Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1988 Aug;56(8):1942–1949. doi: 10.1128/iai.56.8.1942-1949.1988

Scanning electron microscopy of epidermal adherence and cavitation in murine candidiasis: a role for Candida acid proteinase.

T L Ray 1, C D Payne 1
PMCID: PMC259505  PMID: 3294180

Abstract

Adherence of blastoconidia to epidermal corneocytes is an early event in Candida colonization and infection of the skin. Pathogenic species adhere more avidly than nonpathogenic species, transform to hyphal growth, and invade the stratum corneum of the skin. Adherence was studied by scanning electron microscopy of experimental murine cutaneous Candida infections, using six species of Candida. Candida albicans and C. stellatoidea blastoconidia, applied to newborn mouse skin, adhered to the stratum corneum in greater numbers than other species tested, acquired fibrils and strands of amorphous mucinlike material ("cohesin") between spores and the corneocyte cell surface, formed cavitations in the corneocyte surface, and invaded the corneocyte envelope by hyphal growth at sites distant to the point of blastoconidia attachment. Other species showed little or no adherence, colonization, or cavitation of the corneocyte surface, except C. tropicalis, which showed intermediate results. Pepstatin, an inhibitor of Candida acid proteinase, did not alter adherence or cohesion formation, but inhibited formation of corneocyte cavitations about adherent blastoconidia, suggesting that this enzyme may facilitate adherence/invasion events on skin. Depletion of surface lipids did not alter the formation of cohesin material or the adherence process. Adherence and invasion of epithelium by pathogenic Candida species include the interaction of blastoconidia with an epithelial surface cohesin material that participates in the adherence process. Candida acid proteinase, a keratinolytic enzyme, may participate in the cavitation process of the corneocyte surface by C. albicans.

Full text

PDF
1942

Images in this article

1943Image
on p.1943
1944Image
on p.1944
1944Image
on p.1944
1945Image
on p.1945
1946Image
on p.1946
1947Image
on p.1947
1947Image
on p.1947
1948Image
on p.1948

Selected References

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

  1. Calderone R. A., Lehrer N., Segal E. Adherence of Candida albicans to buccal and vaginal epithelial cells: ultrastructural observations. Can J Microbiol. 1984 Aug;30(8):1001–1007. doi: 10.1139/m84-156. [DOI] [PubMed] [Google Scholar]
  2. Critchley I. A., Douglas L. J. Isolation and partial characterization of an adhesin from Candida albicans. J Gen Microbiol. 1987 Mar;133(3):629–636. doi: 10.1099/00221287-133-3-629. [DOI] [PubMed] [Google Scholar]
  3. Daimond R. D., Krzesicki R. Mechanisms of attachment of neutrophils to Candida albicans pseudohyphae in the absence of serum, and of subsequent damage to pseudohyphae by microbicidal processes of neutrophils in vitro. J Clin Invest. 1978 Feb;61(2):360–369. doi: 10.1172/JCI108946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Douglas L. J. Adhesion of Candida species to epithelial surfaces. Crit Rev Microbiol. 1987;15(1):27–43. doi: 10.3109/10408418709104446. [DOI] [PubMed] [Google Scholar]
  5. Howlett J. A., Squier C. A. Candida albicans ultrastructure: colonization and invasion of oral epithelium. Infect Immun. 1980 Jul;29(1):252–260. doi: 10.1128/iai.29.1.252-260.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kimura L. H., Pearsall N. N. Adherence of Candida albicans to human buccal epithelial cells. Infect Immun. 1978 Jul;21(1):64–68. doi: 10.1128/iai.21.1.64-68.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kimura L. H., Pearsall N. N. Relationship between germination of Candida albicans and increased adherence to human buccal epithelial cells. Infect Immun. 1980 May;28(2):464–468. doi: 10.1128/iai.28.2.464-468.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. King R. D., Lee J. C., Morris A. L. Adherence of Candida albicans and other Candida species to mucosal epithelial cells. Infect Immun. 1980 Feb;27(2):667–674. doi: 10.1128/iai.27.2.667-674.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Klotz S. A., Drutz D. J., Harrison J. L., Huppert M. Adherence and penetration of vascular endothelium by Candida yeasts. Infect Immun. 1983 Oct;42(1):374–384. doi: 10.1128/iai.42.1.374-384.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Klotz S. A., Drutz D. J., Zajic J. E. Factors governing adherence of Candida species to plastic surfaces. Infect Immun. 1985 Oct;50(1):97–101. doi: 10.1128/iai.50.1.97-101.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kwon-Chung K. J., Lehman D., Good C., Magee P. T. Genetic evidence for role of extracellular proteinase in virulence of Candida albicans. Infect Immun. 1985 Sep;49(3):571–575. doi: 10.1128/iai.49.3.571-575.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lee J. C., King R. D. Characterization of Candida albicans adherence to human vaginal epithelial cells in vitro. Infect Immun. 1983 Sep;41(3):1024–1030. doi: 10.1128/iai.41.3.1024-1030.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lehrer N., Segal E., Barr-Nea L. In vitro and in vivo adherence of Candida albicans to mucosal surfaces. Ann Microbiol (Paris) 1983 Sep-Oct;134B(2):293–306. doi: 10.1016/s0769-2609(83)80042-8. [DOI] [PubMed] [Google Scholar]
  14. Macdonald F., Odds F. C. Inducible proteinase of Candida albicans in diagnostic serology and in the pathogenesis of systemic candidosis. J Med Microbiol. 1980 Aug;13(3):423–435. doi: 10.1099/00222615-13-3-423. [DOI] [PubMed] [Google Scholar]
  15. Macdonald F. Secretion of inducible proteinase by pathogenic Candida species. Sabouraudia. 1984;22(1):79–82. [PubMed] [Google Scholar]
  16. Marrie T. J., Costerton J. W. The ultrastructure of Candida albicans infections. Can J Microbiol. 1981 Nov;27(11):1156–1164. doi: 10.1139/m81-181. [DOI] [PubMed] [Google Scholar]
  17. McCourtie J., Douglas L. J. Extracellular polymer of Candida albicans: isolation, analysis and role in adhesion. J Gen Microbiol. 1985 Mar;131(3):495–503. doi: 10.1099/00221287-131-3-495. [DOI] [PubMed] [Google Scholar]
  18. Negi M., Tsuboi R., Matsui T., Ogawa H. Isolation and characterization of proteinase from Candida albicans: substrate specificity. J Invest Dermatol. 1984 Jul;83(1):32–36. doi: 10.1111/1523-1747.ep12261656. [DOI] [PubMed] [Google Scholar]
  19. Persi M. A., Burnham J. C., Duhring J. L. Effects of carbon dioxide and pH on adhesion of Candida albicans to vaginal epithelial cells. Infect Immun. 1985 Oct;50(1):82–90. doi: 10.1128/iai.50.1.82-90.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pope L. M., Cole G. T. SEM studies of adherence of candida albicans to the gastrointestinal tract of infant mice. Scan Electron Microsc. 1981;(Pt 3):73–80. [PubMed] [Google Scholar]
  21. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ray T. L., Digre K. B., Payne C. D. Adherence of Candida species to human epidermal corneocytes and buccal mucosal cells: correlation with cutaneous pathogenicity. J Invest Dermatol. 1984 Jul;83(1):37–41. doi: 10.1111/1523-1747.ep12261661. [DOI] [PubMed] [Google Scholar]
  23. Ray T. L., Wuepper K. D. Activation of the alternative (properdin) pathway of complement by Candida albicans and related species. J Invest Dermatol. 1976 Dec;67(6):700–703. doi: 10.1111/1523-1747.ep12598581. [DOI] [PubMed] [Google Scholar]
  24. Ray T. L., Wuepper K. D. Experimental cutaneous candidiasis in rodents. J Invest Dermatol. 1976 Jan;66(1):29–33. doi: 10.1111/1523-1747.ep12478053. [DOI] [PubMed] [Google Scholar]
  25. Ray T. L., Wuepper K. D. Experimental cutaneous candidiasis in rodents; II. Role of the stratum corneum barrier and serum complement as a mediator of a protective infalmmatory response. Arch Dermatol. 1978 Apr;114(4):539–543. doi: 10.1001/archderm.114.4.539. [DOI] [PubMed] [Google Scholar]
  26. Remold H., Fasold H., Staib F. Purification and characterization of a proteolytic enzyme from Candida albicans. Biochim Biophys Acta. 1968 Oct 8;167(2):399–406. doi: 10.1016/0005-2744(68)90219-2. [DOI] [PubMed] [Google Scholar]
  27. Rüchel R. Properties of a purified proteinase from the yeast Candida albicans. Biochim Biophys Acta. 1981 May 14;659(1):99–113. doi: 10.1016/0005-2744(81)90274-6. [DOI] [PubMed] [Google Scholar]
  28. Rüchel R., Uhlemann K., Böning B. Secretion of acid proteinases by different species of the genus Candida. Zentralbl Bakteriol Mikrobiol Hyg A. 1983 Nov;255(4):537–548. [PubMed] [Google Scholar]
  29. Sandin R. L., Rogers A. L., Patterson R. J., Beneke E. S. Evidence for mannose-mediated adherence of Candida albicans to human buccal cells in vitro. Infect Immun. 1982 Jan;35(1):79–85. doi: 10.1128/iai.35.1.79-85.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Segal E., Lehrer N., Ofek I. Adherence of Candida albicans to human vaginal epithelial cells: inhibition by amino sugars. Exp Cell Biol. 1982;50(1):13–17. doi: 10.1159/000163121. [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. Tsuobi R., Kurita Y., Negi M., Ogawa H. A specific inhibitor of keratinolytic proteinase from Candida albicans could inhibit the cell growth of C. albicans. J Invest Dermatol. 1985 Nov;85(5):438–440. doi: 10.1111/1523-1747.ep12277147. [DOI] [PubMed] [Google Scholar]
  33. Wilborn W. H., Montes L. F. Scanning electron microscopy of oral lesions in chronic mucocutaneous candidiasis. JAMA. 1980 Nov 21;244(20):2294–2297. [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES