Female infertility in grt mice is caused by thyroid hormone deficiency, not by insufficient TPST2 activity in the reproductive organs

Journal of Veterinary Medical Science

Volumn 70, Issue 10, 2008, Pages 1043-1049

  Hosoda, Yayoi ^a   Sasaki, Nobuya ^a   Agui, Takashi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Female infertility; Growth retarded mouse; Hypothyroidism; Tyrosylprotein sulfotransferase

Indexed keywords

SULFOTRANSFERASE; THYROID HORMONE; TPST2 PROTEIN, MOUSE;

ANIMAL; ANIMAL DISEASE; ARTICLE; CONGENITAL HYPOTHYROIDISM; CYTOCHEMISTRY; ENZYMOLOGY; EXPERIMENTAL ANIMAL; FEMALE; FEMALE INFERTILITY; GENETICS; LITTER SIZE; MALE; METABOLISM; MOUSE; NEWBORN; ORGAN SIZE; OVARY; PHYSIOLOGY; PREGNANCY; UTERUS; WESTERN BLOTTING;

ANIMALS; ANIMALS, LABORATORY; ANIMALS, NEWBORN; BLOTTING, WESTERN; CONGENITAL HYPOTHYROIDISM; FEMALE; HISTOCYTOCHEMISTRY; INFERTILITY, FEMALE; LITTER SIZE; MALE; MICE; ORGAN SIZE; OVARY; PREGNANCY; SULFOTRANSFERASES; THYROID HORMONES; UTERUS;

MUS;

EID: 55749103691     PISSN: 09167250     EISSN: 13477439     Source Type: Journal    
DOI: 10.1292/jvms.70.1043     Document Type: Article

References (42)

1. Abel, M. H., Wootton, A. N., Wilkins, V., Huhtaniemi, I., Knight, P. G. and Charlton, H. M. 2000. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 141: 1795-1803.
2. Amendola, E., De Luca, P., Macchia, P. E., Terracciano, D., Rosica, A., Chiappetta, G., Kimura, S., Mansouri, A., Affuso, A., Arra, C., Macchia, V., Di Lauro, R. and De Felice, M. 2005. A mouse model demonstrates a multigenic origin of congenital hypothyroidism. Endocrinology 146: 5038-5047.
3. Armada-Dias, L., Carvalho, J. J., Breitenbach, M. M., Franci, C. R. and Moura, E. G. 2001. Is the infertility in hypothyroidism mainly due to ovarian or pituitary functional changes? Braz. J. Med. Biol. Res. 34: 1209-1215.
4. Bonomi, M., Busnelli, M., Persani, L., Vassart, G. and Costagliola, S. 2006. Structural differences in the hinge region of the glycoprotein hormone receptors: evidence from the sulfated tyrosine residues. Mol. Endocrinol. 20: 3351-3363.
5. Borghei, A., Ouyang, Y. B., Westmuckett, A. D., Marcello, M. R., Landel, C. P., Evans, J. P. and Moore, K. L. 2006. Targeted disruption of tyrosylprotein sulfotransferase-2, an enzyme that catalyzes post-translational protein tyrosine O-sulfation, causes male infertility. J. Biol. Chem. 281: 9423-9431.
6. Cecconi, S., Rucci, N., Scaldaferri, M. L., Masciulli, M. P., Rossi, G., Moretti, C., D'Armiento, M. and Ulisse, S. 1999. Thyroid hormone effects on mouse oocyte maturation and granulosa cell aromatase activity. Endocrinology 140: 1783-1788.
7. Chan, W. K. and Tan, C. H. 1986. Inhibition of follicle-stimulating hormone induction of aromatase activity in porcine granulosa cells by thyroxine and triiodothyronine. Endocrinology 119: 2353-2359.
8. Choe, H., Li, W., Wright, P. L., Vasilieva, N., Venturi, M., Huang, C. C., Grundner, C., Dorfman, T., Zwick, M. B., Wang, L., Rosenberg, E. S., Kwong, P. D., Burton, D. R., Robinson, J. E., Sodroski, J. G. and Farzan, M. 2003. Tyrosine sulfation of human antibodies contributes to recognition of the CCR5 binding region of HIV-1 gp120. Cell 114: 161-170.
9. Choksi, N. Y., Jahnke, G. D., St Hilaire, C. and Shelby, M. 2003. Role of thyroid hormones in human and laboratory animal reproductive health. Birth. Defects. Res. B. Dev. Reprod. Toxicol. 68: 479-491.
10. Costagliola, S., Panneels, V., Bonomi, M., Koch, J., Many, M. C., Smits, G. and Vassart, G. 2002. Tyrosine sulfation is required for agonist recognition by glycoprotein hormone receptors. Embo. J. 21: 504-513.
11. Dorfman, T., Moore, M. J., Guth, A. C., Choe, H. and Farzan, M. 2006. A tyrosine-sulfated peptide derived from the heavy-chain CDR3 region of an HIV-1-neutralizing antibody binds gp120 and inhibits HIV-1 infection. J. Biol. Chem. 281: 28529-28535.
12. Furudate, S., Ono, M., Shibayama, K., Ohyama, Y., Kuwada, M., Kimura, T. and Kameya, T. 2005. Rescue from Dwarfism by Thyroid Function Compensation in rdw Rats. Exp. Anim. 54: 455-460.
13. Goldman, S., Dirnfeld, M., Abramovici, H. and Kraiem, Z. 1993. Triiodothyronine (T3) modulates hCG-regulated progesterone secretion, cAMP accumulation and DNA content in cultured human luteinized granulosa cells. Mol. Cell. Endocrinol. 96: 125-131.
14. Gothe, S., Wang, Z., Ng, L., Kindblom, J. M., Barros, A. C., Ohlsson, C., Vennstrom, B. and Forrest, D. 1999. Mice devoid of all known thyroid hormone receptors are viable but exhibit disorders of the pituitary-thyroid axis, growth, and bone maturation. Genes. Dev. 13: 1329-1341.
15. Hatsuta, M., Abe, K., Tamura, K., Ryuno, T., Watanabe, G., Taya, K. and Kogo, H. 2004. Effects of hypothyroidism on the estrous cycle and reproductive hormones in mature female rat. Eur. J. Pharmacol. 486: 343-348.
16. Jiang, J. Y., Imai, Y., Umezu, M. and Sato, E. 2001. Characteristics of infertility in female hypothyroid (hyt) mice. Reproduction 122: 695-700.
17. Jiang, J. Y., Umezu, M. and Sato, E. 2000. Improvement of follicular development rather than gonadotrophin secretion by thyroxine treatment in infertile immature hypothyroid rdw rats. J. Reprod. Fertil. 119: 193-199.
18. Kim, T. H., Hwang, S. B., Jeong, P. Y., Lee, J. and Cho, J. W. 2005. Requirement of tyrosylprotein sulfotransferase-A for proper cuticle formation in the nematode C. elegans. FEBS Lett. 579: 53-58.
19. Kobayashi, K., Kubota, H. and Saegusa, J. 2007. Testicular development in growth-retarded mice. Exp. Anim. (Tokyo) 56: 393-397.
20. Kobayashi, K., Yamamoto, H., Kobayashi, T. and Machida, T. 2001. Responses of the thyroid gland to TSH and other thyroid stimulators in the growth retarded (grt) mouse. Zool. Sci. 18: 955-961.
21. Krassas, G. E. 2000. Thyroid disease and female reproduction. Fertil. Steril. 74: 1063-1070.
22. LaFranchi, S. 2006. Thyroid hormone in hypopituitarism, Graves' disease, congenital hypothyroidism, and maternal thyroid disease during pregnancy. Growth Horm. IGF Res. 16: 20-24.
23. Ma, X., Dong, Y., Matzuk, M. M. and Kumar, T. R. 2004. Targeted disruption of luteinizing hormone beta-subunit leads to hypogonadism, defects in gonadal steroidogenesis, and infertil ity. Proc. Natl. Acad. Sci. U. S. A. 101: 17294-17299.
24. Marchese, P., Murata, M., Mazzucato, M., Pradella, P., De Marco, L., Ware, J. and Ruggeri, Z. M. 1995. Identification of three tyrosine residues of glycoprotein Ib alpha with distinct roles in von Willebrand factor and alpha-thrombin binding. J. Biol. Chem. 270: 9571-9578.
25. Maruo, T., Hayashi, M., Matsuo, H., Yamamoto, T., Okada, H. and Mochizuki, M. 1987. The role of thyroid hormone as a biological amplifier of the actions of follicle-stimulating hormone in the functional differentiation of cultured porcine granulosa cells. Endocrinology 121: 1233-1241.
26. Meh, D. A., Siebenlist, K. R., Brennan, S. O., Holyst, T. and Mosesson, M. W. 2001. The amino acid sequence in fibrin responsible for high affinity thrombin binding. Thromb Haemost. 85: 470-474.
27. Mittag, J., Friedrichsen, S., Heuer, H., Polsfuss, S., Visser, T. J. and Bauer, K. 2005. Athyroid Pax8-/- mice cannot be rescued by the inactivation of thyroid hormone receptor alpha1. Endocrinology 146: 3179-3184.
28. Moore, K. L. 2003. The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278: 24243-24246.
29. Niehrs, C., Huttner, W. B., Carvallo, D. and Degryse, E. 1990. Conversion of recombinant hirudin to the natural form by in vitro tyrosine sulfation. Differential substrate specificities of leech and bovine tyrosylprotein sulfotransferases. J. Biol. Chem. 265: 9314-9318.
30. Ouyang, Y. B., Crawley, J. T., Aston, C. E. and Moore, K. L. 2002. Reduced body weight and increased postimplantation fetal death in tyrosylprotein sulfotransferase-1-deficient mice. J. Biol. Chem. 277: 23781-23787.
31. Ouyang, Y. B. and Moore, K. L. 1998. Molecular cloning and expression of human and mouse tyrosylprotein sulfotransferase-2 and a tyrosylprotein sulfotransferase homologue in Caenorhabditis elegans. J. Biol. Chem. 273: 24770-24774.
32. Panciera, D. L., Purswell, B. J. and Kolster, K. A. 2007. Effect of short-term hypothyroidism on reproduction in the bitch. Theriogenology 68: 316-321.
33. Pittman, D. D., Tomkinson, K. N., Michnick, D., Selighsohn, U. and Kaufman, R. J. 1994. Posttranslational sulfation of factor V is required for efficient thrombin cleavage and activation and for full procoagulant activity. Biochemistry 33: 6952-6959.
34. Pouyani, T. and Seed, B. 1995. PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell 83: 333-343.
35. Rabut, G. E., Konner, J. A., Kajumo, F., Moore, J. P. and Dragic, T. 1998. Alanine substitutions of polar and nonpolar residues in the amino-terminal domain of CCR5 differently impair entry of macrophage- and dualtropic isolates of human immunodeficiency virus type 1. J. Virol. 72: 3464-3468.
36. Sasaki, N., Hosoda, Y., Nagata, A., Ding, M., Cheng, J. M., Miyamoto, T., Okano, S., Asano, A., Miyoshi, I. and Agui, T. 2007. A mutation in Tpst2 encoding tyrosylprotein sulfotransferase causes dwarfism associated with hypothyroidism. Mol. Endocrinol. 21: 1713-1721.
37. Seibert, C., Cadene, M., Sanfiz, A., Chait, B. T. and Sakmar, T. P. 2002. Tyrosine sulfation of CCR5 N-terminal peptide by tyrosylprotein sulfotransferases 1 and 2 follows a discrete pattern and temporal sequence. Proc. Natl. Acad. Sci. U.S.A. 99: 11031-11036.
38. Tapanainen, J. S., Aittomaki, K., Min, J., Vaskivuo, T. and Huhtaniemi, I. T. 1997. Men homozygous for an inactivating mutation of the follicle-stimulating hormone (FSH) receptor gene present variable suppression of spermatogenesis and fertility. Nat. Genet. 15: 205-206.
39. Wakim, A. N., Polizotto, S. L. and Burholt, D. R. 1995. Augmentation by thyroxine of human granulosa cell gonadotrophin-induced steroidogenesis. Hum. Reprod. 10: 2845-2848.
40. Westmuckett, A. D., Hoffhines, A. J., Borghei, A. and Moore, K. L. 2008. Early postnatal pulmonary failure and primary hypothyroidism in mice with combined TPST-1 and TPST-2 deficiency. Gen. Comp. Endocrinol. 156: 145-153.
41. Yoshida, T., Yamanaka, K., Atsumi, S., Tsumura, H., Sasaki, R., Tomita, K., Ishikawa, E., Ozawa, H., Watanabe, K. and Totsuka, T. 1994. A novel hypothyroid 'growth-retarded' mouse derived from Snell's dwarf mouse. J. Endocrinol. 142: 435-446.
42. Zhang, F. P., Poutanen, M., Wilbertz, J. and Huhtaniemi, I. 2001. Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol. Endocrinol. 15: 172-183.