Transcriptomics in human blood incubation reveals the importance of oxidative stress response in Saccharomyces cerevisiae clinical strains

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Llopis, Silvia ^a   Querol, Amparo ^a   Heyken, Antje ^b   Hube, Bernhard ^b,c   Jespersen, Lene ^d   Fernández Espinar, M T ^a   Pérez Torrado, Roberto ^a  

^a INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^b HANS KNÖLL INSTITUTE   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Blood; Clinical strains; Oxidative stress; Saccharomyces cerevisiae; Transcriptomics

Indexed keywords

MESSENGER RNA; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR YAP1;

AMINO ACID SYNTHESIS; ARTICLE; BLOOD ANALYSIS; CANDIDA ALBICANS; CONTROLLED STUDY; FUNGAL CELL; FUNGAL GENE; FUNGAL GENETICS; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS ISOLATION; HUMAN; IN VITRO STUDY; INCUBATION TIME; MOUSE; NONHUMAN; OXIDATIVE STRESS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTOMICS; YAP1 GENE;

AMINO ACIDS; BLOOD; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTOME; VIRULENCE;

CANDIDA ALBICANS; MUS; SACCHAROMYCES CEREVISIAE;

EID: 84865209848     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-419     Document Type: Article

References (47)

1. Enache-Angoulvant A, Hennequin C. Invasive Saccharomyces infection: a comprehensive review. Clin Infect Dis 2005, 41:1559-1568. 10.1086/497832, 16267727.
2. Muñoz P, Bouza E, Cuenca-Estrella M, Eiros JM, Perez MJ, Sanchez-Somolinos M, Rincon C, Hortal J, Pelaez T. Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin Infect Dis 2005, 40:1625-1634. 10.1086/429916, 15889360.
3. de Llanos R, Llopis S, Molero G, Querol A, Gil C, Fernandez-Espinar MT. In vivo virulence of commercial Saccharomyces cerevisiae strains with pathogenicity-associated phenotypical traits. Int J Food Microbiol 2011, 144:393-399. 10.1016/j.ijfoodmicro.2010.10.025, 21081253.
4. Jensen DP, Smith DL. Fever of unknown origin secondary to brewer's yeast ingestion. Arch Intern Med 1976, 136:332-333. 10.1001/archinte.1976.03630030064011, 769716.
5. Smith D, Metzgar D, Wills C, Fierer J. Fatal Saccharomyces cerevisiae aortic graft infection. J Clin Microbiol 2002, 40:2691-2692. 10.1128/JCM.40.7.2691-2692.2002, 120603, 12089311.
6. Herbrecht R, Nivoix Y. Saccharomyces cerevisiae fungemia: an adverse effect of Saccharomyces boulardii probiotic administration. Clin Infect Dis 2005, 40:1635-1637. 10.1086/429926, 15889361.
7. de Llanos R, Fernandez-Espinar MT, Querol A. A comparison of clinical and food Saccharomyces cerevisiae isolates on the basis of potential virulence factors. Antonie Van Leeuwenhoek 2006, 90:221-231. 10.1007/s10482-006-9077-7, 16871421.
8. Swinne D, Nolard N, Van RP, Detandt M. Bloodstream yeast infections: a 15-month survey. Epidemiol Infect 2009, 137:1037-1040. 10.1017/S0950268808001763, 19134233.
9. Lherm T, Monet C, Nougiere B, Soulier M, Larbi D, Le GC, Caen D, Malbrunot C. Seven cases of fungemia with Saccharomyces boulardii in critically ill patients. Intensive Care Med 2002, 28:797-801. 10.1007/s00134-002-1267-9, 12107689.
10. Cassone M, Serra P, Mondello F, Girolamo A, Scafetti S, Pistella E, Venditti M. Outbreak of Saccharomyces cerevisiae subtype boulardii fungemia in patients neighboring those treated with a probiotic preparation of the organism. J Clin Microbiol 2003, 41:5340-5343. 10.1128/JCM.41.11.5340-5343.2003, 262466, 14605200.
11. Graf C, Gavazzi G. Saccharomyces cerevisiae fungemia in an immunocompromised patient not treated with Saccharomyces boulardii preparation. J Infect 2007, 54:310-311. 10.1016/j.jinf.2006.01.019, 16545460.
12. Calderone RA. Candida and candidiasis 2002, New York: American Society for Microbiology, 2.
13. Zelante T, Montagnoli C, Bozza S, Gaziano R, Bellocchio S, Bonifazi P, Moretti S, Fallarino F, Puccetti P, Romani L. Receptors and pathways in innate antifungal immunity: the implication for tolerance and immunity to fungi. Adv Exp Med Biol 2007, 590:209-221. 10.1007/978-0-387-34814-8_15, 17191388.
14. McCusker JH, Clemons KV, Stevens DA, Davis RW. Genetic characterization of pathogenic Saccharomyces cerevisiae isolates. Genetics 1994, 136:1261-1269. 1205906, 8013903.
15. McCusker JH, Clemons KV, Stevens DA, Davis RW. Saccharomyces cerevisiae virulence phenotype as determined with CD-1 mice is associated with the ability to grow at 42 degrees C and form pseudohyphae. Infect Immun 1994, 62:5447-5455. 303287, 7960125.
16. Clemons KV, Hanson LC, Stevens DA. Colony phenotype switching in clinical and non-clinical isolates of Saccharomyces cerevisiae. J Med Vet Mycol 1996, 34:259-264. 10.1080/02681219680000441, 8873885.
17. Klingberg TD, Lesnik U, Arneborg N, Raspor P, Jespersen L. Comparison of Saccharomyces cerevisiae strains of clinical and nonclinical origin by molecular typing and determination of putative virulence traits. FEMS Yeast Res 2008, 8:631-640. 10.1111/j.1567-1364.2008.00365.x, 2430332, 18355272.
18. Yañez A, Murciano C, Llopis S, Fernández-Espinar T, Gil ML, Gozalbo D. In vivo and in vitro studies on virulence and host responses to Saccharomyces cerevisiae clinical and non-clinical isolates. The Open Mycology Journal 2009, 3:37-47.
19. Fradin C, Kretschmar M, Nichterlein T, Gaillardin C. d'Enfert C, Hube B: Stage-specific gene expression of Candida albicans in human blood. Mol Microbiol 2003, 47:1523-1543. 10.1046/j.1365-2958.2003.03396.x, 12622810.
20. Fradin C, De GP, MacCallum D, Schaller M, Klis F, Odds FC, Hube B. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 2005, 56:397-415. 10.1111/j.1365-2958.2005.04557.x, 15813733.
21. Becker J, Craig EA. Heat-shock proteins as molecular chaperones. Eur J Biochem 1994, 219:11-23. 10.1111/j.1432-1033.1994.tb19910.x, 8306977.
22. Memisoglu A, Samson L. Base excision repair in yeast and mammals. Mutat Res 2000, 451:39-51. 10.1016/S0027-5107(00)00039-7, 10915864.
23. Abshire KZ, Neidhardt FC. Analysis of proteins synthesized by Salmonella typhimurium during growth within a host macrophage. J Bacteriol 1993, 175:3734-3743. 204789, 8509328.
24. Rea RB, Gahan CG, Hill C. Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect Immun 2004, 72:717-727. 10.1128/IAI.72.2.717-727.2004, 321596, 14742513.
25. Riboulet E, Verneuil N, La CS, Sauvageot N, Auffray Y, Hartke A, Giard JC. Relationships between oxidative stress response and virulence in Enterococcus faecalis. J Mol Microbiol Biotechnol 2007, 13:140-146. 10.1159/000103605, 17693721.
26. Rubin-Bejerano I, Fraser I, Grisafi P, Fink GR. Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc Natl Acad Sci USA 2003, 100:11007-11012. 10.1073/pnas.1834481100, 196917, 12958213.
27. Lorenz MC, Fink GR. The glyoxylate cycle is required for fungal virulence. Nature 2001, 412:83-86. 10.1038/35083594, 11452311.
28. Kingsbury JM, Goldstein AL, McCusker JH. Role of nitrogen and carbon transport, regulation, and metabolism genes for Saccharomyces cerevisiae survival in vivo. Eukaryot Cell 2006, 5:816-824. 10.1128/EC.5.5.816-824.2006, 1459679, 16682459.
29. Padilla PA, Fuge EK, Crawford ME, Errett A, Werner-Washburne M. The highly conserved, coregulated SNO and SNZ gene families in Saccharomyces cerevisiae respond to nutrient limitation. J Bacteriol 1998, 180:5718-5726. 107633, 9791124.
30. McKinney JD. Honer zu BK, Munoz-Elias EJ, Miczak A, Chen B, Chan WT, Swenson D, Sacchettini JC, Jacobs WR Jr, Russell DG: Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 2000, 406:735-738. 10.1038/35021074, 10963599.
31. Rude TH, Toffaletti DL, Cox GM, Perfect JR. Relationship of the glyoxylate pathway to the pathogenesis of Cryptococcus neoformans. Infect Immun 2002, 70:5684-5694. 10.1128/IAI.70.10.5684-5694.2002, 128360, 12228298.
32. Idnurm A, Howlett BJ. Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola (Brassica napus). Eukaryot Cell 2002, 1:719-724. 10.1128/EC.1.5.719-724.2002, 126752, 12455691.
33. Goldstein AL, McCusker JH. Development of Saccharomyces cerevisiae as a model pathogen A system for the genetic identification of gene products required for survival in the mammalian host environment. Genetics 2001, 159:499-513. 1461844, 11606528.
34. Lorenz MC, Bender JA, Fink GR. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 2004, 3:1076-1087. 10.1128/EC.3.5.1076-1087.2004, 522606, 15470236.
35. Diezmann S, Dietrich FS. Saccharomyces cerevisiae: population divergence and resistance to oxidative stress in clinical, domesticated and wild isolates. PLoS One 2009, 4:e5317. 10.1371/journal.pone.0005317, 2669729, 19390633.
36. Bogdan C, Rollinghoff M, Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 2000, 12:64-76. 10.1016/S0952-7915(99)00052-7, 10679404.
37. Brown AJ, Haynes K, Quinn J. Nitrosative and oxidative stress responses in fungal pathogenicity. Curr Opin Microbiol 2009, 12:384-391. 10.1016/j.mib.2009.06.007, 2728829, 19616469.
38. Rodrigues-Pousada C, Menezes RA, Pimentel C. The Yap family and its role in stress response. Yeast 2010, 27:245-258. 10.1002/yea.1752, 20148391.
39. Lushchak OV, Inoue Y, Lushchak VI. Regulatory protein Yap1 is involved in response of yeast Saccharomyces cerevisiae to nitrosative stress. Biochemistry (Mosc) 2010, 75:629-664.
40. Zakikhany K, Naglik JR, Schmidt-Westhausen A, Holland G, Schaller M, Hube B. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell Microbiol 2007, 9:2938-2954. 10.1111/j.1462-5822.2007.01009.x, 17645752.
41. Missall TA, Lodge JK. Function of the thioredoxin proteins in Cryptococcus neoformans during stress or virulence and regulation by putative transcriptional modulators. Mol Microbiol 2005, 57:847-858. 10.1111/j.1365-2958.2005.04735.x, 16045626.
42. Wright WL, Wenzel RP. Nosocomial Candida Epidemiology, transmission, and prevention. Infect Dis Clin North Am 1997, 11:411-425. 10.1016/S0891-5520(05)70363-9, 9187954.
43. Bodey G, Bueltmann B, Duguid W, Gibbs D, Hanak H, Hotchi M, Mall G, Martino P, Meunier F, Milliken S, et al. Fungal infections in cancer patients: an international autopsy survey. Eur J Clin Microbiol Infect Dis 1992, 11:99-109. 10.1007/BF01967060, 1396746.
44. Güldener U, Heck S, Fiedler T, Beinhauer J, Hegemann JH. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 1996, 13:2519-2524.
45. Goldstein AL, McCusker JH. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 1999, 15:1541-15. 10.1002/(SICI)1097-0061(199910)15:14<1541::AID-YEA476>3.0.CO;2-K, 10514571.
46. Kuge S, Jones N, Nomoto A. Regulation of yAP-1 nuclear localization in response to oxidative stress. EMBO J 1997, 16:1710-1720. 10.1093/emboj/16.7.1710, 1169774, 9130715.
47. Ausubel FM, Brent B, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. Current protocols in molecular biology 2000, Edison, NJ: John Wiley & Sons.