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. 1993 Oct;61(10):4263–4271. doi: 10.1128/iai.61.10.4263-4271.1993

Glycolytic enzymes of Candida albicans are nonubiquitous immunogens during candidiasis.

R K Swoboda 1, G Bertram 1, H Hollander 1, D Greenspan 1, J S Greenspan 1, N A Gow 1, G W Gooday 1, A J Brown 1
PMCID: PMC281153  PMID: 8406815

Abstract

A cDNA library was made with mRNA from Candida albicans grown under conditions favoring the hyphal form. The library was screened for sequences that encode immunogenic proteins by using pooled sera from five patients with oral candidiasis and five uninfected patients. Most of these patients were human immunodeficiency virus positive. From 40,000 cDNA clones screened, 83 positive clones were identified. Of these, 10 clones were chosen at random for further analysis. None of these 10 cDNAs were derived from a multigene family. The 5' and 3' ends of all 10 clones were analyzed by DNA sequencing. Two cDNAs were separate isolates of a sequence with strong homology to pyruvate kinase genes from other fungi (59 to 73%) and humans (60%). A third cDNA had strong sequence homology to the Saccharomyces cerevisiae and Kluyveromyces lactis alcohol dehydrogenase genes (68 to 73%). A fourth cDNA was homologous (81%) to an S. cerevisiae protein of unknown function. The functions of the remaining six C. albicans cDNAs are not known. A more detailed analysis of the clones encoding glycolytic enzymes revealed that sera from few patients recognized them as antigens. Therefore, although glycolytic enzymes constitute a group of C. albicans proteins that are immunogenic during oral and esophageal infections, their detection cannot be exploited as an accurate marker of infection.

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Selected References

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

  1. Adams M. D., Kelley J. M., Gocayne J. D., Dubnick M., Polymeropoulos M. H., Xiao H., Merril C. R., Wu A., Olde B., Moreno R. F. Complementary DNA sequencing: expressed sequence tags and human genome project. Science. 1991 Jun 21;252(5013):1651–1656. doi: 10.1126/science.2047873. [DOI] [PubMed] [Google Scholar]
  2. Bergen M. S., Voss E., Soll D. R. Switching at the cellular level in the white-opaque transition of Candida albicans. J Gen Microbiol. 1990 Oct;136(10):1925–1936. doi: 10.1099/00221287-136-10-1925. [DOI] [PubMed] [Google Scholar]
  3. Borg M., Rüchel R. Expression of extracellular acid proteinase by proteolytic Candida spp. during experimental infection of oral mucosa. Infect Immun. 1988 Mar;56(3):626–631. doi: 10.1128/iai.56.3.626-631.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burke R. L., Tekamp-Olson P., Najarian R. The isolation, characterization, and sequence of the pyruvate kinase gene of Saccharomyces cerevisiae. J Biol Chem. 1983 Feb 25;258(4):2193–2201. [PubMed] [Google Scholar]
  5. 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]
  6. Cutler J. E. Putative virulence factors of Candida albicans. Annu Rev Microbiol. 1991;45:187–218. doi: 10.1146/annurev.mi.45.100191.001155. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  9. Franklyn K. M., Warmington J. R., Ott A. K., Ashman R. B. An immunodominant antigen of Candida albicans shows homology to the enzyme enolase. Immunol Cell Biol. 1990 Jun;68(Pt 3):173–178. doi: 10.1038/icb.1990.24. [DOI] [PubMed] [Google Scholar]
  10. Ishiguro A., Homma M., Torii S., Tanaka K. Identification of Candida albicans antigens reactive with immunoglobulin E antibody of human sera. Infect Immun. 1992 Apr;60(4):1550–1557. doi: 10.1128/iai.60.4.1550-1557.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Krupp G. RNA synthesis: strategies for the use of bacteriophage RNA polymerases. Gene. 1988 Dec 10;72(1-2):75–89. doi: 10.1016/0378-1119(88)90129-1. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Lindquist S. Regulation of protein synthesis during heat shock. Nature. 1981 Sep 24;293(5830):311–314. doi: 10.1038/293311a0. [DOI] [PubMed] [Google Scholar]
  14. Livingston D. M., Hahne S. Isolation of a condensed, intracellular form of the 2-micrometer DNA plasmid of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3727–3731. doi: 10.1073/pnas.76.8.3727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Macdonald F., Odds F. C. Virulence for mice of a proteinase-secreting strain of Candida albicans and a proteinase-deficient mutant. J Gen Microbiol. 1983 Feb;129(2):431–438. doi: 10.1099/00221287-129-2-431. [DOI] [PubMed] [Google Scholar]
  16. Manning-Zweerink M., Maloney C. S., Mitchell T. G., Weston H. Immunoblot analyses of Candida albicans-associated antigens and antibodies in human sera. J Clin Microbiol. 1986 Jan;23(1):46–52. doi: 10.1128/jcm.23.1.46-52.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Martin M. V., Craig G. T., Lamb D. J. An investigation of the role of true hypha production in the pathogenesis of experimental oral candidosis. Sabouraudia. 1984;22(6):471–476. doi: 10.1080/00362178485380741. [DOI] [PubMed] [Google Scholar]
  18. Matthews R. C., Burnie J. P., Tabaqchali S. Isolation of immunodominant antigens from sera of patients with systemic candidiasis and characterization of serological response to Candida albicans. J Clin Microbiol. 1987 Feb;25(2):230–237. doi: 10.1128/jcm.25.2.230-237.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Matthews R., Burnie J., Smith D., Clark I., Midgley J., Conolly M., Gazzard B. Candida and AIDS: evidence for protective antibody. Lancet. 1988 Jul 30;2(8605):263–266. doi: 10.1016/s0140-6736(88)92547-0. [DOI] [PubMed] [Google Scholar]
  20. McNally T., Purvis I. J., Fothergill-Gilmore L. A., Brown A. J. The yeast pyruvate kinase gene does not contain a string of non-preferred codons: revised nucleotide sequence. FEBS Lett. 1989 Apr 24;247(2):312–316. doi: 10.1016/0014-5793(89)81359-6. [DOI] [PubMed] [Google Scholar]
  21. Moore P. A., Sagliocco F. A., Wood R. M., Brown A. J. Yeast glycolytic mRNAs are differentially regulated. Mol Cell Biol. 1991 Oct;11(10):5330–5337. doi: 10.1128/mcb.11.10.5330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rikkerink E. H., Magee B. B., Magee P. T. Opaque-white phenotype transition: a programmed morphological transition in Candida albicans. J Bacteriol. 1988 Feb;170(2):895–899. doi: 10.1128/jb.170.2.895-899.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ross I. K., De Bernardis F., Emerson G. W., Cassone A., Sullivan P. A. The secreted aspartate proteinase of Candida albicans: physiology of secretion and virulence of a proteinase-deficient mutant. J Gen Microbiol. 1990 Apr;136(4):687–694. doi: 10.1099/00221287-136-4-687. [DOI] [PubMed] [Google Scholar]
  24. Russell D. W., Smith M., Williamson V. M., Young E. T. Nucleotide sequence of the yeast alcohol dehydrogenase II gene. J Biol Chem. 1983 Feb 25;258(4):2674–2682. [PubMed] [Google Scholar]
  25. Rustchenko-Bulgac E. P., Sherman F., Hicks J. B. Chromosomal rearrangements associated with morphological mutants provide a means for genetic variation of Candida albicans. J Bacteriol. 1990 Mar;172(3):1276–1283. doi: 10.1128/jb.172.3.1276-1283.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ryley J. F., Ryley N. G. Candida albicans--do mycelia matter? J Med Vet Mycol. 1990;28(3):225–239. [PubMed] [Google Scholar]
  27. Saliola M., Gonnella R., Mazzoni C., Falcone C. Two genes encoding putative mitochondrial alcohol dehydrogenases are present in the yeast Kluyveromyces lactis. Yeast. 1991 May-Jun;7(4):391–400. doi: 10.1002/yea.320070409. [DOI] [PubMed] [Google Scholar]
  28. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Santiago T. C., Purvis I. J., Bettany A. J., Brown A. J. The relationship between mRNA stability and length in Saccharomyces cerevisiae. Nucleic Acids Res. 1986 Nov 11;14(21):8347–8360. doi: 10.1093/nar/14.21.8347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Savolainen J., Viander M., Koivikko A. IgE-, IgA- and IgG-antibody responses to carbohydrate and protein antigens of Candida albicans in asthmatic children. Allergy. 1990 Jan;45(1):54–63. doi: 10.1111/j.1398-9995.1990.tb01084.x. [DOI] [PubMed] [Google Scholar]
  31. Scherer S., Magee P. T. Genetics of Candida albicans. Microbiol Rev. 1990 Sep;54(3):226–241. doi: 10.1128/mr.54.3.226-241.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shain D. H., Salvadore C., Denis C. L. Evolution of the alcohol dehydrogenase (ADH) genes in yeast: characterization of a fourth ADH in Kluyveromyces lactis. Mol Gen Genet. 1992 Apr;232(3):479–488. doi: 10.1007/BF00266253. [DOI] [PubMed] [Google Scholar]
  33. Shen H. D., Choo K. B., Lee H. H., Hsieh J. C., Lin W. L., Lee W. R., Han S. H. The 40-kilodalton allergen of Candida albicans is an alcohol dehydrogenase: molecular cloning and immunological analysis using monoclonal antibodies. Clin Exp Allergy. 1991 Nov;21(6):675–681. doi: 10.1111/j.1365-2222.1991.tb03195.x. [DOI] [PubMed] [Google Scholar]
  34. Shen H. D., Choo K. B., Tang R. B., Lee C. F., Yeh J. Y., Han S. H. Allergenic components of Candida albicans identified by immunoblot analysis. Clin Exp Allergy. 1989 Mar;19(2):191–195. doi: 10.1111/j.1365-2222.1989.tb02363.x. [DOI] [PubMed] [Google Scholar]
  35. Shore D., Squire M., Nasmyth K. A. Characterization of two genes required for the position-effect control of yeast mating-type genes. EMBO J. 1984 Dec 1;3(12):2817–2823. doi: 10.1002/j.1460-2075.1984.tb02214.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Strick C. A., James L. C., O'Donnell M. M., Gollaher M. G., Franke A. E. The isolation and characterization of the pyruvate kinase-encoding gene from the yeast Yarrowia lipolytica. Gene. 1992 Sep 1;118(1):65–72. doi: 10.1016/0378-1119(92)90249-o. [DOI] [PubMed] [Google Scholar]
  37. Takenaka M., Noguchi T., Sadahiro S., Hirai H., Yamada K., Matsuda T., Imai E., Tanaka T. Isolation and characterization of the human pyruvate kinase M gene. Eur J Biochem. 1991 May 23;198(1):101–106. doi: 10.1111/j.1432-1033.1991.tb15991.x. [DOI] [PubMed] [Google Scholar]
  38. Torosantucci A., Boccanera M., Casalinuovo I., Pellegrini G., Cassone A. Differences in the antigenic expression of immunomodulatory mannoprotein constituents on yeast and mycelial forms of Candida albicans. J Gen Microbiol. 1990 Jul;136(7):1421–1428. doi: 10.1099/00221287-136-7-1421. [DOI] [PubMed] [Google Scholar]
  39. Young E. T., Pilgrim D. Isolation and DNA sequence of ADH3, a nuclear gene encoding the mitochondrial isozyme of alcohol dehydrogenase in Saccharomyces cerevisiae. Mol Cell Biol. 1985 Nov;5(11):3024–3034. doi: 10.1128/mcb.5.11.3024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Young R. A., Davis R. W. Efficient isolation of genes by using antibody probes. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1194–1198. doi: 10.1073/pnas.80.5.1194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. de Graaff L., Visser J. Structure of the Aspergillus nidulans pyruvate kinase gene. Curr Genet. 1988 Dec;14(6):553–560. doi: 10.1007/BF00434080. [DOI] [PubMed] [Google Scholar]

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