Vol.12, No. 1 53 Leptin Influences Ovarian Steroidogenesis/Spicer et al.
Endocrine, vol. 12, no. 1, 53–59, February 2000 0969–711X/00/12/1:53–59/$11.75 © 2000 by Humana Press Inc. All rights of any nature whatsoever reserved.
53
To test the hypothesis that leptin signals metabolic
information to the reproductive system in cattle by
directly affecting IGF-I-induced ovarian cell function,
granulosa and thecal cells from bovine ovarian follicles
were cultured for 2 d in serum-free medium with
added hormones. Recombinant human leptin at 30 and
300 ng/mL had no effect on basal thecal cell steroido-
genesis or thecal cell numbers. However, 300 but not
30 ng/mL of leptin attenuated (p < 0.05) luteinizing
hormone–induced androstenedione production by
24% in the absence of IGF-I and by 16% in the presence
of IGF-I. Leptin had no effect on IGF-I-induced estradiol
production in the presence of follicle-stimulating
hormone (FSH), but at 100 ng/mL, leptin inhibited
( p < 0.05) FSH plus IGF-I-induced progesterone pro-
duction and granulosa cell proliferation by 29 and 31%,
respectively. Leptin did not compete for
125
I-IGF-I bind-
ing to granulosa or thecal cells, whereas unlabeled IGF-I
did. In conclusion, leptin has weak inhibitory effects on
gonadotropin- and/or IGF-I-induced steroidogenesis of
thecal and granulosa cells.
Key Words: Leptin; granulosa cells; thecal cells;
steroidogenesis; cattle.
genetically obese (ob/ob) mice that lack endogenous leptin
are injected with leptin, they experience decreased food
intake, a loss in body weight, increased ovarian weight
and number of follicles, and correction of a sterility defect
(5–8,14,15). In mature cows, reproductive performance
decreases as body fat content decreases (16). The latter
observations indicate that leptin may have positive influences
on the reproductive system in mice and cattle. However, recent
in vitro evidence indicates that leptin may also have negative
effects on ovarian cell function (17–19).
Insulin-like growth factor-I (IGF-I) has long been known
to have direct effects on ovarian cell function in several
species including humans, rats, and cattle (20,21) . A
decrease in systemic IGF-I concentrations is associated
with the cessation of estrous cycles as cows are underfed to
become nutritionally anestrus (22). Conversely, increases
in systemic IGF-I concentrations are associated with the
resumption of estrous cycles as nutritionally anestrous cows
and prepubertal heifers are refed to gain weight (22,23).
Thus, IGF-I may be one hormone, in addition to leptin, that
communicates the metabolic status of an animal to the
reproductive system in cattle. We hypothesized that leptin
may directly influence IGF-I-stimulated ovarian follicular
function in cattle and conducted experiments to determine
the effect of leptin on IGF-I-induced proliferation and
steroidogenesis of bovine granulosa and thecal cells in vitro.
Results
Experiment 1
Experiment 1 was conducted to evaluate the dose-response
effect of leptin on basal and luteinizing hormone (LH)–
induced thecal cell proliferation and/or steroidogenesis. The-
cal cells from large ( 8 mm) follicles were cultured for 2 d in
10% fetal calf serum (FCS), and then cultured in serum-free
medium for an additional 2 d with or without 100 ng/mL of LH
in the presence of 0, 30, or 300 ng/mL of leptin. The doses
of LH and leptin were selected based on previous studies
(17,18,24,25). In the absence of leptin, LH increased (p < 0.05)
thecal cell progesterone (Fig. 1A) and androstenedione
(Fig. 1B) production by 2.5- and 3.5-fold, respectively. By
contrast, leptin had no effect (p > 0.10) on basal or LH-induced
progesterone (Fig. 1A) or on basal androstenedione (Fig. 1B)
Ovarian Action of Leptin
Effects on Insulin-Like Growth Factor-I–Stimulated Function of Granulosa and Thecal Cells
Leon J. Spicer, Connie S. Chamberlain, and Cristina C. Francisco
Department of Animal Science, Oklahoma State University, Stillwater, OK
Received September 24, 1999; Revised November 27, 1999; Accepted
December 2, 1999.
Author to whom all correspondence and reprint requests should be addressed:
Dr. Leon J. Spicer, Department of Animal Science, Oklahoma State
University, Stillwater, OK 74078. E-mail: igf1Leo@okstate.edu.
Introduction
Leptin, the recently identified adipose obese (ob) gene
product, is a plasma protein hormone that parallels the
amount of fat reserves in rodents and humans (1–4) and is
thought to regulate satiety (5–8). Whether systemic leptin
concentrations correlate with body fat in cattle remains to
be determined. The initial 167 amino acid sequence of leptin
is highly conserved (i.e., 83–97% homology) as is the 145
amino acid sequence (the secreted form) of leptin (84–97%
homology) across the four species (mouse, rat, human,
monkey) in which it has been characterized (9–13). If