Skip to main content

Extrapituitary TSH in early chick embryos: Pit-1 dependence?

Journal of Molecular Neuroscience volume 18, pages 77–87 (2002)Cite this article

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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • De Vito W.J. (1989) Thyroid hormone regulation of hypothalamic immunoreactive thyrotropin. Endocrinology 125, 1219–1223.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Harvey S., Azumaya Y., and Hull K. L. (2000) Extrapituitary growth hormone: Pit-1 dependence? Can. J. Physiol. Pharmacol. 78, 1013–1028.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Kakar S. S. (1997) Molecular structure of the human gonadotropin-releasing hormone receptor gene. Eur. J. Endocrinol. 137, 183–192.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Murphy A. E. and Harvey S. (2001) Extrapituitary beta TSH and GH in early chick embryos. Mol. Cell Endocrinol. 185, 161–171.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Wang J., Whetsell M., and Klein J. R. (1997) Local hormone networks and intestinal T cell homeostasis. Science 275, 1937–1939.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Article  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Physiology and Perinatal Research Centre, University of Alberta, T6G 2H7, Edmonton, Alberta, Canada

    Amy E. Murphy & Steve Harvey

Authors
  1. Amy E. Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steve Harvey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steve Harvey.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/JMN:18:1-2:77

Index Entries

  • Thyrotropin-stimulating hormone (TSH)
  • pituitary-specific transcription factor (Pit-1)
  • pituitary
  • extrapituitary