubitemid 33151257)
33. Ishii T, Mombaerts P (2008) Expression of nonclassical class I major histocompatibility genes defines a tripartite organization of the mouse vomeronasal system. J Neurosci 28:2332-2341 (Pubitemid 351348179)
34. Ishii T, Mombaerts P (2011) Coordinated coexpression of two vomeronasal receptor V2R genes per neuron in the mouse. Mol Cell Neurosci 46:397-408
35. 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 (Pubitemid 36280456)
36. Isogai Y, Si S, Pont-Lezica L, Tan T, Kapoor V, Murthy VN, Dulac C (2011) Molecular organization of vomeronasal chemoreception. Nature 478:241-245
37. Karn RC, Laukaitis CM (2009) The mechanism of expansion and the volatility it created in three pheromone gene clusters in the mouse (Mus musculus) genome. Genome Biol Evol 1:494-503
38. Keller A (2012) Different noses for different mice and men. BMC Biol 10:75
39. Kelliher KR, Spehr M, Li XH, Zufall F, Leinders-Zufall T (2006) Pheromonal recognition memory induced by TRPC2-independent vomeronasal sensing. Eur J Neurosci 23:3385-3390
40. Kim S, Ma L, Yu CR (2011) Requirement of calcium-activated chloride channels in the activation of mouse vomeronasal neurons. Nat Commun 2:365
41. Kimchi T, Xu J, Dulac C (2007) A functional circuit underlying male sexual behaviour in the femalemouse brain.Nature 448:1009-1014 (Pubitemid 47345587)
42. Kimoto H, Haga S, Sato K, Touhara K (2005) Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898-901 (Pubitemid 41486766)
43. Kimoto H, Sato K, Nodari F, Haga S, Holy TE, Touhara K (2007) Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr Biol 17:1879-1884 (Pubitemid 350016920)
44. Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, Mori K, Sakano H (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503-508 (Pubitemid 350190245)
45. 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 (Pubitemid 30407851)
46. Leinders-Zufall T, Brennan P, Widmayer P, Pc S, Maul-Pavicic A, Jager M, Li XH, Breer H, Zufall F, Boehm T (2004) MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033-1037 (Pubitemid 39482906)
47. Leinders-Zufall T, Ishii T, Mombaerts P, Zufall F, Boehm T (2009) Structural requirements for the activation of vomeronasal sensory neurons by MHC peptides. Nat Neurosci 12:1551-1558
48. 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 USA 99:6376-6381 (Pubitemid 34493319)
49. 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 106:9842-9847
50. Liman ER, Innan H (2003) Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci USA 100:3328-3332 (Pubitemid 36356583)
51. Liman ER, Corey DP, Dulac C (1999) TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc Natl Acad Sci USA 96:5791-5796 (Pubitemid 29234697)
52. 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 (Pubitemid 36331774)
53. Logan DW, Marton TF, Stowers L (2008) Species specificity in major urinary proteins by parallel evolution. PLoS ONE 3:e3280
54. Logan DW, Brunet LJ, Webb WR, Cutforth T, Ngai J, Stowers L (2012) Learned recognition of maternal signature odors mediates the first suckling episode in mice. Curr Biol 22:1998-2007
55. Ma M (2010) Multiple olfactory subsystems convey various sensory signals. In: Menini A (ed) The neurobiology of olfaction. CRC, Boca Raton
56. 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 (Pubitemid 32163125)
57. Matsunami H, Buck LB (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775-784 (Pubitemid 27357968)
58. Matsunami H, Mainland JD, Dey S (2009) Trafficking of mammalian chemosensory receptors by receptor-transporting proteins. Ann N Y Acad Sci 1170:153-156
59. 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 (Pubitemid 32831311)
60. Meslin C, Brimau F, Nagnan-Le Meillour P, Callebaut I, Pascal G, Monget P (2011) The evolutionary history of the SAL1 gene family in eutherian mammals. BMC Evol Biol 11:148
61. Mucignat-Caretta C (2010) The rodent accessory olfactory system. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:767-777
62. Mudge JM, Armstrong SD, McLaren K, Beynon RJ, Hurst JL, Nicholson C, Robertson DH, Wilming LG, Harrow JL (2008) Dynamic instability of the major urinary protein gene family revealed by genomic and phenotypic comparisons between C57 and 129 strain mice. Genome Biol 9:R91
63. Nodari F, Hsu FF, Fu X, Holekamp TF, Kao LF, Turk J, Holy TE (2008) Sulfated steroids as natural ligands of mouse pheromonesensing neurons. J Neurosci 28:6407-6418
64. Norlin EM, Gussing F, Berghard A (2003) Vomeronasal phenotype and behavioral alterations in G alpha i2 mutant mice. Curr Biol 13:1214-1219 (Pubitemid 36872944)
65. Papes F, Logan DW, Stowers L (2010) The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141:692-703
66. Pedersen PE, Williams CL, Blass EM (1982) Activation and odor conditioning of suckling behavior in 3-day-old albino rats. J Exp Psychol Anim Behav Process 8:329-341
67. Petrulis A (2013) Chemosignals, hormones and mammalian reproduction. Horm Behav 63(5):723-741
68. Riviere S, Challet L, Fluegge D, Spehr M, Rodriguez I (2009) Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature 459:574-577
69. Roberts SA, Simpson DM, Armstrong SD, Davidson AJ, Robertson DH, McLean L, Beynon RJ, Hurst JL (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biol 8:75
70. Roberts EK, Lu A, Bergman TJ, Beehner JC (2012a) A Bruce effect in wild geladas. Science 335:1222-1225
71. Roberts SA, Davidson AJ, McLean L, Beynon RJ, Hurst JL (2012b) Pheromonal induction of spatial learning in mice. Science 338:1462-1465
72. Robertson DH, Hurst JL, Bolgar MS, Gaskell SJ, Beynon RJ (1997) Molecular heterogeneity of urinary proteins in wild house mouse populations. Rapid Commun Mass Spectrom 11:786-790 (Pubitemid 27206948)
73. Rodriguez I (2010) The chemical MUPpeteer. Cell 141:568-570
74. 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 (Pubitemid 34121580)
75. Rudolph U, Finegold MJ, Rich SS, Harriman GR, Srinivasan Y, Brabet P, Boulay G, Bradley A, Birnbaumer L (1995) Ulcerative colitis and adenocarcinoma of the colon in G alpha i2-deficient mice. Nat Genet 10:143-150
76. Ryba NJ, Tirindelli R (1997) A new multigene family of putative pheromone receptors. Neuron 19:371-379 (Pubitemid 27374235)
77. Sbarbati A, Osculati F (2006) Allelochemical communication in vertebrates: kairomones, allomones and synomones. Cells Tissues Organs 183:206-219 (Pubitemid 44924468)
78. Schaal B, Coureaud G, Langlois D, Ginies C, Semon E, Perrier G (2003) Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424:68-72 (Pubitemid 36834842)
79. Schellinck HM, Forestell CA, LoLordo VM (2001) A simple and reliable test of olfactory learning and memory in mice. Chem Senses 26:663-672 (Pubitemid 32750518)
80. Sherborne AL, Thom MD, Paterson S, Jury F, Ollier WE, Stockley P, Beynon RJ, Hurst JL (2007) The genetic basis of inbreeding avoidance in house mice. Curr Biol 17:2061-2066 (Pubitemid 350180467)
81. Silvotti L, Moiani A, Gatti R, Tirindelli R (2007) Combinatorial coexpression of pheromone receptors, V2Rs. J Neurochem 103:1753-1763 (Pubitemid 350126612)
82. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, Jackson D, Severin J, Biggs P, Fu J, Nefedov M, de Jong PJ, Stewart AF, Bradley A (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474:337-342
83. Stowers L, Logan DW (2010a) Olfactory mechanisms of stereotyped behavior: on the scent of specialized circuits. Curr Opin Neurobiol 20:274-280
84. Stowers L, Logan DW (2010b) Sexual dimorphism in olfactory signaling. Curr Opin Neurobiol 20:770-775
85. 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 (Pubitemid 34173998)
86. Thom MD, Stockley P, Jury F, Ollier WE, Beynon RJ, Hurst JL (2008) The direct assessment of genetic heterozygosity through scent in the mouse. Curr Biol 18:619-623
87. van der Weyden L, White JK, Adams DJ, Logan DW (2011) The mouse genetics toolkit: revealing function and mechanism. Genome Biol 12:224
88. Wang G, Shi P, Zhu Z, Zhang YP (2010) More functional V1R genes occur in nest-living and nocturnal terricolous mammals. Genome Biol Evol 2:277-283
89. Webb DM, Cortes-Ortiz L, Zhang J (2004) Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys. Mol Biol Evol 21:697-704 (Pubitemid 38452103)
90. Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, Cambridge
91. Wyatt TD (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:685-700
92. Wynn EH, Sanchez-Andrade G, Carss KJ, Logan DW (2012) Genomic variation in the vomeronasal receptor gene repertoires of inbred mice. BMC Genomics 13:415
93. Wysocki CJ, Preti G (2004) Facts, fallacies, fears, and frustrations with human pheromones. Anat Rec A Discov Mol Cell Evol Biol 281:1201-1211 (Pubitemid 39458664)
94. Yang C, Delay RJ (2010) Calcium-activated chloride current amplifies the response to urine in mouse vomeronasal sensory neurons. J Gen Physiol 135:3-13
95. Yang H, Shi P (2010) Molecular and evolutionary analyses of formyl peptide receptors suggest the absence of VNO-specific FPRs in primates. J Genet Genomics 37:771-778
96. Yang H, Shi P, Zhang YP, Zhang J (2005) Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics 86:306-315 (Pubitemid 41096700)
97. Yoshinaga S, Sato T, Hirakane M, Esaki K, Hamaguchi T, Haga-Yamanaka S, Tsunoda M, Kimoto H, Shimada I, Touhara K, Terasawa H (2013) Structure of the mouse sex peptide pheromone ESP1 reveals a molecular basis for specific binding to the class C G-protein-coupled vomeronasal receptor. J Biol Chem 288(22):16064-16072
98. Young JM, Trask BJ (2007) V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet 23:212-215 (Pubitemid 46616968)
99. 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 15:231-240 (Pubitemid 40309387)
100. Young JM, Massa HF, Hsu L, Trask BJ (2010) Extreme variability among mammalian V1R gene families. Genome Res 20:10-18
101. Yu L, Jin W, Wang JX, Zhang X, Chen MM, Zhu ZH, Lee H, Lee M, Zhang YP (2010) Characterization of TRPC2, an essential genetic component of VNS chemoreception, provides insights into the evolution of pheromonal olfaction in secondary-adapted marine mammals. Mol Biol Evol 27:1467-1477
102. Zhang J, Webb DM (2003) Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci USA 100:8337-8341 (Pubitemid 36842546)
103. Zhang X, Rodriguez I, Mombaerts P, Firestein S (2004) Odorant and vomeronasal receptor genes in two mouse genome assemblies. Genomics 83:802-811 (Pubitemid 38469922)
104. Zhang P, Yang C, Delay RJ (2010) Odors activate dual pathways, a TRPC2 and a AA-dependent pathway, in mouse vomeronasal neurons. Am J Physiol Cell Physiol 298:C1253-C1264
105. Zhao H, Xu D, Zhang S, Zhang J (2011) Widespread losses of vomeronasal signal transduction in bats. Mol Biol Evol 28:7-12