P. brasiliensis Virulence Is Affected by SconC, the Negative Regulator of Inorganic Sulfur Assimilation

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Menino, João Filipe ^a,b   Saraiva, Margarida ^a,b   Gomes Rezende, Jéssica ^a,b   Sturme, Mark ^a,b   Pedrosa, Jorge ^a,b   Castro, António Gil ^a,b   Ludovico, Paula ^a,b   Goldman, Gustavo H ^c,d   Rodrigues, Fernando ^a,b  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF MINHO   (Portugal)

^c BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; INORGANIC SULFUR; PROTEIN SCONC; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REGULATOR PROTEIN; SULFUR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL METABOLISM; CONTROLLED STUDY; DOWN REGULATION; FUNGAL VIRULENCE; FUNGUS CULTURE; FUNGUS GROWTH; IN VIVO STUDY; MALE; MICROSCOPY; MOUSE; MYCELIUM; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PARACOCCIDIOIDES BRASILIENSIS; REAL TIME POLYMERASE CHAIN REACTION; SOUTH AMERICAN BLASTOMYCOSIS; SULFUR ASSIMILATION; UPREGULATION; WILD TYPE;

FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; PARACOCCIDIOIDES; PARACOCCIDIOIDOMYCOSIS; SULFUR; VIRULENCE;

EID: 84884191896     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074725     Document Type: Article

References (48)

1. Brummer E, Castaneda E, Restrepo A, (1993) Paracoccidioidomycosis: an update. Clin Microbiol Rev 6: 89-117. PubMed: 8472249.
2. Restrepo A, McEwen JG, Castañeda E, (2001) The habitat of Paracoccidioides brasiliensis: how far from solving the riddle? Med Mycol 39: 233-241. doi:10.1080/mmy.39.3.233.241. PubMed: 11446526.
3. Senaratne RH, De Silva AD, Williams SJ, Mougous JD, Reader JR, et al. (2006) 5'-Adenosinephosphosulphate reductase (CysH) protects Mycobacterium tuberculosis against free radicals during chronic infection phase in mice. Mol Microbiol 59: 1744-1753. doi:10.1111/j.1365-2958.2006.05075.x. PubMed: 16553880.
4. Bhave DP, Muse WB 3rd, Carroll KS, (2007) Drug targets in mycobacterial sulfur metabolism. Infect Disord Drug Targets 7: 140-158. doi:10.2174/187152607781001772. PubMed: 17970225.
5. Fu YH, Paietta JV, Mannix DG, Marzluf GA, (1989) cys-3, the positive-acting sulfur regulatory gene of Neurospora crassa, encodes a protein with a putative leucine zipper DNA-binding element. Mol Cell Biol 9: 1120-1127. PubMed: 2524646.
6. Maresca B, Lambowitz AM, Kumar VB, Grant GA, Kobayashi GS, et al. (1981) Role of cysteine in regulating morphogenesis and mitochondrial activity in the dimorphic fungus Histoplasma capsulatum. Proc Natl Acad Sci U S A 78: 4596-4600. doi:10.1073/pnas.78.7.4596. PubMed: 6945601.
7. Dickinson DA, Forman HJ, (2002) Cellular glutathione and thiols metabolism. Biochem Pharmacol 64: 1019-1026. doi:10.1016/S0006-2952(02)01172-3. PubMed: 12213601.
8. Ziegler DM, (1985) Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu Rev Biochem 54: 305-329. doi:10.1146/annurev.biochem.54.1.305. PubMed: 2862840.
9. Brosnan JT, Brosnan ME, (2006) The sulfur-containing amino acids: an overview. J Nutr 136: 1636S-1640S. PubMed: 16702333.
10. Medoff G, Painter A, Kobayashi GS, (1987) Mycelial- to yeast-phase transitions of the dimorphic fungi Blastomyces dermatitidis and Paracoccidioides brasiliensis. J Bacteriol 169: 4055-4060. PubMed: 3624202.
11. Boguslawski G, Stetler DA, (1979) Aspects of physiology of Histoplasma capsulatum. (A review). Mycopathologia 67: 17-24. doi:10.1007/BF00436235. PubMed: 377084.
12. Paris S, Duran-Gonzalez S, Mariat F, (1985) Nutritional studies on Paracoccidioides brasiliensis: the role of organic sulfur in dimorphism. Sabouraudia 23: 85-92. doi:10.1080/00362178585380151. PubMed: 4012515.
13. Ferreira ME, Marques Edos R, Malavazi I, Torres I, Restrepo A, et al. (2006) Transcriptome analysis and molecular studies on sulfur metabolism in the human pathogenic fungus Paracoccidioides brasiliensis. Mol Genet Genomics 276: 450-463. doi:10.1007/s00438-006-0154-4. PubMed: 16924544.
14. Marques ER, Ferreira ME, Drummond RD, Felix JM, Menossi M, et al. (2004) Identification of genes preferentially expressed in the pathogenic yeast phase of Paracoccidioides brasiliensis, using suppression subtraction hybridization and differential macroarray analysis. Mol Genet Genomics 271: 667-677. PubMed: 15138890.
15. Tavares AH, Silva SS, Dantas A, Campos EG, Andrade RV, et al. (2007) Early transcriptional response of Paracoccidioides brasiliensis upon internalization by murine macrophages. Microbes Infect 9: 583-590. doi:10.1016/j.micinf.2007.01.024. PubMed: 17387029.
16. Andrade RV, Paes HC, Nicola AM, de Carvalho MJ, Fachin AL, et al. (2006) Cell organisation, sulphur metabolism and ion transport-related genes are differentially expressed in Paracoccidioides brasiliensis mycelium and yeast cells. BMC Genomics 7: 208. doi:10.1186/1471-2164-7-208. PubMed: 16907987.
17. Felipe MS, Andrade RV, Arraes FB, Nicola AM, Maranhão AQ, et al. (2005) Transcriptional profiles of the human pathogenic fungus Paracoccidioides brasiliensis in mycelium and yeast cells. J Biol Chem 280: 24706-24714. doi:10.1074/jbc.M500625200. PubMed: 15849188.
18. Marzluf GA, (1997) Molecular genetics of sulfur assimilation in filamentous fungi and yeast. Annu Rev Microbiol 51: 73-96. doi:10.1146/annurev.micro.51.1.73. PubMed: 9343344.
19. Nunes LR, Costa de Oliveira R, Leite DB, da Silva VS, dos Reis Marques E, et al. (2005) Transcriptome analysis of Paracoccidioides brasiliensis cells undergoing mycelium-to-yeast transition. Eukaryot Cell 4: 2115-2128. doi:10.1128/EC.4.12.2115-2128.2005. PubMed: 16339729.
20. Costa M, Borges CL, Bailão AM, Meirelles GV, Mendonça YA, et al. (2007) Transcriptome profiling of Paracoccidioides brasiliensis yeast-phase cells recovered from infected mice brings new insights into fungal response upon host interaction. Microbiology 153: 4194-4207. doi:10.1099/mic.0.2007/009332-0. PubMed: 18048933.
21. Restrepo A, Jiménez BE, (1980) Growth of Paracoccidioides brasiliensis yeast phase in a chemically defined culture medium. J Clin Microbiol 12: 279-281. PubMed: 7229010.
22. Beijersbergen A, Dulk-Ras AD, Schilperoort RA, Hooykaas PJ, (1992) Conjugative Transfer by the Virulence System of Agrobacterium tumefaciens. Science 256: 1324-1327. doi:10.1126/science.256.5061.1324. PubMed: 17736763.
23. Almeida AJ, Carmona JA, Cunha C, Carvalho A, Rappleye CA, et al. (2007) Towards a molecular genetic system for the pathogenic fungus Paracoccidioides brasiliensis. Fungal Genet Biol 44: 1387-1398. doi:10.1016/j.fgb.2007.04.004. PubMed: 17512227.
24. Rappleye CA, Engle JT, Goldman WE, (2004) RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol 53: 153-165. doi:10.1111/j.1365-2958.2004.04131.x. PubMed: 15225311.
25. de Groot MJ, Bundock P, Hooykaas PJ, Beijersbergen AG, (1998) Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nat Biotechnol 16: 839-842. doi:10.1038/nbt0998-839. PubMed: 9743116.
26. Almeida AJ, Cunha C, Carmona JA, Sampaio-Marques B, Carvalho A, et al. (2009) Cdc42p controls yeast-cell shape and virulence of Paracoccidioides brasiliensis. Fungal Genet Biol 46: 919-926. doi:10.1016/j.fgb.2009.08.004. PubMed: 19686860.
27. Ashe MP, De Long SK, Sachs AB, (2000) Glucose depletion rapidly inhibits translation initiation in yeast. Mol Biol Cell 11: 833-848. doi:10.1091/mbc.11.3.833. PubMed: 10712503.
28. Uthman A, Dockal M, Söltz-Szöts J, Tschachler E, (2005) Fluconazole upregulates sconC expression and inhibits sulphur metabolism in Microsporum canis. Fungal Genet Biol 42: 719-725. doi:10.1016/j.fgb.2005.04.005. PubMed: 15922636.
29. Burton EG, Metzenberg RL, (1972) Novel mutation causing derepression of several enzymes of sulfur metabolism in Neurospora crassa. J Bacteriol 109: 140-151. PubMed: 4257980.
30. Piotrowska M, Natorff R, Paszewski A, (2000) sconC, a gene involved in the regulation of sulphur metabolism in Aspergillus nidulans, belongs to the SKP1 gene family. Mol Gen Genet 264: 276-282. doi:10.1007/s004380000319. PubMed: 11085267.
31. Mesquita A, Weinberger M, Silva A, Sampaio-Marques B, Almeida B, et al. (2010) Caloric restriction or catalase inactivation extends yeast chronological lifespan by inducing H2O2 and superoxide dismutase activity. Proc Natl Acad Sci U S A 107: 15123-15128. doi:10.1073/pnas.1004432107. PubMed: 20696905.
32. Menino JF, Osório NS, Sturme MH, Barros D, Gomes-Alves AG, et al. (2012) Morphological heterogeneity of Paracoccidioides brasiliensis: relevance of the Rho-like GTPase PbCDC42. Med Mycol 50: 768-774. doi:10.3109/13693786.2012.665614. PubMed: 22493946.
33. Stambuk BU, Puccia R, de Almeida ML, Travassos LR, Schenkman S, (1988) Secretion of the 43 kDa glycoprotein antigen by Paracoccidioides brasiliensis. J Med Vet Mycol 26: 367-373. doi:10.1080/02681218880000521. PubMed: 3246625.
34. de Almeida SR, de Moraes JZ, de Camargo ZP, Gesztesi JL, Mariano M, et al. (1998) Pattern of immune response to GP43 from Paracoccidioides brasiliensis in susceptible and resistant mice is influenced by antigen-presenting cells. Cell Immunol 190: 68-76. doi:10.1006/cimm.1998.1388. PubMed: 9826448.
35. Almeida SR, Unterkircher CS, Camargo ZP, (1998) Involvement of the major glycoprotein (gp43) of Paracoccidioides brasiliensis in attachment to macrophages. Med Mycol 36: 405-411. doi:10.1080/02681219880000641. PubMed: 10206751.
36. Hernández O, Almeida AJ, Tamayo D, Torres I, Garcia AM, et al. (2012) The hydrolase PbHAD32 participates in the adherence of Paracoccidioides brasiliensis conidia to epithelial lung cells. Med Mycol 50: 533-537. doi:10.3109/13693786.2011.619583. PubMed: 21988701.
37. Hernandez O, Garcia AM, Almeida AJ, Tamayo D, Gonzalez A, et al. (2011) Gene expression during activation of Paracoccidioides brasiliensis conidia. Yeast 28: 771-781. doi:10.1002/yea.1902. PubMed: 21960298.
38. San-Blas G, Restrepo A, Clemons K, Stevens DA, San-Blas F, et al. (1992) Paracoccidioidomycosis. J Med Vet Mycol 30 (Suppl 1):: 59-71. doi:10.1080/02681219280000771. PubMed: 1474460.
39. Terçarioli GR, Bagagli E, Reis GM, Theodoro RC, Bosco Sde M, et al. (2007) Ecological study of Paracoccidioides brasiliensis in soil: growth ability, conidia production and molecular detection. BMC Microbiol 7: 92. doi:10.1186/1471-2180-7-92. PubMed: 17953742.
40. Natorff R, Balińska M, Paszewski A, (1993) At least four regulatory genes control sulphur metabolite repression in Aspergillus nidulans. Mol Gen Genet 238: 185-192. PubMed: 8479426.
41. Thomas D, Kuras L, Barbey R, Cherest H, Blaiseau PL, et al. (1995) Met30p, a yeast transcriptional inhibitor that responds to S-adenosylmethionine, is an essential protein with WD40 repeats. Mol Cell Biol 15: 6526-6534. PubMed: 8524217.
42. Kanetsuna F, Carbonell LM, (1966) Enzymes in glycolysis and the citric acid cycle in the yeast and mycelial forms of Paracoccidioides brasiliensis. J Bacteriol 92: 1315-1320. PubMed: 5924267.
43. Nuttall SL, Martin U, Sinclair AJ, Kendall MJ, (1998) Glutathione: in sickness and in health. Lancet 351: 645-646. doi:10.1016/S0140-6736(05)78428-2. PubMed: 9500325.
44. Sato I, Shimatani K, Fujita K, Abe T, Shimizu M, et al. (2011) Glutathione reductase/glutathione is responsible for cytotoxic elemental sulfur tolerance via polysulfide shuttle in fungi. J Biol Chem 286: 20283-20291. doi:10.1074/jbc.M111.225979. PubMed: 21474441.
45. Townsend DM, Tew KD, Tapiero H, (2004) Sulfur containing amino acids and human disease. Biomed Pharmacother 58: 47-55. doi:10.1016/j.biopha.2003.11.005. PubMed: 14739061.
46. Mapelli V, Hillestrøm PR, Patil K, Larsen EH, Olsson L, (2012) The interplay between sulphur and selenium metabolism influences the intracellular redox balance in Saccharomyces cerevisiae. FEMS Yeast Res 12: 20-32. doi:10.1111/j.1567-1364.2011.00757.x. PubMed: 22093810.
47. Teixeira MM, Theodoro RC, de Carvalho MJ, Fernandes L, Paes HC, et al. (2009) Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus. Mol Phylogenet Evol 52: 273-283. doi:10.1016/j.ympev.2009.04.005. PubMed: 19376249.
48. Gómez BL, Nosanchuk JD, Díez S, Youngchim S, Aisen P, et al. (2001) Detection of melanin-like pigments in the dimorphic fungal pathogen Paracoccidioides brasiliensis in vitro and during infection. Infect Immun 69: 5760-5767. doi:10.1128/IAI.69.9.5760-5767.2001. PubMed: 11500453.