Surgical denervation of porcine ovaries during the middle luteal phase of the oestrous cycle changes their morphology and steroidogenic activity

Abstract

Changes in both the morphology and the steroidogenic activity of porcine ovaries denervated surgically on day 12 of the oestrous cycle were studied. Neurectomy of the plexus and the superior ovarian nerves caused a dramatic reduction in the number (or even a disappearance) of dopamine-β-hydroxylaseand/or neuropeptide tyrosine-immunoreactive nerve terminals. On day 20 of the subsequent oestrous cycle, the number of small follicles increased (P < 0.01) and that of large follicles decreased (P < 0.05) in the denervated ovaries, as compared to the controls. Neurectomy led to a decrease in the level of progesterone (P 4 ; P < 0.001) and androstenedione (A 4 ; P < 0.01) in the fluid from small follicles, A 4 (P < 0.001) and testosterone (T; P < 0.05) in the fluid from medium-sized follicles, as well as in the content of all these steroids in the fluid from large-sized follicles (P < 0.001 for P 4 and P < 0.05 for A 4 and T). Denervation also caused a decrease in the content of A 4 (P < 0.01) and T (P < 0.001) in the wall of follicles. Neurectomy resulted in a significant increase in the immunoexpression of cholesterol side-chain cleavage cytochrome P450 in the follicles and a decrease of 3β-hydroxysteroid dehydrogenase. After denervation, plasma levels of LH, P 4 , A 4 , T, oestrone and oestradiol-17β were lower (P < 0.05-0.001) on the particular days of the study than in the control group. Our data revealed that the denervation of ovaries during the middle luteal phase of the oestrous cycle in gilts caused distinct changes in both the morphology and the steroidogenic activity of the organ, confirming an important role of the peripheral nervous system in the control of the gonad in this species. Acta Veterinaria Hungarica 55, 2007It is well known that mammalian ovaries are fairly innervated by fibres belonging to the adrenergic, cholinergic and/or peptidergic subsets of the autonomic and sensory systems. Ovarian function is thus regulated by both hormonal and neuronal input operating in concert to control follicular development, steroidogenesis and ovulation. Numerous studies performed on laboratory animals showed that the effects of gonad denervation are dependent not only on species and age of animals, but also on the experimental procedure. For instance, the blockade of ovarian innervation development in neonatal rats resulted in limited follicular growth, delayed puberty, decreased oestradiol-17β (E 2 ) secretion and marked irregularities of the oestrous cycles (Lara et al., 1990a). Conversely, chemical sympathectomy induced by guanethidine administration to newborn guinea pigs caused ovulation (Riboni et al., 1997). Although bilateral sectioning of the superior ovarian nerve (SON) in adult rats did not affect ovulation (Chávez et al., 1991), it was able to decrease the plasma levels of progesterone (P 4 ) and E 2 (Erskine and Weaver, 1988). On the other hand, an inhibition of this process occurred in adult guinea pigs exposed to guanethidine (Trujillo and Riboni, 2002). Moreover, it was indicated by Luna et al. ...

Ovarian function and reproductive senescence in the rat: role of ovarian sympathetic innervation

“…Regarding follicular development, the surgical section of the ovarian superior nerve (SON) in pigs increases the number of small follicles (<3 mm) and decreases the number of large follicles (>7 mm). This change in the follicular population is associated with a decrease in the content of steroid hormones in the follicular fluid (Jana et al 2007). A similar effect is found in rats, where a bilateral denervation of the SON decreases the serum level of oestradiol, progesterone and the number of developing follicles.…”

Acute effects of unilateral sectioning the superior ovarian nerve of rats with unilateral ovariectomy on ovarian hormones (progesterone, testosterone and estradiol) levels vary during the estrous cycle

“…In the pig, sectioning of the plexus nerve and the SON led to lower plasma levels of LH, P4, androstenedione (A4), testosterone (T), estrone and estradiol-17beta. Further, a significant increase in the immuno-expression of cholesterol side-chain cleavage cytochrome P450 in follicles, as well as a decrease of 3-betaHSD, and in plasma levels of luteinizing hormone (LH), P4, A4, T, estrone and estrogen have been documented [33]. …”

“…Left-side vagotomy performed to right ULO rats (left ovary in-situ ) resulted in higher ovulation rates, compensatory ovarian hypertrophy, and number of ova shed; while the same procedure to left ULO rats (right ovary in-situ ) resulted in a decrease of the same parameters [2,3]. In rats, the electrical stimulation to the ovarian plexus nerve or the SON produces a vasoconstriction of ovarian arterioles and a reduction of ovarian blood flow in rats [33]. The stimulation of the SON resulted in a significantly decrease of E2, while electrical stimulation of the ovarian plexus nerve did not modify it.…”

Hormonal and Neural Mechanisms Regulating Hormone Steroids Secretion

“…Sectioning the plexus nerve and the SON of pigs led to lower LH, progesterone, androstenedione (A4), testosterone, estrone and estradiol-17beta plasma levels. In addition, a significant increase in the immune-expression of cholesterol side-chain cleavage cytochrome P450 occurs in follicles, as well as a decrease in 3-betaHSD activity, and in LH, progesterone, androstenedione (A4), testosterone, estrone and estrogen plasma levels (Jana et al, 2007). Using an ex vivo celiac ganglion (CG)-SON-ovary (CG-SON-O) system, Aguado's research group has contributed to the understanding of the participation of the SON, the plexus ovarian nerve and the vagus nerve in regulating the secretion of ovarian hormones.…”

“…Neurectomy increased the immune expression of cholesterol side-chain cleavage cytochrome P450, lowered the expression of 33-hydroxysteroid dehydrogenase, and lowered the plasma levels of LH, progesterone, androstenedione, testosterone, estrone and estradiol-17beta. The results suggest that ovarian innervations play a role regulating the steroidogenic activity of the ovary (Jana et al, 2007). Figure 5 shows the comparative effects of ventral unilateral mechanical stimulation of the SON on ovarian hormone secretion.…”