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Physiology

Ovarian estradiol supports sexual behavior but not energy homeostasis in female marmoset monkeys

International Journal of Obesity volume 43, pages 1034–1045 (2019)Cite this article

Subjects

Abstract

Objective

In adult female rodents, ovarian estradiol (E2) regulates body weight, adiposity, energy balance, physical activity, glucose-insulin homeodynamics, and lipid metabolism, while protecting against diet-induced obesity. The same E2 actions are presumed to occur in primates, but confirmatory studies have been lacking.

Methods

We investigated the consequences of ovariectomy (OVX) and E2 replacement in female marmoset monkeys on major metabolic and morphometric endpoints. Sexual behavior and uterine diameters were assessed as positive controls for E2 treatment efficacy. Metabolic parameters were measured 1 mo prior to OVX, and 3 and 6 mo thereafter. During OVX, animals received empty or E2-containing silastic s.c. implants. To test the interaction between E2 and diet, both treatment groups were assigned to either a higher fat diet (HFD) or a low-fat diet (LFD).

Results

As anticipated, OVX animals exhibited diminished frequency (p = 0.04) of sexually receptive behavior and increased rejection behavior (p = 0.04) toward their male partners compared with E2-treated OVX females. OVX also decreased (p = 0.01) uterine diameter. There were no treatment effects on total caloric intake. There were no significant effects of OVX, E2 treatment, or diet on body weight, body composition, energy expenditure, physical activity, fasting glucose, or glucose tolerance. Regardless of E2 treatment, serum triglycerides were higher (p = 0.05) in HFD than LFD females. Postmortem qPCR analysis of hypothalamic tissues revealed higher mRNA expression (p < 0.001) for PGR in E2-treated monkeys versus OVX controls regardless of diet, but no differences between groups in other selected metabolic genes. In contrast, regardless of E2 treatment, there was a decreased mRNA expression of PGC1α (PPARGC1A), HTR1A, and HTR5A in HFD compared with LFD females.

Conclusions

Our findings, overall, document a greatly diminished role for ovarian E2 in the metabolic physiology of a female primate, and encourage consideration that primates, including humans, evolved metabolic control systems regulated by extra-ovarian E2 or are generally less subject to E2 regulation.

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Author notes

  1. These authors contributed equally: Marissa Kraynak, Ricki J. Colman

Authors and Affiliations

  1. Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA

    Marissa Kraynak, Ricki J. Colman, Matthew T. Flowers, David H. Abbott & Jon E. Levine

  2. Endocrinology and Reproductive Physiology Training Program, University of Wisconsin-Madison, Madison, WI, USA

    Marissa Kraynak

  3. Department of Cell and Regenerative Biology, University of Wisconsin-Madison, Madison, WI, USA

    Ricki J. Colman

  4. Department of Neuroscience, University of Wisconsin-Madison, Madison, WI, USA

    Matthew T. Flowers & Jon E. Levine

  5. Department of Obstetrics and Gynecology, University of Wisconsin-Madison, Madison, WI, USA

    David H. Abbott

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Correspondence to Jon E. Levine.

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Kraynak, M., Colman, R.J., Flowers, M.T. et al. Ovarian estradiol supports sexual behavior but not energy homeostasis in female marmoset monkeys. Int J Obes 43, 1034–1045 (2019). https://doi.org/10.1038/s41366-018-0156-4

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