Abstract
The expression of the thyrotropin (TSH) gene in the pituitary gland is thought to be dependent upon the pituitary-specific transcription factor, Pit-1. TSH immunoreactivity is, however, widespread in extrapituitary tissues, and the possibility that this may reflect a widespread distribution of Pit-1 was therefore investigated in embryonic chicks, prior to the ontogenic differentiation of the pituitary gland.
TSH immunoreactivity in chick embryos at the end of the first trimester of the 21d incubation period was present in discrete cells in the developing brain (particularly in ependymal cells lining the diocoele and mesocoele and in cells lining the otic vesicle), spinal cord (ependymal cells), liver (hepatocytes), lungs (in the linings of the bronchi), gut (in the linings of the proventriculus) and limb bud (in skin, muscle, bone and nerve fibers). In some of these tissues (particularly in brain and spinal cord ependymal cells, cells in the otic vesicle and in liver hepatocytes), the distribution of TSH immunoreactivity was overlapped by the distribution of immunoreactive Pit-1, suggesting Pit-1 involvement in TSH expression in these sites. However, in other tissues (e.g., the trigeminal nerve in the head and the marginal mantle layer of the spinal cord), Pit-1 immunoreactivity was intense but TSH immunoreactivity was marginal. Conversely, other tissues (e.g., cells in the skin, blood vessels, limb bud, bronchus, proventriculus, and cardiopleural cavities) had intense TSH staining but little, if any, Pit-1 immunoreactivity. The expression of the TSH gene in these tissues would thus appear to be Pit-1 independent. These results demonstrate the presence of Pit-1 in pituitary and extrapituitary tissues of the domestic fowl and suggest the involvement of Pit-1 in the extrapituitary expression of TSH in chick embryos may be tissue-specific.
Similar content being viewed by others
References
Baumeister H. and Meyerhof W. (1998) Involvement of a Pit-1 binding site in the regulation of the rat somatostatin receptor gene expression. Ann. New York Acad. Sci. 865, 390–392.
Bodey B., Bodey B. Jr., Siegel S. E., and Kaiser H. E. (2000) The role of the reticulo-epithelial (RE) cell network in the immuno-neuroendocrine regulation of intrathymic lymphopoiesis. Anticancer Res. 20, 1871–1888.
Burrows H. L., Douglas K. R., and Camper S. A. (1999) Genealogy of the anterior pituitary gland: tracing a family tree. Trends Endocrinol. Metab. 10, 343–352.
Buys N., Van As P., Volchaert G., and Decuypere E. (1998) Chicken pituitary-specific transcription factor-1 (Pit-1) cDNA cloning and analysis of sequence variation. Biotech. Agron. Soc. Environ. 2, 20.
Candiani S. and Pestarino M. (1998a) Evidence for the presence of the tissue-specific transcription factor Pit-1 in lancelet laevae. J. Comp. Neurol. 400, 310–316.
Candiani S. and Pestarino M. (1998b) Expression of the tissue-specific transcription factor Pit-1 in the lancelet, Branchiostoma lanceolatum. J. Comp. Neurol. 392, 343–351.
Candiano S. and Pestarino M. (1999) The tissue-specific transcription factor Pit-1 is expressed in the spinal cord of the lancelet Branchiostoma lanceolatum. Neurosci. Lett. 260, 25–28.
Catanzaro D. F., Sun J., Gilbert M. T., et al. (1994) A Pit-1 binding site in the human renin gene promoter stimulates activity in pituitary, placental and juxtaglomerular cells. Kid. Intl. 46, 1513–1515.
De Vito W.J. (1989) Thyroid hormone regulation of hypothalamic immunoreactive thyrotropin. Endocrinology 125, 1219–1223.
De Vito W. J., Connors J. M., and Hedge G. A. (1985) Distribution and release of immunoreactive thyroid-stimulating hormone in the rat hypothalamus: effects of thyroidectomy, hypophysectomy and treatment with thyroid hormones. Neuroendocrinology 41, 23–30.
Dolle P., Castrillo J. L., Theill L. E., Deerinck T., Ellisman M., and Karin M. (1990) Expression of GHF-1 protein in mouse pituitaries correlates both temporally and spatially with the onset of growth hormone gene activity. Cell 60, 809–820.
Fan N. C., Peng C., Krisinger J., and Lung P. C. (1995) The human gonadotropin-releasing hormone receptor gene: complete structure including multiple promoters, transcription initiation sites and polyadenylation signals. Mol. Cell Endocrinol. 107, R1-R8.
Gaylinn B. D. (1999) Molecular and cell biology of the growth hormone releasing hormone receptors on thymocytes and splenocytes from rats. Growth Horm. IGS Res. 9 (Suppl. A), 37–44.
Germain S., Konoshita T., Phillippe J., Corvol P., and Pinet F. (1996) Transcriptional induction of the human renin gene by cyclic AMP requires cyclic AMP response element-binding protein (CREB) and a factor binds a pituitary-specific trans-active factor (Pit-1) motif. Biochem. J. 316, 107–113.
Gerris K. L., Van As P., De Groof B., et al. (2002) Growth-hormone secretion in the chicken is a result of a complex interaction between hypothalamic and hypophyseal peptides. In Avian Endocrinol. (Dawson A. and Chaturvedi C. M., eds.), Narosa Publishing House, New Delhi, India, pp. 287–300.
Gilbert M. T., Sun J., Yan Y., et al. (1994) Renin gene promoter activity in GC cells is regulated by cAMP and thyroid hormone through Pit-1 dependent mechanisms. J. Biol. Chem. 269, 28,049–28,054.
Gregory C. C., Dean C. E., and Porter T. E. (1998) Expression of chicken thyroid-stimulating hormone β-subunit messenger ribonucleic acid during embryonic and neonatal development. Endocrinology 139, 474–478.
Harada A. and Hershman J. M. (1978) Extraction of human chorionic thyrotropin (hCT) from term placentas: failure to recover thyrotropic activity. J. Clin. Endocrinol. Metab. 47, 681–685.
Harbour D. V., Kruger T. E., Coppenhaver D., Smith E. M., and Meyer W. J. (1989) Differential expression and regulation of thyrotropin (TSH) in T cell lines. Mol. Cell. Endocrinol. 64, 229–241.
Harvey S., Azumaya Y., and Hull K. L. (2000) Extrapituitary growth hormone: Pit-1 dependence? Can. J. Physiol. Pharmacol. 78, 1013–1028.
He X. I., Treacy M. N., Simmons D. M., Ingraham H. A., Swanson L. W., and Rosenfeld M. G. (1989) Expression of a large family of POU domain regulatory genes in mammalian brain development. Nature (London) 340, 35–42.
Hojvat S., Baker G., Kirsteins L., and Lawrence A. M. (1982a) TSH in the rat and monkey brain. Distribution, characterization and effect of hypophysectomy. Neuroendocrinology 34, 327–332.
Hojvat S., Emanuele N., Baker G., Connick E., Kirsteins L., and Lawrence A. M. (1982b) Growth hormone (GH), thyroid-stimulating hormone (TSH), and luteinizing hormone (LH)-like peptides in the rodent brain: non-parallel ontogenetic development with pituitary counterparts. Brain Res. 256, 427–434.
Hojvat S., Emanuele N., Baker G., Kirsteins L., and Lawrence A. M. (1985) Brain thyroid-stimulating hormone: effects of endocrine manipulations. Brain Res. 360, 257–263.
Hsu S. M., Raine L., and Fanger H. (1981) Use of avidinperoxide complex ABC in immunoperoxidase techniques: a comparison between ABD and unlabeled antibody AAP procedures. J. Histochem. Cytochem. 29, 577–580.
Iguchi G., Okimura Y., Takahashi T., et al. (1999) Cloning and characterization of the 5′-flanking region of the human growth hormone-releasing hormone receptor gene. J. Biol. Chem. 274, 12,108–12,114.
Jones L. C., Day R. N., Pittler S. J., Valentine C. L., and Scammell J. G. (1996) Cell-specific expression of the rat secretogranin II promoter. Endocrinology 137, 3815–3822.
Kakar S. S. (1997) Molecular structure of the human gonadotropin-releasing hormone receptor gene. Eur. J. Endocrinol. 137, 183–192.
Lin C. R., Lin S. C., Chang C. P., and Rosenfeld M. G. (1992) Pit-1 dependent expression of the receptor for growth hormone releasing factor mediates pituitary cell growth. Nature (London) 360, 765–768.
Mikami S.-I. (1983) Avian adenohypophysis: recent progress in immunocytochemical studies. In Avian Endocrinology: Environmental and Ecological Perspectives (Mikami S. I., ed.), Springer-Varlag, Berlin, pp. 38–56.
Miller T. L., Godfrey P. A., Dealmeida V. I., and Mayo K. E. (1999) The rat growth hormone-releasing hormone receptor gene: structure, regulation, and generation of receptor isoforms with different signalling properties. Endocrinology 140, 4152–4165.
Murphy A. E. and Harvey S. (2001) Extrapituitary beta TSH and GH in early chick embryos. Mol. Cell Endocrinol. 185, 161–171.
Ono M., Mochizuki E., Mori Y., Aizawa A., and Harigai T. (1995) The regulatory region and transcription factor required for the expression of rat and salmon pituitary hormone-encoding genes shows cell-type and species specificity. Gene 153, 267–271.
Peele M. E., Carr F. E., Baker J. R. Jr., Wartofsky L., and Burman K. D. (1993) TSH beta subunit gene expression in human lymphocytes. Am. J. Med. Sci. 305, 1–7.
Sakai T., Sakemoto S., Ijima K., Matzubara K., Kato Y., and Inoue K. (1999) Characterization of TSH positive cells in foetal rat pars distalis that fail to express Pit-1 factor and thyroid hormone beta 2 receptors. J. Neuroendocrinol. 11, 187–193.
Seimiya M., Watanabe Y., and Kurosawa Y. (1997) Identification of POU-class homeoboxgenes 1-freshwater sponge and the specific expression of these genes during differentiation. Eur. J. Biochem. 243, 37–31.
Smith E. M., Phan M., Kruger T. E., Coppenhaver D. H., and Blalock J. W. (1983) Human lymphocyte production of immunoreactive thyrotropin. Proc. Natl. Acad. Sci. (USA) 80, 6010–6013.
Takayama Y., Rand-Wenner M., Kawauchi H., and Ono M. (1991) Gene structure of chum salmon somatolactin, a presumed pituitary hormone of the growth hormone/prolactin family. Mol. Endocrinol. 5, 778–786.
Tanaka M., Yamamoto I., Ohkubo T., Akita M., Hoshino S., and Nakashima K. (1999) cDNA cloning and developmental alterations in gene expression of the two Pit-1/GHR-1 transcription factors in the chicken pituitary. Gen. Comp. Endocrinol. 114, 441–448.
Thommes R. C., Martens J. B., Hopkins W. E., Caliendo J., Sorrentino M. J., and Woods J. E. (1983) Hypothalamo-adenohypophyseal-thyroid interrelationships in the chick embryo. IV. Immunocytochemical demonstration of TSH in the hypophyseal pars distalis. Gen. Comp. Endocrinol. 51, 434–443.
Wang J., Whetsell M., and Klein J. R. (1997) Local hormone networks and intestinal T cell homeostasis. Science 275, 1937–1939.
Wong E. A., Silsby J. L., and El Halawani M. E. (1992) Complementary DNA cloning and expression of Pit-1/GHF-1 from the domestic turkey. DNA Cell Biol. 11, 651–660.
Yoshizato H., Fujikawa T., Soya H., Tanaka M., and Nakashima K. (1998) The growth hormone (GH) gene is expressed in the lateral hypothalamus: enhancement by GH-releasing hormone and repression by restraint stress. Endocrinology 139, 2545–2551.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Murphy, A.E., Harvey, S. Extrapituitary TSH in early chick embryos: Pit-1 dependence?. J Mol Neurosci 18, 77–87 (2002). https://doi.org/10.1385/JMN:18:1-2:77
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1385/JMN:18:1-2:77