Amino acids mediate colony and cell differentiation in the fungal pathogen Free

Abstract

is responsible for severe cases of non-albicans systemic candidiasis and is one of the leading causes of mortality in neonates. The molecular mechanisms underlying this organism's virulence remain unknown. Unlike , which can exist in several morphogenetic forms, exists in either the yeast or pseudohyphal forms. The environmental signals that trigger pseudohyphal differentiation and the signalling pathways that transduce these signals are unknown. This paper provides evidence for the role of amino acids in morphogenesis in . The cell and colony morphologies, pseudohyphal differentiation and invasive growth of five isolates were characterized in ammonium-rich minimal media lacking or supplemented with naturally occurring amino acids. underwent dramatic changes in cellular and colony morphology and formed pseudohyphae in response to a specific subset of amino acids. Transport studies showed that these amino acid inducers activate the transport of some, but not all, unrelated amino acids. Interestingly, citrulline, an amino acid that is not transported in the presence of ammonium, strongly induced pseudohyphal morphogenesis in under these conditions. Together the data suggest that amino acids are important morphogens in and that amino-acid-mediated morphogenesis in this organism does not require transport of the ligand across the plasma membrane.

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2006-10-01
2024-03-28
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References

  1. Barlow A. J, Aldersley T, Chattaway F. W. 1974; Factors present in serum and seminal plasma which promote germ-tube formation and mycelial growth of Candida albicans . J Gen Microbiol 82:261–272 [CrossRef]
    [Google Scholar]
  2. Bassetti M, Righi E, Costa A, Fasce R, Molinari M. P, Rosso R, Pallavicini F. B, Viscoli C. 2006; Epidemiological trends in nosocomial candidemia in intensive care. BMC Infect Dis 6:21 [CrossRef]
    [Google Scholar]
  3. Brega E, Zufferey R, Mamoun C. B. 2004; Candida albicans Csy1p is a nutrient sensor important for activation of amino acid uptake and hyphal morphogenesis. Eukaryot Cell 3:135–143 [CrossRef]
    [Google Scholar]
  4. Buckley H. R, Van Uden N. 1963; The identification of Candida albicans within two hours by the use of an egg white slide preparation. Sabouraudia 2:205–208 [CrossRef]
    [Google Scholar]
  5. Chowdhary A, Becker K, Fegeler W, Gugnani H. C, Kapoor L, Randhawa V. S, Mehta G. 2003; An outbreak of candidemia due to Candida tropicalis in a neonatal intensive care unit. Mycoses 46:287–292 [CrossRef]
    [Google Scholar]
  6. Dabrowa N, Taxer S. S, Howard D. H. 1976; Germination of Candida albicans induced by proline. Infect Immun 13:830–835
    [Google Scholar]
  7. Didion T, Regenberg B, Jorgensen M. U, Kielland-Brandt M. C, Andersen H. A. 1998; The permease homologue Ssy1p controls the expression of amino acid and peptide transporter genes in Saccharomyces cerevisiae . Mol Microbiol 27:643–650 [CrossRef]
    [Google Scholar]
  8. Donaton M. C, Holsbeeks I, Lagatie O, Van Zeebroeck G, Crauwels M, Winderickx J, Thevelein J. M. 2003; The Gap1 general amino acid permease acts as an amino acid sensor for activation of protein kinase A targets in the yeast Saccharomyces cerevisiae . Mol Microbiol 50:911–929 [CrossRef]
    [Google Scholar]
  9. Feng Q, Summers E, Guo B, Fink G. 1999; Ras signaling is required for serum-induced hyphal differentiation in Candida albicans . J Bacteriol 181:6339–6346
    [Google Scholar]
  10. Fridkin S. K, Kaufman D, Edwards J. R, Shetty S, Horan T. 2006; Changing incidence of Candida bloodstream infections among NICU patients in the United States: 1995–2004. Pediatrics 117:1680–1687 [CrossRef]
    [Google Scholar]
  11. Grauslund M, Didion T, Kielland-Brandt M. C, Andersen H. A. 1995; BAP2 , a gene encoding a permease for branched-chain amino acids in Saccharomyces cerevisiae . Biochim Biophys Acta 1269:275–280 [CrossRef]
    [Google Scholar]
  12. Hudson D. A, Sciascia Q. L, Sanders R. J, Norris G. E, Edwards P. J, Sullivan P. A, Farley P. C. 2004; Identification of the dialysable serum inducer of germ-tube formation in Candida albicans . Microbiology 150:3041–3049 [CrossRef]
    [Google Scholar]
  13. Iraqui I, Vissers S, Bernard F, Boles E, Urrestarazu A, Andre B, de Craene J. O. 1999; Amino acid signaling in Saccharomyces cerevisiae : a permease-like sensor of external amino acids and F-Box protein Grr1p are required for transcriptional induction of the AGP1 gene, which encodes a broad-specificity amino acid permease. Mol Cell Biol 19:989–1001
    [Google Scholar]
  14. Jauniaux J. C, Grenson M. 1990; GAP1 , the general amino acid permease gene of Saccharomyces cerevisiae . Nucleotide sequence, protein similarity with the other baker's yeast amino acid permeases, and nitrogen catabolite repression. Eur J Biochem 190:39–44 [CrossRef]
    [Google Scholar]
  15. Kataoka S, Kashiwa M, Saku K, Handa N, Akiyama H. 1995; Candidemia in non-neutropenic patients with an intravenous hyperalimentation catheter: good prognosis of Candida parapsilosis infection. Kansenshogaku Zasshi 69:969–974 [CrossRef]
    [Google Scholar]
  16. Klasson H, Fink G. R, Ljungdahl P. O. 1999; Ssy1p and Ptr3p are plasma membrane components of a yeast system that senses extracellular amino acids. Mol Cell Biol 19:5405–5416
    [Google Scholar]
  17. Krcmery V, Barnes A. J. 2002; Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect 50:243–260 [CrossRef]
    [Google Scholar]
  18. Kumamoto C. A, Vinces M. D. 2005; Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol 7:1546–1554 [CrossRef]
    [Google Scholar]
  19. Laffey S. F, Butler G. 2005; Phenotype switching affects biofilm formation by Candida parapsilosis . Microbiology 151:1073–1081 [CrossRef]
    [Google Scholar]
  20. Lee K. L, Buckley H. R, Campbell C. C. 1975; An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans . Sabouraudia 13:148–153 [CrossRef]
    [Google Scholar]
  21. Lee B. E, Cheung P. Y, Robinson J. L, Evanochko C, Robertson C. M. 1998; Comparative study of mortality and morbidity in premature infants (birth weight, <1,250 g) with candidemia or candidal meningitis. Clin Infect Dis 27:559–565 [CrossRef]
    [Google Scholar]
  22. Leibovitz E, Iuster-Reicher A, Amitai M, Mogilner B. 1992; Systemic candidal infections associated with use of peripheral venous catheters in neonates: a 9-year experience. Clin Infect Dis 14:485–491 [CrossRef]
    [Google Scholar]
  23. Levy I, Rubin L. G, Vasishtha S, Tucci V, Sood S. K. 1998; Emergence of Candida parapsilosis as the predominant species causing candidemia in children. Clin Infect Dis 26:1086–1088 [CrossRef]
    [Google Scholar]
  24. MacDonald L, Baker C, Chenoweth C. 1998; Risk factors for candidemia in a children's hospital. Clin Infect Dis 26:642–645 [CrossRef]
    [Google Scholar]
  25. Maidan M. M, De Rop L, Serneels J, Exler S, Rupp S, Tournu H, Thevelein J. M, Van Dijck P. 2005a; The G protein-coupled receptor Gpr1 and the Galpha protein Gpa2 act through the cAMP-protein kinase A pathway to induce morphogenesis in Candida albicans . Mol Biol Cell 16:1971–1986 [CrossRef]
    [Google Scholar]
  26. Maidan M. M, Thevelein J. M, Van Dijck P. 2005b; Carbon source induced yeast-to-hypha transition in Candida albicans is dependent on the presence of amino acids and on the G-protein-coupled receptor Gpr1. Biochem Soc Trans 33:291–293 [CrossRef]
    [Google Scholar]
  27. Martinez P, Ljungdahl P. O. 2004; An ER packaging chaperone determines the amino acid uptake capacity and virulence of Candida albicans . Mol Microbiol 51:371–384 [CrossRef]
    [Google Scholar]
  28. Nosek J, Adamikova L, Zemanova J, Tomaska L, Zufferey R, Mamoun C. B. 2002; Genetic manipulation of the pathogenic yeast Candida parapsilosis . Curr Genet 42:27–35 [CrossRef]
    [Google Scholar]
  29. Resende J. C, Saliba J. L, de Resende M. A. 2002; Prevalence of Candida spp. in hospitalized patients and their risk factors. Mycoses 45:306–312 [CrossRef]
    [Google Scholar]
  30. Reynolds R, Braude A. I. 1956; The filament inducing property of blood for Candida albicans : its nature and significance. Clin Res Proc 4:40
    [Google Scholar]
  31. Sherertz R. J, Gledhill K. S, Hampton K. D, Pfaller M. A, Givner L. B, Abramson J. S, Dillard R. G. 1992; Outbreak of Candida bloodstream infections associated with retrograde medication administration in a neonatal intensive care unit. J Pediatr 120:455–461 [CrossRef]
    [Google Scholar]
  32. Shian W. J, Chi C. S, Wang T. M, Chen C. H. 1993; Candidemia in the neonatal intensive care unit. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi 34:349–355
    [Google Scholar]
  33. 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 other sources. J Clin Microbiol 40:1244–1248 [CrossRef]
    [Google Scholar]
  34. Soetens O, De Craene J. O, Andre B. 2001; Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J Biol Chem 276:43949–43957 [CrossRef]
    [Google Scholar]
  35. Stanbrough M, Magasanik B. 1995; Transcriptional and posttranslational regulation of the general amino acid permease of Saccharomyces cerevisiae . J Bacteriol 177:94–102
    [Google Scholar]
  36. Tavanti A, Davidson A. D, Gow N. A, Maiden M. C, Odds F. C. 2005; Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis groups II and III. J Clin Microbiol 43:284–292 [CrossRef]
    [Google Scholar]
  37. ter Schure E. G, Sillje H. H, Verkleij A. J, Boonstra J, Verrips C. T. 1995; The concentration of ammonia regulates nitrogen metabolism in Saccharomyces cerevisiae . J Bacteriol 177:6672–6675
    [Google Scholar]
  38. Xue C, Bahn Y. S, Cox G. M, Heitman J. 2006; G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans . Mol Biol Cell 17:667–679
    [Google Scholar]
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