Abstract
A previously identified Candida albicans-binding glycoprotein secreted from rat submandibular glands (RSMG) has been further purified from an aqueous RSMG extract by ion-exchange chromatography and gel filtration. Biochemical analysis of the glycoprotein revealed high levels of uronic acid and sulfate, suggesting that it was a proteoglycan. Its amino acid and carbohydrate compositions were similar to those observed for other proteoglycans and differed significantly from those of RSMG mucin, the major secretory glycoprotein of RSMG. In addition, the apparent molecular weight of the glycoprotein was reduced following treatment with either chondroitinase ABC or heparitinase, demonstrating the presence of chondroitin sulfate and heparan sulfate. On the basis of its structure and anatomical source, the glycoprotein is referred to as submandibular gland secreted proteoglycan 1 (SGSP1). SGSP1 also binds monoclonal antibody 1F9, which recognizes the human blood group A carbohydrate epitope found on RSMG mucin. Hence, SGSP1 appears to be a hybrid molecule with carbohydrate structures found in both proteoglycans and RSMG mucin. Enzymatic digestion of SGSP1, followed by its interaction with a radiolabelled C. albicans strain in a filter-binding assay, demonstrated that binding to this strain appears to be mediated primarily via the heparan sulfate side chains of SGSP1 and not via the blood group A oligosaccharide.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ascencio F., Fransson L. A., Wadström T. Affinity of the gastric pathogen Helicobacter pylori for the N-sulphated glycosaminoglycan heparan sulphate. J Med Microbiol. 1993 Apr;38(4):240–244. doi: 10.1099/00222615-38-4-240. [DOI] [PubMed] [Google Scholar]
- BITTER T., MUIR H. M. A modified uronic acid carbazole reaction. Anal Biochem. 1962 Oct;4:330–334. doi: 10.1016/0003-2697(62)90095-7. [DOI] [PubMed] [Google Scholar]
- Bartold P. M. Proteoglycans of the periodontium: structure, role and function. J Periodontal Res. 1987 Nov;22(6):431–444. doi: 10.1111/j.1600-0765.1987.tb02052.x. [DOI] [PubMed] [Google Scholar]
- Bartold P. M., Wiebkin O. W., Thonard J. C. Proteoglycans of human gingival epithelium and connective tissue. Biochem J. 1983 Apr 1;211(1):119–127. doi: 10.1042/bj2110119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Biesbrock A. R., Reddy M. S., Levine M. J. Interaction of a salivary mucin-secretory immunoglobulin A complex with mucosal pathogens. Infect Immun. 1991 Oct;59(10):3492–3497. doi: 10.1128/iai.59.10.3492-3497.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blair E. A., Castle A. M., Castle J. D. Proteoglycan sulfation and storage parallels storage of basic secretory proteins in exocrine cells. Am J Physiol. 1991 Nov;261(5 Pt 1):C897–C905. doi: 10.1152/ajpcell.1991.261.5.C897. [DOI] [PubMed] [Google Scholar]
- Bolton A. E., Hunter W. M. The labelling of proteins to high specific radioactivities by conjugation to a 125I-containing acylating agent. Biochem J. 1973 Jul;133(3):529–539. doi: 10.1042/bj1330529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Budtz-Jörgensen E. Etiology, pathogenesis, therapy, and prophylaxis of oral yeast infections. Acta Odontol Scand. 1990 Feb;48(1):61–69. doi: 10.3109/00016359009012735. [DOI] [PubMed] [Google Scholar]
- Burgess T. L., Kelly R. B. Sorting and secretion of adrenocorticotropin in a pituitary tumor cell line after perturbation of the level of a secretory granule-specific proteoglycan. J Cell Biol. 1984 Dec;99(6):2223–2230. doi: 10.1083/jcb.99.6.2223. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Choi S. H., Stinson M. W. Purification of a Streptococcus mutans protein that binds to heart tissue and glycosaminoglycans. Infect Immun. 1989 Dec;57(12):3834–3840. doi: 10.1128/iai.57.12.3834-3840.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cutler L. S., Christian C. P., Rendell J. K. Glycosaminoglycan synthesis by adult rat submandibular salivary-gland secretory units. Arch Oral Biol. 1987;32(6):413–419. doi: 10.1016/0003-9969(87)90076-8. [DOI] [PubMed] [Google Scholar]
- Cutler L. S., Christian C. P., Rendell J. K. Sulphated glycosaminoglycan synthesis by developing rat submandibular gland secretory units. Arch Oral Biol. 1991;36(5):389–395. doi: 10.1016/0003-9969(91)90010-R. [DOI] [PubMed] [Google Scholar]
- Cutler L. S., Christian C. P., Rozenski D. Xylose-linked proteoglycan synthesis does not have a primary role in the control of secretory cell differentiation in salivary glands. Dev Biol. 1991 Sep;147(1):14–21. doi: 10.1016/s0012-1606(05)80003-x. [DOI] [PubMed] [Google Scholar]
- Ebisu S., Nakae H., Fukuhara H., Okada H. The mechanisms of Eikenella corrodens aggregation by salivary glycoprotein and the effect of the glycoprotein on oral bacterial aggregation. J Periodontal Res. 1992 Nov;27(6):615–622. doi: 10.1111/j.1600-0765.1992.tb01745.x. [DOI] [PubMed] [Google Scholar]
- Epstein J. B., Truelove E. L., Izutzu K. T. Oral candidiasis: pathogenesis and host defense. Rev Infect Dis. 1984 Jan-Feb;6(1):96–106. doi: 10.1093/clinids/6.1.96. [DOI] [PubMed] [Google Scholar]
- Finlay I. G. Oral symptoms and candida in the terminally ill. Br Med J (Clin Res Ed) 1986 Mar 1;292(6520):592–593. doi: 10.1136/bmj.292.6520.592. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gallagher J. T., Lyon M., Steward W. P. Structure and function of heparan sulphate proteoglycans. Biochem J. 1986 Jun 1;236(2):313–325. doi: 10.1042/bj2360313. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gremski W., Cutler L. S. Immunocytochemical localization of heparan sulphate proteoglycan in the rat submandibular gland. Histochem J. 1991 Aug;23(8):339–344. doi: 10.1007/BF01042178. [DOI] [PubMed] [Google Scholar]
- Hoffman M. P., Haidaris C. G. Analysis of Candida albicans adhesion to salivary mucin. Infect Immun. 1993 May;61(5):1940–1949. doi: 10.1128/iai.61.5.1940-1949.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Iversen J. M., Keller P. J., Kauffman D. L., Robinovitch M. R. The presence of chondroitin sulfate in parotid secretory granules and saliva of the rat. Cell Tissue Res. 1987 Oct;250(1):221–226. doi: 10.1007/BF00214675. [DOI] [PubMed] [Google Scholar]
- Kihlström E., Majeed M., Rozalska B., Wadström T. Binding of Chlamydia trachomatis serovar L2 to collagen types I and IV, fibronectin, heparan sulphate, laminin and vitronectin. Zentralbl Bakteriol. 1992 Oct;277(3):329–333. doi: 10.1016/s0934-8840(11)80910-2. [DOI] [PubMed] [Google Scholar]
- Kishimoto E., Hay D. I., Gibbons R. J. A human salivary protein which promotes adhesion of Streptococcus mutans serotype c strains to hydroxyapatite. Infect Immun. 1989 Dec;57(12):3702–3707. doi: 10.1128/iai.57.12.3702-3707.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klotz S. A. Adherence of Candida albicans to components of the subendothelial extracellular matrix. FEMS Microbiol Lett. 1990 Mar 15;56(3):249–254. doi: 10.1016/s0378-1097(05)80049-7. [DOI] [PubMed] [Google Scholar]
- Klotz S. A., Smith R. L. A fibronectin receptor on Candida albicans mediates adherence of the fungus to extracellular matrix. J Infect Dis. 1991 Mar;163(3):604–610. doi: 10.1093/infdis/163.3.604. [DOI] [PubMed] [Google Scholar]
- Klotz S. A., Smith R. L. Glycosaminoglycans inhibit Candida albicans adherence to extracellular matrix proteins. FEMS Microbiol Lett. 1992 Dec 1;78(2-3):205–208. doi: 10.1016/0378-1097(92)90026-k. [DOI] [PubMed] [Google Scholar]
- Klotz S. A., Smith R. L., Stewart B. W. Effect of an arginine-glycine-aspartic acid-containing peptide on hematogenous candidal infections in rabbits. Antimicrob Agents Chemother. 1992 Jan;36(1):132–136. doi: 10.1128/aac.36.1.132. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Levine M. J., Reddy M. S., Tabak L. A., Loomis R. E., Bergey E. J., Jones P. C., Cohen R. E., Stinson M. W., Al-Hashimi I. Structural aspects of salivary glycoproteins. J Dent Res. 1987 Feb;66(2):436–441. doi: 10.1177/00220345870660020901. [DOI] [PubMed] [Google Scholar]
- Liang O. D., Ascencio F., Fransson L. A., Wadström T. Binding of heparan sulfate to Staphylococcus aureus. Infect Immun. 1992 Mar;60(3):899–906. doi: 10.1128/iai.60.3.899-906.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mandel I. D. The functions of saliva. J Dent Res. 1987 Feb;66(Spec No):623–627. doi: 10.1177/00220345870660S203. [DOI] [PubMed] [Google Scholar]
- Meitner S. W., Bowen W. H., Haidaris C. G. Oral and esophageal Candida albicans infection in hyposalivatory rats. Infect Immun. 1990 Jul;58(7):2228–2236. doi: 10.1128/iai.58.7.2228-2236.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mirels L., Bedi G. S., Dickinson D. P., Gross K. W., Tabak L. A. Molecular characterization of glutamic acid/glutamine-rich secretory proteins from rat submandibular glands. J Biol Chem. 1987 May 25;262(15):7289–7297. [PubMed] [Google Scholar]
- Moreira J. E., Tabak L. A., Bedi G. S., Culp D. J., Hand A. R. Light and electron microscopic immunolocalization of rat submandibular gland mucin glycoprotein and glutamine/glutamic acid-rich proteins. J Histochem Cytochem. 1989 Apr;37(4):515–528. doi: 10.1177/37.4.2926128. [DOI] [PubMed] [Google Scholar]
- Murray P. A., Levine M. J., Tabak L. A., Reddy M. S. Specificity of salivary-bacterial interactions: II. Evidence for a lectin on Streptococcus sanguis with specificity for a NeuAc alpha 2, 3Ga1 beta 1, 3Ga1NAc sequence. Biochem Biophys Res Commun. 1982 May 31;106(2):390–396. doi: 10.1016/0006-291x(82)91122-6. [DOI] [PubMed] [Google Scholar]
- Murray P. A., Prakobphol A., Lee T., Hoover C. I., Fisher S. J. Adherence of oral streptococci to salivary glycoproteins. Infect Immun. 1992 Jan;60(1):31–38. doi: 10.1128/iai.60.1.31-38.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nikawa H., Hamada T. Binding of salivary or serum proteins to Candida albicans in vitro. Arch Oral Biol. 1990;35(7):571–573. doi: 10.1016/0003-9969(90)90090-w. [DOI] [PubMed] [Google Scholar]
- Ortega-Barria E., Pereira M. E. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell. 1991 Oct 18;67(2):411–421. doi: 10.1016/0092-8674(91)90192-2. [DOI] [PubMed] [Google Scholar]
- Potter-Perigo S., Prather P., Baker C., Altman L. C., Wight T. N. Partial characterization of proteoglycans synthesized by human gingival epithelial cells in culture. J Periodontal Res. 1993 Mar;28(2):81–91. doi: 10.1111/j.1600-0765.1993.tb01054.x. [DOI] [PubMed] [Google Scholar]
- Robinovitch M. R., Iversen J. M., Izutsu K. T. Inhibition of synthesis of rat parotid secretory proteoglycan in a gland slice system. Arch Oral Biol. 1992 Mar;37(3):209–214. doi: 10.1016/0003-9969(92)90090-u. [DOI] [PubMed] [Google Scholar]
- SPENCER B. The ultramicro determination of inorganic sulphte. Biochem J. 1960 Jun;75:435–440. doi: 10.1042/bj0750435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shibutani T., Nishino W., Shiraki M., Iwayama Y. ELISA detection of glycosaminoglycan (GAG)-linked proteoglycans in gingival crevicular fluid. J Periodontal Res. 1993 Jan;28(1):17–20. doi: 10.1111/j.1600-0765.1993.tb01045.x. [DOI] [PubMed] [Google Scholar]
- Stow J. L., Sawada H., Farquhar M. G. Basement membrane heparan sulfate proteoglycans are concentrated in the laminae rarae and in podocytes of the rat renal glomerulus. Proc Natl Acad Sci U S A. 1985 May;82(10):3296–3300. doi: 10.1073/pnas.82.10.3296. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strömberg N., Borén T., Carlén A., Olsson J. Salivary receptors for GalNAc beta-sensitive adherence of Actinomyces spp.: evidence for heterogeneous GalNAc beta and proline-rich protein receptor properties. Infect Immun. 1992 Aug;60(8):3278–3286. doi: 10.1128/iai.60.8.3278-3286.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tabak L. A., Levine M. J., Jain N. K., Bryan A. R., Cohen R. E., Monte L. D., Zawacki S., Nancollas G. H., Slomiany A., Slomiany B. L. Adsorption of human salivary mucins to hydroxyapatite. Arch Oral Biol. 1985;30(5):423–427. doi: 10.1016/0003-9969(85)90070-6. [DOI] [PubMed] [Google Scholar]
- Tabak L. A., Levine M. J., Mandel I. D., Ellison S. A. Role of salivary mucins in the protection of the oral cavity. J Oral Pathol. 1982 Feb;11(1):1–17. doi: 10.1111/j.1600-0714.1982.tb00138.x. [DOI] [PubMed] [Google Scholar]
- Tabak L. A., Mirels L., Monte L. D., Ridall A. L., Levine M. J., Loomis R. E., Lindauer F., Reddy M. S., Baum B. J. Isolation and characterization of a mucin-glycoprotein from rat submandibular glands. Arch Biochem Biophys. 1985 Nov 1;242(2):383–392. doi: 10.1016/0003-9861(85)90222-x. [DOI] [PubMed] [Google Scholar]
- Vasilas A., Molina L., Hoffman M., Haidaris C. G. The influence of morphological variation on Candida albicans adhesion to denture acrylic in vitro. Arch Oral Biol. 1992 Aug;37(8):613–622. doi: 10.1016/0003-9969(92)90123-p. [DOI] [PubMed] [Google Scholar]
- WARREN L. The thiobarbituric acid assay of sialic acids. J Biol Chem. 1959 Aug;234(8):1971–1975. [PubMed] [Google Scholar]
- Wilkieson C., Samaranayake L. P., MacFarlane T. W., Lamey P. J., MacKenzie D. Oral candidosis in the elderly in long term hospital care. J Oral Pathol Med. 1991 Jan;20(1):13–16. doi: 10.1111/j.1600-0714.1991.tb00880.x. [DOI] [PubMed] [Google Scholar]
- Winters B. D., Ramasubbu N., Stinson M. W. Isolation and characterization of a Streptococcus pyogenes protein that binds to basal laminae of human cardiac muscle. Infect Immun. 1993 Aug;61(8):3259–3264. doi: 10.1128/iai.61.8.3259-3264.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]