Immunoproteomic profiling of Saccharomyces cerevisiae systemic infection in a murine model

Journal of Proteomics

Volumn 112, Issue , 2015, Pages 14-26

  Hernández Haro, Carolina ^a   Llopis, Silvia ^b   Molina, María ^a   Monteoliva, Lucía ^a   Gil, Concha ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

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

Author keywords

Biomarkers; Dietary yeast; Immunoproteomics; S. cerevisiae antigen; Yeast infection

Indexed keywords

BIOLOGICAL MARKER; CHAPERONE; FUNGAL PROTEIN; FUNGUS ANTIGEN; GLUTAMATE AMMONIA LIGASE; PROTEIN AHP1; PROTEIN KES1; PROTEIN OYE2; PROTEIN YHB1; UNCLASSIFIED DRUG; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOMICS; CANDIDA ALBICANS; CANDIDA GLABRATA; CONTROLLED STUDY; CROSS REACTION; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; FEMALE; FUNGAL VIRULENCE; IMMUNODETECTION; IMMUNOPROTEOMICS; MOUSE; MYCOSIS; NONHUMAN; OPPORTUNISTIC INFECTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; SACCHAROMYCES CEREVISIAE; TWO DIMENSIONAL ELECTROPHORESIS; WESTERN BLOTTING; ANIMAL; BLOOD; DISEASE MODEL; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; PATHOGENICITY;

MURINAE; SACCHAROMYCES CEREVISIAE;

ANIMALS; ANTIGENS, FUNGAL; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; MICE; MICE, INBRED ICR; MYCOSES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84907741818     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.08.008     Document Type: Article

References (80)

1. McFarland L.V. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol 2010, 16:2202-2222.
2. Enache-Angoulvant A., Hennequin C. Invasive Saccharomyces infection: a comprehensive review. Clin Infect Dis 2005, 41:1559-1568.
3. Swinne D., Nolard N. P VANR, Detandt M. Bloodstream yeast infections: a 15-month survey. Epidemiol Infect 2009, 137:1037-1040.
4. Sabino R., Verissimo C., Brandao J., Alves C., Parada H., Rosado L., et al. Epidemiology of candidemia in oncology patients: a 6-year survey in a Portuguese central hospital. Med Mycol 2010, 48:346-354.
5. Arendrup M.C., Sulim S., Holm A., Nielsen L., Nielsen S.D., Knudsen J.D., et al. Diagnostic issues, clinical characteristics, and outcomes for patients with fungemia. J Clin Microbiol 2011, 49:3300-3308.
6. Chitasombat M.N., Kofteridis D.P., Jiang Y., Tarrand J., Lewis R.E., Kontoyiannis D.P. Rare opportunistic (non-Candida, non-Cryptococcus) yeast bloodstream infections in patients with cancer. J Infect 2012, 64:68-75.
7. Smith D., Metzgar D., Wills C., Fierer J. Fatal Saccharomyces cerevisiae aortic graft infection. J Clin Microbiol 2002, 40:2691-2692.
8. Jensen D.P., Smith D.L. Fever of unknown origin secondary to brewer's yeast ingestion. Arch Intern Med 1976, 136:332-333.
9. Hazen K.C. New and emerging yeast pathogens. Clin Microbiol Rev 1995, 8:462-478.
10. Murphy A., Kavanagh K. Emergence of Saccharomyces cerevisiae as a human pathogen, Implications for biotechnology. Enzyme Microb Technol 1999, 25:551-557.
11. Ponton J., Ruchel R., Clemons K.V., Coleman D.C., Grillot R., Guarro J., et al. Emerging pathogens. Med Mycol 2000, 38(Suppl. 1):225-236.
12. Smith D.L. Brewer's yeast as a cause of infection. Clin Infect Dis 1996, 22:201.
13. Sobel J., Vazquez J., Lynch M., Meriwether C., Zervos M. Vaginitis due to Saccharomyces cerevisiae: Epidemiology, Clinical aspects, and Therapy. Clin Infect Dis 1993, 16:93-99.
14. McCullough M.J., Clemons K.V., Farina C., McCusker J.H., Stevens D.A. Epidemiological investigation of vaginal Saccharomyces cerevisiae isolates by a genotypic method. J Clin Microbiol 1998, 36:557-562.
15. Nyirjesy P., Vazquez J.A., Ufberg D.D., Sobel J.D., Boikov D.A., Buckley H.R. Saccharomyces cerevisiae vaginitis: transmission from yeast used in baking. Obstet Gynecol 1995, 86:326-329.
16. McCusker J.H., Clemons K.V., Stevens D.A., Davis R.W. 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.
17. McCusker J.H., Clemons K.V., Stevens D.A., Davis R.W. Genetic characterization of pathogenic Saccharomyces cerevisiae isolates. Genetics 1994, 136:1261-1269.
18. de Llanos R., Fernandez-Espinar M.T., 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.
19. Clemons K.V., McCusker J.H., Davis R.W., Stevens D.A. Comparative pathogenesis of clinical and nonclinical isolates of Saccharomyces cerevisiae. J Infect Dis 1994, 169:859-867.
20. Diezmann S., Dietrich F.S. Saccharomyces cerevisiae: population divergence and resistance to oxidative stress in clinical, domesticated and wild isolates. PLoS One 2009, 4:e5317.
21. Diezmann S., Dietrich F.S. Oxidative stress survival in a clinical Saccharomyces cerevisiae isolate is influenced by a major quantitative trait nucleotide. Genetics 2011, 188:709-722.
22. Clemons K.V., Hanson L.C., Stevens D.A. Colony phenotype switching in clinical and non-clinical isolates of Saccharomyces cerevisiae. J Med Vet Mycol 1996, 34:259-264.
23. Llopis S., Hernandez-Haro C., Monteoliva L., Querol A., Molina M., Fernández-Espinar M. Pathogenic potential of Saccharomyces cerevisiae strains of isolated from dietary supplements. PLoS One 2014, 9:e98094.
24. Munoz P., Bouza E., Cuenca-Estrella M., Eiros J.M., Perez M.J., Sanchez-Somolinos M., et al. Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin Infect Dis 2005, 40:1625-1634.
25. de Llanos R., Querol A., Planes A.M., Fernandez-Espinar M.T. Molecular characterization of clinical Saccharomyces cerevisiae isolates and their association with non-clinical strains. Syst Appl Microbiol 2004, 27:427-435.
26. Yáñez A., Murciano C., Llopis S., Fernández-Espinar T., Gil M., Gozalbo D. In Vivo and In Vitro Studies on Virulence and Host Responses to Saccharomyces cerevisiae Clinical and Non-Clinical Isolates. Open Mycol J 2009, 3:12.
27. de Llanos R., Llopis S., Molero G., Querol A., Gil C., Fernandez-Espinar M.T. In vivo virulence of commercial Saccharomyces cerevisiae strains with pathogenicity-associated phenotypical traits. Int J Food Microbiol 2011, 144:393-399.
28. Hennequin C., Kauffmann-Lacroix C., Jobert A., Viard J.P., Ricour C., Jacquemin J.L., et al. Possible role of catheters in Saccharomyces boulardii fungemia. Eur J Clin Microbiol Infect Dis 2000, 19:16-20.
29. Perez-Torrado R., Llopis S., Jespersen L., Fernandez-Espinar T., Querol A. Clinical Saccharomyces cerevisiae isolates cannot cross the epithelial barrier in vitro. Int J Food Microbiol 2012, 157:59-64.
30. Lorenz M.C., Fink G.R. The glyoxylate cycle is required for fungal virulence. Nature 2001, 412:83-86.
31. Lorenz M.C., Bender J.A., Fink G.R. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 2004, 3:1076-1087.
32. Fernandez-Arenas E., Cabezon V., Bermejo C., Arroyo J., Nombela C., Diez-Orejas R., et al. Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol Cell Proteomics 2007, 6:460-478.
33. Llopis S., Querol A., Heyken A., Hube B., Jespersen L., Fernandez-Espinar M.T., et al. Transcriptomics in human blood incubation reveals the importance of oxidative stress response in Saccharomyces cerevisiae clinical strains. BMC Genomics 2012, 13:419.
34. Hodgetts S., Matthews R., Morrissey G., Mitsutake K., Piper P., Burnie J. Over-expression of Saccharomyces cerevisiae hsp90 enhances the virulence of this yeast in mice. FEMS Immunol Med Microbiol 1996, 16:229-234.
35. Wheeler R.T., Kupiec M., Magnelli P., Abeijon C., Fink G.R. A Saccharomyces cerevisiae mutant with increased virulence. Proc Natl Acad Sci U S A 2003, 100:2766-2770.
36. Mendum T.A., Newcombe J., McNeilly C.L., McFadden J. Towards the immunoproteome of Neisseria meningitidis. PLoS One 2009, 4:e5940.
37. Forgber M., Trefzer U., Sterry W., Walden P. Proteome serological determination of tumor-associated antigens in melanoma. PLoS One 2009, 4:e5199.
38. Martinez-Lopez R., Nombela C., Diez-Orejas R., Monteoliva L., Gil C. Immunoproteomic analysis of the protective response obtained from vaccination with Candida albicans ecm33 cell wall mutant in mice. Proteomics 2008, 8:2651-2664.
39. Pitarch A., Jimenez A., Nombela C., Gil C. Decoding serological response to Candida cell wall immunome into novel diagnostic, prognostic, and therapeutic candidates for systemic candidiasis by proteomic and bioinformatic analyses. Mol Cell Proteomics 2006, 5:79-96.
40. Pitarch A., Nombela C., Gil C. Prediction of the clinical outcome in invasive candidiasis patients based on molecular fingerprints of five anti-Candida antibodies in serum. Mol Cell Proteomics 2011, 10(M110):004010.
41. Rothstein R.J. One-step gene disruption in yeast. Methods Enzymol 1983, 101:202-211.
42. Gillum A.M., Tsay E.Y., Kirsch D.R. 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 1984, 198:179-182.
43. Pitarch A., Pardo M., Jimenez A., Pla J., Gil C., Sanchez M., et al. Two-dimensional gel electrophoresis as analytical tool for identifying Candida albicans immunogenic proteins. Electrophoresis 1999, 20:1001-1010.
44. Neil M., Matsui N.M., Smith-Beckerman D., Epstein L. Staining of Preparative 2-D Gels. 2-D Proteome Analysis Protocols. Methods Mol Biol 1999, 12:5.
45. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 1979, 76:4350-4354.
46. Sechi S., Chait B.T. Modification of cysteine residues by alkylation. A tool in peptide mapping and protein identification. Anal Chem 1998, 70:5150-5158.
47. Robinson M.D., Grigull J., Mohammad N., Hughes T.R. FunSpec: a web-based cluster interpreter for yeast. BMC Bioinformatics 2002, 3:35.
48. Brunke S., Hube B. Two unlike cousins: Candida albicans and C. glabrata infection strategies. Cell Microbiol 2013, 15:701-708.
49. Hu Y., Farah C.S., Ashman R.B. Isolates of Candida albicans that differ in virulence for mice elicit strain-specific antibody-mediated protective responses. Microbes Infect 2006, 8:612-620.
50. Pitarch A., Diez-Orejas R., Molero G., Pardo M., Sanchez M., Gil C., et al. Analysis of the serologic response to systemic Candida albicans infection in a murine model. Proteomics 2001, 1:550-559.
51. Pitarch A., Abian J., Carrascal M., Sanchez M., Nombela C., Gil C. Proteomics-based identification of novel Candida albicans antigens for diagnosis of systemic candidiasis in patients with underlying hematological malignancies. Proteomics 2004, 4:3084-3106.
52. Fernandez-Arenas E., Molero G., Nombela C., Diez-Orejas R., Gil C. Contribution of the antibodies response induced by a low virulent Candida albicans strain in protection against systemic candidiasis. Proteomics 2004, 4:1204-1215.
53. Pitarch A., Jimenez A., Nombela C., Gil C. Serological proteome analysis to identify systemic candidiasis patients in the intensive care unit: Analytical, diagnostic and prognostic validation of anti-Candida enolase antibodies on quantitative clinical platforms. Proteomics Clin Appl 2008, 2:596-618.
54. Nombela C., Gil C., Chaffin W.L. Non-conventional protein secretion in yeast. Trends Microbiol 2006, 14:15-21.
55. Henderson B., Martin A. Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun 2011, 79:3476-3491.
56. Martinez J.P., Gil M.L., Lopez-Ribot J.L., Chaffin W.L. Serologic response to cell wall mannoproteins and proteins of Candida albicans. Clin Microbiol Rev 1998, 11:121-141.
57. Pardo M., Monteoliva L., Pla J., Sanchez M., Gil C., Nombela C. Two-dimensional analysis of proteins secreted by Saccharomyces cerevisiae regenerating protoplasts: a novel approach to study the cell wall. Yeast 1999, 15:459-472.
58. Pitarch A., Sanchez M., Nombela C., Gil C. Sequential fractionation and two-dimensional gel analysis unravels the complexity of the dimorphic fungus Candida albicans cell wall proteome. Mol Cell Proteomics 2002, 1:967-982.
59. Crowe J.D., Sievwright I.K., Auld G.C., Moore N.R., Gow N.A., Booth N.A. Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol Microbiol 2003, 47:1637-1651.
60. Urban C., Sohn K., Lottspeich F., Brunner H., Rupp S. Identification of cell surface determinants in Candida albicans reveals Tsa1p, a protein differentially localized in the cell. FEBS Lett 2003, 544:228-235.
61. Hernaez M.L., Ximenez-Embun P., Martinez-Gomariz M., Gutierrez-Blazquez M.D., Nombela C., Gil C. Identification of Candida albicans exposed surface proteins in vivo by a rapid proteomic approach. J Proteome 2010, 73:1404-1409.
62. Insenser M.R., Hernaez M.L., Nombela C., Molina M., Molero G., Gil C. Gel and gel-free proteomics to identify Saccharomyces cerevisiae cell surface proteins. J Proteome 2010, 73:1183-1195.
63. Braconi D., Amato L., Bernardini G., Arena S., Orlandini M., Scaloni A., et al. Surfome analysis of a wild-type wine Saccharomyces cerevisiae strain. Food Microbiol 2011, 28:1220-1230.
64. Jong A.Y., Chen S.H., Stins M.F., Kim K.S., Tuan T.L., Huang S.H. Binding of Candida albicans enolase to plasmin(ogen) results in enhanced invasion of human brain microvascular endothelial cells. J Med Microbiol 2003, 52:615-622.
65. Gozalbo D., Gil-Navarro I., Azorin I., Renau-Piqueras J., Martinez J.P., Gil M.L. The cell wall-associated glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is also a fibronectin and laminin binding protein. Infect Immun 1998, 66:2052-2059.
66. Maresca B., Kobayashi G.S. Hsp70 in parasites: as an inducible protective protein and as an antigen. Experientia 1994, 50:1067-1074.
67. Moseley P. Stress proteins and the immune response. Immunopharmacology 2000, 48:299-302.
68. Pockley A.G. Heat shock proteins as regulators of the immune response. Lancet 2003, 362:469-476.
69. Wang G., Sun M., Fang J., Yang Q., Tong H., Wang L. Protective immune responses against systemic candidiasis mediated by phage-displayed specific epitope of Candida albicans heat shock protein 90 in C57BL/6J mice. Vaccine 2006, 24:6065-6073.
70. Matthews R., Burnie J. Antibodies against Candida: potential therapeutics?. Trends Microbiol 1996, 4:354-358.
71. Matthews R.C., Rigg G., Hodgetts S., Carter T., Chapman C., Gregory C., et al. Preclinical assessment of the efficacy of mycograb, a human recombinant antibody against fungal HSP90. Antimicrob Agents Chemother 2003, 47:2208-2216.
72. Lee J., Spector D., Godon C., Labarre J., Toledano M.B. A new antioxidant with alkyl hydroperoxide defense properties in yeast. J Biol Chem 1999, 274:4537-4544.
73. Odat O., Matta S., Khalil H., Kampranis S.C., Pfau R., Tsichlis P.N., et al. Old yellow enzymes, highly homologous FMN oxidoreductases with modulating roles in oxidative stress and programmed cell death in yeast. J Biol Chem 2007, 282:36010-36023.
74. Trotter E.W., Collinson E.J., Dawes I.W., Grant C.M. Old yellow enzymes protect against acrolein toxicity in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 2006, 72:4885-4892.
75. Liu L., Zeng M., Hausladen A., Heitman J., Stamler J.S. Protection from nitrosative stress by yeast flavohemoglobin. Proc Natl Acad Sci U S A 2000, 97:4672-4676.
76. McAlister L., Holland M.J. Isolation and characterization of yeast strains carrying mutations in the glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 1985, 260:15013-15018.
77. Goehring A.S., Rivers D.M., Sprague G.F. Attachment of the ubiquitin-related protein Urm1p to the antioxidant protein Ahp1p. Eukaryot Cell 2003, 2:930-936.
78. Trivelli X., Krimm I., Ebel C., Verdoucq L., Prouzet-Mauleon V., Chartier Y., et al. Characterization of the yeast peroxiredoxin Ahp1 in its reduced active and overoxidized inactive forms using NMR. Biochemistry 2003, 42:14139-14149.
79. Cassanova N., O'Brien K.M., Stahl B.T., McClure T., Poyton R.O. Yeast flavohemoglobin, a nitric oxide oxidoreductase, is located in both the cytosol and the mitochondrial matrix: effects of respiration, anoxia, and the mitochondrial genome on its intracellular level and distribution. J Biol Chem 2005, 280:7645-7653.
80. Nie S., Lo A., Wu J., Zhu J., Tan Z., Simeone D.M., et al. Glycoprotein Biomarker Panel for Pancreatic Cancer Discovered by Quantitative Proteomics Analysis. J Proteome Res 2014, 13:1873-1884.