Pathogenic potential of Saccharomyces strains isolated from dietary supplements

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Llopis, Silvia ^a   Hernández Haro, Carolina ^b   Monteoliva, Lucía ^b   Querol, Amparo ^a   Molina, María ^b   Fernández Espinar, María T ^a  

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

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; POLYSTYRENE DERIVATIVE; POLYURETHAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVATION; FEMALE; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS IDENTIFICATION; FUNGUS ISOLATION; GASTROINTESTINAL INFECTION; IN VIVO STUDY; MOUSE; MYCOSIS; NONHUMAN; PATHOGEN LOAD; PHENOTYPE; SACCHAROMYCES; SACCHAROMYCES BAYANUS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES KUDRIAVZEVII; SACCHAROMYCETALES; YEAST CELL; ADHESION; ANIMAL; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; EXTRACELLULAR SPACE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOGENICITY; SIGNAL TRANSDUCTION; TEMPERATURE; VIRULENCE;

ADHESIVENESS; ANIMALS; DIETARY SUPPLEMENTS; EXTRACELLULAR SPACE; FEMALE; MAP KINASE SIGNALING SYSTEM; MICE; PHENOTYPE; POLYSTYRENES; POLYURETHANES; SACCHAROMYCES CEREVISIAE; TEMPERATURE; VIRULENCE;

EID: 84902309946     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098094     Document Type: Article

References (76)

1. Moyad MA (2007) Brewer's/baker's yeast (Saccharomyces cerevisiae) and preventive medicine: Part I. Urol Nurs 27: 560-561.
2. Li YC (1994) Effects of brewer's yeast on glucose tolerance and serum lipids in Chinese adults. Biol Trace Elem Res 41: 341-347.
3. Reddy BS, Hirose Y, Lubet RA, Steele VE, Kelloff GJ, et al. (2000) Lack of chemopreventive efficacy of DL-selenomethionine in colon carcinogenesis. Int J Mol Med 5: 327-330.
4. Nakamura T, Agata K, Mizutani M, Lino H (2001) Effects of brewer's yeast cell wall on constipation and defecation in experimentally constipated rats. Biosci Biotechnol Biochem 65: 774-780. (Pubitemid 33614160)
5. Bahijiri SM, Mira SA, Mufti AM, Ajabnoor MA (2000) The effects of inorganic chromium and brewer's yeast supplementation on glucose tolerance, serum lipids and drug dosage in individuals with type 2 diabetes. Saudi Med J 21: 831-837.
6. Enache-Angoulvant A, Hennequin C (2005) Invasive Saccharomyces infection: a comprehensive review. Clin Infect Dis 41: 1559-1568. (Pubitemid 41691593)
7. Smith D, Metzgar D, Wills C, Fierer J (2002) Fatal Saccharomyces cerevisiae aortic graft infection. J Clin Microbiol 40: 2691-2692. (Pubitemid 34747394)
8. Debelian GJ, Olsen I, Tronstad L (1997) Observation of Saccharomyces cerevisiae in blood of patient undergoing root canal treatment. Int Endod J 30: 313-317. (Pubitemid 127490937)
9. Fung KS, Scheel O, Lyon DJ, Cheng AF, Bendeck J (1996) Self-inflicted bacteraemia and fungaemia in Vietnamese migrants. Scand J Infect Dis 28: 83-85. (Pubitemid 26138217)
10. McCusker JH, Clemons KV, Stevens DA, Davis RW (1994) Genetic characterization of pathogenic Saccharomyces cerevisiae isolates. Genetics 136: 1261-1269. (Pubitemid 24097854)
11. McCusker JH, Clemons KV, Stevens DA, Davis RW (1994) Saccharomyces cerevisiae virulence phenotype as determined with CD-1 mice is associated with the ability to grow at 42uC and form pseudohyphae. Infect Immun 62: 5447-5455. (Pubitemid 24364986)
12. Clemons KV, Hanson LC, Stevens DA (1996) Colony phenotype switching in clinical and non-clinical isolates of Saccharomyces cerevisiae . J Med Vet Mycol 34: 259-264. (Pubitemid 26337081)
13. Murphy AR, Kavanagh KA (2001) Adherence of clinical isolates of Saccharomyces cerevisiae to buccal epithelial cells. Med Mycol 39: 123-127.
14. Klingberg TD, Lesnik U, Arneborg N, Raspor P, Jespersen L (2008) Comparison of Saccharomyces cerevisiae strains of clinical and nonclinical origin by molecular typing and determination of putative virulence traits. FEMS Yeast Res 8: 631-640. (Pubitemid 351678647)
15. Byron JK, Clemons KV, McCusker JH, Davis RW, Stevens DA (1995) Pathogenicity of Saccharomyces cerevisiae in complement factor five-deficient mice. Infect Immun 63: 478-485.
16. Clemons KV, McCusker JJ, Davis RW, Stevens DA (1994) Comparative pathogenesis of clinical and nonclinical isolates of Saccharomyces cerevisiae . J Infect Dis 169: 859-867. (Pubitemid 24102121)
17. McCullough MJ, Clemons KV, McCusker JH, Stevens DA (1998) Species identification and virulence attributes of Saccharomyces boulardii (nom inval). J Clin Microbiol 36: 2613-2617. (Pubitemid 28380965)
18. Ghannoum MA (2000) Potential role of phospholipases in virulence and fungal pathogenesis. Clin Microbiol Rev 13: 122-143. (Pubitemid 30039346)
19. Naglik JR, Challacombe SJ, Hube B (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67: 400-428. (Pubitemid 37122527)
20. Mitchell AP (1998) Dimorphism and virulence in Candida albicans. Curr Opin Microbiol 1: 687-692.
21. van Burik JA, Magee PT (2001) Aspects of fungal pathogenesis in humans. Annu Rev Microbiol 55: 743-772.
22. Soll DR (1992) High-frequency switching in Candida albicans. Clin Microbiol Rev. 5: 183-203.
23. Soll DR, Staebell M, Langtimm C, Pfaller M, Hicks J, et al. (1988) Multiple Candida strains in the course of a single systemic infection. J Clin Microbiol 26: 1448-1459.
24. Jain N, Li L, McFadden DC, Banarjee U, Wang X, Cook E, et al. (2006) Phenotypic switching in a Cryptococcus neoformans variety gattii strain is associated with changes in virulence and promotes dissemination to the central nervous system. Infect Immun 74: 896-903. (Pubitemid 43185522)
25. el-Azizi M, Khardori N (1999) Factors influencing adherence of Candida spp. to host tissues and plastic surfaces Indian J Exp Biol. 37: 941-51.
26. Rotrosen D, Calderone RA, Edwards JE Jr (1986) Adherence of Candida species to host tissues and plastic surfaces. Rev Infect Dis 8: 73-85.
27. Román E, Arana DM, Nombela C, Alonso-Monge R, Pla J (2007) MAP kinase pathways as regulators of fungal virulence. Trends Microbiol 15: 181-190. (Pubitemid 46528249)
28. de Llanos R, Fernández-Espinar MT, Querol A (2006) A comparison between clinical and food Saccharomyces cerevisiae isolates on the basis of potential virulence factors. Antonie Van Leeuwenhoek 90: 221-231. (Pubitemid 44314600)
29. Chen RE, Thorner J (2007) Function and regulation in MAPK signaling pathways: Lessons learned from the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1773: 1311-1340. (Pubitemid 47125982)
30. de Llanos R, Hernández-Haro C, Barrio E, Querol A, Fernández-Espinar MT, et al. (2010) Differences in activation of MAP kinases and variability in the polyglutamine tract of Slt2 in clinical and non-clinical isolates of Saccharomyces cerevisiae. Yeast 27: 549-561.
31. de Llanos R, Llopis S, Molero G, Querol A, Gil C, et al. (2011) In vivo virulence of commercial Saccharomyces cerevisiae strains with pathogenicity-associated phenotypical traits. Int J Food Microbiol 144: 393-399.
32. de Llanos R, Querol A, Pemán J, Gobernado M, Fernández- Espinar MT (2006) Food and probiotic strains from the Saccharomyces cerevisiae species as a possible origin of human systemic infections. Int J Food Microbiol 110: 286-290. (Pubitemid 44108263)
33. Hennequin C, Kauffmann-Lacroix C, Jobert A, Viard JP, Ricour C, et al. (2000) Possible role of catheters in Saccharomyces boulardii fungemia. Eur J Clin Microbiol Infect Dis 19: 16-20. (Pubitemid 30093376)
34. Lherm T, Monet C, Nougiere B, Soulier M, Larbi D, et al. (2002) Seven cases of fungemia with Saccharomyces boulardii in critically ill patients. Int Care Med 28: 797-801. (Pubitemid 34639496)
35. Riquelme AJ, Calvo MA, Guzmán AM, Depix MS, García P, et al. (2003) Saccharomyces cerevisiae fungemia after Saccharomyces boulardii treatment in immunocompromised patients. J Clin Gastroenterol 36: 41-43. (Pubitemid 36005347)
36. Jensen DP, Smith DL (1976) Fever of unknown origin secondary to brewer's yeast ingestion. Arch Intern Med 136: 332-333.
37. Yáñez A, Murciano C, Llopis S, Fernández-Espinar MT, Gil ML, et al. (2009) In vivo and in vitro studies on virulence and host responses to Saccharomyces cerevisiae clinical and non-clinical isolates. Open Mycol J 3: 37-47.
38. Fernández-Espinar MT, López V, Ramón D, Bartra E, Querol A (2001) Study of the authenticity of commercial wine yeast strains by molecular techniques. Int J Food Microbiol 70: 1-10. (Pubitemid 32979211)
39. González SS, Barrio E, Querol A (2008) Molecular characterization of new natural hybrids of Saccharomyces cerevisiae and S. kudriavzevii in brewing. Appl Environ Microbiol 74: 2314-2320. (Pubitemid 351555441)
40. González SS, Barrio E, Gafner J, Querol A (2006) Natural hybrids from Saccharomyces cerevisiae, S. bayanus and S. kudriavzevii in wine fermentations. FEMS Yeast Res 6: 1221-1234. (Pubitemid 44800319)
41. Querol A, Bond U (2009) The complex and dynamic genomes of industrial yeasts. FEMS Microbiol Lett 293: 1-10.
42. Gillum AM, Tsay EY, Kirsch DR (1984) Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198: 179-182. (Pubitemid 15180998)
43. Querol A, Barrio E, Ramón D (1992) A comparative study of different methods of yeast strain characterisation. Syst Appl Microbiol 15: 439-446.
44. de Llanos R, Querol A, Planes AM, Fernández-Espinar MT (2004) Molecular characterisation of clinical Saccharomyces cerevisiae isolates and their association with non-clinical strains. System Appl Microbiol 27: 427-435. (Pubitemid 39071017)
45. White TJ, Bruns T, Lee E, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego: Academic Press. 315-322.
46. Lopes CA, Barrio E, Querol A (2010) Natural hybrids of S. cerevisiae x S. kudriavzevii share alleles with European wild populations of Saccharomyces kudriavzevii. FEMS Yeast Res 10: 412-421.
47. Ness F, Lavallée F, Dubordieu D, Aigle M, Dulau L (1993) Identification of yeast strains using the polymerase chain reaction. J Sci Food Agric 62: 84-94.
48. Aoki S, Ito-Kuwa S, Nakamura K, Kato J, Ninomiya K, et al. (1994) Extracellular proteolytic activity of Cryptococcus neoformans. Mycopathologia 128: 143-150.
49. Price MF, Wilkinson ID, Gentry LO (1982) Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia 20: 7-14. (Pubitemid 12161206)
50. Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR (1992) Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68: 1077-1090.
51. Martín H, Rodriguez-Pachón JM, Ruiz C, Nombela C, Molina M (2000) Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J Biol Chem 275: 1511-1519. (Pubitemid 30051213)
52. Martín H, Arroyo H, Sánchez M, Molina M, Nombela C (1993) Activity of the yeast MAPK homologue Slt2 is critically required for cell integrity at 37°C. Mol Gen Genet 241: 177-184. (Pubitemid 23299219)
53. Peeters E, Nelis HJ, Coenye T (2008) Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Methods 72: 157-165.
54. Wells CL, Johnson M, Henry-Stanley MJ, Bendel CM (2007) Candida glabrata colonizes but does not often disseminate from the mouse caecum. J Med Microbiol 56: 688-693. (Pubitemid 46717496)
55. Fernández-Espinar MT; Esteve-Zarzoso B; Querol A, Barrio E (2000) RFLP analysis of the ribosomal internal transcribed spacers and the 5.8S rRNA gene region of the genus Saccharomyces: a fast method for species identification and the differentiation of flor yeasts. Antonie Van Leeuwenhoek 78: 87-97.
56. Gancedo JM (2001) Control of pseudohyphae formation in Saccharomyces cerevisiae. FEMS Microbiol Rev 25: 107-123.
57. Mellado E, Cuenca-Estrella M, Regadera J, González M, Díaz-Guerra TM, et al. (2000) Sustained gastrointestinal colonization and systemic dissemination by Candida albicans, Candida tropicalis and Candida parapsilosis in adult mice. Diagn Microbiol Infect Dis 38: 21-28.
58. Takahashi K, Kita E, Konishi M, Yoshimoto E, Mikasa K, et al. (2003) Translocation model of Candida albicans in DBA-2/J mice with protein calorie malnutrition mimics hematogenous candidiasis in humans. Microb Pathog 35: 179-187. (Pubitemid 37163718)
59. Muñoz P, Bouza E, Cuenca-Estrella M, Eiros JM, Pérez MJ, et al. (2005). Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin Infect Dis 40: 1625-1633.
60. Whelan K, Myers CE (2010) Safety of probiotics in patients receiving nutritional support: a systematic review of case reports, randomized controlled trials, and nonrandomized trials. Am J Clin Nutr 91: 687-703.
61. MacCallum DM, Odds FC (2005) Temporal events in the intravenous challenge model for experimental Candida albicans infections in female mice. Mycoses 48: 141-161.
62. Belloch C, Pérez-Torrado R, González SS, Pérez-Ortín JE, García-Martínez J, et al. (2008) Chimeric genomes of natural hybrids of Saccharomyces cerevisiae and Saccharomyces kudriavzevii. Appl Environ Microbiol 75: 2534-2544.
63. Zupan J, Raspor P (2008) Quantitative agar-invasion assay. JMicrobiol Methods 73: 100-104.
64. Wheeler RT, Kupiec M, Magnelli P, Abeijon C, Fink GR (2003) A Saccharomyces cerevisiae mutant with increased virulence. Proc Nat Acad Sci USA 100: 2766-2770. (Pubitemid 36297573)
65. Pope LM, Cole GT (1982) Comparative studies of gastrointestinal colonization and systemic spread by Candida albicans and nonlethal yeast in the infant mouse. Scan Electron Microsc 4: 1667-1676. (Pubitemid 14486981)
66. Cartwright-Shamoon J, Dickson GR, Dodge J, Carr KE (1995) Morphological aspects of particle translocation in vivo following ingestion of the yeast Saccharomyces boulardii. J Drug Target 3: 61-63.
67. Cartwright-Shamoon J, Dickson GR, Dodge J, Carr KE (1996) Uptake of yeast (Saccharomyces boulardii) in normal and rotavirus treated intestine. Gut 39: 204-209. (Pubitemid 26275996)
68. Peret Filho LA, Penna FJ, Bambirra EA, Nicoli JR (1998) Dose effect of oral Saccharomyces boulardii treatments on morbidity and mortality in immunosupressed mice. J Med Microbiol 47: 111-116. (Pubitemid 28041253)
69. Rodrigues AC, Cara DC, Fretez SH, Cunha FQ, Vieira EC, et al. (2000) Saccharomyces boulardii stimulates sIgA production and the phagocytic system of gnotobiotic mice. J Appl Microbiol 89: 404-414.
70. Martins FS, Rodrigues AC, Tiago FC, Penna FJ, Rosa CA, et al. (2007) Saccharomyces cerevisiae strain 905 reduces the translocation of Salmonella enterica serotype Typhimurium and stimulates the immune system in gnotobiotic and conventional mice. J Med Microbiol 56: 352-359. (Pubitemid 46363980)
71. Samonis G, Falagas ME, Lionakis S, Ntaoukakis M, Kofteridis DP, et al. (2011) Saccharomyces boulardii and Candida albicans experimental colonization of the murine gut. Med Mycol 49: 395-399.
72. Cesaro S, Chinello P, Rossi L, Zanesco L (2000) Saccharomyces cerevisiae fungemia in a neutropenic patient treated with Saccharomyces boulardii. Support Care Cancer 8: 504-505.
73. Herbrecht R, Nivoix Y (2005) Saccharomyces cerevisiae fungemia: adverse effect of Saccharomyces boulardii probiotic administration. Clin Infect Dis 40: 1635-1637. (Pubitemid 40720814)
74. Pérez-Torrado R, Llopis S, Jespersen L, Fernández-Espinar T, Querol A (2012) Clinical Saccharomyces cerevisiae isolates cannot cross the epithelial barrier in vitro. Int J Food Microbiol 157: 59-64.
75. Andrutis KA, Riggle PJ, Kumamoto CA, Tzipori S (2000) Intestinal lesions associated with disseminated candidiasis in an experimental animal model. J Clin Microbiol 38: 2317-2323. (Pubitemid 30414357)
76. Thomas BJ, Rothstein R (1989) Elevated recombination rates in transcriptionally active DNA. Cell 56: 619-630.