Ablation of GalNAc-4-sulfotransferase-1 enhances reproduction by altering the carbohydrate structures of luteinizing hormone in mice

Journal of Clinical Investigation

Volumn 118, Issue 5, 2008, Pages 1815-1824

  Mi, Yiling ^a   Fiete, Dorothy ^a   Baenziger, Jacques U ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; FOLLITROPIN; GLYCOPROTEIN; LECTIN; LUTEINIZING HORMONE; N ACETYLGALACTOSAMINE 4 SULFOTRANSFERASE 1; PROGESTERONE; SULFOTRANSFERASE; TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; FEMALE FERTILITY; FERTILITY; GLYCOSYLATION; HORMONE ACTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LUTEINIZING HORMONE BLOOD LEVEL; MALE; MORPHOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RADIOIMMUNOASSAY; REPRODUCTION; SEMINAL VESICLE; SEXUAL MATURATION; SOUTHERN BLOTTING; TESTIS; WESTERN BLOTTING;

ANIMALS; CARBOHYDRATES; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; LUTEINIZING HORMONE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR STRUCTURE; ORGAN SIZE; REPRODUCTION; SEMINAL VESICLES; SULFATES; SULFOTRANSFERASES; TESTIS; TESTOSTERONE; UTERUS;

EID: 43049118590     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI32467     Document Type: Article

References (62)

1. Ying, S.Y. 1988. Inhibins, activins, and follistatins: gonadal proteins modulating the secretion of follicle-stimulating hormone. Endocr. Rev. 9:267-293.
2. Strauss, J.F., 3rd, and Penning, T.M. 1999. Synthesis of the sex steroid hormones: molecular and structural biology with applications to clinical practise. In Molecular biology in reproductive medicine. B.C.J.M. Fauser, A.J. Rutherford, J.F. Strauss, 3rd, and A. Van Steirteghem, editors. The Parthenon Publishing Group. Carnforth, United Kingdom. 201-232.
3. Bousfield, G.R., Perry, W.M., and Ward, D.N. 1994. Gonadotropins. Chemistry and biosynthesis. In The physiology of reproduction. E. Knobil, and J.D. Neill, editors. Raven Press. New York, New York, USA. 1749-1792.
4. Clarke, I.J., and Cummins, J.T. 1982. The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH) secretion in ovariectomized ewes. Endocrinology. 111:1737-1739.
5. Belchetz, P.E., Plant, T.M., Nakai, Y., Keogh, E.J., and Knobil, E. 1978. Hypophysial responses to continuous and intermittent delivery of hypopthalamic gonadotropin-releasing hormone. Science. 202:631-633.
6. Marshall, J.C., and Kelch, R.P. 1979. Low dose pulsatile gonadotropin-releasing hormone in anorexia nervosa: a model of human pubertal development. J. Clin. Endocrinol. Metab. 49:712-718.
7. Ascoli, M., Fanelli, F., and Segaloff, D.L. 2002. The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23:141-174.
8. Achermann, J.C., Ozisik, G., Meeks, J.J., and Jameson, J.L. 2002. Genetic causes of human reproductive disease. J. Clin. Endocrinol. Metab. 87:2447-2454.
9. Achermann, J.C., and Jameson, J.L. 1999. Fertility and infertility: genetic contributions from the hypothalamic-pituitary-gonadal axis. Mol. Endocrinol. 13:812-818.
10. Seminara, S.B., and Crowley, W.F., Jr. 2001. Perspective: the importance of genetic defects in humans in elucidating the complexities of the hypothalamic-pituitary-gonadal axis. Endocrinology. 142:2173-2177.
11. Themmen, A.P.N., and Huhtaniemi, I.T. 2000. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr. Rev. 21:551-583.
12. Manzella, S.M., Hooper, L.V., and Baenziger, J.U. 1996. Oligosaccharides containing β1,4-linked N-acetylgalactosamine, a paradigm for protein-specific glycosylation. J. Biol. Chem. 271:12117-12120.
13. Combarnous, Y. 1992. Molecular basis of the specificity of binding of glycoprotein hormones to their receptors. Endocr. Rev. 13:670-691.
14. Manzella, S.M., et al. 1995. Evolutionary conservation of the sulfated oligosaccharides on vertebrate glycoprotein hormones that control circulatory half-life. J. Biol. Chem. 270:21665-21671.
15. 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.
16. Pierce, J.G., and Parsons, T.F. 1981. Glycoprotein hormones: structure and function. Annu. Rev. Biochem. 50:465-495.
17. Parsons, T.F., and Pierce, J.G. 1980. Oligosaccharide moieties of glycoprotein hormones: bovine lutropin resists enzymatic deglycosylation because of terminal O-sulfated N-acetylhexosamines. Proc. Natl. Acad. Sci. U. S. A. 77:7089-7093.
18. Green, E.D., and Baenziger, J.U. 1988. Asparagine-linked oligosaccharides on lutropin, follitropin, and thyrotropin: II. Distributions of sulfated and sialylated oligosaccharides on bovine, ovine, and human glycoprotein hormones. J. Biol. Chem. 263:36-44.
19. Green, E.D., and Baenziger, J.U. 1988. Asparagine-linked oligosaccharides on lutropin, follitropin, and thyrotropin: I. Structural elucidation of the sulfated and sialylated oligosaccharides on bovine, ovine, and human pituitary glycoprotein hormones. J. Biol. Chem. 263:25-35.
20. Green, E.D., Van Halbeek, H., Boime, I., and Baenziger, J.U. 1985. Structural elucidation of the disulfated oligosaccharide from bovine lutropin. J. Biol. Chem. 260:15623-15630.
21. Mengeling, B.J., Manzella, S.M., and Baenziger, J.U. 1995. A cluster of basic amino acids within an ahelix is essential for a-subunit recognition by the glycoprotein hormone N-acetylgalactosaminyltransferase. Proc. Natl. Acad. Sci. U. S. A. 92:502-506.
22. Smith, P.L., and Baenziger, J.U. 1992. Molecular basis of recognition by the glycoprotein hormone-specific N-acetylgalactosamine-transferase. Proc. Natl. Acad. Sci. U. S. A. 89:329-333.
23. Baenziger, J.U., and Green, E.D. 1991. Structure, synthesis, and function of the asparagine-linked oligosaccharides on pituitary glycoprotein hormones. In Biology of carbohydrates, volume 3. V. Ginsberg and P.W. Robbins, editors. JAI Press Ltd. London, United Kingdom. 1-46.
24. Smith, P.L., and Baenziger, J.U. 1990. Recognition by the glycoprotein hormone-specific N-acetylgalactosaminetransferase is independent of hormone native conformation. Proc. Natl. Acad. Sci. U. S. A. 87:7275-7279.
25. Smith, P.L., and Baenziger, J.U. 1988. A pituitary N-acetylgalactosamine transferase that specifically recognizes glycoprotein hormones. Science. 242:930-933.
26. 4-4-GalNAcβ1,4GlcNAcβ1,2Manα-specific receptor from rat liver. J. Biol. Chem. 272:14629-14637.
27. 4- 4GalNAcβ1,4GlcNAcβ 1,2Manα that mediates rapid clearance of lutropin. Cell. 67:1103-1110.
28. 4 binding. Proc. Natl. Acad. Sci. U. S. A. 95:2089-2093.
29. 4-4-GalNAcβ1,4GlcNAcβ or Man at independent sites. Proc. Natl. Acad. Sci. U. S. A. 94:11256-11261.
30. Kang, H.G., Evers, M.R., Xia, G., Baenziger, J.U., and Schachner, M. 2001. Molecular cloning and expression of an N-acetylgalactosamine-4-O- sulfotransferase that transfers sulfate to terminal and nonterminal beta 1,4-linked N-acetylgalactosamine. J. Biol. Chem. 276:10861-10869.
31. Xia, G., Evers, M.R., Kang, H.-G., Schachner, M., and Baenziger, J.U. 2000. Molecular cloning and expression of the pituitary glycoprotein hormone N-acetylgalactosamine-4-O-sulfotransferase. J. Biol. Chem. 275:38402-38409.
32. Hiraoka, N., Misra, A., Belot, F., Hindsgaul, O., and Fukuda, M. 2001. Molecular cloning and expression of two distinct human N-acetylgalactosamine 4-O-sulfotransferases that transfer sulfate to GalNAcβ14GlcNAcβ1R in both N- and O-glycans. Glycobiology. 11:495-504.
33. Boregowda, R.K., Mi, Y., Bu, H., and Baenziger, J.U. 2005. Differential expression and enzymatic properties of GalNAc-4-sulfotransferase-1 and GalNAc-4-sulfotransferase-2. Glycobiology. 15:1349-1358.
34. 4-receptor is critical for implantation in vivo. J. Clin. Invest. 109:269-276.
35. Baenziger, J.U., Kumar, S., Brodbeck, R.M., Smith, P.L., and Beranek, M.C. 1992. Circulatory half-life but not interaction with the lutropin/chorionic gonadotropin receptor is modulated by sulfation of bovine lutropin oligosaccharides. Proc. Natl. Acad. Sci. U. S. A. 89:334-338.
36. Smith, P.L., Kaetzel, D., Nilson, J., and Baenziger, J.U. 1990. The sialylated oligosaccharides of recombinant bovine lutropin modulate hormone bioactivity. J. Biol. Chem. 265:874-881.
37. Rivier, J.E., et al. 1995. Gonadotropin-releasing hormone antagonists: novel members of the azaline B family. J. Med. Chem. 38:2649-2662.
38. Herbst, K.L., Anawalt, B.D., Amory, J.K., and Bremner, W.J. 2002. Acyline: the first study in humans of a potent, new gonadotropin-releasing hormone antagonist. J. Clin. Endocrinol. Metab. 87:3215-3220.
39. Park, E.I., Manzella, S.M., and Baenziger, J.U. 2003. Rapid clearance of sialylated glycoproteins by the asialoglycoprotein receptor. J. Biol. Chem. 278:4597-4602.
40. Park, E.I., Mi, Y., Unverzagt, C., Gabius, H.J., and Baenziger, J.U. 2005. The asialoglycoprotein receptor clears glycoconjugates terminating with sialic acid alpha 2,6GalNAc. Proc. Natl. Acad. Sci. U. S. A. 102:17125-17129.
41. Ashwell, G., and Harford, J. 1982. Carbohydrate-specific receptors of the liver. Annu. Rev. Biochem. 51:531-554.
42. Mengeling, B.J., et al. 1991. A microplate assay for analysis of solution phase glycosyltransferase reactions: determination of kinetic constants. Anal. Biochem. 199:286-292.
43. Torres, B.R., McCrumb, D.K., and Smith, D.F. 1988. Glycolipid-lectin interactions: reactivity of lectins from helix pomatia, wisteria floribunda, and dolichos biflorus with glycolipids containing N-acetylgalactosamine. Arch. Biochem. Biophys. 262:1-11.
44. Van Damme, E.J., Barre, A., Rouge, P., Van Leuven, F., and Peumans, W.J. 1996. The NeuAc(alpha-2,6)-Gal/GalNAc-binding lectin from elderberry (Sambucus nigra) bark, a type-2 ribosome-inactivating protein with an unusual specificity and structure. Eur. J. Biochem. 235:128-137.
45. Shibuya, N., et al. 1987. The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(alpha 2-6)Gal/GalNAc sequence. J. Biol. Chem. 262:1596-1601.
46. Park, E.I., and Baenziger, J.U. 2004. Closely related mammals have distinct asialoglycoprotein receptor carbohydrate specificities. J. Biol. Chem. 279:40954-40959.
47. Dharmesh, S.M., and Baenziger, J.U. 1993. Estrogen modulates expression of the glycosyltransferases that synthesize sulfated oligosaccharides on lutropin. Proc. Natl. Acad. Sci. U. S. A. 90:11127-11131.
48. Fiete, D., Mi, Y., Oats, E.L., Beranek, M.C., and Baenziger, J.U. 2007. N-linked oligosaccharides on the low density lipoprotein receptor homolog SorLA/LR11 are modified with terminal GalNAc-4-SO4 in kidney and brain. J. Biol. Chem. 282:1873-1881.
49. 4 [abstract]. Glycobiology. 11:45.
50. Kero, J., et al. 2000. Elevated luteinizing hormone induces expression of its receptor and promotes steroidogenesis in the adrenal cortex. J. Clin. Invest. 105:633-641.
51. Risma, K.A., Hirshfield, A.N., and Nilson, J.H. 1997. Elevated luteinizing hormone in prepubertal transgenic mice causes hyperandrogenemia, precocious puberty, and substantial ovarian pathology. Endocrinology. 138:3540-3547.
52. Risma, K.A., et al. 1995. Targeted overexpression of luteinizing hormone in transgenic mice leads to infertility, polycystic ovaries, and ovarian tumors. Proc. Natl. Acad. Sci. U. S. A. 92:1322-1326.
53. Matzuk, M.M., DeMayo, F.J., Hadsell, L.A., and Kumar, T.R. 2003. Overexpression of human chorionic gonadotropin causes multiple reproductive defects in transgenic mice. Biol. Reprod. 69:338-346.
54. Ahtiainen, P., et al. 2007. Phenotypic characterisation of mice with exaggerated and missing LH/hCG action. Mol. Cell. Endocrinol. 260-262:255-263.
55. Rulli, S.B., et al. 2003. Elevated steroidogenesis, defective reproductive organs, and infertility in transgenic male mice overexpressing human chorionic gonadotropin. Endocrinology. 144:4980-4990.
56. Rulli, S.B., et al. 2002. Reproductive disturbances, pituitary lactotrope adenomas, and mammary gland tumors in transgenic female mice producing high levels of human chorionic gonadotropin. Endocrinology. 143:4084-4095.
57. Cheng, S., Fockler, C., Barnes, W.M., and Higuchi, R. 1994. Effective amplification of long targets from cloned inserts and human genomic DNA. Proc. Natl. Acad. Sci. U. S. A. 91:5695-5699.
58. Barnes, W.M. 1994. PCR amplification of up to 35-kb DNA with high fidelity and high yield from lambda bacteriophage templates. Proc. Natl. Acad. Sci. U. S. A. 91:2216-2220.
59. Barnes, W.M. 2003. In PCR primer: a laboratory manual. C.W.a.D. Dieffenbach, G.S., editor. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, New York, USA. 441-449.
60. Allen, E. 1922. The oestrus cycle in the mouse. Am. J. Anat. 30:297-371.
61. Green, E.D., Baenziger, J.U., and Boime, I. 1985. Cell-free sulfation of human and bovine pituitary hormones: comparison of the sulfated oligosaccharides of lutropin, follitropin, and thyrotropin. J. Biol. Chem. 260:15631-15638.
62. Hindsgaul, V., Hindsgaul, O., and Baenziger, J.U. 1987. Synthesis of oligosaccharide structures unique to pituitary glycoprotein hormones. Can. J. Chem. 65:1645-1652.