Abstract
Background: Mucinases and sialidases contribute to the process of invasion and colonisation in many conditions and infections of the female reproductive tract by degrading the protective cervical mucus. The role of hydrolytic enzymes in the pathogenesis of sexually transmitted diseases and their effect on cervical mucus are discussed in this review.
Methods: Articles were searched for using the keywords "sialidase," "mucinase," "protease," and "sexually transmitted infections." As well as review and other articles held by our group, searches were conducted using PubMed, Grateful Med, and the University of Bath search engine, BIDS.
Results: Numerous publications were found describing the production of hydrolytic enzymes in sexually transmitted diseases. Because the number of publications exceeded the restrictions imposed on the size of the review, the authors selected and discussed those which they considered of the most relevance to sexually transmitted infections.
Key Words: mucinase; sialidase; microbial protease
Abbreviations: BSM (bovine submaxillary mucin), BV (bacterial vaginosis); Fuc (fucose); Gal (galactose); GalNAc (N-acetylgalactosamine); Glc (glucose); GlcNAc (N-acetylglucosamine); Man (mannose); PMN (polymorphonuclear neutrophils), human immunodeficiency virus 1 (HIV-1); sIgA (secretory immunoglobulin A).
Full Text
The Full Text of this article is available as a PDF (148.3 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alugupalli K. R., Kalfas S. Degradation of lactoferrin by periodontitis-associated bacteria. FEMS Microbiol Lett. 1996 Dec 1;145(2):209–214. doi: 10.1111/j.1574-6968.1996.tb08579.x. [DOI] [PubMed] [Google Scholar]
- Audie J. P., Tetaert D., Pigny P., Buisine M. P., Janin A., Aubert J. P., Porchet N., Boersma A. Mucin gene expression in the human endocervix. Hum Reprod. 1995 Jan;10(1):98–102. doi: 10.1093/humrep/10.1.98. [DOI] [PubMed] [Google Scholar]
- Bagriaçik E. U., Miller K. S. Cell surface sialic acid and the regulation of immune cell interactions: the neuraminidase effect reconsidered. Glycobiology. 1999 Mar;9(3):267–275. doi: 10.1093/glycob/9.3.267. [DOI] [PubMed] [Google Scholar]
- Bardsley-Elliot A., Noble S. Oseltamivir. Drugs. 1999 Nov;58(5):851–862. doi: 10.2165/00003495-199958050-00007. [DOI] [PubMed] [Google Scholar]
- Berg J. O., Lindqvist L., Andersson G., Nord C. E. Neuraminidase in Bacteroides fragilis. Appl Environ Microbiol. 1983 Jul;46(1):75–80. doi: 10.1128/aem.46.1.75-80.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Briselden A. M., Moncla B. J., Stevens C. E., Hillier S. L. Sialidases (neuraminidases) in bacterial vaginosis and bacterial vaginosis-associated microflora. J Clin Microbiol. 1992 Mar;30(3):663–666. doi: 10.1128/jcm.30.3.663-666.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bózner P., Demes P. Proteinases in Trichomonas vaginalis and Tritrichomonas mobilensis are not exclusively of cysteine type. Parasitology. 1991 Feb;102(Pt 1):113–115. doi: 10.1017/s0031182000060418. [DOI] [PubMed] [Google Scholar]
- Carlstedt I., Sheehan J. K. Structure and macromolecular properties of cervical mucus glycoproteins. Symp Soc Exp Biol. 1989;43:289–316. [PubMed] [Google Scholar]
- Cauci S., Driussi S., Monte R., Lanzafame P., Pitzus E., Quadrifoglio F. Immunoglobulin A response against Gardnerella vaginalis hemolysin and sialidase activity in bacterial vaginosis. Am J Obstet Gynecol. 1998 Mar;178(3):511–515. doi: 10.1016/s0002-9378(98)70430-2. [DOI] [PubMed] [Google Scholar]
- Connaris S., Greenwell P. Glycosidases in mucin-dwelling protozoans. Glycoconj J. 1997 Nov;14(7):879–882. doi: 10.1023/a:1018554408558. [DOI] [PubMed] [Google Scholar]
- Coombs G. H., North M. J. An analysis of the proteinases of Trichomonas vaginalis by polyacrylamide gel electrophoresis. Parasitology. 1983 Feb;86(Pt 1):1–6. doi: 10.1017/s0031182000057103. [DOI] [PubMed] [Google Scholar]
- Corfield T. Bacterial sialidases--roles in pathogenicity and nutrition. Glycobiology. 1992 Dec;2(6):509–521. doi: 10.1093/glycob/2.6.509. [DOI] [PubMed] [Google Scholar]
- Costerton J. W. Overview of microbial biofilms. J Ind Microbiol. 1995 Sep;15(3):137–140. doi: 10.1007/BF01569816. [DOI] [PubMed] [Google Scholar]
- Domingues R. M., Cavalcanti S. M., Andrade A. F., Ferreira M. C. Sialic acid as receptor of Bacteroides fragilis lectin-like adhesin. Zentralbl Bakteriol. 1992 Oct;277(3):340–344. doi: 10.1016/s0934-8840(11)80912-6. [DOI] [PubMed] [Google Scholar]
- Drzeniek R. Viral and bacterial neuraminidases. Curr Top Microbiol Immunol. 1972;59:35–74. doi: 10.1007/978-3-642-65444-2_2. [DOI] [PubMed] [Google Scholar]
- Dwarakanath A. D., Campbell B. J., Tsai H. H., Sunderland D., Hart C. A., Rhodes J. M. Faecal mucinase activity assessed in inflammatory bowel disease using 14C threonine labelled mucin substrate. Gut. 1995 Jul;37(1):58–62. doi: 10.1136/gut.37.1.58. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eggert-Kruse W., Botz I., Pohl S., Rohr G., Strowitzki T. Antimicrobial activity of human cervical mucus. Hum Reprod. 2000 Apr;15(4):778–784. doi: 10.1093/humrep/15.4.778. [DOI] [PubMed] [Google Scholar]
- Elstein M. Functions and physical properties of mucus in the female genital tract. Br Med Bull. 1978 Jan;34(1):83–88. doi: 10.1093/oxfordjournals.bmb.a071464. [DOI] [PubMed] [Google Scholar]
- Enhörning G., Huldt L., Melén B. Ability of cervical mucus to act as a barrier against bacteria. Am J Obstet Gynecol. 1970 Oct 15;108(4):532–537. doi: 10.1016/0002-9378(70)90227-9. [DOI] [PubMed] [Google Scholar]
- Garber G. E., Lemchuk-Favel L. T. Analysis of the extracellular proteases of Trichomonas vaginalis. Parasitol Res. 1994;80(5):361–365. doi: 10.1007/BF00932372. [DOI] [PubMed] [Google Scholar]
- Gibson S. A., Macfarlane G. T. Characterization of proteases formed by Bacteroides fragilis. J Gen Microbiol. 1988 Aug;134(8):2231–2240. doi: 10.1099/00221287-134-8-2231. [DOI] [PubMed] [Google Scholar]
- Gilks C. B., Reid P. E., Clement P. B., Owen D. A. Histochemical changes in cervical mucus-secreting epithelium during the normal menstrual cycle. Fertil Steril. 1989 Feb;51(2):286–291. doi: 10.1016/s0015-0282(16)60492-2. [DOI] [PubMed] [Google Scholar]
- Gipson I. K., Moccia R., Spurr-Michaud S., Argüeso P., Gargiulo A. R., Hill J. A., 3rd, Offner G. D., Keutmann H. T. The Amount of MUC5B mucin in cervical mucus peaks at midcycle. J Clin Endocrinol Metab. 2001 Feb;86(2):594–600. doi: 10.1210/jcem.86.2.7174. [DOI] [PubMed] [Google Scholar]
- Gipson I. K., Spurr-Michaud S., Moccia R., Zhan Q., Toribara N., Ho S. B., Gargiulo A. R., Hill J. A., 3rd MUC4 and MUC5B transcripts are the prevalent mucin messenger ribonucleic acids of the human endocervix. Biol Reprod. 1999 Jan;60(1):58–64. doi: 10.1095/biolreprod60.1.58. [DOI] [PubMed] [Google Scholar]
- Godoy V. G., Dallas M. M., Russo T. A., Malamy M. H. A role for Bacteroides fragilis neuraminidase in bacterial growth in two model systems. Infect Immun. 1993 Oct;61(10):4415–4426. doi: 10.1128/iai.61.10.4415-4426.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guzmán C. A., Platé M., Pruzzo C. Role of neuraminidase-dependent adherence in Bacteroides fragilis attachment to human epithelial cells. FEMS Microbiol Lett. 1990 Sep 1;59(1-2):187–192. doi: 10.1111/j.1574-6968.1989.tb03107.x. [DOI] [PubMed] [Google Scholar]
- Hedges S. R., Mayo M. S., Kallman L., Mestecky J., Hook E. W., 3rd, Russell M. W. Evaluation of immunoglobulin A1 (IgA1) protease and IgA1 protease-inhibitory activity in human female genital infection with Neisseria gonorrhoeae. Infect Immun. 1998 Dec;66(12):5826–5832. doi: 10.1128/iai.66.12.5826-5832.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herold B. C., Siston A., Bremer J., Kirkpatrick R., Wilbanks G., Fugedi P., Peto C., Cooper M. Sulfated carbohydrate compounds prevent microbial adherence by sexually transmitted disease pathogens. Antimicrob Agents Chemother. 1997 Dec;41(12):2776–2780. doi: 10.1128/aac.41.12.2776. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Howe L., Wiggins R., Soothill P. W., Millar M. R., Horner P. J., Corfield A. P. Mucinase and sialidase activity of the vaginal microflora: implications for the pathogenesis of preterm labour. Int J STD AIDS. 1999 Jul;10(7):442–447. doi: 10.1258/0956462991914438. [DOI] [PubMed] [Google Scholar]
- Kahane I., Reisch-Saada A., Almagor M., Abeliuck P., Yatziv S. Glycosidase activities of mycoplasmas. Zentralbl Bakteriol. 1990 Aug;273(3):300–305. doi: 10.1016/s0934-8840(11)80432-9. [DOI] [PubMed] [Google Scholar]
- Kelm S., Schauer R. Sialic acids in molecular and cellular interactions. Int Rev Cytol. 1997;175:137–240. doi: 10.1016/S0074-7696(08)62127-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kilian M., Reinholdt J., Lomholt H., Poulsen K., Frandsen E. V. Biological significance of IgA1 proteases in bacterial colonization and pathogenesis: critical evaluation of experimental evidence. APMIS. 1996 May;104(5):321–338. doi: 10.1111/j.1699-0463.1996.tb00724.x. [DOI] [PubMed] [Google Scholar]
- Kirjavainen P. V., Ouwehand A. C., Isolauri E., Salminen S. J. The ability of probiotic bacteria to bind to human intestinal mucus. FEMS Microbiol Lett. 1998 Oct 15;167(2):185–189. doi: 10.1111/j.1574-6968.1998.tb13226.x. [DOI] [PubMed] [Google Scholar]
- Lehker M. W., Sweeney D. Trichomonad invasion of the mucous layer requires adhesins, mucinases, and motility. Sex Transm Infect. 1999 Aug;75(4):231–238. doi: 10.1136/sti.75.4.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Macfarlane G. T., Gibson G. R. Formation of glycoprotein degrading enzymes by Bacteroides fragilis. FEMS Microbiol Lett. 1991 Jan 15;61(2-3):289–293. doi: 10.1016/0378-1097(91)90567-t. [DOI] [PubMed] [Google Scholar]
- Macfarlane G. T., Hay S., Gibson G. R. Influence of mucin on glycosidase, protease and arylamidase activities of human gut bacteria grown in a 3-stage continuous culture system. J Appl Bacteriol. 1989 May;66(5):407–417. doi: 10.1111/j.1365-2672.1989.tb05110.x. [DOI] [PubMed] [Google Scholar]
- Mangan D. F., Novak M. J., Vora S. A., Mourad J., Kriger P. S. Lectinlike interactions of Fusobacterium nucleatum with human neutrophils. Infect Immun. 1989 Nov;57(11):3601–3611. doi: 10.1128/iai.57.11.3601-3611.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McGregor J. A., French J. I., Jones W., Milligan K., McKinney P. J., Patterson E., Parker R. Bacterial vaginosis is associated with prematurity and vaginal fluid mucinase and sialidase: results of a controlled trial of topical clindamycin cream. Am J Obstet Gynecol. 1994 Apr;170(4):1048–1060. doi: 10.1016/s0002-9378(94)70098-2. [DOI] [PubMed] [Google Scholar]
- Moncla B. J., Braham P., Hillier S. L. Sialidase (neuraminidase) activity among gram-negative anaerobic and capnophilic bacteria. J Clin Microbiol. 1990 Mar;28(3):422–425. doi: 10.1128/jcm.28.3.422-425.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murray P. A., Kern D. G., Winkler J. R. Identification of a galactose-binding lectin on Fusobacterium nucleatum FN-2. Infect Immun. 1988 May;56(5):1314–1319. doi: 10.1128/iai.56.5.1314-1319.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Namavar F., Van der Bijl M. W., Appelmelk B. J., De Graaff J., MacLaren D. M. The role of neuraminidase in haemagglutination and adherence to colon WiDr cells by Bacteroides fragilis. J Med Microbiol. 1994 Jun;40(6):393–396. doi: 10.1099/00222615-40-6-393. [DOI] [PubMed] [Google Scholar]
- Nieuw Amerongen A. V., Bolscher J. G., Bloemena E., Veerman E. C. Sulfomucins in the human body. Biol Chem. 1998 Jan;379(1):1–18. doi: 10.1515/bchm.1998.379.1.1. [DOI] [PubMed] [Google Scholar]
- Padilla-Vaca F., Anaya-Velázquez F. Biochemical properties of a neuraminidase of Trichomonas vaginalis. J Parasitol. 1997 Dec;83(6):1001–1006. [PubMed] [Google Scholar]
- Pritchard D. G., Lin B. Group B streptococcal neuraminidase is actually a hyaluronidase. Infect Immun. 1993 Aug;61(8):3234–3239. doi: 10.1128/iai.61.8.3234-3239.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Puapermpoonsiri S., Kato N., Watanabe K., Ueno K., Chongsomchai C., Lumbiganon P. Vaginal microflora associated with bacterial vaginosis in Japanese and Thai pregnant women. Clin Infect Dis. 1996 Oct;23(4):748–752. doi: 10.1093/clinids/23.4.748. [DOI] [PubMed] [Google Scholar]
- Robertson A. M., Wright D. P. Bacterial glycosulphatases and sulphomucin degradation. Can J Gastroenterol. 1997 May-Jun;11(4):361–366. doi: 10.1155/1997/642360. [DOI] [PubMed] [Google Scholar]
- Robertson J. A., Stemler M. E., Stemke G. W. Immunoglobulin A protease activity of Ureaplasma urealyticum. J Clin Microbiol. 1984 Feb;19(2):255–258. doi: 10.1128/jcm.19.2.255-258.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruseler-van Embden J. G., van Lieshout L. M. Increased faecal glycosidases in patients with Crohn's disease. Digestion. 1987;37(1):43–50. doi: 10.1159/000199486. [DOI] [PubMed] [Google Scholar]
- Scudder P. R., Chantler E. N. Control of human cervical mucin glycosylation by endogenous fucosyl and sialyltransferases. Adv Exp Med Biol. 1982;144:265–267. doi: 10.1007/978-1-4615-9254-9_40. [DOI] [PubMed] [Google Scholar]
- Smith D. G., Russell W. C., Thirkell D. Adherence of Ureaplasma urealyticum to human epithelial cells. Microbiology. 1994 Oct;140(Pt 10):2893–2898. doi: 10.1099/00221287-140-10-2893. [DOI] [PubMed] [Google Scholar]
- Stewart-Tull D. E., Ollar R. A., Scobie T. S. Studies on the Vibrio cholerae mucinase complex. I. Enzymic activities associated with the complex. J Med Microbiol. 1986 Dec;22(4):325–333. doi: 10.1099/00222615-22-4-325. [DOI] [PubMed] [Google Scholar]
- Swanson A. F., Kuo C. C. Identification of lectin-binding proteins in Chlamydia species. Infect Immun. 1990 Feb;58(2):502–507. doi: 10.1128/iai.58.2.502-507.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vetere A., Borriello S. P., Fontaine E., Reed P. J., Taylor-Robinson D. Characterisation of anaerobic curved rods (Mobiluncus spp.) isolated from the urogenital tract. J Med Microbiol. 1987 May;23(3):279–288. doi: 10.1099/00222615-23-3-279. [DOI] [PubMed] [Google Scholar]
- Vimr E. R. Microbial sialidases: does bigger always mean better? Trends Microbiol. 1994 Aug;2(8):271–277. doi: 10.1016/0966-842x(94)90003-5. [DOI] [PubMed] [Google Scholar]
- Wellmer A. Adhärenz von klinischen Candida-albicans-Isolaten an bukkalen Epithelzellen. Mycoses. 1999;42 (Suppl 1):43–47. doi: 10.1111/j.1439-0507.1999.tb04526.x. [DOI] [PubMed] [Google Scholar]
- Wickström C., Davies J. R., Eriksen G. V., Veerman E. C., Carlstedt I. MUC5B is a major gel-forming, oligomeric mucin from human salivary gland, respiratory tract and endocervix: identification of glycoforms and C-terminal cleavage. Biochem J. 1998 Sep 15;334(Pt 3):685–693. doi: 10.1042/bj3340685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wiggins R., Crowley T., Horner P. J., Soothill P. W., Millar M. R., Corfield A. P. Use of 5-bromo-4-chloro-3-indolyl-alpha-D-N-acetylneuraminic acid in a novel spot test To identify sialidase activity in vaginal swabs from women with bacterial vaginosis. J Clin Microbiol. 2000 Aug;38(8):3096–3097. doi: 10.1128/jcm.38.8.3096-3097.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yolken R. H. Enzymic analysis for rapid detection of microbial infection in human body fluids: an overview. Clin Chem. 1981 Sep;27(9):1490–1498. [PubMed] [Google Scholar]
- Zopf D., Roth S. Oligosaccharide anti-infective agents. Lancet. 1996 Apr 13;347(9007):1017–1021. doi: 10.1016/s0140-6736(96)90150-6. [DOI] [PubMed] [Google Scholar]
- de Repentigny L., Aumont F., Bernard K., Belhumeur P. Characterization of binding of Candida albicans to small intestinal mucin and its role in adherence to mucosal epithelial cells. Infect Immun. 2000 Jun;68(6):3172–3179. doi: 10.1128/iai.68.6.3172-3179.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
