Factors supporting cysteine tolerance and sulfite production in Candida albicans

Eukaryotic Cell

Volumn 12, Issue 4, 2013, Pages 604-613

  Hennicke, Florian ^a   Grumbt, Maria ^a   Lermann, Ulrich ^a   Ueberschaar, Nico ^a   Palige, Katja ^a   Böttcher, Bettina ^a   Jacobsen, Ilse D ^a   Staib, Claudia ^b   Morschhäuser, Joachim ^b   Monod, Michel ^c   Hube, Bernhard ^a,d,e   Hertweck, Christian ^a,d   Staib, Peter ^a  

^a HANS KNÖLL INSTITUTE   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^e JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANION TRANSPORT PROTEIN; CYSTEINE; CYSTEINE DIOXYGENASE; FUNGAL PROTEIN; SULFITE; TRANSCRIPTION FACTOR; ZINC;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; CANDIDA ALBICANS; CANDIDIASIS; DRUG EFFECT; FUNGUS HYPHAE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MORTALITY; MOUSE; MUTATION; SURVIVAL;

ANIMALS; ANION TRANSPORT PROTEINS; CANDIDA ALBICANS; CANDIDIASIS; CYSTEINE; CYSTEINE DIOXYGENASE; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; MICE; MICE, INBRED BALB C; MUTATION; SULFITES; SURVIVAL ANALYSIS; TRANSCRIPTION FACTORS; ZINC;

CANDIDA ALBICANS; FUNGI;

EID: 84875542335     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00336-12     Document Type: Article

References (48)

1. Taylor SL, Higley NA, Bush RK. 1986. Sulfites in foods: uses, analytical methods, residues, fate, exposure assessment, metabolism, toxicity, and hypersensitivity. Adv. Food Res. 30:1-76.
2. Avram D, Bakalinsky AT. 1997. SSU1 encodes a plasma membrane protein with a central rolein a networkof proteins conferring sulfite tolerance in Saccharomyces cerevisiae. J. Bacteriol. 179:5971-5974.
3. Xu X, Wightman JD, Geller BL, Avram D, Bakalinsky AT. 1994. Isolation and characterization of sulfite mutants of Saccharomyces cerevi-siae. Curr. Genet. 25:488-496.
4. Avram D, Leid M, Bakalinsky AT. 1999. Fzf1p of Saccharomyces cerevi-siae is a positive regulator of SSU1 transcription and its first zinc finger region is required for DNA binding. Yeast 15:473-480.
5. Donalies UE, Stahl U. 2002. Increasing sulphite formation in Saccharo-myces cerevisiae by overexpression of MET14 and SSU1. Yeast 19:475- 484.
6. Park H, Bakalinsky AT. 2000. SSU1 mediates sulphite efflux in Saccha-romyces cerevisiae. Yeast 16:881- 888.
7. Hromatka BS, Noble SM, Johnson AD. 2005. Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol. Biol. Cell 16:4814-4826.
8. Sarver A, DeRisi J. 2005. Fzf1p regulates an inducible response to nitro-sative stress in Saccharomyces cerevisiae. Mol. Biol. Cell 16:4781- 4791.
9. Chiranand W, McLeod I, Zhou H, Lynn JJ, Vega LA, Myers H, Yates JR, III, Lorenz MC, Gustin MC. 2008. CTA4 transcription factor mediates induction of nitrosative stress response in Candida albicans. Eukaryot. Cell 7:268-278.
10. Kunert J. 1972. Keratin decomposition by dermatophytes: evidence of the sulphitolysis of the protein. Experientia 28:1025-1026.
11. Kunert J. 1973. The role of sulfite excretion in keratin catabolism by dermatophytes. Dermatol. Monatsschr. 159:456-457. (In German.)
12. Kunert J. 1992. Effect of reducing agents on proteolytic and keratinolytic activity of enzymes of Microsporum gypseum. Mycoses 35:343-348.
13. Léchenne B, Reichard U, Zaugg C, Fratti M, Kunert J, Boulat O, Monod M. 2007. Sulphite efflux pumps in Aspergillus fumigatus and dermato-phytes. Microbiology 153:905-913.
14. Kasperova A, Kunert J, Horynova M, Weigl E, Sebela M, Lenobel R, Raska M. 2011. Isolation of recombinant cysteine dioxygenase protein from Trichophyton mentagrophytes. Mycoses 54:e456-462.
15. Stipanuk MH, Dominy JE, Jr, Lee JI, Coloso RM. 2006. Mammalian cysteine metabolism: new insights into regulation of cysteine metabolism. J. Nutr. 136:1652S-1659S.
16. Allen EH, Hussey GG. 1971. Inhibition of the growth of Helminthospo-rium carbonum by L-cysteine. Can. J. Microbiol. 17:101-103.
17. Carlsson J, Granberg GP, Nyberg GK, Edlund MB. 1979. Bactericidal effect of cysteine exposed to atmospheric oxygen. Appl. Environ. Micro-biol. 37:383-390.
18. De Lucca AJ, Walsh TJ, Daigle DJ. 1996. N-Acetylcysteine inhibits germination of conidia and growth of Aspergillus spp. and Fusarium spp. Antimicrob. Agents Chemother. 40:1274-1276.
19. Galgoczy L, Kovacs L, Krizsan K, Papp T, Vagvolgyi C. 2009. Inhibitory effects of cysteine and cysteine derivatives on germination of sporangio-spores and hyphal growth of different zygomycetes. Mycopathologia 168: 125-134.
20. Gomez RF, Montville T, Blais K. 1980. Toxic effect of cysteine against Salmonella typhimurium. Appl. Environ. Microbiol. 39:1081-1083.
21. Harris CL. 1981. Cysteine and growth inhibition of Escherichia coli: thre-onine deaminase as the target enzyme. J. Bacteriol. 145:1031-1035.
22. Kari C, Nagy Z, Kovacs P, Hernadi F. 1971. Mechanism of the growth inhibitory effect of cysteine on Escherichia coli. J. Gen. Microbiol. 68:349-356.
23. Wain WH, Price MF, Cawson RA. 1975. A re-evaluation of the effect of cysteine on Candida albicans. Sabouraudia 13(Pt 1):74-82.
24. Königsbauer H. 1951. Ü ber die Wirkung schwefelhaltiger Aminosäuren auf das Wachstum verschiedener Fadenpilze "in vitro." Mycopathologia 5:173-177.
25. Grumbt M, Monod M, Yamada T, Hertweck C, Kunert J, Staib P. 25 January 2013. Keratin degradation by dermatophytes relies on cysteine dioxygenase anda sulfite efflux pump. J. Invest. Dermatol. [Epub ahead of print.] doi:10.1038/jid.2013.41.
26. Winsten S, Murray TJ. 1956. Virulence enhancement of a filamentous strain of Candida albicans after growth on media containing cysteine. J. Bacteriol. 71:738.
27. Circu ML, Aw TY. 2011. Redox biology of the intestine. Free Radic. Res. 45:1245-1266.
28. Homann OR, Dea J, Noble SM, Johnson AD. 2009. A phenotypic profile of the Candida albicans regulatory network. PLoS Genet. 5:e1000783. doi: 10.1371/journal.pgen.1000783.
29. McCluskey K, Wiest A, Plamann M. 2010. The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J. Biosci. 35:119-126.
30. Ramirez-Zavala B, Reuss O, Park YN, Ohlsen K, Morschhäuser J. 2008. Environmental induction of white-opaque switching in Candida albicans. PLoS Pathog. 4:e1000089. doi:10.1371/journal.ppat.1000089.
31. Staib P, Lermann U, Blass-Warmuth J, Degel B, Würzner R, Monod M, Schirmeister T, Morschhäuser J. 2008. Tetracycline-inducible expression of individual secreted aspartic proteases in Candida albicans allows isoen-zyme-specific inhibitor screening. Antimicrob. Agents Chemother. 52: 146-156.
32. Reuss O, Morschhäuser J. 2006. A family of oligopeptide transporters is required for growth of Candida albicans on proteins. Mol. Microbiol. 60:795-812.
33. Köhler GA, White TC, Agabian N. 1997. Overexpression of a cloned IMP dehydrogenase gene of Candida albicans confers resistance to the specific inhibitor mycophenolic acid. J. Bacteriol. 179:2331-2338.
34. Reuss O, Vik A, Kolter R, Morschhäuser J. 2004. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341:119- 127.
35. Millon L, Manteaux A, Reboux G, Drobacheff C, Monod M, Barale T, Michel-Briand Y. 1994. Fluconazole-resistant recurrent oral candidiasis in human immunodeficiency virus-positive patients: persistence of Candida albicans strains with the same genotype. J. Clin. Microbiol. 32:1115- 1118.
36. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 1989. Current protocols in molecular biology. John Wiley & Sons, Inc, New York, NY.
37. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
38. Dabas N, Morschhäuser J. 2007. Control of ammonium permease expression andfilamentous growth bythe GATA transcription factors GLN3 and GAT1 in Candida albicans. Eukaryot. Cell 6:875-888.
39. Skrzypek MS, Arnaud MB, Costanzo MC, Inglis DO, Shah P, Binkley G, Miyasato SR, Sherlock G. 2010. New tools at the Candida Genome Database: biochemical pathways and full-text literature search. Nucleic Acids Res. 38:D428-432.
40. Li X, Bazer FW, Gao H, Jobgen W, Johnson GA, Li P, McKnight JR, Satterfield MC, Spencer TE, Wu G. 2009. Amino acids and gaseous signaling. Amino Acids 37:65-78.
41. Schroeder BO, Wu Z, Nuding S, Groscurth S, Marcinowski M, Beisner J, Buchner J, Schaller M, Stange EF, Wehkamp J. 2011. Reduction of disulphide bonds unmasks potent antimicrobial activity of human beta-defensin 1. Nature 469:419-423.
42. Stipanuk MH. 2004. Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu. Rev. Nutr. 24:539-577.
43. Dahm LJ, Jones DP. 1994. Secretion of cysteine and glutathione from mucosa to lumen in rat small intestine. Am. J. Physiol. 267:G292- G300.
44. Siegers CP, Riemann D, Thies E, Younes M. 1988. Glutathione and GSH-dependent enzymesin the gastrointestinal mucosaof the rat. Cancer Lett. 40:71-76.
45. Dominy JE, Jr, Simmons CR, Karplus PA, Gehring AM, Stipanuk MH. 2006. Identification and characterization of bacterial cysteine dioxyge-nases: a new route of cysteine degradation for eubacteria. J. Bacteriol. 188:5561-5569.
46. Kumar A, John L, Alam MM, Gupta A, Sharma G, Pillai B, Sengupta S. 2006. Homocysteine- and cysteine-mediated growth defect is not associated with induction of oxidative stress response genes in yeast. Biochem. J. 396:61-69.
47. Cowman RA, Baron SS, Fitzgerald RJ. 1983. Cysteine toxicity for oral streptococci and effect of branched-chain amino acids. Infect. Immun. 39:1107-1113.
48. Park S, Imlay JA. 2003. High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J. Bacteriol. 185: 1942-1950.