Developmental Expression of Neurotensin in Thyrotropes and Gonadotropes of Male and Female Rats
Aixa R. BelloRicardo ReyesGuadalberto HernándezIsabel NegrínMiriam González‐GómezG. TramuRafael Alonso
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Besides its potential roles as a central neuromodulator or a hypothalamic neurohormone, neurotensin (NT) may also have endocrine function in the anterior pituitary of mammals. We previously found that NT immunoreactivity is present in the secretory granules of gonadotropes and thyrotropes in both male and female rats, where its levels of expression are under the control of sex steroids. In this work, using immunocytochemistry and in situ hybridization, we have studied the postnatal development of NT-like immunoreactivity (NTir) and the mRNA encoding NT (mRNA-NT) in specific anterior pituitary cells of both male and female rats. NT expression starts after birth and displays an identical pattern in both sexes until sexual maturity, with mRNA-NT being detected from day 2 of postnatal life in thyrotropes localized in the central portion of the anterior lobe. This pattern of expression develops progressively throughout the 2nd and 3rd weeks in both sexes. By the beginning of the 3rd week, mRNA-NT can also be detected in gonadotropes localized in the periphery of the gland coinciding with a rise in serum estradiol concentrations in both sexes, and by day 21, mRNA-NT is extensively present in both the periphery and the central region. NTir is observed from days 5–6 in thyrotropes predominantly localized in the central portion of the anterior lobe, and by day 21, NTir is also detected in gonadotropes localized in the periphery of the gland. This pattern remains similar in both sexes until the time of puberty, when female rats start displaying plastic changes in NT expression according to the stage of the estrous cycle. These findings indicate that NT expression in the rat anterior pituitary is cell specific, and develops from birth to adulthood under the control of sex steroid hormones. In addition, preliminary data showing the presence of NT receptors in rat pituitary cells support the hypothesis of a paracrine or an autocrine role for this peptide within the pituitary.Keywords:
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Angiotensin II (Ang II) participates in the regulation of anterior pituitary hormone secretion by acting either directly on the anterior pituitary or indirectly on the hypothalamus. When applied directly on pituitary cells, Ang II increases both ACTH and PRL secretion and has also been reported to affect GH secretion. Three distinct subtypes of Ang II receptors (AT1A, AT1B, and AT2) have been identified; they are unequally distributed and differently regulated in various tissues. We have previously demonstrated that only AT1A receptors are present in the hypothalamus while anterior pituitary cells express predominantly the AT1B subtype. Using in situ hybridization in combination with immunohistochemistry, the aim of the present study was to identify the phenotype of the endocrine cell expressing AT1B receptor messenger RNA (mRNA) in the anterior pituitary of adult male Sprague-Dawley rats. Expression of AT1B receptor mRNA was present in 33.9 ± 1.0% of anterior pituitary cells. AT1B mRNA is predominantly expressed by lactotropes (78.2 ± 2.1% of AT1B mRNA-expressing cells) and to a lower degree by corticotropes (18.3 ± 2.1%) and is not detectable in somatotropes, mammosomatotropes, gonadotropes, or thyrotropes. These results indicate that in adult male rats, Ang II, which has been shown to be synthesized in gonadotropes, can directly stimulate PRL and ACTH release from lactotropes and corticotropes through activation of AT1B receptors. As only 53.8 ± 2.7% of lactotropes and 23.6 ± 2.8% of corticotropes expressed AT1B mRNA, our findings suggest a functional heterogeneity of both cell types regarding their sensitivity to Ang II.
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Zinc ions have been demonstrated in the anterior pituitary of rat by autometallography (AMG) which involves in vivo exposure to sodium selenite leading to creation of zinc selenide crystal lattices that are later silver enhanced by AMG in the sections. In this study, autometallography is combined with immunohistochemistry in order to present the coexistence of zinc ions and hormones in endocrine cells of the rat pituitary. The results showed that the majority of zinc-enriched (ZEN) cells are somatotrophs. All the somatotrophs observed were loaded with AMG grains. Zinc ions were also found to be present in gonadotrophs, corticotrophs and thyrotrophs. A low density of AMG silver grains was found in about 60% of gonadotrophs, 8% of corticotrophs and less than 10% of thyrotrophs. Lactotrophs did not appear to contain zinc ions. The present observations may provide a clue to the physiological function of zinc ions in the rat pituitary.
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Angiotensin II (Ang II) participates in the regulation of anterior pituitary hormone secretion by acting either directly on the anterior pituitary or indirectly on the hypothalamus. When applied directly on pituitary cells, Ang II increases both ACTH and PRL secretion and has also been reported to affect GH secretion. Three distinct subtypes of Ang II receptors (AT1A, AT1B, and AT2) have been identified; they are unequally distributed and differently regulated in various tissues. We have previously demonstrated that only AT1A receptors are present in the hypothalamus while anterior pituitary cells express predominantly the AT1B subtype. Using in situ hybridization in combination with immunohistochemistry, the aim of the present study was to identify the phenotype of the endocrine cell expressing AT1B receptor messenger RNA (mRNA) in the anterior pituitary of adult male Sprague-Dawley rats. Expression of AT1B receptor mRNA was present in 33.9 ± 1.0% of anterior pituitary cells. AT1B mRNA is predominantly expressed by lactotropes (78.2 ± 2.1% of AT1B mRNA-expressing cells) and to a lower degree by corticotropes (18.3 ± 2.1%) and is not detectable in somatotropes, mammosomatotropes, gonadotropes, or thyrotropes. These results indicate that in adult male rats, Ang II, which has been shown to be synthesized in gonadotropes, can directly stimulate PRL and ACTH release from lactotropes and corticotropes through activation of AT1B receptors. As only 53.8 ± 2.7% of lactotropes and 23.6 ± 2.8% of corticotropes expressed AT1B mRNA, our findings suggest a functional heterogeneity of both cell types regarding their sensitivity to Ang II.
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A recent report provides new evidence for the presence of glucokinase (GK) in the anterior pituitary. In the present study, immunohistochemistry was used to identify the cells containing GK in the pituitary of rats and monkeys. In rats, GK was detected as a generalized cytoplasmic staining in a discrete population of cells in the anterior pituitary. In colocalization experiments, the majority of cells expressing follicle-stimulating hormone (FSH) or luteinizing hormone (LH) also contained GK. In addition to the gonadotropes, GK was observed in a subpopulation of corticotropes and thyrotropes. GK was not detected in cells expressing growth hormone or prolactin. In monkeys, GK was also observed in a discrete population of cells. Intracellular distribution differed from the rat in that GK in most cells was concentrated in a perinuclear location that appeared to be associated with the Golgi apparatus. However, similar to rats, colocalization experiments showed that the majority of cells expressing FSH or LH also contained GK. In addition to the gonadotropes, GK was observed in a subpopulation of corticotropes and thyrotropes. In the monkey, only a few cells had generalized cytoplasmic staining for GK. These experiments provide further evidence for the presence of GK in the anterior pituitary. Although some corticotropes and thyrotropes contained GK, the predominant cell type expressing GK was gonadotropes. In view of the generally accepted role of GK as a glucose sensor in a variety of cells including the insulin-producing pancreatic β-cells as the prototypical example, it is hypothesized that hormone synthesis and/or release in pituitary cells containing GK may be directly influenced by blood glucose.
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Abstract A morphometric analysis of the cell types within the adenohypophysis of the female rat was conducted with an emphasis on regional variations. Type I and type II gonadotropes and corticotropes had the largest volumes, mammotropes and somatotropes were of medium size, and thyrotropes and chromophobes were the smallest cells. There was no regional variation in the volumes of the respective cell types. Somatotropes and mammotropes were most numerous, followed by the gonadotropes, chromophobes, corticotropes, and thyrotropes. There was no significant regional localization of the somatotropes, mammotropes, corticotropes, and thyrotropes. Gonadotropes were best defined as two populations with type I cells being localized in the central regions and type II cells being distributed throughout the gland. Chromophobes were the only cells with a significant distribution in the anterior regions and were most numerous in the anterior peripheral regions. These fine‐structural morphometric findings are discussed in relation to other studies of the adenohypophysis that utilize immunocytochemistry.
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The secretory polypeptide 7B2 is produced in different endocrine and neuroendocrine cells, where it is presumed to play a role in the hormone secretion mechanism. In this study, we examined a pattern of 7B2 mRNA expression in the mouse and rat pituitary gland. When [35S]-labeled antisense cRNA probes were used for in situ hybridization, 7B2 mRNA transcripts were detected within virtually all endocrine cells of the anterior lobe (gonadotrophs, thyrotrophs, corticotrophs, somatotrophs and lactotrophs) and of the intermediate lobe (melanotrophs). The posterior lobe was negative. By immunocytochemistry, 7B2 accumulation was observed within melanotrophs in the intermediate lobe and within gonadotrophs and thyrotrophs in the anterior lobe. The question of 7B2 production in other pituitary cells, such as corticotrophs, somatotrophs and lactotrophs, was studied under culture conditions. The corticotroph At T-20 and somatrotroph GH3 cell lines both expressed 7B2 mRNA and contained 7B2 protein detectable by radioimmunoassay. However, this protein could not be visualized by immunocytochemistry. Thus, it is possible that 7B2 is produced in all hormone-synthesizing cells of the pituitary gland, being stored only within some of them and rapidly exported after synthesis from others.
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The histologic association of pituitary endocrine and folliculostellate (FS) cells could be accompanied by complex paracrine interactions. We analyzed the more frequently occurring connections between pituitary endocrine and FS cells by double-immunolabeling histochemistry, by using a streptavidin-biotin-alkaline phosphatase system and electron microscopy. We documented the following cytologic relationships (with 100% representing, in each of the comparisons, the total number of the first cell type mentioned): (a) juxtaposition of somatotrophs with corticotrophs (46%), and contact between thyrotrophs (18%), lactotrophs (17%), and FS cells (19%); (b) connections between lactotrophs and gonadotrophs (58%), somatotrophs (19%), and FS cells (23%); (c) interlinking between thyrotrophs and somatotrophs (35%), FS cells (34%), and other cell types (31%); and (d) interactions between gonadotrophs and lactotrophs (57%), corticotrophs (14%), and FS cells (29%). The immunohistochemical reaction of gonadotrophs was against luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in combination (78%) or individually (11% for each antiserum); (e) short cellular projections from numerous corticotrophs surrounding somatotrophs (58%), gonadotrophs (18%), and FS cells (24%); and (f) FS cells contacting capillaries, gonadotrophs (32%), lactotrophs (21%), corticotrophs (18%), somatotrophs (16%), and thyrotrophs (13%). Electron microscopy revealed long branching processes between hormone-secreting cells and intercellular junctions, such as desmosomes, hemidesmosomes, and zonulae adherentes, in granular and FS cells. Union complexes occluding the follicular lumen can join two endocrine cells, two FS cells, or both types. Gap junctions occur between adjacent FS cells. In the pituitary there thus exist topographic spatial associations along with various interconnections between endocrine and FS cells. These findings may help to clarify the autocrine, juxtacrine, and paracrine mechanisms involved in the hormone-secretory activity of the pituitary gland.
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The cell types of the mature adenohypophysis are derived embryologically from somatic ectoderm associated with Rathke' s pouch. Highly specific trophic factors determine a precise temporal and spatial development of cells expressing unique gene products. The six hormones of the anterior pituitary gland are expressed by at least five distinct hormone-producing cell populations, including corticotrophs (pro-opiomelanocortin, POMC), somatotrophs (growth hormone, GH), lactotrophs (prolactin, PRL), thyrotrophs (thyroid-stimulating hormone, TSH), and gonadotrophs (follicle-stimulating hormone, FSH, and luteinizing hormone, LH) (Table 48-1). Each of these cells are identified by specific assays of polypeptide gene expression, including single-cell mRNA, immunoelectron microscopy, and immunocytochemical assays. The temporal ontogeny of these gene products is initially adrenocorticotropic hormone (ACTH) and α-subunit. After the appearance of Pit-1, apou-domain transcription factor, mixed mammosomatroph products appear. Distinct GH- and PRL-expressing cells PRL-expressing cells follow and TSH, LH, and FSH are the final IPII types to mature at 12 weeks.
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