Tissue-specific posttranslational modification allows functional targeting of thyrotropin

Cell Reports

Volumn 9, Issue 3, 2014, Pages 801-809

  Ikegami, Keisuke ^a,d   Liao, Xiao Hui ^b   Hoshino, Yuta ^a   Ono, Hiroko ^a   Ota, Wataru ^a   Ito, Yuka ^a   Nishiwaki Ohkawa, Taeko ^a   Sato, Chihiro ^a   Kitajima, Ken ^a   Iigo, Masayuki ^c   Shigeyoshi, Yasufumi ^d   Yamada, Masanobu ^e   Murata, Yoshiharu ^a   Refetoff, Samuel ^b   Yoshimura, Takashi ^a,f  

^a NAGOYA UNIVERSITY   (Japan)

^b UNIVERSITY OF CHICAGO   (United States)

^c UTSUNOMIYA UNIVERSITY   (Japan)

^d KINKI UNIVERSITY   (Japan)

^e GUNMA UNIVERSITY   (Japan)

^f NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; GLYCAN; IMMUNOGLOBULIN; THYROTROPIN; ALBUMINOID; IMMUNOGLOBULIN G; PROTIRELIN;

ANIMAL TISSUE; ARTICLE; BEHAVIOR; BIOLOGICAL ACTIVITY; COMPLEX FORMATION; CONTROLLED STUDY; HORMONE METABOLISM; HYPOPHYSIS PARS DISTALIS; HYPOPHYSIS PARS TUBERALIS; LIVER METABOLISM; MOLECULAR INTERACTION; NONHUMAN; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; SIALYLATION; THYROTROPIN RELEASE; TISSUE SPECIFICITY; ADENOHYPOPHYSIS; ANIMAL; ANTIBODY SPECIFICITY; BLOOD; C57BL MOUSE; GLYCOSYLATION; METABOLISM;

ALBUMINS; ANIMALS; GLYCOSYLATION; IMMUNOGLOBULIN G; MICE, INBRED C57BL; ORGAN SPECIFICITY; PITUITARY GLAND, ANTERIOR; PROTEIN PROCESSING, POST-TRANSLATIONAL; THYROTROPIN; THYROTROPIN-RELEASING HORMONE;

EID: 84919771200     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.10.006     Document Type: Article

References (52)

1. Aksentijevich, I., Sachs, D.H., and Sykes, M. (1991). Natural antibodies against bone marrow cells of a concordant xenogeneic species. J. Immunol. 147, 79-85.
2. Andersen, S., Pedersen, K.M., Bruun, N.H., and Laurberg, P. (2002). Narrow individual variations in serum T(4) and T(3) in normal subjects: a clue to the understanding of subclinical thyroid disease. J. Clin. Endocrinol. Metab. 87, 1068-1072.
3. Baenziger, J.U., and Green, E.D. (1988). Pituitary glycoprotein hormone oligosaccharides: structure, synthesis and function of the asparagine-linked oligosaccharides on lutropin, follitropin and thyrotropin. Biochim. Biophys. Acta 947, 287-306.
4. Baker, B.L., and Yu, Y.Y. (1971). Hypophyseal changes induced by thyroid deficiency and thyroxine administration as revealed by immunochemical staining. Endocrinology 89, 996-1004.
5. Beck-Peccoz, P., Amr, S., Menezes-Ferreira, M.M., Faglia, G., and Weintraub, B.D. (1985). Decreased receptor binding of biologically inactive thyrotropin in central hypothyroidism. Effect of treatment with thyrotropin-releasing hormone. N. Engl. J. Med. 312, 1085-1090.
6. Bergmann, M., Wittkowski, W., and Hoffmann, K. (1989). Ultrastructural localization of thyrotropin (TSH)-like immunoreactivity in specific secretory cells of the hypophyseal pars tuberalis in the Djungarian hamster, Phodopus sungorus. Cell Tissue Res. 256, 649-652.
7. Böckers, T.M., Niklowitz, P., Bockmann, J., Fauteck, J.D., Wittkowski, W., and Kreutz, M.R. (1995). Daily melatonin injections induce cytological changes in pars tuberalis-specific cells similar to short photoperiod. J. Neuroendocrinol. 7, 607-613.
8. Bockmann, J., Böckers, T.M., Winter, C., Wittkowski, W., Winterhoff, H., Deufel, T., and Kreutz, M.R. (1997). Thyrotropin expression in hypophyseal pars tuberalis-specific cells is 3,5,30-triiodothyronine, thyrotropin-releasing hormone, and pit-1 independent. Endocrinology 138, 1019-1028.
9. DeCherney, G.S., Gesundheit, N., Gyves, P.W., Showalter, C.R., and Weintraub, B.D. (1989). Alterations in the sialylation and sulfation of secreted mouse thyrotropin in primary hypothyroidism. Biochem. Biophys. Res. Commun. 159, 755-762.
10. Ebihara, S., Marks, T., Hudson, D.J., and Menaker, M. (1986). Genetic control of melatonin synthesis in the pineal gland of the mouse. Science 231, 491-493.
11. Erhardt, F.W., and Scriba, P.C. (1977). High molecular thyrotrophin ("big"-TSH) from human pituitaries: preparation and partial characterization. Acta Endocrinol. (Copenh.) 85, 698-712.
12. Gesundheit, N., Magner, J.A., Chen, T., and Weintraub, B.D. (1986). Differential sulfation and sialylation of secreted mouse thyrotropin (TSH) subunits: regulation by TSH-releasing hormone. Endocrinology 119, 455-463.
13. Hanon, E.A., Lincoln, G.A., Fustin, J.M., Dardente, H., Masson-Pévet, M., Morgan, P.J., and Hazlerigg, D.G. (2008). Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr. Biol. 18, 1147-1152.
14. Helton, T.E., and Magner, J.A. (1995). β-Galactoside α-2,3-sialyltransferase messenger RNA increases in thyrotrophs of hypothyroid mice. Thyroid 5, 315-317.
15. Ikegami, K., Katou, Y., Higashi, K., and Yoshimura, T. (2009). Localization of circadian clock protein BMAL1 in the photoperiodic signal transduction machinery in Japanese quail. J. Comp. Neurol. 517, 397-404.
16. Klosen, P., Bienvenu, C., Demarteau, O., Dardente, H., Guerrero, H., Pévet, P., and Masson-Pévet, M. (2002). The mt1 melatonin receptor and RORbeta receptor are co-localized in specific TSH-immunoreactive cells in the pars tuberalis of the rat pituitary. J. Histochem. Cytochem. 50, 1647-1657.
17. Klug, T.L., and Adelman, R.C. (1977). Evidence for a large thyrotropin and its accumulation during aging in rats. Biochem. Biophys. Res. Commun. 77, 1431-1437.
18. Kourides, I.A., Weintraub, B.D., and Maloof, F. (1978). Large molecular weight TSH-β: the sole immunoactive form of TSH-β in certain human sera. J. Clin. Endocrinol. Metab. 47, 24-33.
19. Lorand, L., and Graham, R.M. (2003). Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4, 140-156.
20. Lutz, H.U. (2012). Naturally Occurring Antibodies (NAbs) (Austin, TX: Landes Bioscience/Springer Science + Business Media).
21. Magner, J.A. (1990). Thyroid-stimulating hormone: biosynthesis, cell biology, and bioactivity. Endocr. Rev. 11, 354-385.
22. McKenzie, J.M. (1958). The bioassay of thyrotropin in serum. Endocrinology 63, 372-382.
23. Moeller, L.C., Kimura, S., Kusakabe, T., Liao, X.H., Van Sande, J., and Refetoff, S. (2003). Hypothyroidism in thyroid transcription factor 1 haploinsufficiency is caused by reduced expression of the thyroid-stimulating hormone receptor. Mol. Endocrinol. 17, 2295-2302.
24. Mori, M., Ohshima, K., Fukuda, H., Kobayashi, I., and Wakabayashi, K. (1984). Changes in the multiple components of rat pituitary TSH and TSH β subunit following thyroidectomy. Acta Endocrinol. (Copenh.) 105, 49-56.
25. Müller, W.E., and Wollert, U. (1979). Human serum albumin as a 'silent receptor' for drugs and endogenous substances. Pharmacology 19, 59-67.
26. Nakao, N., Ono, H., Yamamura, T., Anraku, T., Takagi, T., Higashi, K., Yasuo, S., Katou, Y., Kageyama, S., Uno, Y., et al. (2008). Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452, 317-322.
27. Ono, H., Hoshino, Y., Yasuo, S., Watanabe, M., Nakane, Y., Murai, A., Ebihara, S., Korf, H.W., and Yoshimura, T. (2008). Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc. Natl. Acad. Sci. USA 105, 18238-18242.
28. Perret, J., Ludgate, M., Libert, F., Gerard, C., Dumont, J.E., Vassart, G., and Parmentier, M. (1990). Stable expression of the human TSH receptor in CHO cells and characterization of differentially expressing clones. Biochem. Biophys. Res. Commun. 171, 1044-1050.
29. Persani, L., Borgato, S., Romoli, R., Asteria, C., Pizzocaro, A., and Beck-Peccoz, P. (1998). Changes in the degree of sialylation of carbohydrate chains modify the biological properties of circulating thyrotropin isoforms in various physiological and pathological states. J. Clin. Endocrinol. Metab. 83, 2486-2492.
30. Pierce, J.G., and Parsons, T.F. (1981). Glycoprotein hormones: structure and function. Annu. Rev. Biochem. 50, 465-495.
31. Pohlenz, J., Maqueem, A., Cua, K., Weiss, R.E., Van Sande, J., and Refetoff, S. (1999). Improved radioimmunoassay for measurement of mouse thyrotropin in serum: strain differences in thyrotropin concentration and thyrotroph sensitivity to thyroid hormone. Thyroid 9, 1265-1271.
32. Reiter, R.J. (1980). The pineal and its hormones in the control of reproduction in mammals. Endocr. Rev. 1, 109-131.
33. Sakai, H., Fukuda, G., Suzuki, N., Watanabe, C., and Odawara, M. (2009). Falsely elevated thyroid-stimulating hormone (TSH) level due to macro-TSH. Endocr. J. 56, 435-440.
34. Sakamoto, S., Nakamura, K., Inoue, K., and Sakai, T. (2000). Melatonin stimulates thyroid-stimulating hormone accumulation in the thyrotropes of the rat pars tuberalis. Histochem. Cell Biol. 114, 213-218.
35. Seppälä, M., Koistinen, H., Koistinen, R., Hautala, L., Chiu, P.C., and Yeung, W.S. (2009). Glycodelin in reproductive endocrinology and hormone-related cancer. Eur. J. Endocrinol. 160, 121-133.
36. Spitz, I.M., Le Roith, D., Hirsch, H., Carayon, P., Pekonen, F., Liel, Y., Sobel, R., Chorer, Z., and Weintraub, B. (1981). Increased high-molecular-weight thyrotropin with impaired biologic activity in a euthyroid man. N. Engl. J. Med. 304, 278-282.
37. Strott, C.A. (2002). Sulfonation and molecular action. Endocr. Rev. 23, 703-732.
38. Szkudlinski, M.W., Thotakura, N.R., Bucci, I., Joshi, L.R., Tsai, A., East-Palmer, J., Shiloach, J., and Weintraub, B.D. (1993). Purification and characterization of recombinant human thyrotropin (TSH) isoforms produced by Chinese hamster ovary cells: the role of sialylation and sulfation in TSH bioactivity. Endocrinology 133, 1490-1503.
39. Szkudlinski, M.W., Thotakura, N.R., and Weintraub, B.D. (1995). Subunit-specific functions of N-linked oligosaccharides in human thyrotropin: role of terminal residues of α-and β-subunit oligosaccharides in metabolic clearance and bioactivity. Proc. Natl. Acad. Sci. USA 92, 9062-9066.
40. Szkudlinski, M.W., Fremont, V., Ronin, C., and Weintraub, B.D. (2002). Thyroid-stimulating hormone and thyroid-stimulating hormone receptor structure-function relationships. Physiol. Rev. 82, 473-502.
41. Taylor, T., and Weintraub, B.D. (1989). Altered thyrotropin (TSH) carbohydrate structures in hypothalamic hypothyroidism created by paraventricular nuclear lesions are corrected by in vivo TSH-releasing hormone administration. Endocrinology 125, 2198-2203.
42. Togayachi, A., Akashima, T., Ookubo, R., Kudo, T., Nishihara, S., Iwasaki, H., Natsume, A., Mio, H., Inokuchi, J., Irimura, T., et al. (2001). Molecular cloning and characterization of UDP-GlcNAc:lactosylceramide β 1,3-N-acetylglucosaminyltransferase (β 3Gn-T5), an essential enzyme for the expression of HNK-1 and Lewis X epitopes on glycolipids. J. Biol. Chem. 276, 22032-22040.
43. Vieira, J.G.H., Maciel, R.M.B., Hauache, O.M., Nishida, S.K., Boelter, D.M.G., and Pinheiro, M.F.M.C. (2006). Unexpected high values of TSH: the presence of high molecular weight forms (macro TSH) must be investigated. Arq. Bras. Endocrinol. Metabol. 50, 445-449.
44. Walker, A.K., Soo, K.Y., Levina, V., Talbo, G.H., and Atkin, J.D. (2013). N-linked glycosylation modulates dimerization of protein disulfide isomerase family A member 2 (PDIA2). FEBS J. 280, 233-243.
45. Wheeler, S.F., and Harvey, D.J. (2001). Extension of the in-gel release method for structural analysis of neutral and sialylated N-linked glycans to the analysis of sulfated glycans: application to the glycans from bovine thyroid-stimulating hormone. Anal. Biochem. 296, 92-100.
46. Wide, L., Eriksson, K., Sluss, P.M., and Hall, J.E. (2009). Serum half-life of pituitary gonadotropins is decreased by sulfonation and increased by sialylation in women. J. Clin. Endocrinol. Metab. 94, 958-964.
47. Wittkowski, W., Bergmann, M., Hoffmann, K., and Pera, F. (1988). Photoperiod-dependent changes in TSH-like immunoreactivity of cells in the hypophysial pars tuberalis of the Djungarian hamster, Phodopus sungorus. Cell Tissue Res. 251, 183-187.
48. Wittkowski, W., Bockmann, J., Kreutz, M.R., and Böckers, T.M. (1999). Cell and molecular biology of the pars tuberalis of the pituitary. Int. Rev. Cytol. 185, 157-194.
49. Yamada, M., Saga, Y., Shibusawa, N., Hirato, J., Murakami, M., Iwasaki, T., Hashimoto, K., Satoh, T., Wakabayashi, K., Taketo, M.M., and Mori, M. (1997). Tertiary hypothyroidism and hyperglycemia in mice with targeted disruption of the thyrotropin-releasing hormone gene. Proc. Natl. Acad. Sci. USA 94, 10862-10867.
50. Yasuo, S., Yoshimura, T., Ebihara, S., and Korf, H.W. (2009). Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J. Neurosci. 29, 2885-2889.
51. 3 regulates photoperiodic response of gonads in birds. Nature 426, 178-181.
52. Zou, K., Hosono, T., Nakamura, T., Shiraishi, H., Maeda, T., Komano, H., Yanagisawa, K., and Michikawa,M. (2008). Novel role of presenilins in maturation and transport of integrin β 1. Biochemistry 47, 3370-3378.