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Innervation and gap junction formation in the myometrium of pregnant little brown bats Myotis lucifugus.

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THE ANATOMICAL RECORD 221~611-618(1988)
Innervation and Gap Junction Formation in the
Myometrium of Pregnant Little Brown Bats,
Myotis lucifugus
G.D. BUCHANAN, R.E. GARFIELD, AND E.V. YOUNGLAI
School of Nursing (G.D.B.)and Departments of Neurosciences (R.E.G.) and Obstetrics and
Gynecology (R.E. G., E. V Y), Faculty of Health Sciences, McMaster University, Hamilton,
Ontario, Canada L8N 325
ABSTRACT
Pregnant Myotis lucifugus were captured in mist nets set outside a
large maternity colony and, in most cases, were examined 12-15 hours later. Anterior and posterior halves of uteri were pinned to dental wax and either incubated in
glyoxylic acid to produce adrenergic nerve fluorescence, or fixed in buffered glutaraldehyde for electron microscopy. Blood was collected for radioimmunoassay of
plasma progesterone. We found no evidence of decreased nerve fluorescence even in
late pregnancy when plasma progesterone levels were 10-20 times preovulatory
values. Ultrastructural examination also showed no evidence of damage to, or
destruction of, nerves in the myometrium. However, we did find gap junctions
between myometrial muscle cells during the periparturient period in both normal
and aborting bats. Gap junctions began to form several days before term, increased
in number until parturition, then decreased dramatically within a day or two
thereafter. The percentage of muscle cell plasma membrane involved in gap junction
formation was closely correlated with plasma progesterone levels, although whether
this is causal or coincidental is not certain.
These data do not agree with the conclusions drawn from observations in other
mammals that a disappearance of adrenergic nerves from the myometrium is associated with the initiation of parturition, or that gap junction formation is associated
with changes in nerve function. They do, however, lend further support to the
hypothesis that there is neurogenic control of myometrial contractility in M. lucifugus uteri at term.
A variety of roles have been ascribed to myometrial
contractility during the reproductive cycle, including
sperm transport (Austin, 1974) and positioning of the
conceptus at the implantation site (Boving, 1972), and
expulsion of the uterine contents at parturition (Huszar
and Roberts, 1982). Whereas myometrial function during parturition has been much studied, the factors governing this extraordinarily well organized process are
incompletely understood (Liggins, 1979; Csapo, 1981).
Hypophyseal hormones, ovarian hormones, and prostaglandins modulate myometrial activity (Fuchs, 19781,
but earlier studies indicated that neurogenic modulation was either absent or minimal (Reynolds, 1965).Certainly central nervous control is not essential, since
neither uterine denervation nor spinal cord section prevents parturition (Bell, 1972). However, these procedures do not interrupt postganglionic neurons
originating in the paracervical ganglion of Frankenhauser (Thorbert, 1978). Since these and other neurons are
affected by steroid hormones, it is possible that they
play some intermediary role in the control of myometrial contractility (Owman, 1981).There is also evidence
that autonomic nerves to the female reproductive tract
affect cyclic variation in gonadotropins and steroid hormones (Burden et al., 1981).
0 1988 ALAN R. LISS, INC
In several mammalin species, the uterus is innervated
primarily by postganglionic, adrenergic neurons that
are in close association with blood vessels and myometrial muscle cells (Marshall, 1981; Owman et al., 1986).
Cholinergic innervation is relatively sparse and also
associated with blood vessels and myometrial cells
(Papka et al., 1985; Garfield, 1986).Extensive studies in
the guinea pig (see Owman, 1981) by ultrastructural,
histofluorescent, and biochemical methods show that
adrenergic nerves disappear from the uterus during late
pregnancy. In reviewing these, as well as studies from
other species, Marshall (1981) concluded that the data
collectively suggested a local degeneration of adrenergic
axons in the uterus at term. Whereas loss of adrenergic
nerves may explain in part increased myometrial contractility at term, it does not explain the high degree of
coordinated activity during parturition. There is increasing evidence, however, that gap junctions play a
significant role in myometrial coordination by converting the myometrium into a functional syncytium. Gap
Received February 27,1987; accepted November 24,1987.
Address reprint requests to Dr. G. Dale Buchanan, Faculty of Health
Room 2532, HamSciences, McMaster University, 1200 Main St. W.,
ilton, Ontario, Canada L8N 325.
612
G.D. BUCHANAN ET AL.
junctions are rarely found among myometrial smooth
muscle cells except in the periparturient period, whether
this be at term or premature (Garfield, 1985). Thus,
there is an inverse relationship between disappearance
of adrenergic nerve fibers and appearance of gap junctions in the myometrium. However, whether these
events are causally related or simply represent correlated responses to some other, possibly hormonal change
is not entirely clear.
To our knowledge, myometrial ultrastructure has not
been examined in bats except for our earlier study of
hibernating, nonpregnant Myotis lucifugus, the common
little brown bat (Buchanan and Garfield, 1984).We found
the myometrium to be densely supplied by adrenergic
nerve fibers with axonal varicosities closely associated
with smooth muscle cells as well as blood vessels. Nonadrenergic nerve fibers were mostly associated with
blood vessels; however, 10-15% of axonal varicosities
found in close relation to myometrial muscle contained
small agranular (presumptive cholinergic)secretory vesicles. Injection of estradiol, progesterone, or both did not
alter the appearance of adrenergic fibers or elicit gap
junction formation. Injection of 6-hydroxydopamine,
which depletes catecholamine stores and damages adrenergic nerves (Kostrzewa and Jacobowitz, 1974), did
produce evidence of nerve damage but did not elicit gap
junction formation. Based on these results, we speculated that neurogenic control of the myometrium might
be relatively more important in bats than in the other
species that have been studied. In the present study, we
examined myometria of M. lucifugus during pregnancy,
at parturition, and while undergoing abortion. The results show no evidence of neuronal loss or degeneration
in late pregnancy even when gap junctions are present,
and further support the hypothesis of a neurogenic modulation of the myometrium of M. Zucifugus.
MATERIALS AND METHODS
Animals and Tissues
Pregnant Myotis lucifugus lucifugus were captured in
mist nets set outside a large maternity roost at Red Bay,
Ontario (lat. 44"48'N), brought to Hamilton in small
wooden cages (supplied with water), and usually examined the next morning. Bats kept for more than 24 hours
were maintained in a warm (28-30°C) room and fed
mealworms (Tenebrio molitor larvae) daily. Before autopsy, bats were weighed and then sacrificed by cervical
fracture. The thoracic cavity was opened quickly and
blood was collected from the pectoral and subclavian
veins in heparinized capillary tubes. Reproductivetracts
and adnexa were excised and photographed, after which
uteri were divided into dorsal and ventral halves and
processed as described previously (Buchanan and Garfield, 1984). Briefly, tissues were spread and pinned to
dental wax serosal side down and then incubated as
outlined below. Equal numbers of anterior and posterior
halves were allocated to each procedure.
Histofluorescence
Spread tissues were incubated for 30 minutes at 4°C
in a solution of 2.0 gm glyoxylic acid, 0.92 gm HEPES
buffer, and 37 gm sucrose per 100 ml at pH 7.4. Glyoxylic
acid reacts with catecholamines and, in the absence of
water, produces a bright fluorophore considered specific
for adrenergic nerves (Llewellyn-Smithet al., 1981; Tsu-
kahara et al., 1982). Incubated tissues were partly dried
in a cool air stream, transferred to glass slides, and dried
for 1-2 hours. Dried tissues were incubated at 100°Cfor
4 minutes, mounted in mineral oil under glass coverslips, and examined on a Zeiss Large Universal fluorescent microscope equipped with an epifluorescent
condenser (IIIRS),a BP43615 excitation filter, an LP473
barrier filter, and a 460 beam splitter.
To estimate nerve density, photomicrographs of fluorescent nerves were printed at a magnification of 495 x
such that each photograph represented 0.17 mm2 of
uterine wall. A grid containing 84 lines, 2 cm long, and
2 cm apart on the transverse and vertical axes was
placed over the photograph and the number of intersects
of fluorescent fibers with grid lines counted. Total uterine surface area was estimated by measuring the long
and short dimensions of the uterus from photographs
taken at autopsy and substituting one-half their mean
value (r)in the formula 47r? (surface of a sphere).
Electron Microscopy
To minimize distortion and intersample variation due
to preparatory procedures, tissues were incubated in
Kreb's buffer (pH 7.4) containing 0.05 mM pargyline for
1hour at 37°C before fixation. Pargyline (Sigma Chemicals, St. Louis, MO), a monoamine oxidase inhibitor,
prevents breakdown of norepinephrine during incubation. Incubated tissues were fixed in cacodylate-buffered
glutaraldehyde, postfixed in osmium tetroxide, stained
en bloc with many1 acetate, and embedded in Spurrresin. Sections were cut with a diamond knife, mounted
on 200-mesh grids, stained with lead acetate, and examined in a Philips 301 transmission electron microscope. Gap junctions were quantitated by the method of
Puri and Garfield (1982).
Plasma Progesterone
Blood samples were spun for 10 minutes in a microhematocrit centrifuge and plasma samples were frozen
at -20°C until assayed. Progesterone content of individual plasma samples was determined by radioimmunoassay using an antibody produced in rabbits against
progesterone-11-a-hemisuccinyl-bovine
serum albumin,
and (l,23H) progesterone as the labeled ligand. Details
of the assay procedure are described elsewhere (Buchanan and Younglai, 1986).
RESULTS
Uterine Appearance
Like other holarctic vespertilionid bats, Myotis Zucifugus completes folliculogenesis and mates before entering hibernation, but ovulation and fertilization are
postponed until 1-3 days after arousal the next spring.
Pregnancy lasts approximately 8 weeks and can be divided into 5 stages recognizable by uterine shape and
width (Buchanan and Younglai, 1986). Whereas the
lengths of Stages I and I1 have been established (Buchanan, 1987), the time period given below for later
stages are approximations derived from periodic field
collections. In Stage I (preimplantation, days 1-10], uteri
may show slight hyperemia and edema, but do not differ
from preovulatory uteri in shape or width (4 mm). In
Stage I1 (early implantation, days 10-14), the right uterine horn becomes highly domed antimesometrially. During Stage I11 (embryogenesis, weeks 3 and 4), uteri
GAP JUNCTIONS AND NERVES IN PREGNANT BAT MYOMETRIA
increase from 4 to 7 mm wide and the right uterine horn
becomes ovoid, but the left horn is still distinct. Uterine
width increases to 12 mm during Stage IV (early fetal
period, weeks 5 and 6) and the entire uterus becomes
smoothly ovoid as the left horn is incorporated into the
uterine wall (Fig. 1). Growth is quite rapid in Stage V
(late fetal period, weeks 7 and 8)and the thinly stretched
uterine wall begins to conform to the fetal contours (Fig.
2). Uterine width will reach 21-23 mm at term.
Fluorescent Microscopy
Examination of uterine preparations incubated in gyloxylic acid showed an extensive retiform pattern of
adrenergic nerve fibers with numerous axonal varicosities. There were no differences in either nerve density
or fluorescence between mesometrial and antimesometrial or dorsal and ventral regions. At midpregnancy
(Fig. 31, nerve density-the number of nerve fibers per
unit area-did not appear to differ from nerve density in
earlier specimens. However, in uteri near term (Fig. 41,
nerve density was somewhat reduced, although fluorescence of individual fibers was not detectably changed.
Computation of nerve fiber intersects with a standard
grid (Table 1)confirm that nerve density was, indeed,
statistically less in term uteri. However, the increase in
uterine surface area during pregnancy more than offsets
this decrease in density. In fact, computation of nerve
fiber intersects per entire uterus yields the implausible
result that there were severalfold more nerve fibers at
term than during early pregnancy.
Electron Microscopy
Numerous unmyelinated axons were found in close
association with smooth muscle cells of the myometrium
during pregnancy (Fig. 5) and at term (Fig. 6). The
majority of the axons bore varicosities containing small
(c. 50 nm diam) dense-cored neurosecretory vesicles (Fig.
7), which are considered indicative of adrenergic nerves.
When pregnant bats (early Stage IV)were treated with
5-hydroxydopamine (0.8 mgldayl3 days), many of the
granular vesicles exhibited sharply increased electron
density and some were enlarged (Fig. 8). Most of the
remaining axonal varicosities contained small (c. 50 nm
diam) agranular vesicles, which are characteristic of
cholinergic nerves. We also found axonal varicosities
containing large opaque or large dense-cored neurosecretory vesicles (Fig. 9). The biochemical function of
these latter nerves is undetermined, although they resemble the purinergic vesicles that have been described
by Burnstock (1980).
Gap junctions (Figs. 6,lO) were present in the myometria of normal bats examined during the last quarter of
pregnancy, but were not seen earlier except in two bats
examined during Stage 111. Since gap junctions were
found also in the myometria of bats undergoing abortion
during Stages 111, IV,and V, we suspect that these bats
were about to abort. However, their plasma progesterone levels were within the normal range, and we found
no morphological evidence (ischemia, intrauterine
bleeding, wrinkling of the uterine wall) to justify excluding them. Figure 11compares plasma progesterone levels and gap junction area, expressed as a percent of
plasma membrane area (Puri and Garfield, 1982), in
bats from various stages of pregnancy. As shown, gap
junctions were present in uteri 11 mm wide and larger,
613
increased in area until term, and declined rapidly postpartum. Figure 11 also shows that the change in gap
junction area paralleled the change in plasma progesterone levels.
DISCUSSION
Most knowledge of mammalian uterine innervation is
derived from studies of guinea pigs, rabbits, dogs, cats,
and humans in which myometrial innervation is primarily, if not exclusively, adrenergic, and in all of which
there is a progressive loss of demonstrable nerve fibers
during pregnancy. It has been hypothesized that adrenergic nerves play a role in maintaining uterine quiescence during pregnancy by inhibiting contractility, and
that their loss permits, but does not necessarily initiate,
increased contractility at term (Thorbert, 1978; Marshall, 1981). However, this hypothesis is difficult to reconcile with recent studies showing that rat myometrium
is innervated principally by cholinergic fibers and a
lesser number of adrenergic and peptidergic fibers
(Papka et al., 1985) or nonadrenergic, noncholinergic
fibers (Garfield, 1986).Moreover, the theory that the loss
of nerves contributes to events leading to parturition is
clearly incompatible with the results of the present
study, which showed no evidence of disappearance of
uterine nerves in pregnant M. lucifugus even at term
when gap junctions are present.
As noted in Table 1,fluorescent nerve fiber density in
near-term uteri was only 60% of density in early pregnancy. However, due to the increase in uterine surface
area, the total number of nerve fibers per uterus appears
to be increased considerably. In fact, the calculated number of adrenergic fibers in early and midpregnancy is
probably greatly underestimated since the uterine wall
is much thicker than in late pregnancy and many fibers
are either above or below the focal plane of the photographs. In any case, there was unquestionably no general loss or disappearance of adrenergic fibers as has
been described in other species. This conclusion is also
supported by electron microscopic examination of pregnant uteri, which showed an abundance of unmyelinated nerve fibers closely associated with muscle cells
even when gap junctions have formed (Fig. 6). Most
axonal varicosities contained small dense-cored secretory vesicles (Figs. 5, 71, which are conceded to contain
catecholamines and, hence, be indicative of adrenergic
fibers (Burnstock, 1980).Moreover, after treatment with
5-hydroxydopamine,which accumulates in the secretory
vesicles of adrenergic neurons by acting as a false transmitter (Tranzer and Thoenen, 19671, axonal varicosities
containing very dense, occasionally enlarged vesicles
were seen (Fig. 8). Injections of 6-hydroxydopamine,
which damages and destroys adrenergic nerves (Kostrzewa and Jacobowitz, 1974; Buchanan and Garfield,
1984), were unsuccessful as even minute doses were
highly toxic t o pregnant bats.
The presence of gap junctions between myometrial
muscle cells during the latter part of pregnancy (uteri
11mm wide and larger), and their disappearance shortly
after parturition, agrees generally with observations in
other species, including humans (reviewed by Verhoeff
and Garfield, 1986). However, the implication in Figure
11 that this process begins 2 weeks before term in M.
lucifugus must be viewed with reservation since in other
species gap junctions appear only 1to 2 days prepartum
614
G.D. BUCHANAN ET AL.
Fig. 1. Ventral aspect of a uterus of M. lucifugus during the early
fetal stage (Stage IV,uterine width 9 mm). The greatly enlarged right
uterine horn and uterine body are smoothly ovoid and the left uterine
horn (small arrow) is partially incorporated into the uterine wall. The
cervix is indicated by the large arrow. x4.8.
Fig. 2. Anteroventral view of a uterus of M. Zucifugus approaching
term (Stage V, uterine width 16 mm). A ridge containing enlarged
blood vessels (small arrows lying along the antimesometrial margin
bisects the placental area). The position of the cervix (not visible) is
indicated by the large arrow. The fetal head lies to the left in the
photograph. ~ 4 . 8 .
Fig. 5. A low magnification electron micrograph of the myometrium
of a bat at midpregnancy (Stage 111, uterine width 7 mm). A nerve
lying in close proximity to the muscle cells has several varicosities
(arrows) that contain small densecored secretory vesicles characteristic of adrenergic nerves. x 18,000.
Fig. 3. Fluorescent micrograph of a uterine wholemount from a bat
during the early fetal stage (Stage IV, uterine width 9 mm) after
incubation with glyoxylic acid. The tissue contains an abundant network of fluorescent (adrenergic) nerve fibers with numerous varicosities (arrows). The fibers in the upper right, which appear dim, are
below the focal plane of the photograph. X 160.
Fig. 4. Fluorescent micrograph of a uterine wholemount from a bat
near term (Stage V, uterine width 21 mm) after glyoxylic acid incubation. Numerous fluorescent (adrenergic) fibers bearing varicosities are
present (arrows). Although fluorescence of individual fibers is not
decreased, fewer fibers are visible in the picture (compare to Fig. 3)
probably due to stretching of the uterine wall. X 160.
Fig. 6. A low magnification electron micrograph of the myometrium
of a bat near term (Stage V, uterine width 20.5 mm). Small nerves
containing morphologically normal axons (small arrows) occur in close
approximation to smooth muscle cells. Note gap junction (large arrow)
between two muscle cells. x 18,000.
GAP JUNCTIONS AND NERVES IN PREGNANT BAT MYOMETRIA
615
616
G.D. BUCHANAN ET AL.
(Puri and Garfield, 1982; Garfield, 1985). Because pregnancy is asynchronous by 3 to 4 weeks within a colony
of M. lucifugus (Tuttle and Stevenson, 1982), Buchanan
and Younglai (1986) estimated the lengths of Stages IV
and V by plotting the midpoint of the interval during
which specific stages were collected. The precision of
3
806 f 8b
16.0 f 2.1'
Early
4
701 k 107b
96.0 14.gd this method is limited especially in late pregnancy when
Mid
5
489 f 46"
940.6 k 113.1e growth is very rapid, and we suspect, therefore, that
Late
Stage V (uterine width 13 to 22+ mm) is actually much
aTechniques for calculating intersects and for computing surface area
shorter than the 2 weeks depicted in Figure 11.
are described in Materials and Methods.
Gap junctions may serve to synchronize and propagate
b,c,d,eValues in same column without common superscripts differ
statistically by Duncan's Multiple Range Test (p < 0.05).
myometrial contractions during labor, or to enhance
TABLE 1. Fluorescent nerve fiber density per unit area in
uteri of pregnant Myotis tueifugusa
Stage of
No.
X intersects
X surface
pregnancy
bats
per mm2
area (mm?
Fig. 7. Electron micrograph showing two nerve varicosities (arrows)
Fig. 9. Electron micrograph of a nerve varicosity from the same
containing small dense-cored secretory vesicles that are characteristic uterus shown in Figure 7. The varicosity contains large dense-cored or
of adrenergic nerves. The varicosities are in close proximity to a mus- large opaque neurosecretory vesicles. The function of these vesicles is
cle cell (right of picture). ~ 3 0 , 0 0 0 .
undetermined, but they resemble the purinergic vesicles described by
Burnstock (1980). ~ 3 0 , 0 0 0 .
Fig. 8 . Nerve varicosity in the myometrium of a pregnant M. Zuczfugus (Stage IV,uterine width 8 mm) treated with 5-hydroxydopamine
Fig. 10. High magnification electron micrograph showing a gap
for 3 days. Note increased density and enlargement of neurosecretory junction formed between two smooth muscle cells in the myometrium
vesicles (compare to Fig. 7). x 30,000.
of a bat near term. The limits of the gap junction are indicated by
arrows. x 100.000.
617
GAP JUNCTIONS AND NERVES IN PREGNANT BAT MYOMETRIA
11
Fig. 11. Myometrial gap junction area and plasma progesterone
nant, hibernating bats examined in a n earlier study (Buchanan and
levels in pregnant and postpartum M. lucifugus. Specimens were Garfield, 1984)are included. Solid circles indicate gap junctional area,
grouped by pregnancy stage and uterine width as described by Buch- as a percent of plasma membrane area, for individual bats. Gray bars
anan and Younglai (1986).Postpartum bats had blood in their vaginae, indicate mean plasma progesterone values for all bats in each size
indicating that parturition had taken place the day of capture. Lactat- group. The 2 Stage I11 bats (5 mm and 5.5 mm uterine widths) that
ing bats had delivered 3 or more days before examination, as judged had gap junctions may have been about to abort (see Results).
by degree of uterine involution. For comparison, data from 4 nonpreg-
myometrial response to chemical mediators (Garfield, other chiropterans is unknown; however, several factors
1985). Whatever their precise role, it is likely that the suggest that precise control of myometrial contractility
presence of gap junctions is regulated by changes in may be of particular value to heterothermic bats. First,
steroid hormone or prostaglandin levels (MacKenzie and due to their high energy requirements, especially during
Garfield, 1985) since changes in these hormones accom- late pregnancy and lactation (Studier et al., 1973), M.
pany and are generally conceded to govern the onset of lucifugus can ill afford t o forego daily foraging; and
both normal and premature labor (Thorburn and Chal- evidence from a closely related species, Pipistrellus p i p
lis, 1979). Indeed, in vivo and in vitro studies in the rat istrellus, suggests that if they do so they revert to torpor
show that progesterone inhibits, whereas estrogen stim- (Racey, 1974). Second, although pregnant M. lucifugus
ulates gap junction formation (Garfield et al., 1980, remain away from the maternity (day) roost the entire
1982).In rats there is a prepartum decline in circulating night, occupying separate night roosts in the interim
progesterone and a rise in estrogens, so it is uncertain if between feeding bouts (Anthony et al., 19811, there is no
either progesterone withdrawal per se or the resultant evidence that parturition occurs elsewhere than in the
increase in estrogedprogesterone level triggers gap maternity roost. It is logical to infer, therefore, that
junction formation (Puri and Garfield, 1982).In humans, parturition in M. lucifugus is subject to rigid temporal
plasma progesterone does not decline before gap junc- control, which may be achieved by myometrial nerves
tion appearance (Garfield and Hayashi, 1981);however, acting to either inhibit or stimulate contractility when
estrogen levels rise Vhorburn and Challis, 1979). M. appropriate.
Zucifugus resembles humans in that gap junctions form
while progesterone levels are still elevated (Fig. 11).
ACKNOWLEDGMENTS
Unfortunately, plasma estrogen values are not available, so the possibility that the ratio of estrogen to pro- We thank Francesca C. Bullock for expert technical
help with autopsies and preparation of tissues for fluresgesterone is altered is undetermined.
In conclusion, Myotis lucifugus differs from other cent microscopy, and Debbie Merrett for preparation
mammals thus far studied in that myometrial nerves do and examination of tissues by electron microscopy and
not disappear during pregnancy even in the peripartu- preparation of photographs. We especially thank Mr.
rient period when gap junctions appear. This is concor- Harve Whitcroft, owner of Red Bay Outfitters, and his
dant with our previous suggestion (Buchanan and family for permitting us to collect bats on their premises
Garfield, 1984)that in this bat the myometrium may be and for their kind hospitality and interest in our resubject to greater neurogenic control than in other mam- search. This work was supported by grants from the
mals. Whether myometrial innervation is similar in Medical Research Council of Canada.
618
G.D. BUCHANAN ET AL.
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