Differential proteomic analysis of Aspergillus fumigatus morphotypes reveals putative drug targets

Journal of Proteomics

Volumn 78, Issue , 2013, Pages 522-534

  Kubitschek Barreira, Paula H ^a   Curty, Nathalia ^a   Neves, Gabriela W P ^a   Gil, Concha ^b   Lopes Bezerra, Leila M ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

2D DIGE; Aspergillus fumigatus; Cell surface proteins; Morphogenesis; Proteome

Indexed keywords

CELL SURFACE PROTEIN; CIPC LIKE PROTEIN; FUNGAL PROTEIN; PROTEIN EEF3; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS FUMIGATUS; BIOSYNTHESIS; CELL VIABILITY; DRUG TARGETING; FUNGAL STRAIN; FUNGUS HYPHAE; GERMINATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MORPHOGENESIS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; WESTERN BLOTTING;

ACUTE DISEASE; ANTIFUNGAL AGENTS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; BONE MARROW TRANSPLANTATION; DRUG DELIVERY SYSTEMS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; HYPHAE; LEUKEMIA; NEUTROPENIA; PROTEOMICS; RISK FACTORS; SPORES, FUNGAL;

ASPERGILLUS FUMIGATUS; MAMMALIA;

EID: 84872760557     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.10.022     Document Type: Article

References (61)

1. Latgé J.P. Aspergillus fumigatus, a saprotrophic pathogenic fungus. Mycologist 2003, 17:56-61.
2. Hope W.W., Walsh T.J., Denning D.W. The invasive and saprophytic syndromes due to Aspergillus spp. Med Mycol 2005, 43:207-238.
3. Maschmeyer G., Haas A., Cornely O.A. Invasive aspergillosis: epidemiology, diagnosis and management in immunocompromised patients. Int J Antimicrob Agents 2007, 31(3):193-197.
4. Denning D.W. Invasive aspergillosis. Clin Infect Dis 1998, 26:781-805.
5. Lopes-Bezerra L.M., Filler S.G. Interactions of Aspergillus fumigatus with endothelial cells: internalization, injury, and stimulation of tissue factor activity. Blood 2004, 103:2143-2149.
6. Kamai Y., Lossinsky A.S., Liu H., Sheppard D.C., Filler S.G. Polarized response of endothelial cells to invasion by Aspergillus fumigatus. Cell Microbiol 2009, 11(1):170-182.
7. López-Ribot J.L., Alloush H.M., Masten B.J., Chaffin W.L. Evidence for presence in the cell wall of Candida albicans of a protein related to the hsp70 family. Infect Immun 1996, 64:3333-3340.
8. Yuan S.Y. Protein kinase signalling in the modulation of microvascular permeability. Vasc Pharmacol 2002, 39:213-223.
9. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature Lond 1970, 227:680-685.
10. Pardo M., Ward M., Bains S., Molina M., Blackstock W., Gil C., et al. A proteomic approach for the study of Saccharomyces cerevisiae cell wall biogenesis. Electrophoresis 2000, 21:3396-3410.
11. 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.
12. Lum G., Min X.J. FunSecKB: the Fungal Secretome KnowledgeBase. Database (Oxford) 2011, 6.
13. Chaudhuri R., Ansari F.A., Raghunandanan M.V., Ramachandran S. FungalRV: adhesin prediction and immunoinformatics portal for human fungal pathogens. BMC Genomics 2011, 12:192.
14. Von Mering C., Jensen L.J., Snel B., Hooper S.D., Krupp M., Foglierini M., et al. STRING: known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res 2005, 33:433-437.
15. Millard P.J., Roth B.L., Thi H.P., Yue S.T., Haugland R.P. Development of the FUN-1 family of fluorescent probes for vacuole labeling and viability testing of yeasts. Appl Environ Microbiol 1997, 63:2897-2905.
16. Shaw J.A., Mol P.C., Bowers B., Silverman S.J., Valdivieso M.H., Duran A., et al. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J Cell Biol 1991, 114:111-123.
17. Daniels G.M., Amara S.G. Selective labeling of neurotransmitter transporters at the cell surface. Methods Enzymol 1998, 296:307-318.
18. Rohde M., Schwienbacher M., Nikolaus T., Heesemann J., Ebel F. Detection of early phase specific surface appendages during germination of Aspergillus fumigatus conidia. FEMS Microbiol Lett 2002, 206(1):99-105.
19. Latgé J.P. Tasting the fungal cell wall. Cell Microbiol 2010, 12(7):863-872.
20. Klis F.M., de Jong M., Brul S., de Groot P.W. Extraction of cell surface-associated proteins from living yeast cells. Yeast 2007, 24:253-258.
21. Rodrigues M.L., Nosancuk J.D., Schrank A., Vainstein M.H., Casadevall A., Nimrichter L. Vesicular transport systems in fungi. Future Microbiol 2011, 6(11):1371-1381.
22. Glaser A.G., Kirsh A.I., Zeller S., Menz G., Rhyner C., Grameri R. Molecular and immunological characterization of Aspf34, a novel major cell wall allergen of Aspergillus fumigatus. Allergy 2009, 64:1144-1151.
23. Kinoshita H., Wakahara N., Watanabe M., Kawasaki T., Matsuo H., Kawai Y., et al. Cell surface glyceraldehyde-3-phosphate dehydrogenase (GAPDH) of Lactobacillus plantarum LA 318 recognizes human A and B blood group antigens. Res Microbiol 2008, 159:685-691.
24. Li W.Q., Hu X.C., 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(33):5526-5533.
25. Donofrio F.C., Calil A.C., Miranda E.T., Almeida A.M., Bernard G., Soares C.P., et al. Paracoccidioides brasiliensis enolase is a surface protein that binds plasminogen and mediates interaction of yeast forms with host cells. J Med Microbiol 2009, 58:706-713.
26. Pitarch A., Jiménez 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.
27. Esgleas M., Li Y., Hancock M.A., Harel J., Dubreuil J.D., Gottschalk M. Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 2008, 154:2668-2679.
28. Chen H., Yu S., Shen X., Chen D., Qiu X., Song C., et al. The Mycoplasma gallisepticum α-enolase is cell surface-exposed and mediates adherence by binding to chicken plasminogen. Microb Pathog 2011, 51(4):285-290.
29. Pal-Bhowmick I., Mehta M., Coppens I., Sharma S., Jarori G.K. Protective properties and surface localization of Plasmodium falciparum enolase. Infect Immun 2007, 75:5500-5508.
30. Denikus N., Orfaniotou F., Wulf G., Lehmann P.F., Monod M., Reichard U. Fungal antigens expressed during invasive aspergillosis. Infect Immun 2005, 73:4704-4713.
31. Gozalbo D., Gil Navarro I., Azorín I., Renau-Piqueras J., Martínez 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.
32. Maeda K., Nagata H., Kuboniwa M., Kataoka K., Nishida N., Tanaka M., et al. Characterization of binding of Streptococcus oralis glyceraldehyde-3-phosphate dehydrogenase to Porphyromonas gingivalis major fimbriae. Infect Immun 2004, 72:1341-1348.
33. Barbosa M.S., Báo S.N., Andreotti P.F., de Faria F.P., Felipe M.S., dos Santos Feitosa L., et al. Glyceraldehyde-3-phosphate dehydrogenase of Paracoccidioides brasiliensis is a cell surface protein involved in fungal adhesion to extracellular matrix proteins and interaction with cells. Infect Immun 2006, 74:382-389.
34. Liu M., Gelli A. Elongation factor 3, EF3, associates with the calcium channel Cch1 and targets Cch1 to the plasma membrane in Cryptococcus neoformans. Eukaryot Cell 2008, 7:1118-1126.
35. Anand M., Balar B., Ulloque R., Gross S.R., Kinzy T.G. Domain and nucleotide dependence of the interaction between Saccharomyces cerevisiae translation elongation factors 3 and 1A. J Biol Chem 2006, 281:32318-32326.
36. Olarewaju O., Ortiz P.A., Chowdhury W.Q., Chatterjee I., Kinzy T.G. The translation elongation factor eEF1B plays a role in the oxidative stress response pathway. RNA Biol 2004, 1:89-94.
37. Amiri A., Noei F., Jeganathan S., Kulkarni G., Pinke D.E., Lee J.M. eEF1A2 activates Akt and stimulates Akt-dependent actin remodeling, invasion and migration. Oncogene 2007, 26:3027-3040.
38. Dayton J.S., Sumi M., Nanthakumar N.N., Means A.R. Expression of a constitutively active Ca2+/calmodulin-dependent kinase in Aspergillus nidulans spores prevents germination and entry into the cell cycle. J Biol Chem 1997, 272:3223-3230.
39. Joseph J.D., Means A.R. Identification and characterization of two Ca2+/CaM-dependent protein kinases required for normal nuclear division in Aspergillus nidulans. J Biol Chem 2000, 275:38230-38238.
40. Sebghati T.S., Engle J.T., Goldman W.E. Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science 2000, 290:1368-1372.
41. Blankenship J.R., Wormley F.L., Boyce M.K., Schell W.A., Filler S.G., Perfect J.R., et al. Calcineurin is essential for Candida albicans survival in serum and virulence. Eukaryot Cell 2003, 2:422-430.
42. Sanglard D., Ischer F., Marchetti O., Entenza J., Bille J. Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol Microbiol 2003, 48:959-976.
43. Bencina M., Legisa M., Read N.D. Cross-talk between cAMP and calcium signalling in Aspergillus niger. Mol Microbiol 2005, 56:268-281.
44. Kraus P.R., Nichols C.B., Heitman J. Calcium- and calcineurin-independent roles for calmodulin in Cryptococcus neoformans morphogenesis and high-temperature growth. Eukaryot Cell 2003, 4:1079-1087.
45. Liu M., Du P., Heinrich G., Cox G.M., Gelli A. Cch1 mediates calcium entry in Cryptococcus neoformans and is essential in low-calcium environments. Eukaryot Cell 2006, 5:1788-1796.
46. Hallen H.E., Trail F. The L-type calcium ion channel cch1 affects ascospore discharge and mycelial growth in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot Cell 2008, 7:415-424.
47. Bauer B., Schwienbacher M., Broniszewska M., Israel L., Heesemann J., Ebel F. Characterisation of the CipC-like protein AFUA_5G09330 of the opportunistic human pathogenic mould Aspergillus fumigatus. Mycoses 2010, 53:296-304.
48. Böhmer M., Colby T., Böhmer C., Bräutigam A., Schmidt J., Bölker M. Proteomic analysis of dimorphic transition in the phytopathogenic fungus Ustilago maydis. Proteomics 2007, 7:675-685.
49. Melin P., Schnürer J., Wagner E.G. Characterization of phiA, a gene essential for phialide development in Aspergillus nidulans. Fungal Genet Biol 2003, 40:234-241.
50. Cowen L.E., Lindquist S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 2005, 309:2185-2189.
51. Cowen L.E., Singh S.D., Köhler J.R., Collins C., Zaas A.K., Schell W.A., et al. Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc Natl Acad Sci U S A 2009, 106:2818-2823.
52. Shapiro R.S., Robbins N., Cowen L.E. Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev 2011, 75:213-267.
53. Lambou K., Lamarre C., Beau R., Dufour N., Latge J.P. Functional analysis of the superoxide dismutase family in Aspergillus fumigatus. Mol Microbiol 2010, 75:910-923.
54. Schwienbacher M., Israel L., Heesemann J., Ebel F. Asp f6, an Aspergillus allergen specifically recognized by IgE from patients with allergic bronchopulmonary aspergillosis, is differentially expressed during germination. Allergy 2005, 60:1430-1435.
55. Nombela C., Gil C., Chaffin W.L. Non-conventional protein secretion in yeast. Trends Microbiol 2006, 14:15-21.
56. Naglik J.R., Challacombe S.J., Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 2003, 67:400-428.
57. Eroles P., Sentandreu M., Elorza M.V., Sentandreu R. The highly immunogenic enolase and Hsp70p are adventitious Candida albicans cell wall proteins. Microbiology 1997, 143:313-320.
58. 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.
59. Albuquerque P.C., Nakayasu E.S., Rodrigues M.L., Frases S., Casadevall A., Zancope-Oliveira R.M., et al. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 2008, 10:1695-1710.
60. Rodrigues M.L., Nakayasu E.S., Oliveira D.L., Nimrichter L., Nosanchuk J.D., Almeida I.C., et al. Extracellular vesicles produced by Cryptococcus neoformans contains protein components associated with virulence. Eukaryot Cell 2008, 7:58-67.
61. Casadevall A., Nosanchuk J.D., Williamson P., Rodrigues M.L. Vesicular transport across fungal cell wall. Trends Microbiol 2009, 17:158-162.