269 Connexins in Sheep Ovaries/Grazul-Bilska et al. Vol. 8, No. 3
Received January 6, 1998; Revised February 18, 1998; Accepted March
5, 1998.
Author to whom all correspondence and reprint requests should be addressed:
Dr. Anna T. Grazul-Bilska, Cell Biology Center, 119b Hultz Hall, North
Dakota State University, Fargo, ND 58105. E-mail: grazul@plains.nodak.edu
Current Address: Dr. Albina Jablonka-Shariff, Dept. Obstetrics/Gynecology,
Washington University School of Medicine, St. Louis, MO 63110.
Endocrine, vol. 8, no. 3, 269–279, June 1998 0969–711X/98/8:269–279/$10.75 © 1998 by Humana Press Inc. All rights of any nature whatsoever reserved.
269
Gap Junctional Proteins, Connexin 26, 32,
and 43 in Sheep Ovaries Throughout the Estrous Cycle
Anna T. Grazul-Bilska,
1,2
Dale A. Redmer,
2
Jerzy J. Bilski,
1,2
Albina Jablonka-Shariff,
2
Vinayak Doraiswamy,
2
and Lawrence P. Reynolds
1,2
1
Cell Biology Center, Biotechnology Institute
and
2
Department of Animal and Range Sciences, North Dakota State University, Fargo, ND
Introduction
Ovarian follicles and corpora lutea (CL) are the most
rapidly growing normal tissues in adults that grow, differ-
entiate, and regress during each estrous cycle and/or preg-
nancy (1–4). Successful development of follicles to the
preovulatory stage and subsequent development of the CL
require cellular interactions among ovarian cells to coordi-
nate the functions of these diverse cell types that are prolif-
erating and differentiating extremely rapidly (1–7). Such
cellular interactions may be mediated by several mecha-
nisms, including humoral pathways as well as the contact-
dependent gap junctional pathway (8).
Gap junction-mediated intercellular communication has
been shown to be important for coordination of cellular
metabolism and function during growth and differentiation
of organs and tissues (9–13). Gap junctions are important
in signal transduction, and in transport of nutrients within
avascularized or poorly vascular tissues, such as the folli-
cular granulosa layer or corpora hemorrhagica, since gap
junctional channels allow for transfer of molecules
<1000 M
r
(7,8,12,14–20). Thus, during follicular develop-
ment, gap junctions are thought to be involved in regulating
differentiation and maturation of the cumulus–oocyte com-
plex (21–23). During development of CL, gap junctions
mediate cellular interactions, which may be important for
progesterone production and the luteolytic process (8,15).
Gap junctions are composed of hemichannels (connexons),
which consist of six-subunit proteins named connexins
(9,24). Distribution of connexins is tissue- and cell-specific
(9,24). Several connexins have been identified within ova-
rian tissues of numerous species (5,8,14,15,18,21,25–37).
The aim of the present study was to evaluate the pres-
ence of Cx26, Cx32, and Cx43 in ovine ovaries at several
stages of follicular and luteal development.
Results
Immunohistochemical staining demonstrated punctate
staining for Cx26, Cx32, and Cx43 in several compart-
ments of ovine ovaries throughout various stages of the
Ovarian follicles from days 13, 14, 15, and 16 and
corpora lutea (CL) from days 2, 4, 8, 12, and 15 of the
estrous cycle were evaluated for the presence of
connexins by immunohistochemistry. In addition, CL
from days 5, 10, and 15 of the estrous cycle were used
for immunofluorescent detection of Cx43 followed by
image analysis, and for Western immunoblot. In all
tissues, staining for all connexins appeared punctate,
indicating the presence of assembled gap junctions.
Cx26 was present in the ovarian surface epithelium,
stroma, and blood vessels within the stroma and hilus,
and in the CL. In healthy antral follicles, Cx26 was
present only in the theca layer, whereas Cx43 was
present in granulosa and theca layers. In the majority
of atretic follicles, connexins were not detected, but in
13% of the atretic follicles, Cx43 was present in the
theca layer. Cx32 was detected in the blood vessels of
ovarian stroma and in the CL, and Cx43 was detected
in the CL. Localization and/or expression of connexins
depended on stage of luteal development. Western
analysis demonstrated that expression of Cx32 in luteal
tissues was similar across the estrous cycle. The area
of positive staining for Cx43 and expression of Cx43 in
luteal tissues decreased (p < 0.05) as the estrous cycle
progressed. The pattern of expression of connexins
indicates that gap junctional proteins may be impor-
tant in the regulation of folliculogenesis and follicular
atresia, as well as growth, differentiation, and regres-
sion of the CL.
Key Words: Gap junctions; Cx26; Cx32; Cx43; follicles;
corpora lutea; ovaries; ewe.