Skip to main content
NCBI home page
Infectious Diseases in Obstetrics and Gynecology logoLink to Infectious Diseases in Obstetrics and Gynecology
. 1994;2(2):95–104. doi: 10.1155/S1064744994000463

Virulence Attributes of Low-Virulence Organisms

Bryan Larsen 1,✉
PMCID: PMC2364362  PMID: 18475373

Abstract

The vast majority of infections involving female pelvic structures arise from organisms that are members of the normal flora. In addition, exogenous organisms that invade through the lower genital tract must interact with organisms that are part of the host's flora. In contrast to the concept that the normal flora is entirely innocuous, recent research has begun to identify what appear to be virulence attributes among these ordinarily low-virulence organisms. Most of our understanding of virulence has been derived from highly virulent organisms, of which Neisseria gonorrhoeae provides an example of relevance to the female genital tract. A review of the virulence factors of the gonococcus is presented to serve as an example of the variety of virulence properties associated with pathogenic bacteria. Molecular biology has begun to clarify one of the important paradigms of pathogenic bacteriology—that bacteria change their expression of virulence properties in response to their location within a host or to the stage of infection. Thus, infection involves not only the possession of virulence factors, but also the carefully controlled use of those factors. Virulence is often controlled by the coordinate expression of many virulence-associated genes in response to one environmental signal. With regard to low- virulence organisms present in the female lower genital tract, we are beginning to identify some of their virulence attributes. Examples from the work of our laboratory include the hemolysin of Gardnerella vaginalis and an immunosuppressive mycotoxin produced by Candida albicans. Demonstrating the coordinate expression (or other control mechanisms) of virulence factors in these sometimes innocuous and sometimes inimical organisms represents the next frontier in the study of normal vaginal microbiology.

Full Text

The Full Text of this article is available as a PDF (938.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bessen D., Gotschlich E. C. Interactions of gonococci with HeLa cells: attachment, detachment, replication, penetration, and the role of protein II. Infect Immun. 1986 Oct;54(1):154–160. doi: 10.1128/iai.54.1.154-160.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Black D. B., Morrison J., Snyder L. J., Tally P. Model for clinical social work practice in a health care facility. Soc Work Health Care. 1977 Winter;3(2):143–148. doi: 10.1300/j010v03n02_02. [DOI] [PubMed] [Google Scholar]
  3. Blanton K. J., Biswas G. D., Tsai J., Adams J., Dyer D. W., Davis S. M., Koch G. G., Sen P. K., Sparling P. F. Genetic evidence that Neisseria gonorrhoeae produces specific receptors for transferrin and lactoferrin. J Bacteriol. 1990 Sep;172(9):5225–5235. doi: 10.1128/jb.172.9.5225-5235.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bouali A., Robert R., Tronchin G., Senet J. M. Characterization of binding of human fibrinogen to the surface of germ-tubes and mycelium of candida albicans. J Gen Microbiol. 1987 Mar;133(3):545–551. doi: 10.1099/00221287-133-3-545. [DOI] [PubMed] [Google Scholar]
  5. Bouchara J. P., Tronchin G., Annaix V., Robert R., Senet J. M. Laminin receptors on Candida albicans germ tubes. Infect Immun. 1990 Jan;58(1):48–54. doi: 10.1128/iai.58.1.48-54.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boustouller Y. L., Johnson A. P., Taylor-Robinson D. Pili on Gardnerella vaginalis studied by electronmicroscopy. J Med Microbiol. 1987 Jun;23(4):327–329. doi: 10.1099/00222615-23-4-327. [DOI] [PubMed] [Google Scholar]
  7. Calderone R. A., Braun P. C. Adherence and receptor relationships of Candida albicans. Microbiol Rev. 1991 Mar;55(1):1–20. doi: 10.1128/mr.55.1.1-20.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Calderone R. A., Linehan L., Wadsworth E., Sandberg A. L. Identification of C3d receptors on Candida albicans. Infect Immun. 1988 Jan;56(1):252–258. doi: 10.1128/iai.56.1.252-258.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. De Bernardis F., Molinari A., Boccanera M., Stringaro A., Robert R., Senet J. M., Arancia G., Cassone A. Modulation of cell surface-associated mannoprotein antigen expression in experimental candidal vaginitis. Infect Immun. 1994 Feb;62(2):509–519. doi: 10.1128/iai.62.2.509-519.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eftimiadi C., Buzzi E., Tonetti M., Buffa P., Buffa D., van Steenbergen M. T., de Graaff J., Botta G. A. Short-chain fatty acids produced by anaerobic bacteria alter the physiological responses of human neutrophils to chemotactic peptide. J Infect. 1987 Jan;14(1):43–53. doi: 10.1016/s0163-4453(87)90808-5. [DOI] [PubMed] [Google Scholar]
  11. Gilmore B. J., Retsinas E. M., Lorenz J. S., Hostetter M. K. An iC3b receptor on Candida albicans: structure, function, and correlates for pathogenicity. J Infect Dis. 1988 Jan;157(1):38–46. doi: 10.1093/infdis/157.1.38. [DOI] [PubMed] [Google Scholar]
  12. Gustafson K. S., Vercellotti G. M., Bendel C. M., Hostetter M. K. Molecular mimicry in Candida albicans. Role of an integrin analogue in adhesion of the yeast to human endothelium. J Clin Invest. 1991 Jun;87(6):1896–1902. doi: 10.1172/JCI115214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Heidenreich F., Dierich M. P. Candida albicans and Candida stellatoidea, in contrast to other Candida species, bind iC3b and C3d but not C3b. Infect Immun. 1985 Nov;50(2):598–600. doi: 10.1128/iai.50.2.598-600.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hostetter M. K., Lorenz J. S., Preus L., Kendrick K. E. The iC3b receptor on Candida albicans: subcellular localization and modulation of receptor expression by glucose. J Infect Dis. 1990 Apr;161(4):761–768. doi: 10.1093/infdis/161.4.761. [DOI] [PubMed] [Google Scholar]
  15. Kalo A., Segal E., Sahar E., Dayan D. Interaction of Candida albicans with genital mucosal surfaces: involvement of fibronectin in adherence. J Infect Dis. 1988 Jun;157(6):1253–1256. doi: 10.1093/infdis/157.6.1253. [DOI] [PubMed] [Google Scholar]
  16. Kornfeld S. J., Plaut A. G. Secretory immunity and the bacterial IgA proteases. Rev Infect Dis. 1981 May-Jun;3(3):521–534. doi: 10.1093/clinids/3.3.521. [DOI] [PubMed] [Google Scholar]
  17. Kurtz M. B., Kirsch D. R., Kelly R. The molecular genetics of Candida albicans. Microbiol Sci. 1988 Feb;5(2):58–63. [PubMed] [Google Scholar]
  18. Larsen B., Galask R. P. Influence of estrogen and normal flora on vaginal candidiasis in the rat. J Reprod Med. 1984 Dec;29(12):863–868. [PubMed] [Google Scholar]
  19. McGee Z. A., Johnson A. P., Taylor-Robinson D. Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4. J Infect Dis. 1981 Mar;143(3):413–422. doi: 10.1093/infdis/143.3.413. [DOI] [PubMed] [Google Scholar]
  20. Meyer T. F., Gibbs C. P., Haas R. Variation and control of protein expression in Neisseria. Annu Rev Microbiol. 1990;44:451–477. doi: 10.1146/annurev.mi.44.100190.002315. [DOI] [PubMed] [Google Scholar]
  21. Ollert M. W., Söhnchen R., Korting H. C., Ollert U., Bräutigam S., Bräutigam W. Mechanisms of adherence of Candida albicans to cultured human epidermal keratinocytes. Infect Immun. 1993 Nov;61(11):4560–4568. doi: 10.1128/iai.61.11.4560-4568.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Paruchuri D. K., Seifert H. S., Ajioka R. S., Karlsson K. A., So M. Identification and characterization of a Neisseria gonorrhoeae gene encoding a glycolipid-binding adhesin. Proc Natl Acad Sci U S A. 1990 Jan;87(1):333–337. doi: 10.1073/pnas.87.1.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pohlner J., Halter R., Beyreuther K., Meyer T. F. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. 1987 Jan 29-Feb 4Nature. 325(6103):458–462. doi: 10.1038/325458a0. [DOI] [PubMed] [Google Scholar]
  24. Rottini G., Dobrina A., Forgiarini O., Nardon E., Amirante G. A., Patriarca P. Identification and partial characterization of a cytolytic toxin produced by Gardnerella vaginalis. Infect Immun. 1990 Nov;58(11):3751–3758. doi: 10.1128/iai.58.11.3751-3758.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sandin R. L., Rogers A. L., Beneke E. S., Fernandez M. I. Influence of mucosal cell origin on the in vitro adherence of Candida albicans: are mucosal cells from different sources equivalent? Mycopathologia. 1987 May;98(2):111–119. doi: 10.1007/BF00437297. [DOI] [PubMed] [Google Scholar]
  26. Sawyer R. T., Garner R. E., Hudson J. A. Arg-Gly-Asp (RGD) peptides alter hepatic killing of Candida albicans in the isolated perfused mouse liver model. Infect Immun. 1992 Jan;60(1):213–218. doi: 10.1128/iai.60.1.213-218.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Scott T. G., Curran B., Smyth C. J. Electron microscopy of adhesive interactions between Gardnerella vaginalis and vaginal epithelial cells, McCoy cells and human red blood cells. J Gen Microbiol. 1989 Mar;135(3):475–480. doi: 10.1099/00221287-135-3-475. [DOI] [PubMed] [Google Scholar]
  28. Shah D. T., Larsen B. Clinical isolates of yeast produce a gliotoxin-like substance. Mycopathologia. 1991 Dec;116(3):203–208. doi: 10.1007/BF00436836. [DOI] [PubMed] [Google Scholar]
  29. Skowronski R., Feldman D. Characterization of an estrogen-binding protein in the yeast Candida albicans. Endocrinology. 1989 Apr;124(4):1965–1972. doi: 10.1210/endo-124-4-1965. [DOI] [PubMed] [Google Scholar]
  30. Slutsky B., Buffo J., Soll D. R. High-frequency switching of colony morphology in Candida albicans. Science. 1985 Nov 8;230(4726):666–669. doi: 10.1126/science.3901258. [DOI] [PubMed] [Google Scholar]
  31. Sobel J. D., Myers P. G., Kaye D., Levison M. E. Adherence of Candida albicans to human vaginal and buccal epithelial cells. J Infect Dis. 1981 Jan;143(1):76–82. doi: 10.1093/infdis/143.1.76. [DOI] [PubMed] [Google Scholar]
  32. Soll D. R., Galask R., Isley S., Rao T. V., Stone D., Hicks J., Schmid J., Mac K., Hanna C. Switching of Candida albicans during successive episodes of recurrent vaginitis. J Clin Microbiol. 1989 Apr;27(4):681–690. doi: 10.1128/jcm.27.4.681-690.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stevenson P., Williams P., Griffiths E. Common antigenic domains in transferrin-binding protein 2 of Neisseria meningitidis, Neisseria gonorrhoeae, and Haemophilus influenzae type b. Infect Immun. 1992 Jun;60(6):2391–2396. doi: 10.1128/iai.60.6.2391-2396.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tronchin G., Robert R., Bouali A., Senet J. M. Immunocytochemical localization of in vitro binding of human fibrinogen to Candida albicans germ tube and mycelium. Ann Inst Pasteur Microbiol. 1987 Mar-Apr;138(2):177–187. doi: 10.1016/0769-2609(87)90194-3. [DOI] [PubMed] [Google Scholar]
  35. Weinberg E. D. Role of iron in host-parasite interactions. J Infect Dis. 1971 Oct;124(4):401–410. doi: 10.1093/infdis/124.4.401. [DOI] [PubMed] [Google Scholar]

Articles from Infectious Diseases in Obstetrics and Gynecology are provided here courtesy of Wiley

RESOURCES