Download PDF
Horm Metab Res 2014; 46(03): 211-218
DOI: 10.1055/s-0033-1363958
Endocrine Care
© Georg Thieme Verlag KG Stuttgart · New York

Circulating and Urinary Adrenal Corticosterone, Progesterone, and Estradiol in Response to Acute Stress in Female Mice (Mus musculus)

J. B. Thorpe
1   Department of Psychology, Neuroscience & Behaviour, McMaster University Hamilton, Ontario, Canada
,
K. E. Gould
1   Department of Psychology, Neuroscience & Behaviour, McMaster University Hamilton, Ontario, Canada
,
E. D. Borman
1   Department of Psychology, Neuroscience & Behaviour, McMaster University Hamilton, Ontario, Canada
,
D. deCatanzaro
1   Department of Psychology, Neuroscience & Behaviour, McMaster University Hamilton, Ontario, Canada
› Author Affiliations
Further Information

Publication History

received 19 July 2013

accepted 10 December 2013

Publication Date:
20 January 2014 (online)

Also available at
    Permissions and Reprints

Abstract

In studies of stress, it can be difficult to obtain blood rapidly enough to avoid confounding steroid measures. Noninvasive urinary steroid measures may provide an alternative insofar as they reflect systemic steroids. In Experiment 1, we profiled urinary corticosterone, progesterone, and estradiol in ovariectomized female mice following 1 h on an elevated platform. This increased urinary corticosterone for 3 h and progesterone for 4 h. In Experiment 2, blood and urine samples were obtained at 0–6 h following stressor offset. Females showed increased serum corticosterone and progesterone immediately after stressor offset. Urinary corticosterone was increased at both 0 and 2 h post-stress, while an increase in progesterone 2–6 h after stressor offset was not significant. Estradiol was not influenced by this mild stressor. In Experiment 3, mice were exposed to a more severe 1 h stressor, a rat across a wire-mesh grid. In serum, both corticosterone and progesterone were elevated immediately after stressor offset and returned to baseline within 2 h. In urine, this severe stressor elevated corticosterone immediately and 2 h after stressor offset, and in progesterone 2 h after stressor offset. Estradiol in serum was not dynamic, but it was significantly elevated in urine 4 h after stressor offset. Urinary measures generally reflected systemic measures; however, with a different time course resulting in a longer return to baseline. We suggest that the relative value of serum or urinary steroid measures in mice depends upon the experimental design, and that estradiol may only respond when the stressor is severe.

Key words

stress - corticosterone - progesterone - estradiol - serum - urine
 

  • References

  • 1 McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Horm Behav 2003; 43: 2-15
    CrossrefPubMedGoogle Scholar
  • 2 Korte SM, Koolhaus JM, Wingfield JC, McEwen BS. The Darwinian concept of stress: Benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci Biobehav R 2005; 29: 3-38
    CrossrefPubMedGoogle Scholar
  • 3 Sapolsky RM. The endocrine stress-response and social status in the wild baboon. Horm Behav 1982; 16: 279-292
    CrossrefPubMedGoogle Scholar
  • 4 Hargreaves AL, Hutson GD. The stress response in sheep during routine handling procedures. Appl Anim Behav Sci 1990; 26: 83-90
    CrossrefPubMedGoogle Scholar
  • 5 Nepomnaschy PA, Welch KB, McConnell DS, Low BS, Strassmann BI, England BG. Cortisol levels and very early pregnancy loss in humans. Proc Natl Acad Sci USA 2006; 103: 3938-3942
    CrossrefPubMedGoogle Scholar
  • 6 Young AJ, Carlson AA, Monfort SL, Russell AF, Bennett NC, Clutton-Brock T. Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc Natl Acad Sci USA 2006; 103: 12005-12010
    CrossrefPubMedGoogle Scholar
  • 7 Thorpe JB, Rajabi N, deCatanzaro D. Circadian rhythm and response to an acute stressor of urinary corticosterone, testosterone, and creatinine in adult male mice. Horm Metab Res 2012; 44: 429-435
    Article in Thieme ConnectPubMedGoogle Scholar
  • 8 Touma C, Palme R, Sachser N. Analyzing corticosterone metabolite in fecal samples of mice: A noninvasive technique to monitor stress hormones. Horm Behav 2004; 45: 10-22
    CrossrefPubMedGoogle Scholar
  • 9 Plas-Roser S, Aron C. Stress related effects in the control of sexual receptivity and the secretion of progesterone by the adrenals in cyclic female rats. Physiol Behav 1981; 27: 261-264
    CrossrefPubMedGoogle Scholar
  • 10 Resko JA. Endocrine control of adrenal progesterone secretion in the ovariectomized rat. Science 1969; 164: 71
    CrossrefPubMedGoogle Scholar
  • 11 Watson ED, Munro CD. Adrenal progesterone production in the cow. Brit Vet J 1984; 140: 300-306
    CrossrefPubMedGoogle Scholar
  • 12 Asher GW, Peterson AJ, Duganzich D. Adrenal and ovarian sources of progesterone secretion in young female fallow deer, Dama dama. J Reprod Fertil 1989; 85: 667-675
    PubMedGoogle Scholar
  • 13 Galea LM, McEwen BS, Tanapat P, Deak T, Spencer RL, Dhabhar FS. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997; 81: 689-697
    CrossrefPubMedGoogle Scholar
  • 14 Shors TJ, Pickett J, Wood G, Paczynski M. Acute stress persistently enhances estrogen levels in the female rat. Stress 1999; 3: 163-171
    CrossrefPubMedGoogle Scholar
  • 15 MacNiven E, deCatanzaro D, Younglai EV. Chronic stress increases estrogen and other steroids in inseminated rats. Physiol Behav 1992; 52: 159-162
    CrossrefPubMedGoogle Scholar
  • 16 Misdrahi D, Pardon MC, Perez-Diaz F, Hanoun N, Cohen-Salmon C. Prepartum chronic ultramild stress increases corticosterone and estradiol levels in gestating mice: Implications for postpartum depressive disorders. Psychiat Res 2005; 137: 123-130
    CrossrefPubMedGoogle Scholar
  • 17 Thorpe JB, Burgess PS, Sadkowski M, deCatanzaro D. Estrogen-progesterone balance in the context of blastocyst implantation failure induced by predator stress. Psychoneuroendocrinology 2013; 38: 3048-3056
    CrossrefPubMedGoogle Scholar
  • 18 Agrawal V, Jaiswal MK, Jaiswal YK. Lipopolysaccharide induces alterations in ovaries and serum level of progesterone and 17β-estradiol in the mouse. Fertil Steril 2011; 95: 1471-1474
    CrossrefPubMedGoogle Scholar
  • 19 Wood GE, Shors TJ. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. PNAS 1998; 95: 4066-4071
    CrossrefPubMedGoogle Scholar
  • 20 Gärtner K, Büttner D, Döhler K, Friedel R, Lindena J, Trautschold I. Stress response of rats to handling and experimental procedures. Lab Anim 1980; 14: 267-274
    CrossrefPubMedGoogle Scholar
  • 21 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
    CrossrefPubMedGoogle Scholar
  • 22 Vella ES, deCatanzaro D. Novel male mice show gradual decline in the capacity to disrupt early pregnancy and in urinary excretion of testosterone and 17β-estradiol during the weeks immediately following castration. Horm Metab Res 2001; 33: 681-686
    Article in Thieme ConnectPubMedGoogle Scholar
  • 23 deCatanzaro D, Muir C, Beaton E, Jetha M, Nadella K. Enzymeimmunoassay of oestradiol, testosterone and progesterone in urine samples from female mice before and after insemination. Reproduction 2003; 126: 407-414
    CrossrefPubMedGoogle Scholar
  • 24 Thorpe JB, deCatanzaro D. Oestradiol treatment restores the capacity of castrated males to induce both the Vandenbergh and the Bruce effects in mice (Mus musculus). Reproduction 2012; 143: 123-132
    CrossrefPubMedGoogle Scholar
  • 25 Touma C, Sachser N, Möstl E, Palme R. Effects of sex and time on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocr 2003; 130: 267-278
    CrossrefPubMedGoogle Scholar
  • 26 Viau V, Meaney MJ. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991; 129: 2503-2511
    CrossrefPubMedGoogle Scholar
  • 27 Khan A, Bellefontaine N, deCatanzaro D. Onset of sexual maturation in female mice as measured in behavior and fertility: interactions of exposure to males, phytoestrogen content of diet, and ano-genital distance. Physiol Behav 2008; 93: 588-594
    CrossrefPubMedGoogle Scholar
  • 28 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 29 Munro CJ, Stabenfeldt GH, Cragun JR, Addiego LA, Overstreet JW, Lasley BL. Relationship of serum estradiol and progesterone concentrations to the excretion profiles of their major urinary metabolites as measured by enzyme immunoassay and radioimmunoassay. Clin Chem 1991; 37: 838-844
    PubMedGoogle Scholar
  • 30 Haisenleder DJ, Schoenfelder AH, Marcinko ES, Geddis LM, Marshall JC. Estimation of estradiol in mouse serum samples: Evaluation of commercial estradiol immunoassays. Endocrinology 2011; 152: 4443-4447
    CrossrefPubMedGoogle Scholar
  • 31 Khan A, Berger RG, deCatanzaro D. The onset of puberty in female mice as reflected in urinary steroids and uterine/ovarian mass: Interactions of exposure to males, phyto-oestrogen content of diet, and ano-genital distance. Reproduction 2008; 135: 99-106
    CrossrefPubMedGoogle Scholar
  • 32 Beaton EA, Khan A, deCatanzaro D. Urinary sex steroids during sexual development in female mice and in proximate novel males. Horm Metab Res 2006; 38: 501-506
    Article in Thieme ConnectPubMedGoogle Scholar
  • 33 deCatanzaro D, Beaton EA, Khan A, Vella E. Urinary oestradiol and testosterone levels from novel male mice approach values sufficient to disrupt pregnancy in nearby inseminated females. Reproduction 2006; 132: 309-317
    CrossrefPubMedGoogle Scholar
  • 34 deCatanzaro D, Khan A, Berger RG, Lewis E. Exposure to developing females induces polyuria, polydipsia, and altered urinary levels of creatinine, 17β-estradiol, and testosterone in adult male mice (Mus musculus). Horm Behav 2009; 55: 240-247
    CrossrefPubMedGoogle Scholar
  • 35 Perkins LM, Payne AH. Quantification of P450scc, P45017α, and iron sulfur protein reductase in leydig cells and adrenals of inbred strains of mice. Endocrinology 1988; 123: 2675-2682
    CrossrefPubMedGoogle Scholar
  • 36 van Weerden WM, Biering HG, van Steenbrugge GJ, de Jong FH, Schröder FH. Adrenal glands of the mouse and rat do not synthesize androgens. Life Sci 1992; 50: 857-861
    CrossrefPubMedGoogle Scholar
  • 37 Tait AD, Hodge LC. Adrenal androgen biosynthesis by a sesterpene pathway. J Steroid Biochem 1998; 30: 485-488
    PubMedGoogle Scholar
  • 38 Touitou Y, Auzeby A, Bogdan A. Cortisol and cortisone production in rat and mouse adrenal incubations. J Steroid Biochem 1990; 37: 279-284
    CrossrefPubMedGoogle Scholar
  • 39 deCatanzaro D. Blastocyst implantation is vulnerable to stress-induced rises in endogenous estrogens and also to excretions of estrogens by proximate males. J Reprod Immunol 2011; 90: 14-20
    CrossrefPubMedGoogle Scholar
  • 40 Maruniak JA, Owen K, Bronson FH, Desjardins C. Urinary marking in male house mice: responses to novel environmental and social stimuli. Physiol Behav 1974; 12: 1035-1039
    CrossrefPubMedGoogle Scholar
  • 41 Levine R, Levine S. Role of the pituitary-adrenal hormones in the acquisition of schedule-induced polydipsia. Behav Neurosci 1989; 103: 621-637
    CrossrefPubMedGoogle Scholar