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. 1993 Jul 1;90(13):6052–6055. doi: 10.1073/pnas.90.13.6052

cDNA cloning of the beta subunit of teleost thyrotropin.

M Ito 1, Y Koide 1, N Takamatsu 1, H Kawauchi 1, T Shiba 1
PMCID: PMC46865  PMID: 8327483

Abstract

cDNA clones encoding the beta subunit of thyrotropin (thyroid-stimulating hormone; TSH) were isolated from a cDNA library made from the pituitaries of immature rainbow trout and sequenced. The precursor of rainbow trout TSH beta consists of 147 aa, which can be cleaved into a signal peptide (20 aa) and a mature protein (127 aa) containing one potential N-glycosylation site and 12 cysteine residues. The protein showed highest homology with human TSH beta (51%) and lesser homology with human follitropin (42%), human lutropin (32%), and salmon gonadotropin (31-33%) beta subunits. The identification of TSH in addition to two gonadotropins (gonadotropins I and II) in the teleost fish suggests that the divergence of three kinds of glycoprotein hormones from an ancestral molecule took place earlier than the time of divergence of teleosts from the main line of evolution leading to tetrapods. Northern blot analysis showed that the expression of the rainbow trout TSH beta gene is specific to the pituitary gland and is significantly higher in immature fish than in mature fish, suggesting that TSH plays some role in the biological processes of immature fish.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Brown C. L., Grau E. G., Stetson M. H. Functional specificity of gonadotropin and thyrotropin in Fundulus heteroclitus. Gen Comp Endocrinol. 1985 May;58(2):252–258. doi: 10.1016/0016-6480(85)90341-7. [DOI] [PubMed] [Google Scholar]
  2. Carr F. E., Need L. R., Chin W. W. Isolation and characterization of the rat thyrotropin beta-subunit gene. Differential regulation of two transcriptional start sites by thyroid hormone. J Biol Chem. 1987 Jan 25;262(3):981–987. [PubMed] [Google Scholar]
  3. Esch F. S., Mason A. J., Cooksey K., Mercado M., Shimasaki S. Cloning and DNA sequence analysis of the cDNA for the precursor of the beta chain of bovine follicle stimulating hormone. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6618–6621. doi: 10.1073/pnas.83.17.6618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. FONTAINE Y. A., CONDLIFFE P. G. PURIFICATION DE L'HORMONE THYR'EOTHROPE D'UN T'EL'EOSTE'EN (L'ANGUILLE). PARALL'ELE ENTRE LA SP'ECIFICIT'E ZOOLOGIQUE DE CETTE HORMONE ET QUELQUES-UNS DE SES CARACT'ERES PHYSICOCHIMIQUES. Bull Soc Chim Biol (Paris) 1963 Aug 31;45:681–693. [PubMed] [Google Scholar]
  5. Fontaine Y. A., Burzawa-Gerard E. Esquisse de l'evolution des hormones gonadotropes et thyreotropes des vertébrés. Gen Comp Endocrinol. 1977 Jul;32(3):341–347. doi: 10.1016/0016-6480(77)90213-1. [DOI] [PubMed] [Google Scholar]
  6. Giudice L. C., Pierce J. G. Studies on the disulfide bonds of glycoprotein hormones. Complete reduction and reoxidation of the disulfide bonds of the alpha subunit of bovine luteinizing hormone. J Biol Chem. 1976 Oct 25;251(20):6392–6399. [PubMed] [Google Scholar]
  7. Grau E. G., Stetson M. H. The effects of prolactin and TSH on thyroid function in Fundulus heteroclitus. Gen Comp Endocrinol. 1977 Nov;33(3):329–335. doi: 10.1016/0016-6480(77)90047-8. [DOI] [PubMed] [Google Scholar]
  8. Gurr J. A., Catterall J. F., Kourides I. A. Cloning of cDNA encoding the pre-beta subunit of mouse thyrotropin. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2122–2126. doi: 10.1073/pnas.80.8.2122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hayashizaki Y., Miyai K., Kato K., Matsubara K. Molecular cloning of the human thyrotropin-beta subunit gene. FEBS Lett. 1985 Sep 2;188(2):394–400. doi: 10.1016/0014-5793(85)80409-9. [DOI] [PubMed] [Google Scholar]
  10. Hsiao K. A fast and simple procedure for sequencing double stranded DNA with sequenase. Nucleic Acids Res. 1991 May 25;19(10):2787–2787. doi: 10.1093/nar/19.10.2787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Inui Y., Miwa S. Thyroid hormone induces metamorphosis of flounder larvae. Gen Comp Endocrinol. 1985 Dec;60(3):450–454. doi: 10.1016/0016-6480(85)90080-2. [DOI] [PubMed] [Google Scholar]
  12. Jameson J. L., Becker C. B., Lindell C. M., Habener J. F. Human follicle-stimulating hormone beta-subunit gene encodes multiple messenger ribonucleic acids. Mol Endocrinol. 1988 Sep;2(9):806–815. doi: 10.1210/mend-2-9-806. [DOI] [PubMed] [Google Scholar]
  13. Koide Y., Itoh H., Kawauchi H. Isolation and characterization of two distinct gonadotropins, GTHI and GTHII, from bonito (Katsuwonus plelamis) pituitary glands. Int J Pept Protein Res. 1993 Jan;41(1):52–65. doi: 10.1111/j.1399-3011.1993.tb00115.x. [DOI] [PubMed] [Google Scholar]
  14. Kreil G. Transfer of proteins across membranes. Annu Rev Biochem. 1981;50:317–348. doi: 10.1146/annurev.bi.50.070181.001533. [DOI] [PubMed] [Google Scholar]
  15. Kühn E. R., Huybrechts L., Govaerts F., Verbeeck E., Ollevier F. The thyroxine-stimulating activity is only present in the glycoprotein and not in the protein fraction of a carp hypophyseal homogenate. Gen Comp Endocrinol. 1986 Sep;63(3):321–327. doi: 10.1016/0016-6480(86)90130-9. [DOI] [PubMed] [Google Scholar]
  16. Licht P., Papkoff H., Farmer S. W., Muller C. H., Tsui H. W., Crews D. Evolution of gonadotropin structure and function. Recent Prog Horm Res. 1976;33:169–248. doi: 10.1016/b978-0-12-571133-3.50012-x. [DOI] [PubMed] [Google Scholar]
  17. MacKenzie D. S., Licht P., Papkoff H. Purification of thyrotropin from the pituitaries of two turtles: the green sea turtle and the snapping turtle. Gen Comp Endocrinol. 1981 Sep;45(1):39–48. doi: 10.1016/0016-6480(81)90166-0. [DOI] [PubMed] [Google Scholar]
  18. MacKenzie D. S., Licht P., Papkoff H. Thyrotropin from amphibian (Rana catesbeiana) pituitaries and evidence for heterothyrotropic activity of bullfrog luteinizing hormone in reptiles. Gen Comp Endocrinol. 1978 Dec;36(4):566–574. doi: 10.1016/0016-6480(78)90097-7. [DOI] [PubMed] [Google Scholar]
  19. MacKenzie D. S. Stimulation of the thyroid gland of a teleost fish, Gillichthys mirabilis, by tetrapod pituitary glycoprotein hormones. Comp Biochem Physiol A Comp Physiol. 1982;72(3):477–482. doi: 10.1016/0300-9629(82)90111-6. [DOI] [PubMed] [Google Scholar]
  20. Marchelidon J., Huet J. C., Salmon C., Pernollet J. C., Fontaine Y. A. Purification et caractérisation des sous-unités présumées de l'hormone thyréotrope d'un poisson télóestéen, l'anguille (Anguilla anguilla). C R Acad Sci III. 1991;313(6):253–258. [PubMed] [Google Scholar]
  21. Maurer R. A. Analysis of several bovine lutropin beta subunit cDNAs reveals heterogeneity in nucleotide sequence. J Biol Chem. 1985 Apr 25;260(8):4684–4687. [PubMed] [Google Scholar]
  22. Maurer R. A., Croyle M. L., Donelson J. E. The sequence of a cloned cDNA for the beta subunit of bovine thyrotropin predicts a protein containing both NH2-and COOH-terminal extensions. J Biol Chem. 1984 Apr 25;259(8):5024–5027. [PubMed] [Google Scholar]
  23. Morley J. E. Neuroendocrine control of thyrotropin secretion. Endocr Rev. 1981 Fall;2(4):396–436. doi: 10.1210/edrv-2-4-396. [DOI] [PubMed] [Google Scholar]
  24. Mullin B. R., Fishman P. H., Lee G., Aloj S. M., Ledley F. D., Winand R. J., Kohn L. D., Brady R. O. Thyrotropin-ganglioside interactions and their relationship to the structure and function of thyrotropin receptors. Proc Natl Acad Sci U S A. 1976 Mar;73(3):842–846. doi: 10.1073/pnas.73.3.842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ng T. B., Idler D. R., Eales J. G. Pituitary hormones that stimulate the thyroidal system in teleost fishes. Gen Comp Endocrinol. 1982 Nov;48(3):372–389. doi: 10.1016/0016-6480(82)90150-2. [DOI] [PubMed] [Google Scholar]
  26. Papkoff H., Licht P., Bona-Gallo A., MacKenzie D. S., Oelofsen W., Oosthuizen M. M. Biochemical and immunological characterization of pituitary hormones from the ostrich (Struthio camelus). Gen Comp Endocrinol. 1982 Oct;48(2):181–195. doi: 10.1016/0016-6480(82)90016-8. [DOI] [PubMed] [Google Scholar]
  27. Pierce J. G., Parsons T. F. Glycoprotein hormones: structure and function. Annu Rev Biochem. 1981;50:465–495. doi: 10.1146/annurev.bi.50.070181.002341. [DOI] [PubMed] [Google Scholar]
  28. Rathnam P., Saxena B. B. Studies on modification of tryptophan, methionine, tyrosine and arginine residues of human follicle-stimulating hormone and its subunits. Biochim Biophys Acta. 1979 Jan 25;576(1):81–87. doi: 10.1016/0005-2795(79)90486-0. [DOI] [PubMed] [Google Scholar]
  29. Sairam M. R., Bhargavi G. N. A role for glycosylation of the alpha subunit in transduction of biological signal in glycoprotein hormones. Science. 1985 Jul 5;229(4708):65–67. doi: 10.1126/science.2990039. [DOI] [PubMed] [Google Scholar]
  30. Sairam M. R., Li C. H. Human pituitary lutropin. Isolation, properties, and the complete amino acid sequence of the beta-subunit. Biochim Biophys Acta. 1975 Nov 18;412(1):70–81. [PubMed] [Google Scholar]
  31. Sairam M. R., Li C. H. Human pituitary thyrotropin. The primary structure of the alpha and beta subunits. Can J Biochem. 1977 Jul;55(7):755–760. doi: 10.1139/o77-108. [DOI] [PubMed] [Google Scholar]
  32. Sekine S., Saito A., Itoh H., Kawauchi H., Itoh S. Molecular cloning and sequence analysis of chum salmon gonadotropin cDNAs. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8645–8649. doi: 10.1073/pnas.86.22.8645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Suzuki K., Kanamori A., Nagahama Y., Kawauchi H. Development of salmon GTH I and GTH II radioimmunoassays. Gen Comp Endocrinol. 1988 Sep;71(3):459–467. doi: 10.1016/0016-6480(88)90275-4. [DOI] [PubMed] [Google Scholar]
  34. Suzuki K., Kawauchi H., Nagahama Y. Isolation and characterization of two distinct gonadotropins from chum salmon pituitary glands. Gen Comp Endocrinol. 1988 Aug;71(2):292–301. doi: 10.1016/0016-6480(88)90257-2. [DOI] [PubMed] [Google Scholar]
  35. Swanson P., Dickhoff W. W., Gorbman A. Pituitary thyrotropin and gonadotropin of coho salmon (Oncorhynchus kisutch): separation by chromatofocusing. Gen Comp Endocrinol. 1987 Feb;65(2):269–287. doi: 10.1016/0016-6480(87)90175-4. [DOI] [PubMed] [Google Scholar]
  36. Swanson P., Grau E. G., Helms L. M., Dickhoff W. W. Thyrotropic activity of salmon pituitary glycoprotein hormones in the Hawaiian parrotfish thyroid in vitro. J Exp Zool. 1988 Feb;245(2):194–199. doi: 10.1002/jez.1402450208. [DOI] [PubMed] [Google Scholar]
  37. Tagawa M., Hirano T. Changes in tissue and blood concentrations of thyroid hormones in developing chum salmon. Gen Comp Endocrinol. 1989 Dec;76(3):437–443. doi: 10.1016/0016-6480(89)90140-8. [DOI] [PubMed] [Google Scholar]
  38. Tagawa M., Hirano T. Presence of thyroxine in eggs and changes in its content during early development of chum salmon, Oncorhynchus keta. Gen Comp Endocrinol. 1987 Oct;68(1):129–135. doi: 10.1016/0016-6480(87)90068-2. [DOI] [PubMed] [Google Scholar]
  39. Wallis M. The molecular evolution of pituitary hormones. Biol Rev Camb Philos Soc. 1975 Feb;50(1):35–98. doi: 10.1111/j.1469-185x.1975.tb00989.x. [DOI] [PubMed] [Google Scholar]

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