In defense of the oral cavity: Structure, biosynthesis, and function of salivary mucins

Annual Review of Physiology

Volumn 57, Issue , 1995, Pages 547-564

  Tabak, Lawrence A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

GalNAc transferase; glycoprotein; mucin biosynthesis; O glycosylation; saliva

Indexed keywords

GLYCOPROTEIN; MUCIN;

GLYCOSYLATION; HUMAN; MOUTH CAVITY; MOUTH FLORA; MOUTH MUCOSA; NONHUMAN; PRIORITY JOURNAL; REVIEW; SALIVA;

EID: 0028942854     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ph.57.030195.002555     Document Type: Review

References (88)

1. Aguirre A, Testa-Weintraub LA, Banderas JA, Haraszthy GG, Reddy MS, Levine MJ. 1993. Sialochemistry: A diagnostic tool? Crit. Rev. Oral Biol. Med. 4(3/4):343-50
2. Al-Hashimi I, Levine MJ. 1989. Characterization of in vivo salivary-derived enamel pellicle. Arch. Oral Biol. 34(4): 289-95
3. Albone EF, Hagen FK, VanWuyckhuyse BC, Tabak LA. 1994. Molecular cloning of a rat submandibular gland apomucin. J. Biol. Chem. 269:16845-52
4. Bertram U. 1967. Xerostomia: Clinical aspects, pathology and pathogenesis. Acta Odontol. Scand. 25(Suppl. 49): 11-126
5. Beyer TA, Rearick JI, Paulson JC, Prieels J-P, Sadler JE, Hill RL. 1979. Biosynthesis of mammalian glycoproteins. J. Biol. Chem. 254(24):12531-41
6. Bhargava AK, Woitach JT, Davidson EA, Bhavanandan VP. 1990. Cloning and cDNA sequence of a bovine submaxillary gland mucin-like protein containing two distinct domains. Proc. Natl. Acad. Sci. USA 87:6798-802
7. Biesbrock AR, Reddy MS, Levine MJ. 1991. Interaction of a salivary mucin-secretory immunoglobulin A complex with mucosal pathogens. Infect. Immunol. 59:3492-97
8. Blixt-Johansen G, Ek A-C, Ganowiak W, Granérus A-K, von Schenck H, et al. 1992. Improvement of oral mucosa with mucin containing artificial saliva in geriatric patients. Arch. Gerontol. Geriatr. 14:193-201
9. Bobek LA, Tsai H, Biesbrock AR, Levine MJ. 1993. Molecular cloning, sequence, and specificity of expression of the gene encoding the low molecular weight human salivary mucin (MUC7). J. Biol. Chem. 268(27):20563-69
10. Bradway SD, Bergey EJ, Scannapieco FA, Ramasubbu N, Zawacki S, Levine MJ. 1992. Formation of salivary-mucosal pellicle: The role of transglutaminase. Biochem. J. 284:557-64
11. Brockhausen I, Möller G, Merz G, Adermann K, Paulsen H. 1990. Control of mucin synthesis: The peptide portion of synthetic O-glycopeptide substrates influences the activity of O-glycan core 1 UDPgalactose:N-acetyl-α-galactosaminyl-R β3-galactosyltransferase. Biochemistry 29:10206-12
12. Chilton BS, Kaplan HA, Lennarz WJ. 1988. Estrogen regulation of the central enzymes involved in O-and N-linked glycoprotein assembly in the developing and the adult rabbit endocervix. Endocrinology 123(3):1237-44
13. Collins LMC, Dawes C. 1987. The surface area of the adult human mouth and thickness of the salivary film covering the teeth and oral mucosa. J. Dent. Res. 66(8):1300-2
14. Corfield T. 1992. Mucus glycoproteins, super glycoforms: How to solve a sticky problem? Glycoconj. J. 9:217-21
15. Dekker J, Strous GJ. 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(30): 18116-22
16. Denny PA, Denny PC. 1982. A mouse submandibular sialomucin containing both N-and O-glycosylic linkages. Carbohydr. Res. 110:305-14
17. Denny PA, Hong SH, Klauser DK, Denny PC. 1992. Increased mucin levels in submandibular saliva from mice following repeated isoproterenol treatment. Arch. Oral Biol. 37(1):73-75
18. Denny PA, Klauser DK, Villa BJ, Hong SH, Denny PC. 1991. The effect of ageing on mucin contents in mouse sub-mandibular glands. Arch. Oral Biol. 36(7):477-81
19. Denny PC, Denny PA, Klauser DK, Hong SH, Navazesh M, Tabak LA. 1991. Age-related changes in mucins from human whole saliva. J. Dent. Res. 70(10):1320-27
20. Denny PC, Denny PA, Villa BJ, Klauser DK. 1991. Increased mucin levels in submandibular glands of aged male mice after chronic isoproterenol treatment. Arch. Oral Biol. 36(7):483-89
21. Duxbury AJ, Thakker NS, Wastell DO. 1989. A double-blind cross-over trial of a mucin-containing artificial saliva. Br. Dent. J. 166:115-20
22. Eckhardt AE, Timpte CS, Abernethy JL, Toumadje A, Johnson WC, Hill RL. 1987. Structural properties of porcine submaxillary gland apomucin. J. Biol. Chem. 262(23):11339-44
23. Eckhardt AE, Timpte CS, Abernethy JL, Zhao Y, Hill RL. 1991. Porcine sub-maxillary mucin contains a cystine-rich, carboxylterminal domain in addition to a highly repetitive, glycosylated domain. J. Biol. Chem. 266(15):9678-86
24. Elhammer AP, Poorman RA, Brown E, Magiora LL, Hoogerheide JG, Kézky FJ. 1993. The specificity of UDP-GalNAc:polypeptide N-Acetylgalactos-aminyltransferase as inferred from a database of in vivo substrates and from the in vitro glycosylation of proteins and eptides. J. Biol. Chem. 268(14):10029-38
25. Fontenot JD, Tjandra N, Bu D, Ho C, Montelaro RC, Finn OJ. 1993. Biophysical characterization of one-, two-and three-tandem repeats of human mucin (muc-1) protein core. Cancer Res. 53: 5386-94
26. Fox PC, Busch KA, Baum BJ. 1987. Subjective reports of xerostomia and objective measures of salivary gland performance. J. Am. Dent. Assoc. 115:581-84
27. Gans RF, Watson GE, Tabak LA. 1990. A new assessment in vitro of human salivary lubrication using a compliant substrate. Arch. Oral Biol. 35(7):487-92
28. 13 NMR spectroscopy. Biochemistry 26:4689-99
29. Gibbons RJ, van Houte J. 1975. Bacterial adherence in oral microbial ecology. Annu. Rev. Microbiol. 29:19-44
30. Guarente L. 1993. Strategies for the identification of interacting proteins. Proc. Natl. Acad. Sci. USA 90:1639-41
31. Gupta R, Jentoft N. 1989. Subunit structure of porcine submaxillary mucin. Biochemistry 28:6114-21
32. Hagen FK, VanWuyckhuyse B, Tabak LA. 1993. Purification, cloning, and expression of a bovine UDP-GalNAc:polypeptide N-acetyl-galactosaminyltransferase. J. Biol. Chem. 268(25):18960-65
33. Homa FL, Hollander T, Lehman DJ, Thomsen DR, Elhammer AP. 1993. Isolation and expression of a cDNA clone encoding a bovine UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase. J. Biol. Chem. 268(17):12609-16
34. Hoskins LC, Agustines M, McKee WB, Boulding ET, Kriaris M, Niedermeyer G. 1985. Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J. Clin. Invest. 75:944-53
35. Hughes CV, Baum BJ, Fox PC, Marmary Y, Yeh CK, Sonies BC. 1987. Oral-pharyngeal dysphagia: a common sequela of salivary gland dysfunction. Dysphagia 1:173-77
36. Hull SR, Sugarman ED, Spielman J, Carraway KL. 1991. Biosynthetic maturation of an ascites tumor cell surface sialomucin. J. Biol. Chem. 266(21): 13580-86
37. Ichikawa Y, Look GC, Wong C-H. 1992. Enzyme-catalyzed oligosaccharide synthesis. Anal. Biochem. 202:215-38
38. Jentoft N. 1990. Why are proteins O-glycosylated? Trends Biochem. Sci. 15: 291-94
39. Koop HM, Valentijn-Benz M, Nieuw Amerongen AV, Roukema PA, de Graaff J. 1990. Aggregation of oral bacteria by human salivary mucins in comparison to salivary and gastric mucins of animal origin. Anlonie van Leeuwen-hoek J. Microbiol. Serol. 58:255-63
40. Levine MJ, Aguirre A, Hatton MN, Tabak LA. 1987. Artificial salivas: present and future. J. Dent. Res. 66(Spec. Issue):693-98
41. Levine MJ, Herzberg MC, Levine MS, Ellison SA, Stinson MW, et al. 1978. Specificity of salivary-bacterial interactions: Role of terminal sialic acid residues in the interaction of salivary glycoproteins with Streptococcus sanguis and Streptococcus mutans. Infect. Immunol. 19(1):107-15
42. Levine MJ, Jones PC, Loomis RE, Reddy MS, Al-Hashimi I, et al. 1987. Functions of human saliva and salivary mucins: An overview. In Oral Mucosal Disease: Biology, Etiology, Therapy. Proc. Second Dows Symp., ed. IC Mackenzie, CA Squier, E Dablesteen, pp. 24-27. Copenhagen: Laegeforeningens Forlag
43. Levine MJ, Reddy MS, Tabak LA, Loomis RE, Bergey EJ, et al. 1987. Structural aspects of salivary glycoproteins. J. Dent. Res. 66:436-41
44. Ligtenberg AJM, Walgreen-Weterings E, Veerman ECI, de Soet JJ, de Graaff J, Nieuw Amerongen AV. 1992. Influence of saliva on aggregation and adherence of Streptococcus gordonii HG 222. Infect. Immunol. 60(9):3878-84
45. Loomis RE, Prakobphol A, Levine MJ, Reddy MS, Jones PC. 1987. Biochemical and biophysical comparison of two mucins from human submandibular-sub-lingual saliva. Arch. Biochem. Biophys. 258(2):452-64
46. Matsuura S, Hand AR. 1991. Quantitative immunocytochemistry of rat sub-mandibular secretory proteins during chronic isoproterenol administration and recovery. J. Histochem. Cytochem. 39(7):945-54
47. McBride BC, Gisslow MT. 1977. Role of sialic acid in saliva-induced aggregation of Streptococcus sanguis. Infect. Immunol. 18:35-40
48. Metzgar RS, Hollingsworth MA, Kaufman B. 1993. Pancreatic mucins. In The Pancreas: Biology, Pathobiology and Disease, ed. VLW Go, EP DiMagno, JD Gardner, E Lebenthal, HA Reber, GA Scheele, 17:351-67. New York: Raven. 2nd ed.
49. Moch T, Hoschützky H, Hacker J, Kröncke K-D, Jann K. 1987. Isolation and characterization of the α-sialyl-β-2,3-galactosyl-specific adhesin from fimbriated Escherichia coli. Proc. Natl. Acad. Sci. USA 84:3462-66
50. Murray PA, Levine MJ, Tabak LA, Reddy MS. 1982. Specificity of salivary-bacterial interactions: II. Evidence for a lectin on Streptococcus sanguis with specificity for a NeuAcα2,3-Galβ1,3GalNAc sequence. Biochem. Biophys. Res. Comm. 106(2):390-96
51. Murray PA, Prakobphol A, Lee T, Hoover CI, Fischer SJ. 1992. Adherence of oral streptococci to salivary glycoproteins. Infect. Immunol. 60(1):31-38
52. Närhi TO. 1994. Prevalence of subjective feelings of dry mouth in the elderly. J. Dent. Res. 73(1):20-25
53. Nieuw Amerongen AV, Oderkerk CH, Driessen AA. 1987. Role of mucins from human whole saliva in the protection of tooth enamel against demineralization in vitro. Caries Res. 21:297-309
54. O'Connell B, Hagen FK, Tabak LA. 1992. The influence of flanking sequence on the O-glycosylation of threonine in vitro. J. Biol. Chem. 267(35): 25010-18
55. O'Connell B, Tabak LA, Ramasubbu N. 1991. The influence of flanking sequences on O-glycosylation. Biochem. Biophys. Res. Comm. 180(2):1024-30
56. O'Connell BC, Tabak LA. 1993. A comparison of serine and threonine O-glycosylation by UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase. J. Dent. Res. 72(12):1554-58
57. Oldenburg KR, Loganathan D, Goldstein IJ, Schultz PC, Gallop MA. 1992. Peptide ligands for a sugar-binding protein isolated from a random peptide li brary. Proc. Natl. Acad. Sci. USA 89: 5393-97
58. Piller V, Piller F, Fukuda M. 1990. Biosynthesis of truncated O-glycans in the T cell line Jurkat. J. Biol. Chem. 265(16):9264-71
59. Pisano A, Redmond JW, Williams KL, Gooley AA, 1993. Glycosylation sites identified by solid-phase Edman degradation: O-linked glycosylation motifs on human glycophorin A. Glycobiology 3(5):429-35
60. Prakobphol A, Levine MJ, Tabak LA, Reddy MS. 1982. Purification of a low-molecular weight, mucin-type glycoprotein from human submandibular-sublingual saliva. Carbohydr. Res. 108: 111-22
61. Reddy MS, Bobek LA, Haraszthy GG, Biesbrock AR, Levine MJ. 1992. Structural features of the low-molecular-mass human salivary mucin. Biochem. J. 287: 639-43
62. Reddy MS, Levine MJ. 1993. Low-molecular-mass human salivary mucin, MG2: Structure and binding of Pseudomonas aeruginosa. Cril. Rev. Oral Biol. Med. 4(3/4):315-23
63. Rochu D, Crespeau H, Fine A, Gane P, Rouger P, et al. 1990. ABO-blood-group-related idiotypic network: Mimicry of oligosaccharide epitope by rabbit antiidiotypic antibodies to murine monoclonal anti-A antibody. Res. Immunol. 141:373-87
64. Sarosiek J, Bilski J, Murty VLN, Slomiany A, Slomiany BL. 1988. Role of salivary epidermal growth factor in the maintenance of physicochemical characteristics of oral and gastric mucosal mucus coat. Biochem. Biophys. Res. Comm. 152(3):1421-27
65. Schachter H. 1986. Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem. Cell Biol. 64: 163-81
66. Sellers LA, Allen A, Morris ER, Ross-Murphy SB. 1988. Submaxillary mucins: Intermolecular interactions and gel-forming potential of concentrated solutions. Biochem. J. 256:599-607
67. Shogren R, Gerken TA, Jentoft N. 1989. Role of glycosylation on the conformation and chain dimensions of O-linked glycoproteins: Light-scattering studies of ovine submaxillary mucin. Biochemistry 28:5525-36
68. Shogren RL, Jamieson AM, Blackwell J, Jentoft N. 1986. Conformation of mucous glycoproteins in aqueous solvents. Biopolymers 25:1505-17
69. Stinson MW, Levine MJ, Cavese JM, Prakobphol A, Murray PA, et al. 1982. Adherence of Streptococcus sanguis to salivary mucin bound to glass. J. Dent. Res. 61(12):1390-93
70. Slomiany BL, Murty VLN, Mandel ID, Zalesna G, Slomiany A. 1989. Physico-chemical characteristics of mucus glycoproteins and lipids of the human oral mucosal mucus coat in relation to caries susceptibility. Arch. Oral Biol. 34(4): 229-37
71. Slomiany BL, Piotrowski J, Czajkowski A, Shovlin FE, Slomiany A. 1993. Differential expression of salivary mucin bacterial aggregating activity with caries status. Int. J. Biochem. 25(6):935-40
72. Soby L, Jamieson AM, Blackwell J, Jentoft N. 1990. Viscoelastic properties of solutions of ovine submaxillary mucin Biopolymers 29:1359-66
73. Strahl-Bolsinger S, Immervoll T, Deutzmann R, Tanner W. 1993. PMT1, the gene for a key enzyme of protein O-glycosylation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 90: 8164-68
74. Tabak LA. 1991. Genetic control of salivary mucin formation. Mol. Genet. Mouth; Front. Oral Physiol. 8:77-94
75. Tabak LA, Bowen WH. 1989 Roles of saliva (pellicle), diet, and nutrition on plaque formation. J. Dent. Res. 68(Spec. Issue): 1560-66
76. Tabak LA, Levine MJ, Jain NK, Bryan AR, Cohen RE, et al. 1985. Adsorption of human salivary mucins to hydroxyapatite. Arch. Oral Biol. 30(5): 423-27
77. Tabak LA, Levine MJ, Mandel ID, Ellison SA. 1982. Role of salivary mucins in the protection of the oral cavity. J. Oral Pathol. 11:1-17
78. Tabak LA, Mirels L, Monte LD, Ridall AL, Levine MJ, et al. 1985. Isolation and characterization of a mucin-glycoprotein from rat submandibular glands. Arch. Biochem. Biophys. 242(2):383-92
79. Thomsen DR, Post LE, Elhammer AP. 1990. Structure of O-glycosidically linked oligosaccharides synthesized by the insect cell line Sf9. J. Cell. Biochem. 43:67-79
80. Timpte CS, Eckhardt AE, Abemethy JL, Hill RL. 1988. Porcine submaxillary gland apomucin contains tandemly repeated identical sequences of 81 residues. J. Biol. Chem. 263:1081-88
81. van der Hoeven JS, Camp PJM. 1991. Synergistic degradation of mucin by Streptococcus oralis and Streptococcus sanguis in mixed chemostat cultures. J. Dent. Res. 70(7):1041-44
82. Wang Y, Abernethy JL, Eckhardt AE, Hill RL. 1992. Purification and characterization of a UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase specific for glycosylation of threonine residues. J. Biol. Chem. 267(18):12709-16
83. Wang Y, Agrwal N, Eckhardt AE, Stevens RD, Hill RL. 1993. The acceptor substrate specificity of porcine submaxillary UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase is dependent on the amino acid sequences adjacent to serine and threonine residues. J. Biol. Chem. 268(31):22979-83
84. Williams D, Longmore G, Malta KL, Schachter H. 1980. Mucin synthesis. J. Biol. Chem. 255(23):11253-61
85. Willoughby RE. 1993. Rotaviruses preferentially bind O-linked sialylglyco-conjugates and sialomucins. Glycobiology 3(5):437-45
86. Wilson IBH, Gavel Y, von Heijne G. 1991. Amino acid distributions around O-linked glycosylation sites. Biochem. J. 275:529-34
87. Wolff A, Fox PC, Ship JA, Atkinson JC, Macynski AA, Baum BJ. 1990. Oral mucosal status and major salivary gland function. Oral Surg. Med. Oral Pathol. 70:49-54
88. Wong C-H, Schuster M, Wang P, Sears P. 1993. Enzymatic synthesis of N-and O-linked glycopeptides. J. Am. Chem. Soc. 115(14):5893-5901