Evidence that a peptide corresponding to the rat Muc2 C-terminus undergoes disulphide-mediated dimerization

European Journal of Biochemistry

Volumn 253, Issue 1, 1998, Pages 123-131

  Bell, Sherilyn L ^b   Khatri, Ismat A ^b   Xu, Gongqiao ^b   Forstner, Janet F ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b NONE

Author keywords

Cystine knot; Dimer; Disulfide; Muc2; Mucin

Indexed keywords

DISULFIDE; MUCIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRAIN COS1; CONTROLLED STUDY; DIMERIZATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RAT;

ACETYLGALACTOSAMINE; ANIMALS; BASE SEQUENCE; BENZYL COMPOUNDS; COS CELLS; CYSTINE; DIMERIZATION; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOSYLATION; HUMANS; MOLECULAR WEIGHT; MUCINS; NEURAMINIDASE; PEPTIDE FRAGMENTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RECOMBINANT PROTEINS; TRANSFECTION;

ANIMALIA;

EID: 0032053625     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1998.2530123.x     Document Type: Article

References (56)

1. Neutra, M. R. & Forstner, J. F. (1987) Gastrointestinal mucus: synthesis, secretion, and function, in Physiology of the gastrointestinal tract (Johnson, L. R., ed.) pp. 975 - 1008. Raven Press, New York.
2. Strous, G. J. & Dekker, J. (1992) Mucin-type glycoproteins, Crit. Rev. Biochem. Mol. Biol. 27, 57 - 92.
3. Forstner, J. F. & Forstner, G. G. (1994) Gastrointestinal mucus, in Physiology of the gastrointestinal tract (Johnson, L. R., ed.) pp. 1255 - 1283, Raven Press, New York.
4. Forstner, J. F., Oliver, M. G. & Sylvester, F. A. (1995) Production, structure, and biologic relevance of gastrointestinal mucins. in Infections of the gastrointestinal tract (Blaser, M. J., Smith, P. D., Ravdin, J. I., Greenberg, H. B. & Guerrant, R. L., eds) pp. 71 - 88. Raven Press, Ltd, New York.
5. Allen, A., Flemström, G., Garner, A. & Kivilaakso, E. (1993) Gastroduodenal mucosal protection, Physiol. Rev. 73, 823 - 857.
6. Xu, G., Huan, L.-J., Khatri, I. A., Wang, D., Bennick, A., Fahim, R. E. F., Forstner, G. G. & Forstner, J. F. (1992) cDNA for the carboxylterminal region of a rat intestinal mucin-like peptide, J. Biol. Chem. 267, 5401 - 5407.
7. Huan, L. J., Xu, G., Forstner, G. & Forstner, J. (1992) A serine, threonine and proline-rich region near the carboxyl-terminus of a rat intestinal mucin peptide, Biochim. Bioyhys. Acta 1132, 79 - 82.
8. Gum, J. R. Jr, Hicks, J. W., Toribara, N. W., Rothe, E.-M., Legace, R. E. & Kim, Y. S. (1992) The human MUC2 intestinal mucin has cysteine-rich subdomains located both upstream and downstream of its central repetitive region, J. Biol. Chem. 267, 21 375 - 21 383.
9. Probst, J. C., Gertzen, E.-M. & Hoffmann, W. (1990) An integumentary mucin (FIM-B.1) from Xenopus laevis homologous with von Willebrand factor, Biochemistry 29, 6240 - 6244.
10. Bhargava, A. K., Woitach, J. T., Davidson, E. A. & Bhavanandan, V. P. (1990) Cloning and cDNA sequencing of a bovine submaxillary gland mucin-like protein containing two distinct domains. Proc. Natl Acad. Sci. USA 87, 6798 - 6802.
11. Eckhardt, A. E., Timpte, C. S., Abernethy, J. L., Zhao, Y. & Hill, R. L. (1991) Porcine submaxillary mucin contains a cystine-rich. carboxyl-terminal domain in addition to a highly repetitive, glycosylated domain, J. Biol. Chem, 266, 9678 - 9686.
12. Meerzaman, D., Charles, P., Daskal, E., Polymeropoulos, M. H., Martin, B. M. & Rose, M. C. (1994) Cloning and analysis of cDNA encoding a major airway glycoprotein. human tracheobronchial mucin (MUC5), J. Biol. Chem. 269, 12 932 - 12 939.
13. Lesuffleur, T., Roche, F., Hill, A. S., Lacasa, M., Fox, M., Swallow, D. M., Zweibaum, A. & Real, F. X. (1995) Characterization of a mucin cDNA clone isolated from HT-29 mucus-secreting cells, J. Biol. Chem. 270, 13 665 - 13 673.
14. Daopin, S., Piez, K. A., Ogawa, Y. & Davies, D. R. (1992) Crystal structure of transforming growth factor-β2 an unusual fold for the superfamily, Science 257, 369 - 373.
15. McDonald, N. Q., Lapatto, R., Murray-Rust, J., Gunning, J., Wlodawer, A. & Blundell, T. L. (1991) New protein fold revealed by a 2.3-Å resolution crystal structure of nerve-growth factor. Nature 354, 411 - 414.
16. Meindl, A., Berger, W., Meitinger, T., van de Pol, D., Achatz, H., Dörner, C., Haasemann, M., Hellebrand, H., Gal, A., Cremers, F. & Ropers, H.-H. (1992) Norrie disease is caused by mutations in an extracellular protein resembling C-terminal globular domain of mucins, Nat. Genet. 2, 139 - 143.
17. Meitinger, T., Meindl, A., Bork, P., Rost, B., Sander, C., Haasemann, M. & Murken, J. (1993) Molecular modelling of the Norrie disease protein predicts a cystine knot growth factor tertiary structure, Nat. Genet. 5, 376 - 380.
18. Lapthorn, A. J., Harris, D. C., Linlejohn, A., Lustbader, J. W., Canfield, R. E., Machin, K. J., Morgan, F. J. & Isaacs, N. W. (1994) Crystal structure of human chorionic gonadotropin, Nature 369, 455 - 461.
19. Haniu, M., Hui, J., Young, Y., Le, J., Katta, V., Lee, R., Shimamoto, G. & Ronde, M. F. (1996) Glial cell line-derived neurotrophic factor: selective reduction of the intermolecular disulfide linkage and characterization of its disulfide structure, Biochemistry 35, 16 799 - 16 805.
20. Voorberg, J., Fontijn, R., Calafat, J., Janssen, H., van Mourik, J. A. & Pannekoek, H. (1991) Assembly and routing of von Willebrand factor variants: the requirements for disulfide-linked dimerization reside within the carboxy-terminal 151 amino acids, J. Cell Biol. 113, 195 - 205.
21. Khatri, I., Forstner, G. & Forstner, J. (1993) Preparation of polyclonal antibodies to native and modified mucin antigens, in Methods in molecular biology, vol. 14: Glycoprotein analysis in biomedicine (Hounsell, E. F., ed.) pp. 225 - 235, Humana Press Inc., Totowa, NJ.
22. Xu, G., Forstner, G. G. & Forstner, J. F. (1996) Interaction of heparin with synthetic peptides corresponding to the C-terminal domain of intestinal mucins, Glycoconj. J. 13, 81 - 90.
23. Ohmori, H., Dohrman, A. F., Gallup, M., Tsuda, T., Kai, H., Gum, J. R. Jr, Kim, Y. S. & Basbaum, C. B. (1994) Molecular cloning of the amino-terminal region of a rat MUC2 mucin gene homologue, J. Biol. Chem. 269, 17 833 - 17 840.
24. Higuchi, R. (1990) Recombinant PCR, in PCR protocols: a guide to methods and applications (Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J., eds) pp. 177 - 183. Academic Press. Inc., Toronto.
25. MacGregor, G. R., Mogg, A. E., Burke, J. F. & Caskey, C. T. (1987) Histochemical staining of clonal mammalian cell lines expressing E. coli β galactosidase indicates heterogeneous expression of the bacterial gene, Somat. Cell Mol. Genet. 13, 253 - 265.
26. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680 - 685.
27. Kojima, N., Handa, K., Newman, W. & Hakomori, S. (1992) Inhibition of selectin-dependent tumor cell adhesion to endothelial cells and platelets by blocking O-glycosylation of these cells, Biochem. Biophys. Res. Commun. 182, 1288 - 1295.
28. Perez-Vilar, J., Eckhardt, A. E. & Hill, R. L. (1996) Porcine submaxillary mucin forms disulfide-bonded dimers between its carboxylterminal domains, J. Biol. Chem. 271, 9845 - 9850.
29. Edge, A. S. B., Faltynek, C. R., Hof, L., Reichert, L. E. Jr & Weber, P. (1981) Deglycosylation of glycoproteins by trifluoromethanesulfonic acid, Anal. Biochem. 118, 131 - 137.
30. Gerken, T. A., Gupta, R. & Jentoft, N. (1992) A novel approach for chemically deglycosylating O-linked glycoproteins. The deglycosylation of submaxillary and respiratory mucins, Biochemistry 31, 639 - 648.
31. Xu, G., Huan, L., Khatri, I., Sajjan, U. S., McCool, D., Wang, D., Jones, C., Forstner, G. & Forstner, J. (1992) Human intestinal mucin-like protein (MLP) is homologous with rat MLP in the C-terminal region, and is encoded by a gene on chromosome 11 p 15.5, Biochem. Biophys. Res. Commun. 183, 821 - 828.
32. Fahim, R. E. F., Specian, R. D., Forstner, G. G. & Forstner. J. F. (1987) Characterization and localization of the putative 'link' component in rat small-intestinal mucin, Biochem. J. 243, 631 - 640.
33. Tarentino, A. L., Gómez. C. M. & Plummer, T. H. Jr (1985) Deglycosylation of asparagine-linked glycans by peptide: N-glycosidase F. Biochemistry 24, 4665 - 4671.
34. Kuan, S.-F., Byrd, J. C., Basbaum, C. & Kim, Y. S. (1989) Inhibition of mucin glycosylation by aryl-N-acetyl-α-galactosaminides in human colon cancer cells, J. Biol. chem. 264, 19 271 - 19 277.
35. Delannoy, P., Kim, I., Emery, N., De Bolos, C., Verhert, A., Degand, P. & Huet, G. (1996) Benzyl-N-acetyl-α-D-galactosamide inhibits the sialylalion and the secretion of mucins by a mucin secreting HT-29 cell subpopulation, Biochem. J. 13, 717 - 726.
36. Dekker, J. & Strous, G. J. (1990) Covalent oligomerization of rat gastric mucin occurs in the rough endoplasmic reticulum, is N-glycosylation-dependent, and precedes initial O-glycosylation. J. Biol. Chem. 265, 18 116 - 18 122.
37. Tytgat, K. M. A. J., Büller, H. A., Opdam, F. J. M., Kim, Y. S., Einerhand, A. W. C. & Dekker, J. (1994) Biosynthesis of human colonic mucin : MUC2 Is the prominent secretory mucin. Gastroenterology 107, 1352 - 1363.
38. Van Klinken, B. J.-W., Tytgat, K. M. A. J., Büller, H. A., Einerhand, A. W. C. & Dekker, J. (1995) Biosynthesis of intestinal nuicins: MUC1, MUC2, MUC3 and more. Biochem. Soc. Trans. 23, 814 - 818.
39. Tytgat, K. M. A. J., Klomp, L. W. J., Bovelander, F.-J., Opdam, F. J. M., Van der Wurff, A., Einerhand, A. W. C., Büller, H. A., Strous, G. J. & Dekker, J. (1995) Preparation of anti-mucin polypeptide antisera to study mucin biosynthesis. Anal. Biochem. 226, 331 - 341.
40. Tytgat, K. M. A. J., Swallow, D. M., Van Klinken, B. J.-W., Büller, H. A., Einerhand, A. W. C. & Dekker, J. (1995) Unpredictable behaviour of mucins in SDS/polyacrylamide-gel electrophoresis. Biochem. J. 310, 1053 - 1054.
41. Pan, Y. T. & Elbein, A. D. (1995) How can N-linked glycosylation and processing inhibitors be used to study carbohydrate synthesis and function, in Glycoproteins (Montreuil, J., Schachter, H. & Vliegenthart, J. F. G., eds) pp. 415-454. Elsevier Science B.V., Amsterdam.
42. Halban, P. A. & Irminger, J.-C. (1994) Sorting and processing of secretory proteins, Biochem. J. 299, 1 - 18.
43. Helenius, A. (1994) How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reliculum. Mol. Biol. Cell 5, 253 - 265.
44. Letourneur, O., Sechi, S., Willette-Brown, J., Robertson, M. W. & Kinet, J.-P. (1995) Glycosylation of human truncated FceRI a chain is necessary for efficient folding in the endoplasmic reticulum, J. Biol. Chem. 270, 8249 - 8256.
45. Asker, N., Baeckström, D., Axelsson, M. A. B., Carlstedt, I. & Hansson, G. C. (1995) The human MUC2 mucin apoprotein appears to dimerize before O-glycosylalion and shares epitopes with the 'insoluble' mucin of rat small intestine, Biochem. J. 308, 873 - 880.
46. Roth, J. (1995) Compartmentation of glycoprotein biosynthesis, in Glycoproteins (Montreuil, J., Schachter, H. & Vliegenthart, J. F. G., eds) pp. 287 - 312, Elsevier Science B.V., Amsterdam.
47. Dekker, J., Van Beurden-Lamers, W. M. O. & Strous, G. J. (1989) Biosynthesis of gastric mucus glycoprotein of the rat, J. Biol. Chem. 264, 10 431 - 10 437.
48. Klomp, L. W. J., van Rens, L. & Strous, G. J. (1994) Identification of a human gastric mucin precursor: N-linked glycosylation and oligomerization, Biochem. J. 304, 693 - 698.
49. Klomp, L. W. J., de Lely, A. J. & Strous, G. J. (1994) Biosynthesis of a human gall-bladder mucin, Biochem. J. 304, 737 - 744.
50. Tytgat, K. M. A. J., Bovelander, F.-J., Opdam, F. J. M., Einerhand, A. W. C., Büller, H. A. & Dekker, J. (1995) Biosynthesis of rat MUC2 in colon and its analogy with human MUC2. Biochem. J. 309, 221 - 229.
51. Camphausen, R. T., Yu, H.-A. & Cumming, D. A. (1995) The role of polypeptide in the biosynthesis of protein-linked oligosaccharides, in Glycoproteins (Montreuil. J., Schachter, H. & Vliegenthart, J. F. G., eds) pp. 391 - 414, Elsevier Science B. V., Amsterdam.
52. Lynch, D. C., Williams, R., Zimmerman, T. S., Kirby, E. P. & Livingston, D. M. (1983) Biosynthesis of the suhunits of factor VIIIR by bovine aortic endothelial cells, Proc. Natl Acad. Sci. USA 80, 2738 - 2742.
53. McCool, D. J., Forstner, J. F. & Forstner, G. G. (1994) Synthesis and secretion of mucin by the human colonie tumour cell line LS180. Biochem. J. 302, 111 - 118.
54. Wagner, D. D., Mayadas, T. & Marder, V. J. (1986) Initial glycosylation and acidic pH in the golgi apparatus are required for multimerization of von Willebrand factor, J. Cell Biol. 102, 1320 - 1324.
55. Schneppenheim, R., Brassard, J., Krey, S., Budde, U., Kunick, T. J., Holmberg, L., Ware, J. & Ruggeri, Z. M. (1996) Defective dimerization of von Willebrand factor subunits due to a cys→arg mutation in type IID von Willebrand disease, Proc. Natl Acad. Sci. USA 93, 3581 - 3586.
56. Meno, C., Saijoh, Y., Fujii, H., Ikeda, M., Yokoyama, T., Yokoyama, M., Toyoda, Y. & Hamada, H. (1996) Left-right asymmetric expression of the TGFβ-family member lefty in mouse embryos, Nature 381, 151 - 155.