Modulation of mannose and asialoglycoprotein receptor expression determines glycoprotein hormone half-life at critical points in the reproductive cycle

Journal of Biological Chemistry

Volumn 289, Issue 17, 2014, Pages 12157-12167

  Mi, Yiling ^a   Lin, Angela ^a   Fiete, Dorothy ^a   Steirer, Lindsay ^a   Baenziger, Jacques U ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEINS; HORMONES;

ASIALOGLYCOPROTEIN RECEPTORS; CLEARANCE RATES; GLYCAN STRUCTURES; GLYCANS; GLYCOPROTEIN HORMONES; RECEPTOR EXPRESSION; REPRODUCTIVE CYCLE;

POLYSACCHARIDES;

ASIALOGLYCOPROTEIN RECEPTOR; LUTEINIZING HORMONE; MANNOSE RECEPTOR; MESSENGER RNA; PROGESTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CLEARANCE; CONTROLLED STUDY; FEMALE; HALF LIFE TIME; IN VIVO STUDY; LIFE CYCLE; LIVER; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREGNANCY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN METABOLISM; REPRODUCTION; SEXUAL MATURATION; STEADY STATE;

CARBOHYDRATE FUNCTION; CARBOHYDRATE GLYCOPROTEIN; CARBOHYDRATE-BINDING PROTEIN; CIRCULATORY HALF-LIFE; ENDOCRINOLOGY; ENDOCYTOSIS; HORMONES;

ANIMALS; ASIALOGLYCOPROTEIN RECEPTOR; BASE SEQUENCE; DNA PRIMERS; FEMALE; GLYCOPROTEINS; MALE; MANNOSE; MICE; PREGNANCY; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCTION; RNA, MESSENGER;

EID: 84899425036     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.544973     Document Type: Article

References (36)

1. 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 (Pubitemid 18041038
2. 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 pituitary glycoprotein hormones. J. Biol. Chem. 263, 36-44 (Pubitemid 18041039
3. 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 (Pubitemid 16173187
4. 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
5. Fiete, D., Srivastava, V., Hindsgaul, O., and Baenziger, J. U. (1991) A hepatic reticuloendothelial cell receptor specific for SO4-4GalNAc β1,4GlcNAcβ1,2Man α that mediates rapid clearance of lutropin. Cell 67, 1103-1110
6. Fiete, D., Beranek, M., and Baenziger, J. U. (2012) Molecular basis for proteinspecific transfer of N-acetylgalactosamine to N-linked glycans by the glycosyltransferases β1,4-N-acetylgalactosaminyl transferase 3 (β4GalNAc-T3) and β4GalNAc-T4. J. Biol. Chem. 287, 29194-29203
7. Fiete, D., Beranek, M., and Baenziger, J. U. (2012) Peptide-specific transfer of N-acetylgalactosamine to O-linked glycans by the glycosyltransferases β1,4-N-acetylgalactosaminyl transferase 3 (β4GalNAc-T3) and β4GalNAc-T4. J. Biol. Chem. 287, 29204-29212
8. Miller, E., Fiete, D., Blake, N. M., Beranek, M., Oates, E. L., Mi, Y., Roseman, D. S., and Baenziger, J. U. (2008) A necessary and sufficient determinant for protein-selective glycosylation in vivo. J. Biol. Chem. 283, 1985-1991
9. Ashwell, G., and Harford, J. (1982) Carbohydrate-specific receptors of the liver. Annu. Rev. Biochem. 51, 531-554
10. Stockert, R. J. (1995) The asialoglycoprotein receptor: relationships between structure, function, and expression. Physiol. Rev. 75, 591-609
11. Hubbard, A. L., Wilson, G., Ashwell, G., and Stukenbrok, H. (1979) An electron microscope autoradiographic study of the carbohydrate recognition systems in rat liver. I: distribution of 125I-ligands among the liver cell types. J. Cell Biol. 83, 47-64 (Pubitemid 10197033)
12. Drickamer, K., Mamon, J. F., Binns, G., and Leung, J. O. (1984) Primary structure of the rat liver asialoglycoprotein receptor: structural evidence for multiple polypeptide species. J. Biol. Chem. 259, 770-778 (Pubitemid 14192139)
13. Halberg, D. F., Wager, R. E., Farrell, D. C., Hildreth, J., 4th., Quesenberry, M. S., Loeb, J. A., Holland, E. C., and Drickamer, K. (1987) Major and minor forms of the rat liver asialoglycoprotein receptor are independent galactose-binding proteins: primary structure and glycosylation heterogeneity of minor receptor forms. J. Biol. Chem. 262, 9828-9838
14. Paietta, E., Stockert, R. J., and Racevskis, J. (1992) Alternatively spliced variants of the human hepatic asialoglycoprotein receptor, H2, differ in cellular trafficking and regulation of phosphorylation. J. Biol. Chem. 267, 11078-11084
15. Ishibashi, S., Hammer, R. E., and Herz, J. (1994) Asialoglycoprotein receptor deficiency in mice lacking the minor receptor subunit. J. Biol. Chem. 269, 27803-27806 (Pubitemid 24354498
16. Braun, J. R., Willnow, T. E., Ishibashi, S., Ashwell, G., and Herz, J. (1996) The major subunit of the asialoglycoprotein receptor is expressed on the hepatocellular surface in mice lacking the minor receptor subunit. J. Biol. Chem. 271, 21160-21166 (Pubitemid 26292968
17. Tozawa, R., Ishibashi, S., Osuga, J., Yamamoto, K., Yagyu, H., Ohashi, K., Tamura, Y., Yahagi, N., Iizuka, Y., Okazaki, H., Harada, K., Gotoda, T., Shimano, H., Kimura, S., Nagai, R., and Yamada, N. (2001) Asialoglycoprotein receptor deficiency in mice lacking the major receptor subunit: its obligate requirement for the stable expression of oligomeric receptor. J. Biol. Chem. 276, 12624-12628
18. Fiete, D. J., Beranek, M. C., and Baenziger, J. U. (1998) A cysteine-rich domain of the "mannose" receptor mediates GalNAc-4-SO4 binding. Proc. Natl. Acad. Sci. U.S.A. 95, 2089-2093
19. Roseman, D. S., and Baenziger, J. U. (2000) Molecular basis of lutropin recognition by the mannose/GalNAc-4-SO4 receptor. Proc. Natl. Acad. Sci. U.S.A. 97, 9949-9954
20. Liu, Y., Chirino, A. J., Misulovin, Z., Leteux, C., Feizi, T., Nussenzweig, M. C., and Bjorkman, P. J. (2000) Crystal structure of the cysteine-rich domain of mannose receptor complexed with a sulfated carbohydrate ligand. J. Exp. Med. 191, 1105-1116
21. Fiete, D., and Baenziger, J. U. (1997) Isolation of the SO4-4-GalNAcβ1,4GlcNAcβ1,2Manα-specific receptor from rat liver. J. Biol. Chem. 272, 14629-14637 (Pubitemid 27251725)
22. Baenziger, J. U., and Fiete, D. (1980) Galactose and N- acetylgalactosamine- specific endocytosis of glycopeptides by isolated rat hepatocytes. Cell 22, 611-620 (Pubitemid 11199918)
23. Grewal, P. K., Uchiyama, S., Ditto, D., Varki, N., Le, D. T., Nizet, V., and Marth, J. D. (2008) The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat. Med. 14, 648-655 (Pubitemid 351809544)
24. 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 (Pubitemid 36800957
25. Steirer, L. M., Park, E. I., Townsend, R. R., and Baenziger, J. U. (2009) The asialoglycoprotein receptor regulates levels of plasma glycoproteins terminating with sialic acid α2,6-galactose. J. Biol. Chem. 284, 3777-3783
26. Lee, S. J., Evers, S., Roeder, D., Parlow, A. F., Risteli, J., Risteli, L., Lee, Y. C., Feizi, T., Langen, H., and Nussenzweig, M. C. (2002) Mannose receptormediated regulation of serum glycoprotein homeostasis. Science 295, 1898-1901 (Pubitemid 34218139)
27. Fiete, D., Beranek, M. C., and Baenziger, J. U. (1997) The macrophage/ endothelial cell mannose receptor cDNA encodes a protein that binds oligosaccharides terminating with SO4-4-GalNAcβ1,4GlcNAcβ or Man at independent sites. Proc. Natl. Acad. Sci. U.S.A. 94, 11256-11261
28. Mi, Y., Fiete, D., and Baenziger, J. U. (2008) Ablation of GalNAc-4-sulfotransferase- 1 enhances reproduction by altering the carbohydrate structures of luteinizing hormone in mice. J. Clin. Invest. 118, 1815-1824 (Pubitemid 351632384)
29. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
30. Mengeling, B. J., Smith, P. L., Stults, N. L., Smith, D. F., and Baenziger, J. U. (1991) A microplate assay for analysis of solution-phase glycosyltransferase reactions: determination of kinetic constants. Anal. Biochem. 199, 286-292
31. 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
32. Milona, A., Owen, B. M., van Mil, S., Dormann, D., Mataki, C., Boudjelal, M., Cairns, W., Schoonjans, K., Milligan, S., Parker, M., White, R., and Williamson, C. (2010) The normal mechanisms of pregnancy-induced liver growth are not maintained in mice lacking the bile acid sensor Fxr. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G151-158
33. Dai, G., Bustamante, J. J., Zou, Y., Myronovych, A., Bao, Q., Kumar, S., and Soares, M. J. (2011) Maternal hepatic growth response to pregnancy in the mouse. Exp. Biol. Med. 236, 1322-1332
34. McLellan, A. S., Fischer, B., Dveksler, G., Hori, T., Wynne, F., Ball, M., Okumura, K., Moore, T., and Zimmermann, W. (2005) Structure and evolution of the mouse pregnancy-specific glycoprotein (Psg) gene locus. BMC Genomics 6, 4
35. Patnaik, S. K., and Stanley, P. (2006) Lectin-resistant CHO glycosylation mutants. Methods Enzymol. 416, 159-182 (Pubitemid 44750110)
36. Collins, J. C., Stockert, R. J., and Morell, A. G. (1984) Asialoglycoprotein receptor expression in murine pregnancy and development. Hepatology 4, 80-83 (Pubitemid 14185429)