Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-28T06:52:15.199Z Has data issue: false hasContentIssue false
  • English
  • Français

Ultrastructural Imaging of Candida albicans Adhesion to Rat Genital Epithelium through Scanning and Transmission Electron Microscopy

Published online by Cambridge University Press:  07 April 2010

Edilson Damke ,
Agenor Storti-Filho ,
Mary M.T. Irie ,
Márcia A. Carrara ,
Marcia R. Batista ,
Lucélia Donatti ,
Luciene S.A. Gunther ,
Eliana V. Patussi ,
Terezinha I.E. Svidzinski  and
Márcia E.L. Consolaro
Edilson Damke
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
Agenor Storti-Filho
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
Mary M.T. Irie
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
Márcia A. Carrara
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
Marcia R. Batista
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
Lucélia Donatti
Affiliation:
Department of Cell Biology, Federal University of Paraná, Curitiba, 85131-990, Paraná, Brazil
Luciene S.A. Gunther
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
Eliana V. Patussi
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
Terezinha I.E. Svidzinski
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
Márcia E.L. Consolaro*
Affiliation:
Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil
*
Corresponding author. E-mail: melconsolaro@yahoo.com.br
Get access

Abstract

The adhesion of Candida albicans to the genital epithelium has not been fully investigated in vivo. The objective of this study was to evaluate the ultrastructural aspects of C. albicans adhesion in the lower genital system of female Wistar rats through scanning and transmission electron microscopy. The genital infection persisted until the end of the experiment, and all rats showed the same adhesion aspects. Various associated yeast/hyphae were observed in the lumen and adhered both at the vaginal and endocervical levels where the fungal filamentation process occurred. In the vaginal epithelium, closely adhered yeasts were observed as stretched strands bridging between yeasts and the epithelium surface. Different stages of the adhesion, where yeasts internalized into the epithelial cell inside a cytoplasmic vacuole, resembling endocytosis, and a wide fibrillar-floccular, glycocalyx-like layer on the yeasts were observed. On the endocervix, the adhesion occurred between the cilia. In the uterine body, only a yeast-like form was observed with superficial contact. This study reached the initial goal of demonstrating an experimental model for in vivo studies. Continuation of this line of research is important for studies of vulvovaginal candidiasis.

Keywords

Candida albicansadhesion in vivoultrastructuregenital epithelium
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 16 , Issue 3 , June 2010 , pp. 337 - 345
Copyright
Copyright © Microscopy Society of America 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bernhardt, J., Herman, D., Sheridan, M. & Calderone, R. (2001). Adherence and invasion studies of Candida albicans strains, using in vitro models of esophageal candidiasis. J Infect Dis 184, 1170–1175.CrossRefGoogle ScholarPubMed
Bibbo, M. (1997). Comprehensive Cytopathology. Philadelphia, PA: W.B. Saunder Company.Google Scholar
Calderone, R.A. & Fonzi, W.A. (2001). Virulence factors of Candida albicans. Trends Microbiol 9, 327–335.CrossRefGoogle ScholarPubMed
Clemons, K.V., Spearow, J.L., Parmar, R., Espiritu, M. & Stevens, D.A. (2004). Genetic susceptibility of mice to Candida albicans vaginitis correlates with host estrogen sensitivity. Infect Immun 72(8), 4878–4880.CrossRefGoogle ScholarPubMed
Consolaro, M.E.L., Albertoni, T.A., Svidzinski, A.E., Peralta, R.M. & Svidzinski, T.I.E. (2005). Vulvovaginal candidiasis is associated with the production of germ tubes by Candida albicans. Mycopathol 159, 501–507.CrossRefGoogle ScholarPubMed
De Bernardis, F., Lucciarini, R., Boccanera, M., Amantini, C., Arancia, S., Morrone, S., Mosca, M., Cassone, A. & Santoni, G. (2006). Phenotypic and fuctional characterization of vaginal dendritic cells in a rats model of Candida albicans vaginitis. Infect Immun 74, 4282–4294.CrossRefGoogle Scholar
Dehio, C., Meyer, M., Berger, J., Schwarz, H. & Lanz, C. (1997). Interaction of Bartonella henselae with endothelial cells results in bacterial aggregation on the cell surface and the subsequent engulfment and internalization of the bacterial aggregate by a unique structure, the invasome. J Cell Sci 110, 2141–2154.CrossRefGoogle Scholar
Drago, L., Bárbara, M., De Vechi, E., Bonaccorso, C., Fassina, M.C. & Gismondo, M.R. (2000). Candida albicans cellular internalization: A new pathogenic factor? Int J Antim Ag 16, 545–547.CrossRefGoogle ScholarPubMed
Filler, S.G., Swerdloff, J.N., Hobbs, C. & Luckett, P.M. (1995). Penetration and damage of endothelial cells by Candida albicans. Infect Immun 63, 976–983.CrossRefGoogle ScholarPubMed
Howlett, J.A. & Squier, A. (1980). Candida albicans ultrastructure: Colonization and invasion of oral ephitelium. Infect Immun 29, 252–260.CrossRefGoogle Scholar
Irie, M.M.T., Consolaro, M.E.L., Guedes, T.A., Donatti, L., Patussi, E.V. & Svidzinski, T.I.E. (2006). A simplified technique for evaluating the adherence of yeasts to human vaginal epithelial cells. J Clin Lab Anal 20, 195–203.CrossRefGoogle Scholar
Jabra-Rizk, M.A., Falkler, W.A. Jr., Merz, W.G., Baqui, A.A.M.A., Kelley, J.I. & Meiller, T.F. (2001). Cell surface hydrofobicity associated adherence of Candida dubliniensis to human bucal ephitelial cells. Rev Iberoam Micol 18, 17–22.Google Scholar
Jayatilake, J.A., Saramanayake, Y.H. & Saramanayake, L.P. (2005). An ultrastructural and a cytochemical study of candidal invasion of reconstituted human oral epithelium. J Oral Pathol Med 34, 240–246.CrossRefGoogle Scholar
Kamai, Y., Kubota, M., Hosokawa, T., Fukuoka, T. & Filler, S.G. (2002). Contribution of Candida albicans ALS1 to the pathogenesis of experimental oropharyngeal candidiasis. Infect Immun 70, 5256–5258.CrossRefGoogle Scholar
Kaposzta, R., Marodi, L., Hollinshead, M., Gordon, S. & Da Silva, R.P. (1999). Rapid recruitment of late endossomes and lysossomes in mouse macrophages ingesting Candida albicans. J Cell Sci 112, 3237–3248.CrossRefGoogle Scholar
Karnovsky, M.J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27, 137–138.Google Scholar
Kurtzmann, C.P. & Fell, F.W. (1998). The Yeast. A Taxonomia Study. Amsterdam: Elsevier.Google Scholar
Mandl, A.M. (1951). The phases of the estrous cycle in the adult white rat. J Exp Biol 28, 576–584.CrossRefGoogle Scholar
Mardh, P.A., Rodrigues, A.G., Genc, M., Novikova, N., Martinez-de-Oliveira, J. & Guaschino, S. (2002). Facts and myths on recurrent vulvovaginal candidosis: A review on epidemiology, clinical manifestations, diagnosis, pathogenesis and therapy. Int J STD AIDS 13, 522–539.CrossRefGoogle ScholarPubMed
Marodi, L. (1997). Local and systemic host defense mechanisms against Candida: Immunophatology of candidal infections. Paediatr Infect Dis J 16, 795–801.CrossRefGoogle Scholar
Montes, L.F. & Wilborn, W.H. (1968). Ultrastructural features of host-parasite relationship in oral candidiasis. J Bacteriol 96, 1349–1356.CrossRefGoogle ScholarPubMed
Palmer, L.M., Reilly, T., Utsalo, S.J. & Bonnenberg, M.S. (1997). Internalization of Escherichia coli by human renal ephitelial cells is associated with tyrosine phosphorylation of specific host cell proteins. Infect Immun 65, 2570–2575.CrossRefGoogle Scholar
Phan, Q.T., Belanger, P.H. & Filler, S.G. (2000). Role of hyphal formation in interactions of Candida albicans with endothelial cells. Infect Immun 68, 3485–3490.CrossRefGoogle ScholarPubMed
Pichová, I., Pavlicková, J., Dostál, J., Dolejsi, E., Hrusková-Heindigsfeldová, O., Weber, J., Ruml, T. & Soucek, M. (2001). Secreted aspartic protinases of Candida albicans, Candida tropicalis, Candida parapsilosis and Candida lusitaniae: Inhibition with peptidomimetic inhibitors. Eur J Biochem 268, 2669–2677.CrossRefGoogle ScholarPubMed
Ray, T.L., Digre, K.B. & Payne, C.D. (1984). Adherence of Candida species to human epidermal corneocytes and bucal mucosal cells: Correlation with cutaneous pathogenicity. J Invest Dermatol 83, 37–41.CrossRefGoogle Scholar
Shin, J.H., Kee, S.J., Shin, M.G., Kim, S.H., Shin, D.H., Lee, S.K., Suh, S.P. & Ryang, D.W. (2002). Biofilm production by isolates of Candida species recovered from nonneutropenic patients comparison of bloodstream isolates with isolates from others sources. J Clin Microb 40, 1244–1256.CrossRefGoogle Scholar
Sobel, J.D. (1993). Candidal vulvovaginitis. Clin Obstet Gynecol 36, 153–212.CrossRefGoogle ScholarPubMed
Sobel, J.D. (2007). Vulvovaginal candidosis. Lanc 369, 1961–1971.CrossRefGoogle ScholarPubMed
Sugita, T., Kurosaka, S., Yajitate, M., Sato, H. & Nishikawa, A. (2002). Extracellular proteinase and phospholipase activity of three genotypic strains of a human pathogenic yeast, Candida albicans. Microbiol Immunol 46, 881–883.CrossRefGoogle ScholarPubMed
Vitkov, L., Krautgartner, W.D., Hannig, M., Weitgasser, R. & Stoiber, W. (2002). Candida attachment to oral ephitelium. Oral Microbiol Immunol 17, 60–64.CrossRefGoogle Scholar
Yu, L., Lee, K.K., Ens, K., Doig, P.C., Carpenter, M.R., Staddon, W. & Hodges, R.S. (1994). Partial characterization of a Candida albicans fimbrial adhesion. Infect Immun 62, 2834–2842.CrossRefGoogle Scholar