Ultrastructural Changes in Lactotrophs and Folliculo‐Stellate Cells in the Ovine Pituitary during the Annual Reproductive Cycle

Abstract

In seasonal mammals living in temperate zones, photoperiod regulates prolactin secretion, such that prolactin plasma concentrations peak during the summer months and are lowest during the winter. In sheep, a short-day breeder, circulating prolactin has important modulatory effects on the reproductive system via inhibitory actions on pituitary gonadotrophs and hypothalamic gonadotrophin-releasing hormone release. The exact cellular mechanisms that account for the chronic hypersecretion of prolactin during the summer is not known, although evidence supports an intrapituitary mechanism regulated by melatonin. Folliculo-stellate (FS) cells are non-endocrine cells that play a crucial role in paracrine communication within the pituitary and produce factors controlling prolactin and gonadotrophin release. The present study examined the morphology of the FS and lactotroph cell populations and their distribution in the sheep pituitary during the annual reproductive cycle. Ovine pituitary glands were collected in the winter (breeding season; BS) and summer (nonbreeding season; NBS) and were prepared for quantitative electron microscopy to assess the effects of season on FS and lactotroph cell density, morphology and distribution, as well as on junctional contacts between cells. It was found that lactotrophs in the NBS are larger in size and contain more numerous PRL granules than lactotrophs in the BS. FS cells were also larger in the NBS compared to BS and showed altered morphology such that, in the BS, long cell processes surrounded clusters of adjacent secretory cells. Although no significant change in the number of junctions was observed between lactotrophs and FS cells, or lactotrophs and gonadotrophs, there was a significant increase in the number of adherens junctions between lactotrophs and between FS cells. These findings demonstrate seasonal plasticity in the morphology of lactotrophs and FS cells that reflect changes in PRL secretion.

Roles of connexins and pannexins in (neuro)endocrine physiology

“…Furthermore, gap junction inhibition using alpha glycyrrhetinic acid reduces dye coupling and prevents the network from displaying lactating-like wiring patterns during demand, most likely due to blockade of long-range signal entrainment [65]. Similarly, recent electron microscopy studies in the ovine pituitary have shown that lactotroph-lactotroph junctional contacts increase in line with the circannual peak of PRL during the nonbreeding season [84]. Therefore, episodes of structural and functional plasticity within the lactotroph population/network …”

Intrapituitary mechanisms underlying the control of fertility: key players in seasonal breeding

“…In long- and short-day seasonal breeders, we have shown that although the gonadotrope cell population in the pars distalis remains relatively constant throughout the annual reproductive cycle, with little or no change in gonadotrope subtypes, incidence, and intergonadotrope contacts [7], [12], [13], [62], the lactotrope cell population displays increased intercellular contacts and gonadal-independent enhanced cellular prevalence during the long days of summer [7], [13]. The upregulation in lactotrope intercellular communication was shown to be accompanied by changes in cellular ultrastructure, with increased rough endoplasmic reticulum, secretory granule density, and total cell area at this time of year.…”

“…The incidence of gonadotropes is relatively constant throughout the year in the pars distalis [7], [11] and has been shown to be upregulated only in the pars tuberalis of sexually active females [10], [12]; conversely, the lactotrope population, which is only present in the pars distalis, undergoes dynamic changes in response to photoperiod. In sheep, the lactotrope cell area is larger in the nonbreeding season (summer) [13], [14], whereas in the horse, gonadal independent effects of season were reported in orchidectomized animals, with an increase in the incidence of lactotropes in the breeding season (summer) [7]. Moreover, the ultrastructure of lactotrope cells exhibits dynamic changes throughout the year in the ovine pituitary, with hypertrophy, increased cytoplasmic area, and increased rough endoplasmic reticulum and density of prolactin secretory granules during the long days of summer [13].…”

“…In sheep, the lactotrope cell area is larger in the nonbreeding season (summer) [13], [14], whereas in the horse, gonadal independent effects of season were reported in orchidectomized animals, with an increase in the incidence of lactotropes in the breeding season (summer) [7]. Moreover, the ultrastructure of lactotrope cells exhibits dynamic changes throughout the year in the ovine pituitary, with hypertrophy, increased cytoplasmic area, and increased rough endoplasmic reticulum and density of prolactin secretory granules during the long days of summer [13]. Similar ultrastructural changes in response to season were reported in another photoperiodic species, the white tail deer [15], [16].…”

Profile of gonadotropic hormone secretion in sheep with disturbed rhythm of seasonality

“…The observed increase in the secretion of LH from the pituitary gonadotropic cell in response to the prolonged administration of melatonin results from the increase in the GnRH pulse frequency released by the hypothalamus (Clarke and Arbabi 2016;Ciechanowska et al 2017). The effects of melatonin on the hypothalamic-pituitary axis are related to its diffusion into the cerebrospinal fluid (CSF) in the third ventricle of the brain, which enables the direct effect of melatonin on the secretion of hormones from the pituitary gland (Tricoire et al 2002;Christian et al 2015).…”