Sulfated steroids as natural ligands of mouse pheromone-sensing neurons

Journal of Neuroscience

Volumn 28, Issue 25, 2008, Pages 6407-6418

  Nodari, Francesco ^a   Hsu, Fong Fu ^a   Fu, Xiaoyan ^a   Holekamp, Terrence F ^a   Kao, Lung Fa ^a   Turk, John ^a   Holy, Timothy E ^a,b  

^a WASHINGTON UNIVERSITY   (United States)

^b Campus Box 8108 ^*  (United States)

Author keywords

Glucocorticoids; Multielectrode array; Olfactory; Stress; Tuning; Vomeronasal

Indexed keywords

4 PREGNENE 11,20,21 TRIOL 3 ONE 21 SULFATE; CORTICOSTERONE 21 SULFATE; GLUCOCORTICOID; PHEROMONE; SULFATASE; SULFATED STEROID DERIVATIVE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 2; UNCLASSIFIED DRUG; LIGAND; STEROID; SULFATE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROPHOBICITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; STRESS; SULFATION; URINE; VOMERONASAL ORGAN; ANIMAL; BAGG ALBINO MOUSE; COMPARATIVE STUDY; METABOLISM; NERVE CELL;

ANIMALS; FEMALE; LIGANDS; MALE; MICE; MICE, INBRED BALB C; NEURONS; PHEROMONES; STEROIDS; SULFATES; VOMERONASAL ORGAN;

EID: 46749147573     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1425-08.2008     Document Type: Article

References (51)

1. Alnouti Y, Klaassen CD (2006) Tissue distribution and ontogeny of sulfotransferase enzymes in mice. Toxicol Sci 93:242-255.
2. Annesley TM (2003) Ion suppression in mass spectrometry. Clin Chem 49:1041-1044.
3. Boschat C, Pélofi 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.
4. Boyle MP, Kolber BJ, Vogt SK, Wozniak DF, Muglia LJ (2006) Forebrain glucocorticoid receptors modulate anxiety-associated locomotor activation and adrenal responsiveness. J Neurosci 26:1971-1978.
5. Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond B Biol Sci 361:2061-2078.
6. Brennan PA, Zufall F (2006) Pheromonal communication in vertebrates. Nature 444:308-315.
7. Brunet LJ, Gold GH, Ngai J (1996) General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17:681-693.
8. 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.
9. De Kloet ER, Vreugdenhil E, Oitzl MS, Joëls M (1998) Brain corticosteroid receptor balance in health and disease. Endocr Rev 19:269-301.
10. 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.
11. Dulac C, Torello AT (2003) Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 4:551-562.
12. Dulka JG (1993) Sex pheromone systems in goldfish: comparisons to vomeronasal systems in tetrapods. Brain Behav Evol 42:265-280.
13. Firestein S (2001) How the olfactory system makes sense of scents. Nature 413:211-218.
14. Guilford T (1995) Animal signals: all honesty and light? Trends Ecol Evol 10:100-101.
15. Halpern M, Martínez-Marcos A (2003) Structure and function of the vomeronasal system: an update. Prog Neurobiol 70:245-318.
16. Holekamp TF, Turaga D, Holy TE (2008) Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron 57:661-672.
17. Holy TE, Dulac C, Meister M (2000) Responses of vomeronasal neurons to natural stimuli. Science 289:1569-1572.
18. Hudson R, Distel H (1986) Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol Behav 37:123-128.
19. Jemiolo B, Andreolini F, Xie TM, Wiesler D, Novotny M (1989) Puberty-affecting synthetic analogs of urinary chemosignals in the house mouse, Mus domesticus. Physiol Behav 46:293-298.
20. Kimchi T, Xu J, Dulac C (2007) A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448:1009-1014.
21. Kimoto H, Haga S, Sato K, Touhara K (2005) Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898-901.
22. 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.
23. Larsen PR, Williams RH, eds (2003) Williams textbook of endocrinology, Ed 10. Philadelphia: Saunders.
24. 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.
25. Leinders-Zufall T, Brennan P, Widmayer P, S PC, Maul-Pavicic A, Jäger M, Li XH, Breer H, Zufall F, Boehm T (2004) MHCclass I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033-1037.
26. Lewis DA (1969) Androgen sulphate formation in male and female mice. Biochem J 115:489-493.
27. 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.
28. Lin DY, Zhang SZ, Block E, Katz LC (2005) Encoding social signals in the mouse main olfactory bulb. Nature 434:470-477.
29. Luo M, Fee MS, Katz LC (2003) Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299:1196-1201.
30. Ma W, Miao Z, Novotny MV (1999) Induction of estrus in grouped female mice (Mus domesticus) by synthetic analogues of preputial gland constituents. Chem Senses 24:289-293.
31. 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.
32. Michael RP, Keverne EB, Bonsall RW (1971) Pheromones: isolation of male sex attractants from a female primate. Science 172:964-966.
33. Mucignat-Caretta C, Caretta A, Cavaggioni A (1995) Acceleration of puberty onset in female mice by male urinary proteins. J Physiol (Lond) 486:517-522.
34. 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.
35. Novotny M, Harvey S, Jemiolo B (1990) Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 46:109-113.
36. Novotny MV, Ma W, Wiesler D, Zidek L (1999) Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein. Proc Biol Sci 266:2017-2022.
37. Oitzl MS, van Haarst AD, Sutanto W, de Kloet ER (1995) Corticosterone, brain mineralocorticoid receptors (MRs) and the activity of the hypothalamic-pituitary-adrenal (HPA) axis: the Lewis rat as an example of increased central MR capacity and a hyporesponsive HPA axis. Psychoneuroendocrinology 20:655-675.
38. Sam M, Vora S, Malnic B, Ma W, Novotny MV, Buck LB (2001) Odorants may arouse instinctive behaviours. Nature 412:142.
39. Saraiva LR, Korsching SI (2007) A novel olfactory receptor gene family in teleost fish. Genome Res 17:1448-1457.
40. Scalia F, Winans SS (1975) The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol 161:31-55.
41. Schaal B, Coureaud G, Langlois D, Giniès C, Sémon E, Perrier G (2003) Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424:68-72.
42. Segev R, Goodhouse J, Puchalla J, Berry 2nd MJ (2004) Recording spikes from a large fraction of the ganglion cells in a retinal patch. Nat Neurosci 7:1154-1161.
43. 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 17:166-174.
44. Singer AG, Agosta WC, O'Connell RJ, Pfaffmann C, Bowen DV, Field FH (1976) Dimethyl disulfide: an attractant pheromone in hamster vaginal secretion. Science 191:948-950.
45. Sorensen PW, Scott AP, Stacey NE, Bowdin L (1995) Sulfated 17,20 beta-dihydroxy-4-pregnen-3-one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. Gen Comp Endocrinol 100:128-142.
46. Sorensen PW, Fine JM, Dvornikovs V, Jeffrey CS, Shao F, Wang J, Vrieze LA, Anderson KR, Hoye TR (2005) Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nat Chem Biol 1:324-328.
47. 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.
48. Trinh K, Storm D (2003) Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat Neurosci 6:519-525.
49. Wyatt TD (2003) Pheromones and animal behaviour. Cambridge, UK: Cambridge UP.
50. Wysocki CJ, Lepri JJ (1991) Consequences of removing the vomeronasal organ. J Steroid Biochem Mol Biol 39:661-669.
51. Zahavi A (1975) Mate selection-a selection for a handicap. J Theor Biol 53:205-214.