Skip to main content
SpringerLink
Log in

Stimulation of Estrus in Female Mice by Male Urinary Proteins

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Stimulation of estrus in adult female mice was obtained with major urinary proteins (MUPs) with the natural volatile ligands bound. The MUP threshold concentration for this effect was about 1.8 mg/ml. MUPs without the ligands bound, as purified by organic extraction of hydrophobic compounds, stimulated estrus in mice only when dissolved in carrier urine of juvenile or castrated adult male mouse or ovariectomized female mouse. They did not stimulate estrus when dissolved in water. Mice that had the vomeronasal organ removed were insensitive to MUPs. It is concluded that MUPs are an integral part of the mouse male pheromones that stimulate hormonal activity in females and that the vomeronasal system is involved in the estrus-stimulating effect of the major urinary proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  • Bacchini, A., Geatani, E., and Cavaggioni, A. 1992. Pheromone binding protein of the mouse, Mus musculus. Experientia 48:419-421.

    Google Scholar 

  • Bellringer, J. F., Pratt, H., and Keverne, E. B. 1980. Involvement of the vomeronasal organ and prolactin in pheromonal induction of delayed implantation in mice. J. Reprod. Fertil. 59:223-228.

    Google Scholar 

  • BÖCskei, Z., Groom, C. R., Flower, D. R., Wright, C. E., Phillips, S. E. V., Cavaggioni, A., Findlay, J. B. C., and North, A. C. T. 1992. Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography. Nature 360:186-188.

    Google Scholar 

  • Brennan, P. A., Schellinck, H. M., and Keverne, E. B. 1999. Patterns of expression of the immediate-early gene egr-1 in the accessory olfactory bulb of female mice exposed to pheromonal constituents of male urine. Neuroscience 90:1463-1470.

    Google Scholar 

  • Bronson, F. H., and Whitten, W. K. 1968. Oestrus accelerating pheromone of mice: assay, androgen-dependence and presence in bladder urine. J. Reprod. Fertil. 15:131-134.

    Google Scholar 

  • Bruce, H. M. 1959. An exteroreceptive block to pregnancy in the mouse. Nature 184:105.

    Google Scholar 

  • Cavaggioni, A., Sorbi, R. T., Keen, J. N., Pappin, D. J. C., and Findlay, J. C. B. 1987. Homology between the pyrazine-binding protein from nasal mucosa and urinary proteins. FEBS Lett. 2:225-228.

    Google Scholar 

  • Cavaggioni, A., Findlay, J. B., and Tirindelli, R. 1990. Ligand binding characteristics of homologous rat and mouse urinary proteins and pyrazine-binding protein of the calf. Comp. Biochem. Physiol. 96B:513-520.

    Google Scholar 

  • Clark, A. J., Clissold, P. M., and Bishop, J. O. 1982. Variation between mouse major urinary protein genes isolated from a single inbred line. Gene 18:221-230.

    Google Scholar 

  • Clissold, P. M., and Bishop, J. O. 1982. Variation in the mouse major urinary protein (MUP) genes and the MUP gene products within and between inbred lines. Gene 18:211-220.

    Google Scholar 

  • Ferrari, E., Lodi, T., Sorbi, R. T., Tirindelli, R., Cavaggioni, A., Spisni, A. 1977. Expression of a lipocalin in Pichia pastoris: Secretion, purification and binding activity of a recombinant mouse major urinary protein. FEBS Lett. 401:73-77.

    Google Scholar 

  • Finlayson, J. S., Potter, Shinnick, C. S., and Smithies, O. 1974. Components of the major urinary protein complex of inbred mice: determination of NH2-terminal sequences and comparison with homologous components from wild mice. Biochem. Genet. 11:325-335.

    Google Scholar 

  • Flower, D. R. 1994. The lipocalin protein family: a role in cell regulation. FEBS Lett. 354:7-11.

    Google Scholar 

  • Flower, D. R., North, A. C. T., and Attwood, T. K. 1993. Structure and sequence relationships in the lipocalins and related proteins. Protein Sci. 2:753-761.

    Google Scholar 

  • Ghazal, P., Clark, A. J., and Bishop, J. O. 1985. Evolutionary amplification of a pseudogene. Proc. Natl. Acad. Sci. U.S.A. 82:4182-4185.

    Google Scholar 

  • Hoover, J. E., and Drickamer, L. C. 1979. Effect of urine from pregnant and lactating female house mice on oestrous cycles of adult females. J. Reprod. Fertil. 55:297-301.

    Google Scholar 

  • Hurst, J. L., Robertson, D. H. L., Tolladay, U., and Beynon, R. J. 1998. Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim. Behav. 55:1289-1297.

    Google Scholar 

  • Jemiolo, B., Harvey, S., and Novotny, M. 1986. Promotion of the Whitten effect in female mice by synthetic analogs of male urinary constituents. Proc. Natl. Acad. Sci. U.S.A. 83:4576-4579.

    Google Scholar 

  • Jemiolo, B., Andreolini, F., Wiesler, D., and Novotny, M. 1987. Variations in mouse (Mus musculus) urinary volatiles during different periods of pregnancy and lactation. J. Chem. Ecol. 13:1941-1956.

    Google Scholar 

  • Johnson, D., Al-Shawi, R., and Bishop, J. O. 1995. Sexual dimorphism and growth hormone induction of murine pheromone binding proteins. J. Mol. Endocrinol. 14:21-34.

    Google Scholar 

  • Kuhn, N. J., Woodwort-Gutai, H., Gross, K. W., and Held, W. A. 1984. Subfamilies of the mouse major urinary protein (MUP) multi-gene family: Sequence analysis of cDNA clones and differential regulation by the liver. Nucleic Acids Res. 12:6073-6090.

    Google Scholar 

  • Lomas, D. E., and Keverne, E. B. 1982. Role of the vomeronasal organ and prolactin in the acceleration of puberty in female mice. J. Reprod. Fertil. 66:101-107.

    Google Scholar 

  • Marchese, S., Pes, D., Scaloni, A., Carbone, V., and Pelosi, P. 1998. Lipocalins of boar salivary glands binding odours and pheromones. Eur. J. Biochem. 252:563-568.

    Google Scholar 

  • Marchlewska-Koj, A. 1977. Pregnancy block elicited by urinary proteins of male mice. Biol. Reprod. 17:729-732.

    Google Scholar 

  • Marchlewska-Koj, A., and Kruczek, M. 1986. Acceleration and suppression of oestrous cycle in mice by pheromones: The lights effect. Folia Biol. (Crac.) 34:221-226.

    Google Scholar 

  • Marchlewska-Koj, A., Kruczek, M., and Tach, E. 1983. Suppression of estrous cycle of female mice by ovariectomized females. Horm. Behav. 17:233-236.

    Google Scholar 

  • Marchlewska-Koj, A., Pochron, E., and Sliwowska, A. 1990. Salivary glands and preputial glands of males as source of estrus-stimulating pheromone in female mice. J. Chem. Ecol. 16:2817-2822.

    Google Scholar 

  • Marchlewska-Koj, A., Pochrone, E., Galewicz-Sojecka, A., and Galas, J. 1994. Suppression of estrus in female mice by the presence of conspecifics or by foot shock. Physiol. Behav. 55:317-321.

    Google Scholar 

  • Miyawaki, A., Matsushuta, F., Ryo, Y., and Mikoshiba, K. 1994. Possible pheromone-carrier of two lipocalin proteins in the vomeronasal organ. The EMBO J. 13:5835-5842.

    Google Scholar 

  • Moss, R. L., Flynn, R. E., Shen, X.-M., Shi, J., and Novotny, M. 1997. Urinary-derived compound evokes membrane responses in mouse vomeronasal receptor neurons. J. Neurophysiol. 77:2856-2862.

    Google Scholar 

  • Mucignat-Caretta, C., Caretta, A., and Cavaggioni, A. 1995. Acceleration of puberty onset in female mice by male urinary proteins. J. Physiol. 486:517-522.

    Google Scholar 

  • Novotny, M., Jemiolo, B., and Harvey, S. 1990. Chemistry of rodent pheromones: Molecular insights into chemical signalling in mammals, pp. 1-22, in D. W. Macdonald, D. Müller-Schwarze, and S. E. Natynczuch(eds.). Signals in Vertebrates, Vol. 5. Oxford University Press, New York.

    Google Scholar 

  • Novotny, M., Ma, W., Zidek, L., and Daev, E. 1999. Recent biochemical insights into puberty acceleration, estrus induction and puberty delay in the house mouse, pp. 99-116, in R. E. Johnston, D. Müller-Schwarze, and A. Sorensen (eds.). Advances in Chemical Communication in Vertebrates. vol. VIII. Plenum Press, New York.

    Google Scholar 

  • Robertson, D. H. L., Beynon, R. J., and Evershed, R. P. 1993. Extraction, characterization, and binding analysis of two pheromonally active proteins of the house mouse (Mus musculus). J. Chem. Ecol. 19:1405-1416.

    Google Scholar 

  • Robertson, D., Hurst, J., Hubbard, S., Gaskell, S. J., and Beynon, R. 1998. Ligands of urinary lipocalins from the mouse: Uptake of environmentally derived chemicals. J. Chem. Ecol. 24:1127-1140.

    Google Scholar 

  • Sansom, C. E., North, A. C. T., and Sawyer, L. 1994. Structural analysis and classification of lipocalins and related proteins using a profile-search method. Biochim. Biophys. Acta 1208:247-255.

    Google Scholar 

  • Schwende, F., Wiesler, D., Jorgenson, J. W., Cormack, M., and Novotny, M. 1986. Urinary volatiles constituents of the house mice (Mus musculus). J. Chem. Ecol. 12:277-295.

    Google Scholar 

  • Shahan, K., Gilmartin, M., and Derman, E. 1987. Nucleotide sequences of liver, lacrimal, and submaxillary gland mouse major urinary protein in RNAs: Mosaic structure and construction of panel of gene-specific synthetic oligonucleotide probes. Mol. Cell Biol. 7:1938-1946.

    Google Scholar 

  • Shaw, P. H., Held, W. A., and Hasting, N. D. 1983. The gene family of MUP: Expression in several secretory tissues of mouse. Cell 32:755-761.

    Google Scholar 

  • Vandenbergh, J. G. 1967. Effect of presence of a male on the sexual maturation of female mice. Endocrinology 81:345-349.

    Google Scholar 

  • Vandenbergh, J. G., Whitsett, J., and Lombardi, J. R. 1975. Partial isolation of a pheromone accelerating puberty in female mice. J. Reprod. Fertil. 43:515-523.

    Google Scholar 

  • Whitten, W. K. 1956. Modification of oestrous cycle of the mouse by external stimuli associated with the male. J. Endocrinol. 13:399-404.

    Google Scholar 

  • Wysocki, C. J., Kruczek, M., Wysocki, L., and Lepri, J. J. 1991. Activation of reproduction in nulliparous and primiparous voles is blocked by vomeronasal organ removal. Biol. Reprod. 45:611-616.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Environmental Sciences, Jagiellonian University, Ingardena 6, 30-060, Krakow, Poland

    Anna Marchlewska-Koj

  2. Dipartimento di Anatomia e Fisiologia Umana, Università di Padova, 35100, Padova, Italy

    Andrea Cavaggioni & Carla Mucignat-Caretta

  3. Institute of Environmental Sciences, Jagiellonian University, Ingardena 6, 30-060, Krakow, Poland

    Paweł Olejniczak

Authors
  1. Anna Marchlewska-Koj
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Cavaggioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carla Mucignat-Caretta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paweł Olejniczak
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marchlewska-Koj, A., Cavaggioni, A., Mucignat-Caretta, C. et al. Stimulation of Estrus in Female Mice by Male Urinary Proteins. J Chem Ecol 26, 2355–2366 (2000). https://doi.org/10.1023/A:1005578911652

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005578911652

Search

Navigation