Abstract
The ALS (agglutinin-like sequence) gene family of Candida albicans encodes cell-surface glycoproteins implicated in adhesion of the organism to host surfaces. Southern blot analysis with ALS-specific probes suggested the presence of ALS gene families in C. dubliniensis and C. tropicalis; three partial ALS genes were isolated from each organism. Northern blot analysis demonstrated that mechanisms governing expression of ALS genes in C. albicans and C. dubliniensis are different. Western blots with an anti-Als serum showed that cross-reactive proteins are linked by beta 1,6-glucan in the cell wall of each non-albicans Candida, suggesting similar cell wall architecture and conserved processing of Als proteins in these organisms. Although an ALS family is present in each organism, phylogenetic analysis of the C. albicans, C. dubliniensis, and C. tropicalis ALS genes indicated that, within each species, sequence diversification is extensive and unique ALS sequences have arisen. Phylogenetic analysis of the ALS and SAP (secreted aspartyl proteinase) families show that the ALS family is younger than the SAP family. ALS genes in C. albicans, C. dubliniensis, and C. tropicalis tend to be located on chromosomes that also encode genes from the SAP family, yet the two families have unexpectedly different evolutionary histories. Homologous recombination between the tandem repeat sequences present in ALS genes could explain the different histories for co-localized genes in a predominantly clonal organism like C. albicans.
Full Text
The Full Text of this article is available as a PDF (490.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Barns S. M., Lane D. J., Sogin M. L., Bibeau C., Weisburg W. G. Evolutionary relationships among pathogenic Candida species and relatives. J Bacteriol. 1991 Apr;173(7):2250–2255. doi: 10.1128/jb.173.7.2250-2255.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bierne H., Michel B. When replication forks stop. Mol Microbiol. 1994 Jul;13(1):17–23. doi: 10.1111/j.1365-2958.1994.tb00398.x. [DOI] [PubMed] [Google Scholar]
- Borg-von Zepelin M., Meyer I., Thomssen R., Würzner R., Sanglard D., Telenti A., Monod M. HIV-Protease inhibitors reduce cell adherence of Candida albicans strains by inhibition of yeast secreted aspartic proteases. J Invest Dermatol. 1999 Nov;113(5):747–751. doi: 10.1046/j.1523-1747.1999.00747.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Cassone A., De Bernardis F., Torosantucci A., Tacconelli E., Tumbarello M., Cauda R. In vitro and in vivo anticandidal activity of human immunodeficiency virus protease inhibitors. J Infect Dis. 1999 Aug;180(2):448–453. doi: 10.1086/314871. [DOI] [PubMed] [Google Scholar]
- Darwazah A., Berg G., Faris B. Candida parapsilosis: an unusual organism causing prosthetic heart valve infective endocarditis. J Infect. 1999 Mar;38(2):130–131. doi: 10.1016/s0163-4453(99)90084-1. [DOI] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fridkin S. K., Jarvis W. R. Epidemiology of nosocomial fungal infections. Clin Microbiol Rev. 1996 Oct;9(4):499–511. doi: 10.1128/cmr.9.4.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fu Y., Rieg G., Fonzi W. A., Belanger P. H., Edwards J. E., Jr, Filler S. G. Expression of the Candida albicans gene ALS1 in Saccharomyces cerevisiae induces adherence to endothelial and epithelial cells. Infect Immun. 1998 Apr;66(4):1783–1786. doi: 10.1128/iai.66.4.1783-1786.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gaur N. K., Klotz S. A. Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect Immun. 1997 Dec;65(12):5289–5294. doi: 10.1128/iai.65.12.5289-5294.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilfillan G. D., Sullivan D. J., Haynes K., Parkinson T., Coleman D. C., Gow N. A. Candida dubliniensis: phylogeny and putative virulence factors. Microbiology. 1998 Apr;144(Pt 4):829–838. doi: 10.1099/00221287-144-4-829. [DOI] [PubMed] [Google Scholar]
- Gruber A., Speth C., Lukasser-Vogl E., Zangerle R., Borg-von Zepelin M., Dierich M. P., Würzner R. Human immunodeficiency virus type 1 protease inhibitor attenuates Candida albicans virulence properties in vitro. Immunopharmacology. 1999 Apr;41(3):227–234. doi: 10.1016/s0162-3109(99)00035-1. [DOI] [PubMed] [Google Scholar]
- Hoegl L., Thoma-Greber E., Röcken M., Korting H. C. HIV protease inhibitors influence the prevalence of oral candidosis in HIV-infected patients: a 2-year study. Mycoses. 1998 Sep-Oct;41(7-8):321–325. doi: 10.1111/j.1439-0507.1998.tb00345.x. [DOI] [PubMed] [Google Scholar]
- Hoppe J. E., Klausner M., Klingebiel T., Niethammer D. Retrospective analysis of yeast colonization and infections in paediatric bone marrow transplant recipients. Mycoses. 1997 Jan-Feb;40(1-2):47–54. doi: 10.1111/j.1439-0507.1997.tb00170.x. [DOI] [PubMed] [Google Scholar]
- Hoyer L. L., Hecht J. E. The ALS5 gene of Candida albicans and analysis of the Als5p N-terminal domain. Yeast. 2001 Jan 15;18(1):49–60. doi: 10.1002/1097-0061(200101)18:1<49::AID-YEA646>3.0.CO;2-M. [DOI] [PubMed] [Google Scholar]
- Hoyer L. L., Hecht J. E. The ALS6 and ALS7 genes of Candida albicans. Yeast. 2000 Jun 30;16(9):847–855. doi: 10.1002/1097-0061(20000630)16:9<847::AID-YEA562>3.0.CO;2-9. [DOI] [PubMed] [Google Scholar]
- Hoyer L. L., Payne T. L., Bell M., Myers A. M., Scherer S. Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr Genet. 1998 Jun;33(6):451–459. doi: 10.1007/s002940050359. [DOI] [PubMed] [Google Scholar]
- Hoyer L. L., Payne T. L., Hecht J. E. Identification of Candida albicans ALS2 and ALS4 and localization of als proteins to the fungal cell surface. J Bacteriol. 1998 Oct;180(20):5334–5343. doi: 10.1128/jb.180.20.5334-5343.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoyer L. L., Scherer S., Shatzman A. R., Livi G. P. Candida albicans ALS1: domains related to a Saccharomyces cerevisiae sexual agglutinin separated by a repeating motif. Mol Microbiol. 1995 Jan;15(1):39–54. doi: 10.1111/j.1365-2958.1995.tb02219.x. [DOI] [PubMed] [Google Scholar]
- Hube B., Monod M., Schofield D. A., Brown A. J., Gow N. A. Expression of seven members of the gene family encoding secretory aspartyl proteinases in Candida albicans. Mol Microbiol. 1994 Oct;14(1):87–99. doi: 10.1111/j.1365-2958.1994.tb01269.x. [DOI] [PubMed] [Google Scholar]
- Hube B., Rüchel R., Monod M., Sanglard D., Odds F. C. Functional aspects of secreted Candida proteinases. Adv Exp Med Biol. 1998;436:339–344. doi: 10.1007/978-1-4615-5373-1_47. [DOI] [PubMed] [Google Scholar]
- Hughes A. L. Concerted evolution of exons and introns in the MHC-linked tenascin-X gene of mammals. Mol Biol Evol. 1999 Nov;16(11):1558–1567. doi: 10.1093/oxfordjournals.molbev.a026068. [DOI] [PubMed] [Google Scholar]
- Hull C. M., Raisner R. M., Johnson A. D. Evidence for mating of the "asexual" yeast Candida albicans in a mammalian host. Science. 2000 Jul 14;289(5477):307–310. doi: 10.1126/science.289.5477.307. [DOI] [PubMed] [Google Scholar]
- Kapteyn J. C., Hoyer L. L., Hecht J. E., Müller W. H., Andel A., Verkleij A. J., Makarow M., Van Den Ende H., Klis F. M. The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol Microbiol. 2000 Feb;35(3):601–611. doi: 10.1046/j.1365-2958.2000.01729.x. [DOI] [PubMed] [Google Scholar]
- Kapteyn J. C., Van Den Ende H., Klis F. M. The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim Biophys Acta. 1999 Jan 6;1426(2):373–383. doi: 10.1016/s0304-4165(98)00137-8. [DOI] [PubMed] [Google Scholar]
- Kunova A., Trupl J., Demitrovicova A., Jesenska Z., Grausova S., Grey E., Pichna P., Kralovicova K., Sorkovska D., Krupova I. Eight-year surveillance of non-albicans Candida spp. in an oncology department prior to and after fluconazole had been introduced into antifungal prophylaxis. Microb Drug Resist. 1997 Fall;3(3):283–287. doi: 10.1089/mdr.1997.3.283. [DOI] [PubMed] [Google Scholar]
- Lipke P. N., Wojciechowicz D., Kurjan J. AG alpha 1 is the structural gene for the Saccharomyces cerevisiae alpha-agglutinin, a cell surface glycoprotein involved in cell-cell interactions during mating. Mol Cell Biol. 1989 Aug;9(8):3155–3165. doi: 10.1128/mcb.9.8.3155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Magee B. B., Magee P. T. Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains. Science. 2000 Jul 14;289(5477):310–313. doi: 10.1126/science.289.5477.310. [DOI] [PubMed] [Google Scholar]
- Mahrous M., Sawant A. D., Pruitt W. R., Lott T., Meyer S. A., Ahearn D. G. DNA relatedness, karyotyping and gene probing of Candida tropicalis, Candida albicans and its synonyms Candida stellatoidea and Candida claussenii. Eur J Epidemiol. 1992 May;8(3):444–451. doi: 10.1007/BF00158581. [DOI] [PubMed] [Google Scholar]
- Monod M., Hube B., Hess D., Sanglard D. Differential regulation of SAP8 and SAP9, which encode two new members of the secreted aspartic proteinase family in Candida albicans. Microbiology. 1998 Oct;144(Pt 10):2731–2737. doi: 10.1099/00221287-144-10-2731. [DOI] [PubMed] [Google Scholar]
- Monod M., Togni G., Hube B., Sanglard D. Multiplicity of genes encoding secreted aspartic proteinases in Candida species. Mol Microbiol. 1994 Jul;13(2):357–368. doi: 10.1111/j.1365-2958.1994.tb00429.x. [DOI] [PubMed] [Google Scholar]
- Ortí G., Pearse D. E., Avise J. C. Phylogenetic assessment of length variation at a microsatellite locus. Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10745–10749. doi: 10.1073/pnas.94.20.10745. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parniske M., Jones J. D. Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. Proc Natl Acad Sci U S A. 1999 May 11;96(10):5850–5855. doi: 10.1073/pnas.96.10.5850. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanglard D., Hube B., Monod M., Odds F. C., Gow N. A. A triple deletion of the secreted aspartyl proteinase genes SAP4, SAP5, and SAP6 of Candida albicans causes attenuated virulence. Infect Immun. 1997 Sep;65(9):3539–3546. doi: 10.1128/iai.65.9.3539-3546.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaller M., Korting H. C., Schäfer W., Bastert J., Chen W., Hube B. Secreted aspartic proteinase (Sap) activity contributes to tissue damage in a model of human oral candidosis. Mol Microbiol. 1999 Oct;34(1):169–180. doi: 10.1046/j.1365-2958.1999.01590.x. [DOI] [PubMed] [Google Scholar]
- Smits G. J., Kapteyn J. C., van den Ende H., Klis F. M. Cell wall dynamics in yeast. Curr Opin Microbiol. 1999 Aug;2(4):348–352. doi: 10.1016/s1369-5274(99)80061-7. [DOI] [PubMed] [Google Scholar]
- Sugita T., Nakase T. Non-universal usage of the leucine CUG codon and the molecular phylogeny of the genus Candida. Syst Appl Microbiol. 1999 Feb;22(1):79–86. doi: 10.1016/S0723-2020(99)80030-7. [DOI] [PubMed] [Google Scholar]
- Sullivan D. J., Westerneng T. J., Haynes K. A., Bennett D. E., Coleman D. C. Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology. 1995 Jul;141(Pt 7):1507–1521. doi: 10.1099/13500872-141-7-1507. [DOI] [PubMed] [Google Scholar]
- Sullivan D., Coleman D. Candida dubliniensis: an emerging opportunistic pathogen. Curr Top Med Mycol. 1997 Dec;8(1-2):15–25. [PubMed] [Google Scholar]
- Weinberger M., Sacks T., Sulkes J., Shapiro M., Polacheck I. Increasing fungal isolation from clinical specimens: experience in a university hospital over a decade. J Hosp Infect. 1997 Mar;35(3):185–195. doi: 10.1016/s0195-6701(97)90206-1. [DOI] [PubMed] [Google Scholar]
- Wickes B., Staudinger J., Magee B. B., Kwon-Chung K. J., Magee P. T., Scherer S. Physical and genetic mapping of Candida albicans: several genes previously assigned to chromosome 1 map to chromosome R, the rDNA-containing linkage group. Infect Immun. 1991 Jul;59(7):2480–2484. doi: 10.1128/iai.59.7.2480-2484.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wingard J. R. Importance of Candida species other than C. albicans as pathogens in oncology patients. Clin Infect Dis. 1995 Jan;20(1):115–125. doi: 10.1093/clinids/20.1.115. [DOI] [PubMed] [Google Scholar]
- Wingard J. R., Merz W. G., Saral R. Candida tropicalis: a major pathogen in immunocompromised patients. Ann Intern Med. 1979 Oct;91(4):539–543. doi: 10.7326/0003-4819-91-4-539. [DOI] [PubMed] [Google Scholar]
- Zimmer E. A., Martin S. L., Beverley S. M., Kan Y. W., Wilson A. C. Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2158–2162. doi: 10.1073/pnas.77.4.2158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Viragh P. A., Sanglard D., Togni G., Falchetto R., Monod M. Cloning and sequencing of two Candida parapsilosis genes encoding acid proteases. J Gen Microbiol. 1993 Feb;139(2):335–342. doi: 10.1099/00221287-139-2-335. [DOI] [PubMed] [Google Scholar]
- van 't Wout J. W. Fluconazole treatment of candidal infections caused by non-albicans Candida species. Eur J Clin Microbiol Infect Dis. 1996 Mar;15(3):238–242. doi: 10.1007/BF01591361. [DOI] [PubMed] [Google Scholar]