From sexual attraction to maternal aggression: When pheromones change their behavioural significance

Hormones and Behavior

Volumn 68, Issue , 2015, Pages 65?76-76

  Martín Sánchez, Ana ^a   McLean, Lynn ^b   Beynon, Robert J ^b   Hurst, Jane L ^b   Ayala, Guillermo ^c   Lanuza, Enrique ^a   Martínez Garcia, Fernando ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c Department of Statistics and Operative Research   (Spain)

Author keywords

Darcin; Major urinary proteins; Mouse; Olfactory; Socio sexual behaviour; Vomeronasal

Indexed keywords

ADENYLATE CYCLASE; CELL PROTEIN; DARCIN; ESP1 PROTEIN; MAJOR URINARY PROTEIN 20; SEX PHEROMONE; TEAR PROTEIN; UNCLASSIFIED DRUG; DARCIN PROTEIN, MOUSE; PHEROMONE; PROTEIN;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; BEHAVIOR CHANGE; CHEMOSENSITIVITY; CONTROLLED STUDY; FEMALE; FEMALE GENITAL SYSTEM; HORMONE DETERMINATION; LACTATION; LATENT PERIOD; LORDOSIS; MATERNAL AGGRESSION; MATERNAL BEHAVIOR; MOUSE; NONHUMAN; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PLACE PREFERENCE; PREGNANCY; PROTEIN FUNCTION; REVIEW; SEXUAL ATTRACTION; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; SMELLING; STIMULUS RESPONSE; URINE ODOR; VOCALIZATION; VOMERONASAL ORGAN; ANIMAL; MALE; PHYSIOLOGY;

AGGRESSION; ANIMALS; FEMALE; MALE; MATERNAL BEHAVIOR; MICE; PHEROMONES; PROTEINS; SEXUAL BEHAVIOR, ANIMAL;

EID: 84922470048     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2014.08.007     Document Type: Review

References (100)

1. Adams D.C., Anthony C.D. Using randomization techniques to analyse behavioural data. Anim. Behav. 1996, 51:733-738.
2. Alekseyenko O.V., Baum M.J., Cherry J.A. Sex and gonadal steroid modulation of pheromone receptor gene expression in the mouse vomeronasal organ. Neuroscience 2006, 140:1349-1357.
3. Armstrong S.D., Robertson D.H., Cheetham S.A., Hurst J.L., Beynon R.J. Structural and functional differences in isoforms of mouse major urinary proteins: a male-specific protein that preferentially binds a male pheromone. Biochem. J. 2005, 391:343-350.
4. Baum M.J. Contribution of pheromones processed by the main olfactory system to mate recognition in female mammals. Front. Neuroanat. 2012, 6:20.
5. Baum M.J., Bakker J. Roles of sex and gonadal steroids in mammalian pheromonal communication. Front. Neuroendocrinol. 2013, 34:268-284.
6. Bean N.J., Wysocki C.J. Vomeronasal organ removal and female mouse aggression: the role of experience. Physiol. Behav. 1989, 45:875-882.
7. Bosch O.J. Maternal aggression in rodents: brain oxytocin and vasopressin mediate pup defence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:20130085.
8. Bridges R.S., Ronsheim P.M. Prolactin (PRL) regulation of maternal behavior in rats: bromocriptine treatment delays and PRL promotes the rapid onset of behavior. Endocrinology 1990, 126:837-848.
9. Byers S.L., Wiles M.V., Dunn S.L., Taft R.A. Mouse estrous cycle identification tool and images. PLoS One 2012, 7:e35538.
10. Chamero P., Marton T.F., Logan D.W., Flanagan K., Cruz J.R., Saghatelian A., Cravatt B.F., Stowers L. Identification of protein pheromones that promote aggressive behaviour. Nature 2007, 450:899-902.
11. Chamero P., Katsoulidou V., Hendrix P., Bufe B., Roberts R., Matsunami H., Abramowitz J., Birnbaumer L., Zufall F., Leinders-Zufall T. G protein G(alpha)o is essential for vomeronasal function and aggressive behavior in mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:12898-12903.
12. Cheetham S.A., Smith A.L., Armstrong S.D., Beynon R.J., Hurst J.L. Limited variation in the major urinary proteins of laboratory mice. Physiol. Behav. 2009, 96:253-261.
13. Clancy A.N., Coquelin A., Macrides F., Gorski R.A., Noble E.P. Sexual behavior and aggression in male mice: involvement of the vomeronasal system. J. Neurosci. 1984, 4:2222-2229.
14. Del Punta K., Leinders-Zufall T., Rodriguez I., Jukam D., Wysocki C.J., Ogawa S., Zufall F., Mombaerts P. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 2002, 419:70-74.
15. DiBenedictis B.T., Ingraham K.L., Baum M.J., Cherry J.A. Disruption of urinary odor preference and lordosis behavior in female mice given lesions of the medial amygdala. Physiol. Behav. 2012, 105:554-559.
16. Drickamer L.C. Odor preference of wild stock female house mice (Mus domesticus) tested at three ages using urine and other cues from conspecific males and females. J. Chem. Ecol. 1989, 15:1971-1987.
17. Ermisch A., Rühle H.J., Landgraf R., Hess J. Blood-brain barrier and peptides. J. Cereb. Blood Flow Metab. 1985, 5:350-357.
18. Ferrero D.M., Moeller L.M., Osakada T., Horio N., Li Q., Roy D.S., Cichy A., Spehr M., Touhara K., Liberles S.D. A juvenile mouse pheromone inhibits sexual behaviour through the vomeronasal system. Nature 2013, 502:368-371.
19. Fleming A.S., Rosenblatt J.S. Olfactory regulation of maternal behavior in rats. I. Effects of olfactory bulb removal in experienced and inexperienced lactating and cycling females. J. Comp. Physiol. Psychol. 1974, 86:221-232.
20. Fortes-Marco L., Lanuza E., Martinez-Garcia F. Of pheromones and kairomones: what receptors mediate innate emotional responses?. Anat. Rec. (Hoboken) 2013, 296:1346-1363.
21. Gandelman R. Mice: postpartum aggression elicited by the presence of an intruder. Horm. Behav. 1972, 3:23-28.
22. Gandelman R., Zarrow M.X., Denenberg V.H. Stimulus control of cannibalism and maternal behavior in anosmic mice. Physiol. Behav. 1971, 7:583-586.
23. Gandelman R., Zarrow M.X., Denenberg V.H., Myers M. Olfactory bulb removal eliminates maternal behavior in the mouse. Science 1971, 171:210-211.
24. Gandelman R., Zarrow M.X., Denenberg V.H. Reproductive and maternal performance in the mouse following removal of the olfactory bulbs. J. Reprod. Fertil. 1972, 28:453-456.
25. Good P.I. Permutation, Parametric, and Bootstrap Tests of Hypotheses 2005, Springer, New York.
26. Gordon S., Kiernan L.A., Nieuwenhuijsen M.J., Cook A.D., Tee R.D., Newman Taylor A.J. Measurement of exposure to mouse urinary proteins in an epidemiological study. Occup. Environ. Med. 1997, 54:135-140.
27. Guo Z., Holy T.E. Sex selectivity of mouse ultrasonic songs. Chem. Senses 2007, 32:463-473.
28. Haga S., Hattori T., Sato T., Sato K., Matsuda S., Kobayakawa R., Sakano H., Yoshihara Y., Kikusui T., Touhara K. The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 2010, 466:118-122.
29. Harvey S., Jemiolo B., Novotny M. Pattern of volatile compounds in dominant and subordinate male mouse urine. J. Chem. Ecol. 1989, 15:2061-2072.
30. Hasen N.S., Gammie S.C. Trpc2 gene impacts on maternal aggression, accessory olfactory bulb anatomy and brain activity. Genes Brain Behav. 2009, 8:639-649.
31. Hasen N.S., Gammie S.C. Trpc2-deficient lactating mice exhibit altered brain and behavioral responses to bedding stimuli. Behav. Brain Res. 2011, 217:347-353.
32. Holy T.E., Guo Z. Ultrasonic songs of male mice. PLoS Biol. 2005, 3:e386.
33. Hurst J.L. The functions of urine marking in a free-living population of house mice, Mus domesticus Rutty. Anim. Behav. 1987, 35:1433-1442.
34. Ishii T., Hirota J., Mombaerts P. Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Curr. Biol. 2003, 13:394-400.
35. Jemiolo B., Alberts J., Sochinski-Wiggins S., Harvey S., Novotny M. Behavioural and endocrine responses of female mice to synthetic analogues of volatile compounds in male urine. Anim. Behav. 1985, 33:1114-1118.
36. Jemiolo B., Andreolini F., Xie T.M., Wiesler D., Novotny M. Puberty-affecting synthetic analogs of urinary chemosignals in the house mouse, Mus domesticus. Physiol. Behav. 1989, 46:293-298.
37. Jemiolo B., Xie T.M., Novotny M. Socio-sexual olfactory preference in female mice: attractiveness of synthetic chemosignals. Physiol. Behav. 1991, 50:1119-1122.
38. Jouhanneau M., Cornilleau F., Keller M. Peripubertal exposure to male odors influences female puberty and adult expression of male-directed odor preference in mice. Horm. Behav. 2014, 65:128-133.
39. Karlson P., Luscher M. Pheromones': a new term for a class of biologically active substances. Nature 1959, 183:55-56.
40. Kaur A.W., Ackels T., Kuo T.H., Cichy A., Dey S., Hays C., Kateri M., Logan D.W., Marton T.F., Spehr M., Stowers L. Murine pheromone proteins constitute a context-dependent combinatorial code governing multiple social behaviors. Cell 2014, 157:676-688.
41. Keller M., Douhard Q., Baum M.J., Bakker J. Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chem. Senses 2006, 31:315-323.
42. Keller M., Pierman S., Douhard Q., Baum M.J., Bakker J. The vomeronasal organ is required for the expression of lordosis behaviour, but not sex discrimination in female mice. Eur. J. Neurosci. 2006, 23:521-530.
43. Kelliher K.R., Spehr M., Li X.H., Zufall F., Leinders-Zufall T. Pheromonal recognition memory induced by TRPC2-independent vomeronasal sensing. Eur. J. Neurosci. 2006, 23:3385-3390.
44. Kim S., Ma L., Yu C.R. Requirement of calcium-activated chloride channels in the activation of mouse vomeronasal neurons. Nat. Commun. 2011, 2:365-372.
45. Kim S., Ma L., Jensen K.L., Kim M.M. Paradoxical contribution of SK3 and GIRK channels to the activation of mouse vomeronasal organ. Nat. Neurosci. 2012, 15:1236-1244.
46. Kimchi T., Xu J., Dulac C. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 2007, 448:1009-1014.
47. Kimoto H., Haga S., Sato K., Touhara K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 2005, 437:898-901.
48. Kimoto H., Sato K., Nodari F., Haga S., Holy T.E., Touhara K. Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr. Biol. 2007, 17:1879-1884.
49. Leinders-Zufall T., Lane A.P., Puche A.C., Ma W., Novotny M.V., Shipley M.T., Zufall F. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 2000, 405:792-796.
50. Leinders-Zufall T., Brennan P., Widmayer P., Chandramani P.S., Maul-Pavicic A., Jäger M., Li X.H., Breer H., Zufall F., Boehm T. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 2004, 306:1033-1037.
51. Leinders-Zufall T., Ishii T., Chamero P., Hendrix P., Oboti L., Schmid A., Kircher S., Pyrski M., Akiyoshi S., Khan M., Vaes E., Zufall F., Mombaerts P. A family of nonclassical class I MHC genes contributes to ultrasensitive chemodetection by mouse vomeronasal sensory neurons. J. Neurosci. 2014, 34:5121-5133.
52. Leypold B.G., Yu C.R., Leinders-Zufall T., Kim M.M., Zufall F., Axel R. Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:6376-6381.
53. Lin D.Y., Zhang S.Z., Block E., Katz L.C. Encoding social signals in the mouse main olfactory bulb. Nature 2005, 434:470-477.
54. Lin D., Boyle M.P., Dollar P., Lee H., Lein E.S., Perona P., Anderson D.J. Functional identification of an aggression locus in the mouse hypothalamus. Nature 2011, 470:221-226.
55. Loconto J., Papes F., Chang E., Stowers L., Jones E.P., Takada T., Kumanovics A., Fischer Lindahl K., Dulac C. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 2003, 112:607-618.
56. Lonstein J.S., Gammie S.C. Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci. Biobehav. Rev. 2002, 26:869-888.
57. Lorenz K. Das sogenannte Böse zur Naturgeschichte der Aggression 1963, Dr. G Borotha-Schoeler, Wien.
58. Luo M., Fee M.S., Katz L.C. Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 2003, 299:1196-1201.
59. Mandiyan V.S., Coats J.K., Shah N.M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat. Neurosci. 2005, 8:1660-1662.
60. Mann M., Michael S., Svare B. Ergot drugs suppress plasma prolactin and lactation but not aggression in parturient mice. Horm. Behav. 1980, 14:319-328.
61. Mann M.A., Konen C., Svare B. The role of progesterone in pregnancy-induced aggression in mice. Horm. Behav. 1984, 18:140-160.
62. Martinez-Garcia F., Martinez-Ricos J., Agustin-Pavon C., Martinez-Hernandez J., Novejarque A., Lanuza E. Refining the dual olfactory hypothesis: pheromone reward and odour experience. Behav. Brain Res. 2009, 200:277-286.
63. Martinez-Ricos J., Agustin-Pavon C., Lanuza E., Martinez-Garcia F. Intraspecific communication through chemical signals in female mice: reinforcing properties of involatile male sexual pheromones. Chem. Senses 2007, 32:139-148.
64. Martinez-Ricos J., Agustin-Pavon C., Lanuza E., Martinez-Garcia F. Role of the vomeronasal system in intersexual attraction in female mice. Neuroscience 2008, 153:383-395.
65. Moncho-Bogani J., Lanuza E., Hernandez A., Novejarque A., Martinez-Garcia F. Attractive properties of sexual pheromones in mice. Innate or learned?. Physiol. Behav. 2002, 77:167-176.
66. Moncho-Bogani J., Lanuza E., Lorente M.J., Martinez-Garcia F. Attraction to male pheromones and sexual behaviour show different regulatory mechanisms in female mice. Physiol. Behav. 2004, 81:427-434.
67. Mucignat-Caretta C., Caretta A., Baldini E. Protein-bound male urinary pheromones: differential responses according to age and gender. Chem. Senses 1998, 23:67-70.
68. Mugford R.A., Nowell N.W. Pheromones and their effect on aggression in mice. Nature 1970, 226:967-968.
69. Norlin E.M., Gussing F., Berghard A. Vomeronasal phenotype and behavioral alterations in G alpha i2 mutant mice. Curr. Biol. 2003, 13:1214-1219.
70. Novotny M., Harvey S., Jemiolo B., Alberts J. Synthetic pheromones that promote intermale aggression in mice. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:2059-2061.
71. Novotny M.V., Ma W., Wiesler D., Zidek L. Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein. Proc. R. Soc. Lond. B Biol. Sci. 1999, 266:2017-2022.
72. Nyby J., Wysocki C.J., Whitney G., Dizinno G., Schneider J., Nunez A.A. Stimuli for male mouse (Mus musculus) ultrasonic courtship vocalizations: presence of female chemosignals and/or absence of male chemosignals. J. Comp. Physiol. Psychol. 1981, 95:623-629.
73. Omura M., Mombaerts P. Trpc2-expressing sensory neurons in the main olfactory epithelium of the mouse. Cell Rep. 2014, 8:583-595.
74. Pfeiffer C.A., Johnston R.E. Hormonal and behavioral responses of male hamsters to females and female odors: roles of olfaction, the vomeronasal system, and sexual experience. Physiol. Behav. 1994, 55:129-138.
75. Ramm S.A., Cheetham S.A., Hurst J.L. Encoding choosiness: female attraction requires prior physical contact with individual male scents in mice. Proc. Biol. Sci. 2008, 275:1727-1735.
76. Roberts S.A., Simpson D.M., Armstrong S.D., Davidson A.J., Robertson D.H., McLean L., Beynon R.J., Hurst J.L. Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biol. 2010, 8:75.
77. Roberts S.A., Davidson A.J., McLean L., Beynon R.J., Hurst J.L. Pheromonal induction of spatial learning in mice. Science 2012, 338:1462-1465.
78. Rosenson L.M., Asheroff A.K. Maternal aggression in CD-1 mice: influence of the hormonal condition of the intruder. Behav. Biol. 1975, 15:219-224.
79. Sato A., Nakagawasai O., Tan-No K., Onogi H., Niijima F., Tadano T. Effect of non-selective dopaminergic receptor agonist on disrupted maternal behavior in olfactory bulbectomized mice. Behav. Brain Res. 2010, 210:251-256.
80. Schleidt W.M., Schleidt M., Magg M. Störung der Mutter-Kind-Beziehung bei Truthühnern durch Gehörverlust. Behaviour 1960, 16:254-260.
81. Scott J.P. Agonistic behavior of mice and rats: a review. Am. Zool. 1966, 6:683-701.
82. Seegal R.F., Denenberg V.H. Maternal experience prevents pup-killing in mice induced by peripheral anosmia. Physiol. Behav. 1974, 13:339-341.
83. Song C., Leonard B.E. The olfactory bulbectomised rat as a model of depression. Neurosci. Biobehav. Rev. 2005, 29:627-647.
84. Spehr M., Kelliher K.R., Li X.H., Boehm T., Leinders-Zufall T., Zufall F. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J. Neurosci. 2006, 26:1961-1970.
85. Stockley P., Bottell L., Hurst J.L. Wake up and smell the conflict: odour signals in female competition. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:20130082.
86. Stolzenberg D.S., Rissman E.F. Oestrogen-independent, experience-induced maternal behaviour in female mice. J. Neuroendocrinol. 2011, 23:345-354.
87. Stowers L., Dey S. Regulation of pheromone signaling by female hormones. ASAB and the Biochemical Society Joint Meeting "Behaviour Meets Biochemistry: Animals Making Sense of Molecules Making Scents" 2014, S008.
88. Stowers L., Holy T.E., Meister M., Dulac C., Koentges G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 2002, 295:1493-1500.
89. Svare B., Gandelman R. Suckling stimulation induces aggression in virgin female mice. Nature 1976, 260:606-608.
90. Svare B., Betteridge C., Katz D., Samuels O. Some situational and experiential determinants of maternal aggression in mice. Physiol. Behav. 1981, 26:253-258.
91. Svare B., Mann M., Broida J., Michael S. Maternal aggression exhibited by hypophysectomized parturient mice. Horm. Behav. 1982, 4:455-461.
92. Tachikawa K.S., Yoshihara Y., Kuroda K.O. Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. J. Neurosci. 2013, 33:5120-5126.
93. Vandenbergh J.G. Effects of central and peripheral anosmia on reproduction of female mice. Physiol. Behav. 1973, 10:257-261.
94. vom Saal F.S., Howard L.S. The regulation of infanticide and parental behavior: implications for reproductive success in male mice. Science 1982, 215:1270-1272.
95. Wang Z., Storm D.R. Maternal behavior is impaired in female mice lacking type 3 adenylyl cyclase. Neuropsychopharmacology 2011, 36:772-781.
96. Wang Z., Balet Sindreu C., Li V., Nudelman A., Chan G.C., Storm D.R. Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J. Neurosci. 2006, 26:7375-7379.
97. Wysocki C.J., Wellington J.L., Beauchamp G.K. Access of urinary nonvolatiles to the mammalian vomeronasal organ. Science 1980, 207:781-783.
98. Yang C., Delay R.J. Calcium-activated chloride current amplifies the response to urine in mouse vomeronasal sensory neurons. J. Gen. Physiol. 2010, 135:3-13.
99. Zhang J.X., Liu Y.J., Zhang J.H., Sun L. Dual role of preputial gland secretion and its major components in sex recognition of mice. Physiol. Behav. 2008, 95:388-394.
100. Zijlstra M., Bix M., Simister N.E., Loring J.M., Raulet D.H., Jaenisch R. Beta 2-microglobulin deficient mice lack CD4-8+ cytolytic T cells. Nature 1990, 344:742-746.