Acceleration of Puberty Onset in Female Mice by Male Urinary Odours: Chemosensory, Physiological and Neuroendocrine Mechanisms
Among many environmental factors, social factors, especially olfactory cues, can profoundly influence the timing of puberty onset. This is particularly well established in the house mouse (Mus musculus) where male urinary odours have been shown to accelerate puberty onset in prepubertal females. The urinary chemosignal(s) accelerate vaginal opening, the first oestrus and uterine growth, three parameters indicative of puberty onset. Several puberty-accelerating chemosignals, the majority of which are small volatile ligands bound to the major urinary proteins (MUPs), have been isolated from male urine; however when they are efficient, it is usually to a lower extent than male urine. These puberty-accelerating chemosignals are detected by the accessory olfactory system and the olfactory information is then transmitted to the hypothalamus. Among various potential neurological targets of the olfactory information, we focus on the hypothalamic neurons expressing neuropeptide kisspeptin, identified as a major regulator of the hypothalamic–pituitary–gonadal axis governing puberty onset. Preliminary results indicate that male odours seems to accelerate the structural changes usually observed in this neuronal population at puberty onset, thus suggesting that it could be a central hypothalamic relay of pheromonal information.
KeywordsLuteinizing Hormone GnRH Neuron Uterine Weight Main Olfactory Bulb Vaginal Opening
The experiments reported in this chapter were performed with the support of the French National Research Agency (ANR) grants: ANR-PHEROSEX, -MALE-EFFECT, -BIMUCE; Mélanie Jouhanneau is a PhD student supported by INRA PHASE Department and Région Centre. Matthieu Keller is a CNRS permanent research fellow.
- Castro BM (1967) Age of puberty in female mice: relationship to population density and the presence of adult males. An Acad Bras Cienc 39:289–292Google Scholar
- d’Anglemont de Tassigny X, Fagg LA, Dixon JP, Day K, Leitch HG, Hendrick AG, Zahn D, Franceschini I, Caraty A, Carlton MB, Aparicio SA, Colledge WH (2007) Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proc Natl Acad Sci U S A 104:10714–10719Google Scholar
- d’Anglemont de Tassigny X, Colledge WH (2010) The role of kisspeptin signaling in reproduction. Physiology 25:207–217Google Scholar
- Eisen EJ (1975) Influence of the male’s presence on sexual maturation, growth and feed efficiency of female mice. J Anim Sci 40:816–825Google Scholar
- Fullerton C, Cowley JJ (1971) The differential effect of the presence of adult male and female mice on the growth and development of the young. J Genet Psychol 3:179–189Google Scholar
- Khan A, Berger RG, Decatanzaro D (2009) Preputialectomised and intact adult male mice exhibit an elevated urinary ratio of oestradiol to creatinine in the presence of developing females, whilst promoting uterine and ovarian growth of these females. Reprod Fertil Dev 21:860–868PubMedCrossRefGoogle Scholar
- Liang H, Shi D (2007) Tactical reduction of copulatory competition: effects of male urine odour on maturation rates of Brandt’s voles, Lasiopodomys brandtii. Folia Zool Brno 56:144–152Google Scholar
- Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA (2005) Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci U S A 102:1761–1766PubMedCrossRefGoogle Scholar
- Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M (2004) Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 145:4565–4574PubMedCrossRefGoogle Scholar
- Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic, San DiegoGoogle Scholar
- Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H (2010) Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci 30:3124–3132PubMedCrossRefGoogle Scholar