Urinary Sex Steroids during Sexual Development in Female Mice and in Proximate Novel Males

Abstract

The experiments described here were designed to determine whether males' capacity to accelerate female pubertal development is reflected in females' urinary steroid levels in mice, and whether steroids in males' urine are influenced by exposure to developing females. In the first experiment, measures from urine collected daily from female mice aged 31-59 days showed a gradual rise in 17β-estradiol levels and a distinct linear rise in progesterone levels. In a second experiment, daily steroids were measured in females aged 30-42 days while they were either housed alone or underneath two novel outbred males. Females exposed to males showed accelerated development at day 43 in uterine weight, and to a lesser extent in ovarian and whole-body weights. Average steroid levels did not significantly differ between conditions, but intra-individual variance in estradiol measures was greater in male-exposed than in isolated females. Creatinine levels were higher in isolated females. Males exposed to developing females excreted higher levels of estradiol in their urine compared to isolated males. These data suggest that excreted steroids can reflect general pubertal development, but may not fully reflect substantial morphological impacts of exposure to novel males. Elevations of estrogen levels in males exposed to developing females could help to account for precocious puberty in such females.

17β-estradiol - ELISA - excretions - mice - non-invasive - estrous cycling - progesterone - puberty - urine - Vandenbergh effect

References

• 1 Vandenbergh JG. Effect of the presence of a male on the sexual maturation of female mice.  Endocrinology. 1967;  81 345-349
• 2 Vandenbergh JG. Male odor accelerates female maturation in mice.  Endocrinology. 1969;  84 658-660
• 3 Bronson FH, Desjardins C. Circulating concentrations of FSH, LH, estradiol and progesterone associated with acute male-induced puberty in female mice.  Endocrinology. 1974;  94 1658-1668
• 4 Bronson FH, Stetson MH. Gonadotrophin release in prepubertal female mice following male exposure: a comparison with an adult cycle.  Biol Reprod. 1973;  9 449-459
• 5 Feder HH. Estrous cyclicity in mammals. In: Adler NT (Ed.) Neuroendocrinology of Reproduction New York: Plenum Press 1981: 279-348
• 6 Drickamer LC. Sexual maturation of female house mice: social inhibition.  Devel Psychobiol. 1974;  7 257-265
• 7 Vandenbergh JG, Drickamer LC, Colby DR. Social and dietary factors in the sexual maturation of female mice.  J Reprod Fertil. 1972;  28 397-405
• 8 Vandenbergh JG. Acceleration of sexual maturation in female rats by male stimulation.  J Reprod Fertil. 1976;  46 451-453
• 9 Whitten WK. Modification of the estrous cycle of the mouse by external stimuli associated with the male.  J Endocrinol. 1956;  13 399-404
• 10 Diamond M. Intromission pattern and species vaginal code in relation to induction of pseudopregnancy.  Science. 1970;  169 995-997
• 11 Komisaruk BR, Steinman JL. Genital stimulation as a trigger for neuroendocrine and behavioural control of reproduction.  An NY Acad Sci. 1986;  474 64-74
• 12 deCatanzaro D, MacNiven E. Psychogenic pregnancy disruptions in mammals.  Neurosci Biobehav Rev. 1992;  16 43-53
• 13 deCatanzaro D, Muir C, Beaton E, Jetha M, Nadella K. Enzymeimmunoassay of estradiol, testosterone and progesterone in urine samples from female mice before and after insemination.  Reproduction. 2003;  126 407-414
• 14 deCatanzaro D, Muir C, Beaton EA, Jetha M. Non-invasive repeated measurement of urinary progesterone, 17β-estradiol, and testosterone in developing, cycling, pregnant, and postpartum female mice.  Steroids. 2004;  69 687-696
• 15 Muir C, Vella ES, Pisani N, deCatanzaro D. Enzyme immunoassay of 17β-estradiol, estrone conjugates, and testosterone in urinary and fecal samples from male and female mice.  Horm Metab Res. 2001;  33 653-658
• 16 Bailey KJ. Diurnal progesterone rhythms in the female mouse.  J Endocrinol. 1987;  112 15-21
• 17 Michael SD. Plasma prolactin and progesterone during estrous cycle in the mouse.  Proc Soc Exper Biol Med. 1976;  153 254-257
• 18 Bronson FH. Male-induced precocial puberty in female mice: confirmation of the role of estrogen.  Endocrinology. 1975;  96 511-514
• 19 Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA, Bazer FW, Spencer TE. Developmental biology of uterine glands.  Biol Reprod. 2001;  65 1311-1323
• 20 Beaton EA, deCatanzaro D. Novel males' capacity to disrupt early pregnancy in mice (Mus musculus) is attenuate via a chronic reduction of males' urinary 17β-estradiol.  Psychoneuroendocrinology. 2005;  30 688-697
• 21 Reynolds E. Urination as a social response in mice.  Nature. 1971;  234 481-483
• 22 Weber WW, Grossman M, Thom JV, Sax J, Chan JJ, Duffy MP. Drug contamination with diethylstilbestrol. Outbreak of precocious puberty due to contaminated isonicocinic acid hydrazide (INH).  New Eng J Med. 1963;  268 411-415
• 23 Ogasawara Y, Okamoto S, Kitamura Y, Matsumoto K. Proliferative pattern of uterine cells from birth to adulthood in intact, neonatally castrated and/or adrenalectomized mice, assayed by incorporation of [125I] iododeoxyuridine.  Endocrinology. 1983;  113 582-587
• 24 Kahlert S, Nuedling S, van Eickels M, Vetter H, Meyer R, Grohé C. Estrogen receptor α rapidly activates the IGF-1 receptor pathway.  J Biol Chem. 2000;  275 18447-18453
• 25 Leung KC, Johannsson G, Leong GM, Ho KKY. Estrogen regulation of growth hormone action.  Endocrinology. 2004;  25 693-721
• 26 Sato T, Wang G, Hardy M, Kurita T, Cunha GR, Cooke P. Role of systemic and local IGF-1 in the effects of estrogen on growth and epithelial proliferation of mouse uterus.  Endocrinology. 2002;  143 2673-2679
• 27 Brain PF. 1975 What does individual housing mean to a mouse?.  Life Sci. 1975;  16 187-200
• 28 Drickamer LC. Rates of urine excretion by house mouse (Mus domesticus): differences by age, sex, social status, and reproductive condition.  J Chem Ecol. 1995;  21 1481-1493
• 29 Alessio L, Berlin A, Dell'Orto A, Toffoletto F, Ghezzi I. Reliability of urinary creatinine as a parameter used to adjust values of urinary biological indicators.  Int Arch Occup Envir Health. 1985;  55 99-106
• 30 Greenberg GN, Levine RJ. Urinary creatinine excretion is not stable: a new method for assessing toxic substance concentrations.  J Occup Med. 1989;  31 832-838

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