Structures of the Oligosaccharide Chains in Swine Trachea Mucin Glycoproteins*

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1 THE JOURNAL OF BOLOGCAL CHEMSTRY by The American Society of Biological Chemists, nc Vol. 259, No. ssue Structures of the Oligosaccharide Chains in Swine Trachea Mucin Glycoproteins* (Received for publication, March 12,1984) E. V. Chandrasekaran, Surjit S. Rana, Mark Davila, and Joseph MendicinoS From the Department of Biochemistry, University of Georgia, Athens, Georgia The structures of large 0-glycosidically linked oligosaccharides derived from swine trachea mucin glycoprotein were established. Reduced oligosaccharides released by treatment with alkaline borohydride were separated by gel filtration on Bio-Gel P-6 and the neutral oligosaccharides were isolated by chromatography on DEAE-cellulose. Eight oligosaccharides (Da to B), ranging in length from 8 to 15 sugar units, were isolated. On the basis of carbohydrate composition and analytical data from sequential treatment with exoglycosidases and permethylation analysis, the following structures were assigned to these oligosaccharides: Da Db /1 7 D Galj31,3 /1 C Fucal,2Gal#31,4GlcNAci31,6 /f GaW1,3 C 1,6 7 7 * * This study was supported by Grant HL from the Division defrayed in part by the payment of page charges. This article must of Lung Diseases, National Heart, Lung and Blood nstitute, National therefore be hereby marked advertisement in accordance with 18 nstitutes of Health. A preliminary report of this work was presented U.S.C. Section 1734 solely to indicate this fact. at the Meeting of American Society of Biological Chemists in New $ To whom correspondence should be addressed. Orleans, LA, April The costs of publication of this article were 12908

2 Oligosaccharides of Trachea Mucin Glycoproteins ol CL GalNacol 7 7 B GlcNAcfl1,3 law Gal NAc B GalNAc la13 7 Gal/3l,4GlcNAcfll,3Ga~l,3 2 ~ 4 3 GalNAc The surface epithelium of the tracheobronchial airway is coated with a discontinous mucus layer which is constantly being removed by ciliated epithelial cells (1, 2). The viscoelastic properties of respiratory mucus, which are essential for its role in the clearance of particulate matter and maintenance of water balance, are dependent on the amount and composition of glycoprotein components (1-4). These large mucin glycoproteins usually have apparent molecular weights in excess of 1 x O6 and they contain about 50 to 70% carbohydrate. Numerous oligosaccharide side chains containing varying amounts of L-fucose, galactose, GlcNAc, GalNAc, sialic acid, and sulfate are 0-glycosidically linked through GalNAc to the hydroxyl groups of seryl and threonyl residues in the polypeptide chain (2-5). These glycoproteins have distinct blood group activity (4). The mucin glycoprotein present on the epithelial surface of swine trachea was purified in our previous investigation (6). The glycoprotein had an apparent molecular weight of about 1 x lo6 and it showed both blood group A' and H' activities. The oligosaccharide chains were released by treatment with alkaline borohydride and the structures of the short chains in trachea mucin glycoprotein were compared with those present in Cowper's gland mucin glycoprotein. The structures of the tri-, tetra-, penta-, and hexasaccharides present in swine trachea mucin glycoprotein were established (6). The present report is concerned with the elucidation of the structure of more complex oligosaccharides, containing 7 to 15 monosaccharide units and having both blood group A' and H' activity. EXPERMENTAL PROCEDURES AND RESULTS' DSCUSSON A large number of oligosaccharide chains of different sizes Portions of this paper (including "Experimental Procedures," "Results," Tables -V, and Figs. 1-3) are presented in miniprint at the end of this paper. Miniprint is easily read with the aid of a standard magnifying glass. Full size photocopies are available from the Journal of Biological Chemistry, 9650 Rockville Pike, Bethesda, MD Request Document No. 84M-0753, cite the authors, and and structures are present in mucin glycoproteins isolated from swine trachea epithelium. Despite the apparent variety of oligosaccharide structures described here and in the preceding report (6), many of the oligosaccharides have common properties in the sense that the more complex structure include simpler ones as structural elements. The branched trisaccharide unit, Gal~1,3(GlcNAc~1,6)GalNAc, is present in most of the oligosaccharides. Thus, the majority of the oligosaccharides in trachea mucin glycoproteins are O-glycosidically linked to serine and threonine units through this branched core structure. Extension of the oligosaccharide chain from this branched core trisaccharide structure can occur by the addition of a GlcNAc residue to position 3 of the p3-linked galactose in the core structure or by the addition of 2 GlcNAc units to this galactosyl unit through p3- and B6- linkages forming a second branch point (oligosaccharide D). THe consecutive addition of more &-linked galactose or GlcNAc units and termination by the addition of a2-linked fucose leads to structures found in oligosaccharides D., DL,, and C. The oligosaccharide chain originating from the p6-linked GlcNAc unit in the core structure usually contained only the disaccharide Fucal,2GalBl,4. This chain was never branched and consistently appeared in all of the more complex oligosaccharide structures in trachea mucinglycoproteins. The presence of the sequence Fuc~l,2Gal~l,4GlcNAc- in many of the oligosaccharide chains in trachea mucin glycoproteins may account for the blood group H' activity of these glycoproteins. n many of the larger oligosaccharide chains branching occurred only after a P3-linked GlcNAc unit and a P4-linked galactose unit were sequentially added to the p3-linked galactose residue in the core structure. The branching then occurred by the addition of 2 GlcNAc units through P3 and p6 linkages as seen in oligosaccharides C, C, B, and B. Thus, branching in trachea mucin glycoproteins can occur include a check or money order for $10.00 per set of photocopies. Full size photocopies are also included in the microfilm edition of the Journal that is available from Waverly Press.

3 12910 Oligosaccharides Glycoproteins of Mucin Trachea earlier on 83-linked galactose (oligosaccharides D and C) and in milk or later on 04-linked galactose (oligosaccharides C and C). oligosaccharides reveal antigenic activities toward two differ- The structures of some of the oligosaccharide chains iso- ent populations of human serum anti--ma cold agglutinins lated from swine trachea mucin glycoprotein were very similar (32) and these sequences are similar to those found in many to the structures of oligosaccharides in blood group substances of the oligosaccharides isolated from swine trachea mucin H', B', and Le isolated from human ovarian cyst fluids by gtycoprotein (6). Rovis et al. (20) and Maisonrouge-McAnliffe and Kabat (21) and those isolated from pig stomach lining by Kochetkov and his coworkers (22-24). The presence of similar types of oligosaccharide chains in mucin glycoprotein from swine trachea REFERENCES 1. Dulfano, M. J., and Philipoff, W. (1973) in Sputum Fundamentals and Clinical Pathology (Dulfano, M. J., ed) pp , Charles and pig stomach lining suggest that some of the functions of C Thomas, Springfield, L these glycoproteins may be similar, and may indicate that the 2. Clamp, J. R., Allen, A., Gibbons, R. A,, and Roberts, G. P. (1978) Br. Med. Bull. 34, same types of glycosyltransferase systems may be present in 3. Holden, K. G., and Griggs, L. J. (1977) in Glycoconjugates (Pigboth tissues. Both of the glycoproteins had blood group A+ man, W., and Horowitz, A., eds) Vol. 1, pp , Academic and H' activities. Press, New York However, some distinct differences were observed in these 4. Carlson, D. M. (1977) in Modern Problems in Pediatrics mucin glycoproteins. Oligosaccharides from blood group sub- (Forstner, G. G., ed) Vol. 19, pp. 1-10, S. Karger, New York 5. Glass, G. stances contain 3-substituted GlcNAc units (20, 21), whereas B. J., and Slomiany, B. L. (1977) in Mww in Health and Disease (Elstein, M., and Parke, D. V., eds) pp , the neutral oligosaccharides isolated from swine trachea mu- Plenum Press, New York cin glycoprotein did not contain this linkage. Further the 6. Rana, S. Chandrasekaran, S., E. V., Kennedy, J., and Mendicino, oligosaccharides from trachea mucin glycoprotein did not J. (1984) J. Biol. Chem. 259, contain GlcNAc residues attached to other GlcNAc units. 7. Cautrecasas, P., and lliano, G. (1971) Biochem. Biophys. Res. Hog gastric mucin blood group A+ + H' active substances Commun. 44, Li, Y. T., and Li, S. C. (1972) Methods Enzymol. 28, (25) and hog gastric mucin sulfated glycoproteins (26, 27) 9. Rao, A. K., Garver, F., and Mendicino, J. (1976) Biochemistry contain these linkages. We did not observe any oligosaccha- 15, rides which contained in their core struc- 10. Rao, A. K., and Mendicino, J. (1979) in Glycoconjugate Research tures. Slomiany et al. (18) reported the presence of this (Jeanloz, R. W., ed) Vol. 2, pp , Academic Press, New structure in oligosaccharides isolated from rat colonic mucin York glycoprotein. n oligosaccharides from rat colonic mucin gly- 11. Hakomori, S. (1964) J. Biochem. (Tokyo) 55, Conrad, H. E. (1972) Methods Carbohyd. Chem. 6, coprotein (as), is substituted at position 3 with a 13. Slomiany, A., and Slomiany, B. L. (1978) J. Biol. Chem. GlcNAc and position 6 of is either free or terminates in sialic acid. n this regard it should be noted that 14. Stellner, K., Saito, K., and Hakomori, S. (1973) Arch. Biochem. the oligosaccharides isolated from rat colonic mucus glycopro- Biophy~. 155, tein showed only blood group A activity, while oligosaccharides isolated from swine trachea mucin glycoprotein show either H+ (short-chain oligosaccharides) or both A' + H' (long-chain oligosaccharides) blood group activities. No oligosaccharide structures containing GalNAcfil,3GalNAc residues at the reducing end of the chain were found in trachea mucin glycoprotein. The presence of this sequence in blood group substances has been shown by isolation of a glycopep- tide, from the degradation products of pig blood group substance (29) and an oligosaccharide, GalNAcfil,3GalNAc, from human blood group substances B,, and i (21). Terminal sugar residues found at the nonreducing end of oligosaccharide chains from trachea mucin glycoprotein include ul,2-linked fucose, al,3-linked GalNAc, GlcNAc. The attachment of fucose to form the F~c~~1,2Gal~l,4GlcNAc sequence terminates chain growth on chain (oligosaccharides D. through B) and confers blood group H' activity to the oligosaccharide. The addition of oll,3-linked GalNAc to the penultimate galactose residue (oligosaccharides C, B, and B) on chains may account for the blood group A+ activity in these oligosaccharides. Porcine submaxillary mucin contains a pentasaccharide which shows blood group A+ activity (30). Oligosaccharides with terminal GlcNAc or galactose residues (6) may represent intermediates in the biosynthesis of more complex chains. However, some of these chains may also be determinants of different immunological activities as well. A broad spectrum of and i activities has been observed in blood group ABO, Le substances (31). The sequences 15. Cbandrasekaran, E. V., Davila, M., Nixon, D. W., Goldfarb, M., and Mendicino, J. (1983) J. Biol. Chem. 258, Rana, S. S., Barlow, J. J., and Matta, K. L. (1983) Carbohydr. Res. 113, Mendicino, J., Sivakami, S., Davila, M., and Chandrasekaran, E. V. (1982) J. Biol. Chem. 257, Rana, S. S., and Matta, K. L. (1983) Carbohydr. Res. 116, Siddiqui, B., Kwanami, J., Li, Y. T., and Hakomori, S. (1972) Lipid Res. 13, Rovis, L., Anderson, B., Kabat, E. A,, Cruezo, F., and Liao, J. (1973) Biochemistry 12, Maisonrouge-McAnliffe, F., and Kabat, E. A. (1976) Arch. Biochern. Biophys. 175, Derevitskaya, V. A., Arbatsky, N. P., and Kochetkov, N. K. (1975) zu. Akad. Nauk SSSR 223, Kochetkov, N. K., Derevitskaya, V. A., and Arbatsky, N. P. (1976) Eur. J. Biochem. 67, Derevitskaya, V. A., Arbatsky, N. P., and Kochetkov, N. K. (1978) Eur. J. Biochem. 86, Kochetkov, N. K., Derevitskaya, V. A., Lichosherstov, L. M., Martynova, M. D., and Senchenkova, S. N. (1970) Carbohydr. Res. 12, Slomiany, B. L., and Meyer, K. (1972) J. Biol. Chem. 247, Slomiany, B. L., and Meyer, K. (1973) J. Biol. Chem. 248, Slomiany, B. L., Murty, V. L. N., and Slomiany, A. (1980) J. Bid. Chem. 255, Kochetkov, N. K., Derevitskaya, V. A., Likhosherstov, L. M., and Medveder, S. A. (1974) Biochem. Biophys. Res. Commun. 56, Carlson, D. M. (1968) J. Biol. Chem. 243, Feizi, T., and Kabat, E. A. (1972) J. Exp. Med. 135, Zopf, D. A,, and Ginsburg, V. (1975) Arch. Biochern. Biophys. 167,

4 Oligosaccharides of Trachea Mucin Glycoproteins 12911

5 12912 Oligosaccharides of Trachea Mucin Glycoproteins B.

6 Oligosaccharides of Mucin Trachea Glycoproteins C

7 12914 Oligosaccharides of Mucin Trachea i Glycoproteins t W z 0 g 0.2-0

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