Abstract
Proliferating cells in the male rat anterior pituitary at 1, 3, 5, and 8 weeks of age were labeled with bromodeoxyuridine (BrdU) and studied by light and electron microscopic immunocytochemistry using anti-BrdU. They decreased in number from 402±31/mm2 at 1 week to 50±1.5/mm2 at 8 weeks, while their cell area increased by about twofold during this period. They had a slightly higher nucleus/whole cell (N/C) ratio than non-proliferating cells. According to their ultrastructure we classified them into granular and agranular cells. The percentage of granular cells ranged from 73% to 82% of all the proliferating cells during the period studied. They had many granules of various sizes and shapes, and some contained growth hormone and prolactin. Agranular cells, constituting 18–27% of proliferating cells, were small and had a high N/C ratio, indicating their immaturity. Moreover, they showed several features of folliculo-stellate (FS) cells: they showed no secretory granules in the cytoplasm, extended thin cytoplasmic processes, and sometimes they constructed a follicle among them. These results suggest: (1) the majority of proliferating cells were mature cells producing anterior pituitary hormone(s) and (2) most of the agranular proliferating cells maybe FS cells. The possibility of the latter is discussed.
Similar content being viewed by others
References
Bendayan M (1982) Double immunocytochemical labeling applying the protein A–gold technique. J Histochem Cytochem 30:81–85
Carbajo-Perez E, Watanabe YG (1990) Cellular proliferation in the anterior pituitary of the rat during the postnatal period. Cell Tissue Res 261:333–338
Ceccatelli S, Hulting AL, Zhang X, Gustafsson L, Villar M, Hokfelt T (1993) Nitric oxide synthase in the rat anterior pituitary gland and the role of nitric oxide in regulation of luteinizing hormone secretion. Proc Natl Acad Sci U S A 90:11292–11296
Cocchia D, Miani N (1980) Immunocytochemical localization of the brain-specific S-100 protein in the pituitary gland of adult rat. J Neurocytol 9:771–782
Drewett N, Jacobi JM, Willgoss DA, Lloyd HM (1993) Apoptosis in the anterior pituitary gland of the rat: studies with estrogen and bromocriptine. Neuroendocrinology 57:89–95
Farquhar MG (1957) "Corticotrophs" of the rat adenohypophysis as revealed by electron microscopy. Anat Rec 127:291
Fauquier T, Guerineau NC, McKinney RA, Bauer K, Mollard P (2001) Folliculostellate cell network: a route for long-distance communication in the anterior pituitary. Proc Natl Acad Sci U S A 8891–8896
Ferrara N, Henzel W (1989) Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161:851–858
Ferrara N, Schweigerer L, Neufeld G, Mitchell R, Gospodarowicz D (1987) Pituitary follicular cells produce basic fibroblast growth factor. Proc Natl Acad Sci U S A 84:5773–5777
Friend JP (1979) Cell size and cell division of the anterior pituitary: time course in the growing rat. Experientia 35:1577–1578
Goluboff LG, MacRae ME, Ezrin C, Sellers EA (1970) Autoradiography of tritiated thymidine labeled anterior pituitary cells in propylthiouracil treated rats. Endocrinology 87:1113–1118
Gospodarowicz D, Lau K (1989) Pituitary follicular cells secrete both vascular endothelial growth factor and follistatin. Biochem Biophys Res Commun 165:292–298
Gratzner HG (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474–475
Horvath E, Kovacs K (2002) Folliculo-stellate cells of the human pituitary: a type of adult stem cell? Ultrastruct Pathol 26:219–228
Hunt TE (1942) Mitotic activity in the anterior hypophysis of female rats. Anat Rec 82:263–276
Hunt TE, Hunt EA (1966) A radioautographic study of the proliferative activity of adrenocortical and hypophyseal cells of the rat at different periods of the estrous cycle. Anat Rec 156:361–368
Inoue K, Kurosumi K (1981) Mode of proliferation of gonadotrophic cells of the anterior pituitary after castration: immunocytochemical and autoradiographic studies. Arch Histol Jpn 44:71–85
Inoue K, Taniguchi Y, Kurosumi K (1987) Differentiation of striated muscle fibers in pituitary glands grafts transplanted beneath the kidney capsule. Arch Histol Jpn 50:567–578
Inoue K, Mogi C, Ogawa S, Tomida M, Miyai S (2002) Are folliculo-stellate cells in the anterior pituitary gland supportive cells or organ-specific stem cells? Arch Physiol Biochem 110:50–53
Jones HB, Harbottle SJ, Bowdler AL (1994) Assessment of the labeling index of cohorts of the anterior pituitary cell population in phenobarbital-treated male rats by a double immunohistochemical technique for bromodeoxyuridine and pituitary hormones. J Histochem Cytochem 42:543–549
Kaiser UB LB, Carroll RS, Unabia G, Chin WW, Childs GV (1992) Follistatin gene expression in the pituitary: localization in gonadotropes and folliculostellate cells in diestrous rats. Endocrinology 130:3048–3056
Kurosumi K (1971) Mitosis of the rat anterior pituitary cells: an electron microscope study. Arch Histol Jpn 33:145–160
Kurotani R, Tahara S, Sanno N, Teramoto A, Mellon P, Inoue K, Yoshimura S, Osamura RY (1999) Expression of Ptx1 in the adult rat pituitary glands and pituitary cell lines: hormone-secreting cells and folliculo-stellate cells. Cell Tissue Res 298:55–61
Leblond CP, Walker BE (1956) Renewal of cell populations. Physiol Rev 36:255–276
Mastro A, Hymer WC, Therrien CD (1969a) DNA synthesis in adult rat anterior pituitary glands in organ culture. Exp Cell Res 54:407–414
Mastro A, Shelton E, Hymer WC (1969b) DNA synthesis in the rat anterior pituitary. J Cell Biol 43:626–629
Nakai T, Watanabe T, Kigawa T, Ajika K, Murasawa Y, Kobayashi T, Kobayashi T (1969) Developmental cell dynamics in the hypothalamus, the anterior pituitary and the ovary of the rat. Endocrinol Jpn 16:379–382
Nakajima T, Yamaguchi H, Takahashi K (1980) S100 protein in folliculostellate cells of the rat pituitary anterior lobe. Brain Res 191:523–531
Nakane P (1968) Simultaneous localization of multiple tissue antigens using the peroxidase-labeled antibody method: a study on pituitary glands of the rat. J Histochem Cytochem 16:557–560
Nouet JC, Kujas M (1975) Variations of mitotic activity in the adenohypophysis of male rats during a 24-hour cycle. Cell Tissue Res 164:193–200
Oishi Y, Okuda M, Takahashi H, Fujii T, Morii S (1993) Cellular proliferation in the anterior pituitary gland of normal adult rats: influences of sex, estrous cycle, and circadian change. Anat Rec 235:111–120
Pomerat GR (1941) Mitotic activity in the pituitary of the white rat following castration. Am J Anat 69:89–121
Rennels EG (1964) Electron microscopic alterations in the rat hypophysis after scalding. Am J Anat 114:71–91
Rienhart JF, Farquhar MG (1953) Electron microscopic studies of the anterior pituitary gland. J Histochem Cytochem 1:93–113
Shirasawa N, Yoshimura F (1982) Immunohistochemical and electron microscopical studies of mitotic adenohypophysial cells in different ages of rats. Anat Embryol 165:51–61
Shirasawa N, Kihara H, Yamaguchi S, Yoshimura F (1983) Pituitary folliculo-stellate cells immunostained with S-100 protein antiserum in postnatal, castrated and thyroidectomized rats. Cell Tissue Res 231:235–249
Stadtler F, Stocker E, Dhom G, Tietze HU (1970) Autoradiographic studies on nuclear DNA and RNA synthesis in the adenohypophysis of castrated rats. Acta Endocrinol 64:324–338
Stepien H, Wolaniuk A, Pawlikowski M (1978) Effects of pimozide and bromocriptine on anterior pituitary cell proliferation. J Neural Transm 42:239–244
Stokreef JC, Reifel CW, Shin SH (1986) A possible phagocytic role for folliculo-stellate cells of anterior pituitary following estrogen withdrawal from primed male rats. Cell Tissue Res 243:255–261
Stratmann IE, Ezrin C, Sellers EA, Simon GT (1972) The origin of thyroidectomy cells as revealed by high resolution radioautography. Endocrinology 90:728–734
Tamatani R, Taniguchi Y, Kawarai Y (1995) Ultrastructural study of proliferating cells with an improved immunocytochemical detection of DNA-incorporated bromodeoxyuridine. J Histochem Cytochem 43:21–29
Taniguchi Y, Tamatani R, Yasutaka S, Kawarai Y (1995) Proliferation of pituitary corticotrophs following adrenalectomy as revealed by immunohistochemistry combined with bromodeoxyuridine-labeling. Histochem Cell Biol 103:127–130
Traverso V, Christian HC, Morris JF, Buckingham JC (1999) Lipocortin 1 (annexin 1): a candidate paracrine agent localized in pituitary folliculo-stellate cells. Endocrinology 140:4311–4319
Vankelecom H, Matthys P, Van Damme J, Heremans H, Billiau A, Denef C (1993) Immunocytochemical evidence that S-100-positive cells of the mouse anterior pituitary contain interleukin-6 immunoreactivity. J Histochem Cytochem 41:151–156
Vila-Porcile E (1972) Le reseau des cellules folliculo-stellaries et les follicules de I'adenohypophyse du rat (pars distalis). Z Zellforsh 129:328–369
Yoshimura F, Soji T, Sato S, Yokoyama M (1977) Development and differentiation of rat pituitary follicular cells under normal and some experimental conditions with special reference to an interpretation of renewal cell system. Endocrinol Jpn 24:435–449
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kominami, R., Yasutaka, S., Taniguchi, Y. et al. Proliferating cells in the rat anterior pituitary during the postnatal period: immunoelectron microscopic observations using monoclonal anti-bromodeoxyuridine antibody. Histochem Cell Biol 120, 223–233 (2003). https://doi.org/10.1007/s00418-003-0565-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00418-003-0565-9