Seroprofiling at the Candida albicans protein species level unveils an accurate molecular discriminator for candidemia

Journal of Proteomics

Volumn 134, Issue , 2016, Pages 144-162

  Pitarch, Aida ^a   Nombela, César ^a   Gil, Concha ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Biomarkers; Candidemia; Diagnosis; Immunome; Immunoproteomics; Invasive candidiasis; Protein species; Sensitivity and specificity; Serologic response; Serological proteome analysis

Indexed keywords

ENOLASE; EPITOPE; IMMUNOGLOBULIN G ANTIBODY; INDUCIBLE T CELL COSTIMULATOR; PHOSPHOGLYCERATE KINASE; PROTEOME; FUNGAL PROTEIN; FUNGUS ANTIBODY; IMMUNOGLOBULIN G;

ADULT; AGED; ANTIBODY RESPONSE; ANTIGEN RECOGNITION; ARTICLE; CANDIDA ALBICANS; CANDIDEMIA; CLINICAL ARTICLE; COMMENSALISM; CONTROLLED STUDY; FEMALE; HUMAN; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SEROPREVALENCE; SPECIES DIFFERENTIATION; BLOOD; METABOLISM; MIDDLE AGED;

ADULT; AGED; ANTIBODIES, FUNGAL; CANDIDA ALBICANS; CANDIDEMIA; FEMALE; FUNGAL PROTEINS; HUMANS; IMMUNOGLOBULIN G; MALE; MIDDLE AGED;

EID: 84958164162     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.10.022     Document Type: Article

References (93)

1. Pfaller M.A., Diekema D.J. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 2007, 20:133-163.
2. Magill S.S., Edwards J.R., Bamberg W., Beldavs Z.G., Dumyati G., Kainer M.A., et al. Multistate point-prevalence survey of health care-associated infections. N. Engl. J. Med. 2014, 370:1198-1208.
3. Cleveland A.A., Farley M.M., Harrison L.H., Stein B., Hollick R., Lockhart S.R., et al. Changes in incidence and antifungal drug resistance in candidemia: results from population-based laboratory surveillance in Atlanta and Baltimore, 2008-2011. Clin. Infect. Dis. 2012, 55:1352-1361.
4. Asmundsdottir L.R., Erlendsdottir H., Gottfredsson M. Nationwide study of candidemia, antifungal use, and antifungal drug resistance in Iceland, 2000 to 2011. J. Clin. Microbiol. 2013, 51:841-848.
5. Puig-Asensio M., Padilla B., Garnacho-Montero J., Zaragoza O., Aguado J.M., Zaragoza R., et al. Epidemiology and predictive factors for early and late mortality in Candida bloodstream infections: a population-based surveillance in Spain. Clin. Microbiol. Infect. 2014, 20:O245-O254.
6. Moran C., Grussemeyer C.A., Spalding J.R., Benjamin D.K., Reed S.D. Comparison of costs, length of stay, and mortality associated with Candida glabrata and Candida albicans bloodstream infections. Am. J. Infect. Control 2010, 38:78-80.
7. Arnold H.M., Micek S.T., Shorr A.F., Zilberberg M.D., Labelle A.J., Kothari S., et al. Hospital resource utilization and costs of inappropriate treatment of candidemia. Pharmacotherapy 2010, 30:361-368.
8. Chang A., Neofytos D., Horn D. Candidemia in the 21st century. Future Microbiol 2008, 3:463-472.
9. Ellepola A.N., Morrison C.J. Laboratory diagnosis of invasive candidiasis. J. Microbiol. 2005, 43:65-84.
10. Ahmad S., Khan Z. Invasive candidiasis: a review of nonculture-based laboratory diagnostic methods. Indian J. Med. Microbiol. 2012, 30:264-269.
11. Akin H., Akalin H., Budak F., Ener B., Ocakoglu G., Gurcuoglu E., et al. Alterations of serum cytokine levels and their relation with inflammatory markers in candidemia. Med. Mycol. 2015, 53:258-268.
12. Pazos C., Moragues M.D., Quindos G., Ponton J., del Palacio A. Diagnostic potential of (1,3)-beta-D-glucan and anti-Candida albicans germ tube antibodies for the diagnosis and therapeutic monitoring of invasive candidiasis in neutropenic adult patients. Rev. Iberoam. Micol. 2006, 23:209-215.
13. Clancy C.J., Nguyen M.L., Cheng S., Huang H., Fan G., Jaber R.A., et al. Immunoglobulin G responses to a panel of Candida albicans antigens as accurate and early markers for the presence of systemic candidiasis. J. Clin. Microbiol. 2008, 46:1647-1654.
14. Pitarch A., Nombela C., Gil C. Serum antibody signature directed against Candida albicans Hsp90 and enolase detects invasive candidiasis in non-neutropenic patients. J. Proteome Res. 2014, 13:5165-5184.
15. Taira C.L., Okay T.S., Delgado A.F., Ceccon M.E., de Almeida M.T., Del Negro G.M. A multiplex nested PCR for the detection and identification of Candida species in blood samples of critically ill paediatric patients. BMC Infect. Dis. 2014, 14:406.
16. Panda A., Ghosh A.K., Mirdha B.R., Xess I., Paul S., Samantaray J.C., et al. MALDI-TOF mass spectrometry for rapid identification of clinical fungal isolates based on ribosomal protein biomarkers. J. Microbiol. Methods 2015, 109:93-105.
17. Leon C., Ruiz-Santana S., Saavedra P., Galvan B., Blanco A., Castro C., et al. Usefulness of the "Candida score" for discriminating between Candida colonization and invasive candidiasis in non-neutropenic critically ill patients: a prospective multicenter study. Crit. Care Med. 2009, 37:1624-1633.
18. Neely L.A., Audeh M., Phung N.A., Min M., Suchocki A., Plourde D., et al. T2 magnetic resonance enables nanoparticle-mediated rapid detection of candidemia in whole blood. Sci. Transl. Med. 2013, 5:182ra154.
19. Krah A., Jungblut P.R. Immunoproteomics. Methods Mol. Med. 2004, 94:19-32.
20. Pitarch A., Nombela C., Gil C. Proteomic profiling of serologic response to Candida albicans during host-commensal and host-pathogen interactions. Methods Mol. Biol. 2009, 470:369-411.
21. Jungblut P.R., Bumann D. Immunoproteome of Helicobacter pylori. Methods Enzymol. 2002, 358:307-316.
22. Thomas D.P., Pitarch A., Monteoliva L., Gil C., Lopez-Ribot J.L. Proteomics to study Candida albicans biology and pathogenicity. Infect. Disord. Drug Targets 2006, 6:335-341.
23. Pitarch A., Gil C., Nombela C. La inmunoproteómica en el descubrimiento de biomarcadores de tercera generación. El ejemplo de las candidiasis invasivas. Biomarcadores: Analítica, Diagnóstico y Terapéutica 2010, 55-83. Real Academia Nacional de Farmacia, Madrid. F. Ortega (Ed.).
24. Krah A., Miehlke S., Pleissner K.-P., Zimny-Arndt U., Kirsch C., Lehn N., et al. Identification of candidate antigens for serologic detection of Helicobacter pylori-infected patients with gastric carcinoma. Int. J. Cancer 2004, 108:456-463.
25. Wu Z., Sahin O., Wang F., Zhang Q. Proteomic identification of immunodominant membrane-related antigens in Campylobacter jejuni associated with sheep abortion. J. Proteome 2014, 99:111-122.
26. Dea-Ayuela M.A., Ubeira F.M., Pitarch A., Gil C., Martinez-Fernandez A.R., Bolas F. A comparison of antigenic peptides in muscle larvae of several Trichinella species by two-dimensional western-blot analysis with monoclonal antibodies. Parasite 2001, 8:S117-S119.
27. Wang J., Zhao F., Yu C.X., Xiao D., Song L.J., Yin X.R., et al. Identification of proteins inducing short-lived antibody responses from excreted/secretory products of Schistosoma japonicum adult worms by immunoproteomic analysis. J. Proteome 2013, 87:53-67.
28. Pitarch A., Nombela C., Gil C. Proteomics, a new challenge for clinical microbiology. Enferm. Infecc. Microbiol. Clin. 2010, 28:489-491.
29. Jungblut P.R., Grabher G., Stoffler G. Comprehensive detection of immunorelevant Borrelia garinii antigens by two-dimensional electrophoresis. Electrophoresis 1999, 20:3611-3622.
30. Jungblut P., Thiede B., Zimny-Arndt U., Muller E.C., Scheler C., Wittmann-Liebold B., et al. Resolution power of two-dimensional electrophoresis and identification of proteins from gels. Electrophoresis 1996, 17:839-847.
31. Jungblut P.R., Holzhutter H.G., Apweiler R., Schluter H. The speciation of the proteome. Chem. Cent. J. 2008, 2:16.
32. Schluter H., Apweiler R., Holzhutter H.G., Jungblut P.R. Finding one's way in proteomics: a protein species nomenclature. Chem. Cent. J. 2009, 3:11.
33. Pitarch A., Nombela C., Gil C. Contributions of proteomics to diagnosis, treatment, and prevention of candidiasis. Methods Biochem. Anal. 2006, 49:331-361.
34. 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.
35. 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.
36. 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.
37. 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.
38. Hernando F.L., Calvo E., Abad A., Ramirez A., Rementeria A., Sevilla M.J., et al. Identification of protein and mannoprotein antigens of Candida albicans of relevance for the serodiagnosis of invasive candidiasis. Int. Microbiol. 2007, 10:103-108.
39. Lee P.Y., Gam L.H., Yong V.C., Rosli R., Ng K.P., Chong P.P. Immunoproteomic analysis of antibody response to cell wall-associated proteins of Candida tropicalis. J. Appl. Microbiol. 2014, 117:854-865.
40. Lange S., Rosenkrands I., Stein R., Andersen P., Kaufmann S.H., Jungblut P.R. Analysis of protein species differentiation among mycobacterial low-Mr-secreted proteins by narrow pH range immobiline gel 2-DE-MALDI-MS. J. Proteome 2014, 97:235-244.
41. Pitarch A., Nombela C., Gil C. The Candida immunome as a mine for clinical biomarker development for invasive candidiasis: from biomarker discovery to assay validation. Pathogenic Fungi: Insights in Molecular Biology 2008, 103-142. Caister Academic Press, Wymondham. G. San-Blas, R. Calderone (Eds.).
42. 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. 10.1074/mcp.M110.004010.
43. Rutjes A.W., Reitsma J.B., Vandenbroucke J.P., Glas A.S., Bossuyt P.M. Case-control and two-gate designs in diagnostic accuracy studies. Clin. Chem. 2005, 51:1335-1341.
44. Mischak H., Apweiler R., Banks R.E., Conaway M., Coon J., Dominiczak A., et al. Clinical proteomics: a need to define the field and to begin to set adequate standards. Proteomics Clin. Appl. 2007, 1:148-156.
45. Korevaar D.A., Wang J., van Enst W.A., Leeflang M.M., Hooft L., Smidt N., et al. Reporting diagnostic accuracy studies: some improvements after 10 years of STARD. Radiology 2015, 274:781-789.
46. Bruns D.E., Huth E.J., Magid E., Young D.S. Toward a checklist for reporting of studies of diagnostic accuracy of medical tests. Clin. Chem. 2000, 46:893-895.
47. Pitarch A., Nombela C., Gil C. Top-down characterization data on the speciation of the Candida albicans immunome in candidemia 2015, (Data in brief 2016).
48. Valdes I., Pitarch A., Gil C., Bermudez A., Llorente M., Nombela C., et al. Novel procedure for the identification of proteins by mass fingerprinting combining two-dimensional electrophoresis with fluorescent SYPRO red staining. J. Mass Spectrom. 2000, 35:672-682.
49. Pardo M., Ward M., Pitarch A., Sanchez M., Nombela C., Blackstock W., et al. Cross-species identification of novel Candida albicans immunogenic proteins by combination of two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Electrophoresis 2000, 21:2651-2659.
50. Pitarch A., Sanchez M., Nombela C., Gil C. Analysis of the Candida albicans proteome. II. Protein information technology on the Net (update 2002). J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2003, 787:129-148.
51. Pitarch A., Molero G., Moteoliva L., Thomas D.P., López-Ribot J.L., Nombela C., et al. Proteomics in Candida Species. Candida: Comparative and Functional Genomics 2007, 169-194. Caister Academic Press, Norfolk. C. d'Enfert, B. Hube (Eds.).
52. Chen J., Liu H., Yang J., Chou K.C. Prediction of linear B-cell epitopes using amino acid pair antigenicity scale. Amino Acids 2007, 33:423-428.
53. Suh M.J., Alami H., Clark D.J., Parmar P.P., Robinson J.M., Huang S.T., et al. Widespread occurrence of non-enzymatic deamidations of asparagine residues in Yersinia pestis proteins resulting from alkaline pH membrane extraction conditions. Open Proteomics J. 2008, 1:106-115.
54. 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.
55. Chaffin W.L. Candida albicans cell wall proteins. Microbiol. Mol. Biol. Rev. 2008, 72:495-544.
56. Pitarch A., Nombela C., Gil C. Collection of proteins secreted from yeast protoplasts in active cell wall regeneration. Methods Mol. Biol. 2008, 425:241-263.
57. Gil-Bona A., Parra-Giraldo C.M., Hernaez M.L., Reales-Calderon J.A., Solis N.V., Filler S.G., et al. Candida albicans cell shaving uncovers new proteins involved in cell wall integrity, yeast to hypha transition, stress response and host-pathogen interaction. J. Proteome 2015, 127:340-351.
58. Silva R.C., Padovan A.C., Pimenta D.C., Ferreira R.C., da Silva C.V., Briones M.R. Extracellular enolase of Candida albicans is involved in colonization of mammalian intestinal epithelium. Front. Cell. Infect. Microbiol. 2014, 4:66.
59. Monteoliva L., Martinez-Lopez R., Pitarch A., Hernaez M.L., Serna A., Nombela C., et al. Quantitative proteome and acidic subproteome profiling of Candida albicans yeast-to-hypha transition. J. Proteome Res. 2011, 10:502-517.
60. O'Meara T.R., Cowen L.E. Hsp90-dependent regulatory circuitry controlling temperature-dependent fungal development and virulence. Cell. Microbiol. 2014, 16:473-481.
61. Pitarch A., Nombela C., Gil C. Candida albicans biology and pathogenicity: insights from proteomics. Methods Biochem. Anal. 2006, 49:285-330.
62. Wilson D., Thewes S., Zakikhany K., Fradin C., Albrecht A., Almeida R., et al. Identifying infection-associated genes of Candida albicans in the postgenomic era. FEMS Yeast Res. 2009, 9:688-700.
63. 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.
64. Fradin C., De Groot P., MacCallum D., Schaller M., Klis F., Odds F.C., et al. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 2005, 56:397-415.
65. Kusch H., Engelmann S., Bode R., Albrecht D., Morschhauser J., Hecker M. A proteomic view of Candida albicans yeast cell metabolism in exponential and stationary growth phases. Int. J. Med. Microbiol. 2008, 298:291-318.
66. Mayer F.L., Wilson D., Hube B. Candida albicans pathogenicity mechanisms. Virulence 2013, 4:119-128.
67. 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.
68. Hernandez-Haro C., Llopis S., Molina M., Monteoliva L., Gil C. Immunoproteomic profiling of Saccharomyces cerevisiae systemic infection in a murine model. J. Proteome 2015, 112:14-26.
69. Jungblut P.R. The proteomics quantification dilemma. J. Proteome 2014, 107:98-102.
70. Jungblut P.R., Schluter H. Towards the analysis of protein species: an overview about strategies and methods. Amino Acids 2011, 41:219-222.
71. Hoehenwarter W., Ackermann R., Zimny-Arndt U., Kumar N.M., Jungblut P.R. The necessity of functional proteomics: protein species and molecular function elucidation exemplified by in vivo alpha a crystallin N-terminal truncation. Amino Acids 2006, 31:317-323.
72. van Els C.A., Corbiere V., Smits K., van Gaans-van den Brink J.A., Poelen M.C., Mascart F., et al. Toward understanding the essence of post-translational modifications for the Mycobacterium tuberculosis immunoproteome. Front. Immunol. 2014, 5:361.
73. Mochon A.B., Jin Y., Kayala M.A., Wingard J.R., Clancy C.J., Nguyen M.H., et al. Serological profiling of a Candida albicans protein microarray reveals permanent host-pathogen interplay and stage-specific responses during candidemia. PLoS Pathog. 2010, 6.
74. Hayman L., Steffen M.J., Stevens J., Badger E., Tempro P., Fuller B., et al. Smoking and periodontal disease: discrimination of antibody responses to pathogenic and commensal oral bacteria. Clin. Exp. Immunol. 2011, 164:118-126.
75. Jacobsen I.D., Wilson D., Wachtler B., Brunke S., Naglik J.R., Hube B. Candida albicans dimorphism as a therapeutic target. Expert Rev. Anti-Infect. Ther. 2012, 10:85-93.
76. Madi A., Kenett D.Y., Bransburg-Zabary S., Merbl Y., Quintana F.J., Boccaletti S., et al. Analyses of antigen dependency networks unveil immune system reorganization between birth and adulthood. Chaos 2011, 21:016109.
77. Bransburg-Zabary S., Kenett D.Y., Dar G., Madi A., Merbl Y., Quintana F.J., et al. Individual and meta-immune networks. Phys. Biol. 2013, 10:025003.
78. Ardizzoni A., Posteraro B., Baschieri M.C., Bugli F., Saez-Roson A., Manca L., et al. An antibody reactivity-based assay for diagnosis of invasive candidiasis using protein array. Int. J. Immunopathol. Pharmacol. 2014, 27:403-412.
79. Kouzmitcheva G.A., Petrenko V.A., Smith G.P. Identifying diagnostic peptides for Lyme disease through epitope discovery. Clin. Diagn. Lab. Immunol. 2001, 8:150-160.
80. Mitsutake K., Kohno S., Miyazaki T., Miyazaki H., Maesaki S., Koga H. Detection of Candida enolase antibody in patients with candidiasis. J. Clin. Lab. Anal. 1994, 8:207-210.
81. Lain A., Moragues M.D., Ruiz J.C., Mendoza J., Camacho A., Del Palacio A., et al. Evaluation of a novel enzyme-linked immunosorbent assay to detect immunoglobulin G antibody to enolase for serodiagnosis of invasive candidiasis. Clin. Vaccine Immunol. 2007, 14:318-319.
82. Li F.Q., Ma C.F., Shi L.N., Lu J.F., Wang Y., Huang M., et al. Diagnostic value of immunoglobulin G antibodies against Candida enolase and fructose-bisphosphate aldolase for candidemia. BMC Infect. Dis. 2013, 13:253.
83. van Deventer A.J., van Vliet H.J., Hop W.C., Goessens W.H. Diagnostic value of anti-Candida enolase antibodies. J. Clin. Microbiol. 1994, 32:17-23.
84. Pitarch A., Nombela C., Gil C. Reliability of antibodies to Candida methionine synthase for diagnosis, prognosis and risk stratification in systemic candidiasis: a generic strategy for the prototype development phase of proteomic markers. Proteomics Clin. Appl. 2007, 1:1221-1242.
85. Bromuro C., La Valle R., Sandini S., Urbani F., Ausiello C.M., Morelli L., et al. A 70-kilodalton recombinant heat shock protein of Candida albicans is highly immunogenic and enhances systemic murine candidiasis. Infect. Immun. 1998, 66:2154-2162.
86. Peterson P., Perheentupa J., Krohn K.J. Detection of candidal antigens in autoimmune polyglandular syndrome type I. Clin. Diagn. Lab. Immunol. 1996, 3:290-294.
87. Chou H., Tam M.F., Chang C.Y., Lai H.Y., Huang M.H., Chou C.T., et al. Characterization of a novel Candida albicans 29 kDa IgE-binding protein - purification, cDNA isolation and heterologous expression of Cand a 3. Allergy 2003, 58:1157-1164.
88. Shibasaki S., Aoki W., Nomura T., Karasaki M., Sewaki T., Ueda M. Evaluation of Mdh1 protein as an antigenic candidate for a vaccine against candidiasis. Biocontrol Sci. 2014, 19:51-55.
89. Xin H., Dziadek S., Bundle D.R., Cutler J.E. Synthetic glycopeptide vaccines combining beta-mannan and peptide epitopes induce protection against candidiasis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13526-13531.
90. Xin H., Cutler J.E. Vaccine and monoclonal antibody that enhance mouse resistance to candidiasis. Clin. Vaccine Immunol. 2011, 18:1656-1667.
91. Li W., Hu X., Zhang X., Ge Y., Zhao S., Hu Y., et al. Immunisation with the glycolytic enzyme enolase confers effective protection against Candida albicans infection in mice. Vaccine 2011, 29:5526-5533.
92. Raska M., Belakova J., Wudattu N.K., Kafkova L., Ruzickova K., Sebestova M., et al. Comparison of protective effect of protein and DNA vaccines Hsp90 in murine model of systemic candidiasis. Folia Microbiol. 2005, 50:77-82.
93. Hanley J.A., McNeil B.J. A method of comparing the areas under receiver operating characteristic curves derived from the same cases. Radiology 1983, 148:839-843.