The Paternally Expressed Gene Peg3 Regulates Sexual Experience-Dependent Preferences for Estrous Odors

Behavioral Neuroscience

Volumn 122, Issue 5, 2008, Pages 963-973

  Swaney, William T ^a   Curley, James P ^a   Champagne, Frances A ^a   Keverne, Eric B ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

genomic imprinting; learning; olfaction; sexual experience

Indexed keywords

AGGRESSION; ANIMAL EXPERIMENT; ANTICIPATION; ARTICLE; ESTRUS; GENE; GENE EXPRESSION; HABITUATION; MALE; MOUSE; NONHUMAN; OLFACTORY SYSTEM; ONCOGENE C FOS; PEG3 GENE; PYRIFORM CORTEX; SEXUAL BEHAVIOR; SEXUALITY; SMELLING; URINE ODOR;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CHOICE BEHAVIOR; ESTRUS; FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ODORS; OLFACTORY PATHWAYS; PROTO-ONCOGENE PROTEINS C-FOS; SEXUAL BEHAVIOR, ANIMAL; SMELL; URINE;

EID: 54049119743     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/a0012706     Document Type: Article

References (63)

1. Allen N.D., Logan K., Lally G., Drage D.J., Norris M.L., and Keverne E.B. Distribution of parthenogenetic cells in the mouse brain and their influence on brain development and behavior. Proceedings of the National Academy of Sciences of the United States of America 92 (1995) 10782-10786
2. Arendash G.W., and Gorski R.A. Effects of discrete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats. Brain Research Bulletin 10 (1983) 147-154
3. Baum M.J., and Keverne E.B. Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Hormones and Behavior 41 (2002) 213-219
4. Brain P.F., and Al-Maliki S. A comparison of effects of simple experimental manipulations on fighting generated by breeding activity and predatory aggression in 'To' strain mice. Behaviour 69 (1979) 183-199
5. Brennan P.A., and Keverne E.B. Neural mechanisms of mammalian olfactory learning. Progress in Neurobiology 51 (1997) 457-481
6. Brennan P.A., and Zufall F. Pheromonal communication in vertebrates. Nature 444 (2006) 308-315
7. Carr W.J., Loeb L.S., and Dissinger M.L. Responses of rats to sex odors. Journal of Comparative and Physiological Psychology 59 (1965) 370-377
8. Champagne F.A., Curley J.P., Swaney W.T., and Keverne E.B. Regulation of olfaction, anxiety and maternal behavior in mice by paternally expressed genes. Hormones and Behavior 48 (2005) 92-93
9. Claro F., Segovia S., Guilamon A., and Del Abril A. Lesions in the medial posterior region of the BST impair sexual behavior in sexually experienced and inexperienced male rats. Brain Research Bulletin 36 (1995) 1-10
10. Coan P.M., Burton G.J., and Ferguson-Smith A.C. Imprinted genes in the placenta - a review. Placenta 26 Suppl A (2005) S10-20
11. Coolen L.M., and Wood R.I. Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain: Simultaneous anterograde and retrograde tract tracing. Journal of Comparative Neurology 399 (1998) 189-209
12. Curley J.P., Barton S., Surani A., and Keverne E.B. Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proceedings of the Royal Society of London Series B: Biological Sciences 271 (2004) 1303-1309
13. Deng Y.B., and Wu X.W. Peg3/Pw1 promotes pp. 53-mediated apoptosis by inducing Bax translocation from cytosol to mitochondria. Proceedings of the National Academy of Sciences of the United States of America 97 (2000) 12050-12055
14. Dewsbury D.A. Copulatory behaviour of rats (Rattus norvegicus) as a function of prior copulatory experience. Animal Behaviour 17 (1969) 217-223
15. Galef Jr. B.G., Lim T.C.W., and Gilbert G.S. Evidence of mate choice copying in Norway rats, Rattus norvegicus. Animal Behaviour 75 (2008) 117-123
16. Glenn C.C., Driscoll D.J., Yang T.P., and Nicholls R.D. Genomic imprinting: Potential function and mechanisms revealed by the Prader-Willi and Angelman syndromes. Molecular Human Reproduction 3 (1997) 321-332
17. Goyens J., and Noirot E. Effects of cohabitation with females on aggressive behavior between male mice. Developmental Psychobiology 8 (1975) 79-84
18. Hayashi S., and Kimura T. A sex attractant emitted by female mice. Physiology & Behavior 13 (1974) 563-567
19. Hosokawa N., and Chiba A. Effects of sexual experience on conspecific odor preference and estrous odor-induced activation of the vomeronasal projection pathway and the nucleus accumbens in male rats. Brain Research 1066 (2005) 101-108
20. Illig K.R., and Haberly L.B. Odor-evoked activity is spatially distributed in piriform cortex. Journal of Comparative Neurology 457 (2003) 361-373
21. Kaneko-Ishino T., Kohda T., and Ishino F. The regulation and biological significance of genomic imprinting in mammals. Journal of Biochemistry (Tokyo) 133 (2003) 699-711
22. Keller M., Douhard Q., Baum M.J., and Bakker J. Sexual experience does not compensate for the disruptive effects of zinc sulfate-lesioning of the main olfactory epithelium on sexual behavior in male mice. Chemical Senses 31 (2006) 753-762
23. Keverne E.B. Genomic imprinting, maternal care, and brain evolution. Hormones and Behavior 40 (2001) 146-155
24. Keverne E.B. Genomic imprinting and the evolution of sex differences in mammalian reproductive strategies. Advances in Genetics 59 (2007) 217-243
25. Keverne E.B., Fundele R., Narasimha M., Barton S.C., and Surani M.A. Genomic imprinting and the differential roles of parental genomes in brain development. Developmental Brain Research 92 (1996) 91-100
26. Killian J.K., Nolan C.M., Stewart N., Munday B.L., Andersen N.A., Nicol S., et al. Monotreme IGF2 expression and ancestral origin of genomic imprinting. Journal of Experimental Zoology 291 (2001) 205-212
27. Kondo Y. Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats. Physiology & Behavior 51 (1992) 939-943
28. Kritzer M. The distribution of immunoreactivity for intracellular androgen receptors in the cerebral cortex of hormonally intact adult male and female rats: Localization in pyramidal neurons making corticocortical connections. Cerebral Cortex 14 (2004) 268-280
29. Kuroiwa Y., Kaneko-Ishino T., Kagitani F., Kohda T., Li L.L., Tada M., et al. Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nature Genetics 12 (1996) 186-190
30. Larsson K. Experience and maturation in the development of sexual behaviour in male puberty rat. Behaviour 14 (1959) 101-107
31. Li L., Keverne E.B., Aparicio S.A., Ishino F., Barton S.C., and Surani M.A. Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284 (1999) 330-333
32. Lisk R.D., and Heimann J. The effects of sexual experience and frequency of testing on retention of copulatory behavior following castration in the male hamster. Behavioral and Neural Biology 28 (1980) 156-171
33. López H.H., and Ettenberg A. Exposure to female rats produces differences in c-Fos induction between sexually-naive and experienced male rats. Brain Research 947 (2002) 57-66
34. López H.H., Olster D.H., and Ettenberg A. Sexual motivation in the male rat: The role of primary inventives and copulatory experience. Hormones and Behavior 36 (1999) 176-185
35. Lumley L.A., and Hull E.M. Effects of a D1 antagonist and of sexual experience on copulation-induced Fos-like immunoreactivity in the medial preoptic nucleus. Brain Research 829 (1999) 55-68
36. Lydell K., and Doty R.L. Male rat odor preferences for female urine as a function of sexual experience, urine age and urine source. Hormones and Behavior 3 (1972) 205-212
37. Majak K., Ronkko S., Kemppainen S., and Pitkanen A. Projections from the amygdaloid complex to the piriform cortex: A PHA-L study in the rat. Journal of Comparative Neurology 476 (2004) 414-428
38. Mandiyan V.S., Coats J.K., and Shah N.M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nature Neuroscience 8 (2005) 1660-1662
39. Moncho-Bogani J., Lanuza E., Hernandez A., Novejarque A., and Martinez-Garcia F. Attractive properties of sexual pheromones in mice: Innate or learned?. Physiology and Behavior 77 (2002) 167-176
40. Morison I.M., Ramsay J.P., and Spencer H.G. A census of mammalian imprinting. Trends in Genetics 21 (2005) 457-465
41. Nevison C.M., Armstrong S., Beynon R.J., Humphries R.E., and Hurst J.L. The ownership signature in mouse scent marks is involatile. Proceedings of the Royal Society of London Series B: Biological Sciences 270 (2003) 1957-1963
42. Newman S.W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Annals of the New York Academy of Sciences 877 (1999) 242-257
43. Nishitani S., Moriya T., Kondo Y., Sakuma Y., and Shinohara K. Induction of Fos immunoreactivity in oxytocin neurons in the paraventricular nucleus after female odor exposure in male rats: Effects of sexual experience. Cellular and Molecular Neurobiology 24 (2004) 283-291
44. Paxinos G., and Franklin K.B.J. The mouse brain in stereotaxic coordinates. 2nd ed. (2001), Academic, San Diego, CA
45. Pfeiffer C.A., and Johnston R.E. Hormonal and behavioral responses of male hamsters to females and female odors: Roles of olfaction, the vomeronasal system, and sexual experience. Physiology & Behavior 55 (1994) 129-138
46. Phelps S.M., Lydon J.P., O'Malley B.W., and Crews D. Regulation of male sexual behavior by progesterone receptor, sexual experience, and androgen. Hormones and Behavior 34 (1998) 294-302
47. Pro-Sistiaga P., Mohedano-Moriano A., Ubeda-Bañon I., del mar Arroyo-Jimenez M., Marcos P., Artacho-Pérula E., et al. Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. The Journal of Comparative Neurology 504 (2007) 346-362
48. Rastogi R.K., Milone M., and Chieffi G. Impact of socio-sexual conditions on the epididymis and fertility in the male mouse. Journal of Reproduction and Fertility 63 (1981) 331-334
49. Relaix F., Wei X.J., Li W., Pan J.J., Lin Y.H., Bowtell D.D., et al. Pw1/Peg3 is a potential cell death mediator and cooperates with Siah1a in pp. 53-mediated apoptosis. Proceedings of the National Academy of Sciences of the United States of America 97 (2000) 2105-2110
50. Relaix F., Weng X., Marazzi G., Yang E., Copeland N., Jenkins N., et al. Pw1, a novel zinc finger gene implicated in the myogenic and neuronal lineages. Developmental Biology 177 (1996) 383-396
51. Schaefer M.L., Yamazaki K., Osada K., Restrepo D., and Beauchamp G.K. Olfactory fingerprints for major histocompatibility complex-determined body odors II: Relationship among odor maps, genetics, odor composition, and behavior. Journal of Neuroscience 22 (2002) 9513-9521
52. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. Journal of Comparative Neurology 388 (1997) 507-525
53. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: An in situ hybridization study. Journal of Comparative Neurology 294 (1990) 76-95
54. Sipos M.L., Kerchner M., and Nyby J.G. An ephemeral sex pheromone in the urine of female house mice (Mus domesticus). Behavioral and Neural Biology 58 (1992) 138-143
55. Sipos M.L., Wysocki C.J., Nyby J.G., Wysocki L., and Nemura T.A. An ephemeral pheromone of female house mice: Perception via the main and accessory olfactory systems. Physiology & Behavior 58 (1995) 529-534
56. Staubli U., Schottler F., and Nejat-Bina D. Role of dorsomedial thalamic nucleus and piriform cortex in processing olfactory information. Behavioural Brain Research 25 (1987) 117-129
57. Stern J.J. Responses of male rats to sex odors. Physiology & Behavior 5 (1970) 519-524
58. Swaney W.T., Curley J.P., Champagne F.A., and Keverne E.B. Genomic imprinting mediates sexual experience-dependent olfactory learning in male mice. Proceedings of the National Academy of Sciences of the United States of America 104 (2007) 6084-6089
59. Tycko B., and Morison I.M. Physiological functions of imprinted genes. Journal of Cellular Physiology 192 (2002) 245-258
60. Valenstein E.S., and Goy R.W. Further studies of the organization and display of sexual behavior in male guinea pigs. Journal of Comparative and Physiological Psychology 50 (1957) 115-119
61. Valenstein E.S., Riss W., and Young W.C. Experiential and genetic factors in the organization of sexual behavior in male guinea pigs. Journal of Comparative and Physiological Psychology 48 (1955) 397-403
62. Wang Z., Hulihan T.J., and Insel T.R. Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles. Brain Research 767 (1997) 321-332
63. Xu F., Schaefer M., Kida I., Schafer J., Liu N., Rothman D.L., et al. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. The Journal of Comparative Neurology 489 (2005) 491-500