Glycosylation of the receptor guanylate cyclase C: Role in ligand binding and catalytic activity

Biochemical Journal

Volumn 379, Issue 3, 2004, Pages 653-663

  Ghanekar, Yashoda ^a   Chandrashaker, Akhila ^a   Tatu, Utpal ^a   Visweswariah, Sandhya S ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Glycosylation; Guanylate cyclase C; Human embryonic kidney 293 cells (HEK 293 cells); N acetylglucosaminyltransferase; Surface localization

Indexed keywords

BIOCHEMISTRY; BIOLOGICAL ORGANS; CATALYSIS; CELLS; CONFORMATIONS; HEAT STABILIZERS;

ENTEROTOXINS; GLYCOSYLATION; LIGAND-STIMULATED ACTIVATION;

ENZYMES;

GALACTOSE; GUANYLATE CYCLASE; GUANYLATE CYCLASE C; SIALIC ACID; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELL MEMBRANE; CELL SURFACE; EMBRYO; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME GLYCOSYLATION; HUMAN; HUMAN CELL; LIGAND BINDING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANIMALS; CATALYSIS; CELL LINE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; GALACTOSE; GLYCOSYLATION; GUANYLATE CYCLASE; HALF-LIFE; HUMANS; LIGANDS; MANNOSE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; N-ACETYLGLUCOSAMINYLTRANSFERASES; N-ACETYLNEURAMINIC ACID; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RECEPTORS, PEPTIDE; TRYPSIN;

EID: 2542580835     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040001     Document Type: Article

References (44)

1. Lucas, K. A., Pitari, G. M., Kazerounian, S., Ruiz-Stewart, I., Park, J., Schulz, S., Chepenik, K. P. and Waldman, S. A. (2000) Guanylyl cyclases and signaling by cyclic GMP. Pharmacol. Rev. 52, 375-414
2. Vaandrager, A. B. (2002) Structure and function of the heat-stable enterotoxin receptor/guanylyl cyclase C. Mol. Cell. Biochem. 230, 73-83
3. Nandi, A., Bhandari, R. and Visweswariah, S. S. (1997) Epitope conservation and immunohistochemical localization of the guanylin/stable toxin peptide receptor, guanylyl cyclase C. J. Cell. Biochem. 66, 500-511
4. Qian, X., Prabhakar, S., Nandi, A., Visweswariah, S. S. and Goy, M. F. (2000) Expression of GC-C, a receptor-guanylate cyclase, and its endogenous ligands uroguanylin and guanylin along the rostrocaudal axis of the intestine. Endocrinology 141, 3210-3224
5. London, R. M., Eber, S. L., Visweswariah, S. S., Krause, W. J. and Forte, L. R. (1999) Structure and activity of OK-GC: a kidney receptor guanylate cyclase activated by guanylin peptides. Am. J. Physiol. 276, F882-F891
6. Jaleel, M., London, R. M., Eber, S. L., Forte, L. R. and Visweswariah, S. S. (2002) Expression of the receptor guanylyl cyclase C and its ligands in reproductive tissues of the rat: a potential role for a novel signaling pathway in the epididymis. Biol. Reprod. 67, 1975-1980
7. Scheving, L. A. and Russell, W. E. (1996) Guanylyl cyclase C is up-regulated by nonparenchymal cells and hepatocytes in regenerating rat liver. Cancer Res. 56, 5186-5191
8. - channel by heat-stable enterotoxin and guanylin via cAMP-dependent protein kinase. Embo J. 13, 1065-1072
9. Shailubhai, K., Yu, H. H., Karunanandaa, K., Wang, J. Y., Eber, S. L., Wang, Y., Joo, N. S., Kim, H. D., Miedema, B. W., Abbas, S. Z. et al. (2000) Uroguanylin treatment suppresses polyp formation in the Apc(Min/+) mouse and induces apoptosis in human colon adenocarcinoma cells via cyclic GMP. Cancer Res. 60, 5151-5157
10. Pitari, G. M., Di Guglielmo, M. D., Park, J., Schulz, S. and Waldman, S. A. (2001) Guanylyl cyclase C agonists regulate progression through the cell cycle of human colon carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 98, 7846-7851
11. Pitari, G. M., Zingman, L. V., Hodgson, D. M., Alekseev, A. E., Kazerounian, S., Bienengraeber, M., Hajnoczky, G., Terzic, A. and Waldman, S. A. (2003) Bacterial enterotoxins are associated with resistance to colon cancer. Proc. Natl. Acad. Sci. U.S.A. 100, 2695-2699
12. Bhandari, R., Srinivasan, N., Mahaboobi, M., Ghanekar, Y., Suguna, K. and Visweswariah, S. S. (2001) Functional inactivation of the human guanylyl cyclase C receptor: modeling and mutation of the protein kinase-like domain. Biochemistry 40, 9196-9206
13. Crane, J. K. and Shanks, K. L. (1996) Phosphorylation and activation of the intestinal guanylyl cyclase receptor for Escherichia coli heat-stable toxin by protein kinase C. Mol. Cell. Biochem. 165, 111-120
14. Wada, A., Hasegawa, M., Matsumoto, K., Niidome, T., Kawano, Y., Hidaka, Y., Padilla, P. I., Kurazono, H., Shimonishi, Y. and Hirayama, T. (1996) The significance of Ser1029 of the heat-stable enterotoxin receptor (STaR): relation of STa-mediated guanylyl cyclase activation and signaling by phorbol myristate acetate. FEBS Lett. 384, 75-77
15. Roy, N., Guruprasad, M. R., Kondaiah, P., Mann, E. A., Giannella, R. A. and Visweswariah, S. S. (2001) Protein kinase C regulates transcription of the human guanylate cyclase C gene. Eur. J. Biochem. 268, 2160-2171
16. Bakre, M. M. and Visweswariah, S. S. (1997) Dual regulation of heat-stable enterotoxin-mediated cGMP accumulation in T84 cells by receptor desensitization and increased phosphodiesterase activity. FEBS Lett. 408, 345-349
17. Bakre, M. M., Ghanekar, Y. and Visweswariah, S. S. (2000) Homologous desensitization of the human guanylate cyclase C receptor. Cell-specific regulation of catalytic activity. Eur. J. Biochem. 267, 179-187
18. Nandi, A., Mathew, R. and Visweswariah, S. S. (1996) Expression of the extracellular domain of the human heat-stable enterotoxin receptor in Escherichia coli and generation of neutralizing antibodies. Protein Expr. Purif. 8, 151-159
19. Hasegawa, M., Hidaka, Y., Wada, A., Hirayama, T. and Shimonishi, Y. (1999) The relevance of N-linked glycosylatjon to the binding of a ligand to guanylate cyclase C. Eur. J. Biochem. 263, 338-346
20. Koller, K. J., Lipari, M. T. and Goeddel, D. V. (1993) Proper glycosylation and phosphorylation of the type A natriuretic peptide receptor are required for hormone-stimulated guanylyl cyclase activity, J. Biol. Chem. 268, 5997-6003
21. Miyagi, M., Zhang, X. and Misono, K. S. (2000) Glycosylation sites in the atrial natriuretic peptide receptor: oligosaccharide structures are not required for hormone binding. Eur. J. Biochem. 267, 5758-5768
22. Fenrick, R., Bouchard, N., McNicoll, N. and de Lean, A. (1997) Glycosylation of asparagine 24 of the natriuretic peptide receptor-B is crucial for the formation of a competent ligand binding domain. Mol. Cell. Biochem. 173, 25-32
23. Fenrick, R., McNicoll, N. and de Lean, A. (1996) Glycosylation is critical for natriuretic peptide receptor-B function. Mol. Cell. Biochem. 165, 103-109
24. He, X., Chow, D., Martick, M. M. and Garcia, K. C. (2001) Allosteric activation of a spring-loaded natriuretic peptide receptor dimer by hormone. Science 293, 1657-1662
25. Ghanekar, Y., Chandrashaker, A. and Visweswariah, S. S. (2003) Cellular refractoriness to the heat-stable enterotoxin peptide is associated with alterations in levels of the differentially glycosylated forms of guanylyl cyclase C. Eur. J. Biochem. 270, 3848-3857
26. Scheving, L. A., Russell, W. E. and Chong, K. M. (1996) Structure, glycosylation, and localization of rat intestinal guanylyl cyclase C: modulation by fasting. Am. J. Physiol. 271, G959-G968
27. Vaandrager, A. B., Schulz, S., de Jonge, H. R. and Garbers, D. L. (1993) Guanylyl cyclase C is an N-linked glycoprotein receptor that accounts for multiple heat-stable enterotoxin-binding proteins in the intestine. J. Biol. Chem. 268, 2174-2179
28. Scheving, L. A. and Jin, W. H. (1999) Circadian regulation of uroguanylin and guanylin in the rat intestine. Am. J. Physiol. 277, C1177-C1183
29. Reeves, P. J., Callewaert, N., Contreras, R. and Khorana, H. G. (2002) Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl. Acad. Sci. U.S.A. 99, 13419-13424
30. Zor, T. and Selinger, Z. (1996) Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal. Biochem. 236, 302-308
31. Sindice, A., Basoglu, C., Cerci, A., Hirsch, J. R., Potthast, R., Kuhn, M., Ghanekar, Y., Visweswariah, S. S. and Schlatter, E. (2002) Guanylin, uroguanylin, and heat-stable enterotoxin activate guanylate cyclase C and/or a pertussis toxin-sensitive G protein in human proximal tubule cells. J. Biol. Chem. 277, 17758-17764
32. Baumann, N. A., Vidugiriene, J., Machamer, C. E. and Menon, A. K. (2000) Cell surface display and intracellular trafficking of free glycosylphosphatidylinositols in mammalian cells. J. Biol. Chem. 275, 7378-7389
33. Visweswariah, S. S., Ramachandran, V., Ramamohan, S., Das, G. and Ramachandran, J. (1994) Characterization and partial purification of the human receptor for the heat-stable enterotoxin. Eur. J. Biochem. 219, 727-736
34. Visweswariah, S. S., Shanthi, G. and Balganesh, T. S. (1992) Interaction of heat-stable enterotoxins with human colonic (T84) cells: modulation of the activation of guanylyl cyclase. Microb. Pathog. 12, 209-218
35. Matlin, K. S. and Simons, K. (1983) Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell (Cambridge, Mass.) 34, 233-243
36. Vaandrager, A. B., van der Wiel, E. and de Jonge, H. R. (1993) Heat-stable enterotoxin activation of immunopurified guanylyl cyclase C. Modulation by adenine nucleotides. J. Biol. Chem. 268, 19598-19603
37. Tang, W. J. and Hurley, J. H. (1998) Catalytic mechanism and regulation of mammalian adenylyl cyclases. Mol. Pharmacol. 54, 231-240
38. Wada, A., Hirayama, T., Kitaura, H., Fujisawa, J., Hasegawa, M., Hidaka, Y. and Shimonishi, Y. (1996) Identification of ligand recognition sites in heat-stable enterotoxin receptor, membrane-associated guanylyl cyclase C by site-directed mutational analysis. Infect. Immun. 64, 5144-5150
39. Hasegawa, M., Hidaka, Y., Matsumoto, Y., Sanni, T. and Shimonishi, Y. (1999) Determination of the binding site on the extracellular domain of guanylyl cyclase C to heat-stable enterotoxin. J. Biol. Chem. 274, 31713-31718
40. Crane, J. K., Azar, S. S., Stam, A. and Newburg, D. S. (1994) Oligosaccharides from human milk block binding and activity of the Escherichia coli heat-stable enterotoxin (STa) in T84 intestinal cells. J. Nutr. 124, 2358-2364
41. Moloney, D. J., Panin, V. M., Johnston, S. H., Chen, J., Shao, L., Wilson, R., Wang, Y., Stanley, P., Irvine, K. D., Haltiwanger, R. S. et al. (2000) Fringe is a glycosyltransferase that modifies notch. Nature (London) 406, 369-375
42. Chen, J., Moloney, D. J. and Stanley, P. (2001) Fringe modulation of jagged1-induced notch signaling requires the action of β 4galactosyltransferase-1. Proc. Natl. Acad. Sci. U.S.A. 98, 13716-13721
43. Tsuda, T., Ikeda, Y. and Taniguchi, N. (2000) The Asn-420-linked sugar chain in human epidermal growth factor receptor suppresses ligand-independent spontaneous oligomerization. Possible role of a specific sugar chain in controllable receptor activation. J. Biol. Chem. 275, 21988-21994
44. Watson, F. L., Porcionatto, M. A., Bhattacharyya, A., Stiles, C. D. and Segal, R. A. (1999) TrkA glycosylation regulates receptor localization and activity. J. Neurobiol. 39, 323-336