Vesicular mechanisms of traffic of fungal molecules to the extracellular space

Current Opinion in Microbiology

Volumn 16, Issue 4, 2013, Pages 414-420

  Rodrigues, Marcio L ^a,b   Franzen, Anderson J ^d   Nimrichter, Leonardo ^b   Miranda, Kildare ^b,c  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c INSTITUTO NACIONAL DE METROLOGIA   (Brazil)

^d Laboratory of Research in Environmental Biotechnology   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CELL MEMBRANE; CELL VACUOLE; CRYPTOCOCCUS NEOFORMANS; CYTOPLASM; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; EXTRACELLULAR SPACE; FUNGAL CELL; FUNGUS GROWTH; NONHUMAN; PARACOCCIDIOIDES BRASILIENSIS; REVIEW; SACCHAROMYCES CEREVISIAE;

EXOSOMES; FUNGAL PROTEINS; FUNGI;

EID: 84882923976     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2013.04.002     Document Type: Review

References (52)

1. Schekman R. Charting the secretory pathway in a simple eukaryote. Mol Biol Cell 2010, 21:3781-3784.
2. Lyman S.K., Schekman R. Polypeptide translocation machinery of the yeast endoplasmic reticulum. Experientia 1996, 52:1042-1049.
3. Schekman R.W. Regulation of membrane traffic in the secretory pathway. Harvey Lect 1994, 90:41-57.
4. Stephens C. Protein secretion: getting folded proteins across membranes. Curr Biol 1998, 8:R578-R581.
5. Rabouille C., Malhotra V., Nickel W. Diversity in unconventional protein secretion. J Cell Sci 2012, 125:5251-5255.
6. Nickel W. Pathways of unconventional protein secretion. Curr Opin Biotechnol 2010, 21:621-626.
7. Nickel W., Rabouille C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009, 10:148-155.
8. Nickel W. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 2003, 270:2109-2119.
9. Ding Y., Wang J., Wang J., Stierhof Y.D., Robinson D.G., Jiang L. Unconventional protein secretion. Trends Plant Sci 2012, 17:606-615.
10. Giuliani F., Grieve A., Rabouille C. Unconventional secretion: a stress on GRASP. Curr Opin Cell Biol 2011, 23:498-504.
11. Nimrichter L., Rodrigues M.L., Rodrigues E.G., Travassos L.R. The multitude of targets for the immune system and drug therapy in the fungal cell wall. Microbes Infect 2005, 7:789-798.
12. Rodrigues M.L., Nosanchuk J.D., Schrank A., Vainstein M.H., Casadevall A., Nimrichter L. Vesicular transport systems in fungi. Future Microbiol 2011, 6:1371-1381.
13. Vallejo M.C., Nakayasu E.S., Matsuo A.L., Sobreira T.J., Longo L.V., Ganiko L., Almeida I.C., Puccia R. Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: comparative analysis with other pathogenic fungi. J Proteome Res 2012, 11:1676-1685.
14. Sorgo A.G., Heilmann C.J., Dekker H.L., Brul S., de Koster C.G., Klis F.M. Mass spectrometric analysis of the secretome of Candida albicans. Yeast 2010, 27:661-672.
15. Weber S.S., Parente A.F., Borges C.L., Parente J.A., Bailao A.M., de Almeida Soares C.M. Analysis of the secretomes of Paracoccidioides mycelia and yeast cells. PLoS ONE 2012, 7:e52470.
16. Albuquerque P.C., Nakayasu E.S., Rodrigues M.L., Frases S., Casadevall A., Zancope-Oliveira R.M., Almeida I.C., Nosanchuk J.D. 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.
17. Rodrigues M.L., Nakayasu E.S., Oliveira D.L., Nimrichter L., Nosanchuk J.D., Almeida I.C., Casadevall A. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 2008, 7:58-67.
18. Oliveira D.L., Nakayasu E.S., Joffe L.S., Guimaraes A.J., Sobreira T.J., Nosanchuk J.D., Cordero R.J., Frases S., Casadevall A., Almeida I.C., et al. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS ONE 2010, 5:e11113.
19. Queiroz-Telles F., Escuissato D.L. Pulmonary paracoccidioidomycosis. Semin Respir Crit Care Med 2011, 32:764-774.
20. Park B.J., Wannemuehler K.A., Marston B.J., Govender N., Pappas P.G., Chiller T.M. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 2009, 23:525-530.
21. Sorgo A.G., Heilmann C.J., Brul S., de Koster C.G., Klis F.M. Beyond the wall: Candida albicans secret(e)s to survive. FEMS Microbiol Lett 2013, 338:10-17.
22. Ene I.V., Heilmann C.J., Sorgo A.G., Walker L.A., de Koster C.G., Munro C.A., Klis F.M., Brown A.J. Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans. Proteomics 2012, 12:3164-3179.
23. Sorgo A.G., Heilmann C.J., Dekker H.L., Bekker M., Brul S., de Koster C.G., de Koning L.J., Klis F.M. Effects of fluconazole on the secretome, the wall proteome, and wall integrity of the clinical fungus Candida albicans. Eukaryot Cell 2011, 10:1071-1081.
24. Kubitschek-Barreira P.H., Curty N., Neves G.W., Gil C., Lopes-Bezerra L.M. Differential proteomic analysis of Aspergillus fumigatus morphotypes reveals putative drug targets. J Proteomics 2013, 78:522-534.
25. Zaragoza O., Rodrigues M.L., De Jesus M., Frases S., Dadachova E., Casadevall A. The capsule of the fungal pathogen Cryptococcus neoformans. Adv Appl Microbiol 2009, 68:133-216.
26. Gomez B.L., Nosanchuk J.D. Melanin and fungi. Curr Opin Infect Dis 2003, 16:91-96.
27. Santos A.L., Palmeira V.F., Rozental S., Kneipp L.F., Nimrichter L., Alviano D.S., Rodrigues M.L., Alviano C.S. Biology and pathogenesis of Fonsecaea pedrosoi, the major etiologic agent of chromoblastomycosis. FEMS Microbiol Rev 2007, 31:570-591.
28. Huang S.H., Wu C.H., Chang Y.C., Kwon-Chung K.J., Brown R.J., Jong A. Cryptococcus neoformans-derived microvesicles enhance the pathogenesis of fungal brain infection. PLoS ONE 2012, 7:e48570.
29. Oliveira D.L., Freire-de-Lima C.G., Nosanchuk J.D., Casadevall A., Rodrigues M.L., Nimrichter L. Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect Immun 2010, 78:1601-1609.
30. Vallejo M.C., Nakayasu E.S., Longo L.V., Ganiko L., Lopes F.G., Matsuo A.L., Almeida I.C., Puccia R. Lipidomic analysis of extracellular vesicles from the pathogenic phase of Paracoccidioides brasiliensis. PLoS ONE 2012, 7:e39463.
31. Robertson E.J., Wolf J.M., Casadevall A. EDTA inhibits biofilm formation, extracellular vesicular secretion, and shedding of the capsular polysaccharide glucuronoxylomannan by Cryptococcus neoformans. Appl Environ Microbiol 2012, 78:7977-7984.
32. Wolf J.M., Rivera J., Casadevall A. Serum albumin disrupts Cryptococcus neoformans and Bacillus anthracis extracellular vesicles. Cell Microbiol 2012, 14:762-773.
33. Rodrigues M.L., Djordjevic J.T. Unravelling secretion in Cryptococcus neoformans: more than one way to skin a cat. Mycopathologia 2012, 173:407-418.
34. Albuquerque P.C., Cordero R.J., Fonseca F.L., Peres da Silva R., Ramos C.L., Miranda K.R., Casadevall A., Puccia R., Nosanchuk J.D., Nimrichter L., et al. A Paracoccidioides brasiliensis glycan shares serologic and functional properties with cryptococcal glucuronoxylomannan. Fungal Genet Biol 2012, 49:943-954.
35. Vallejo M.C., Matsuo A.L., Ganiko L., Medeiros L.C., Miranda K., Silva L.S., Freymuller-Haapalainen E., Sinigaglia-Coimbra R., Almeida I.C., Puccia R. The pathogenic fungus Paracoccidioides brasiliensis exports extracellular vesicles containing highly immunogenic alpha-Galactosyl epitopes. Eukaryot Cell 2011, 10:343-351.
36. Gehrmann U., Qazi K.R., Johansson C., Hultenby K., Karlsson M., Lundeberg L., Gabrielsson S., Scheynius A. Nanovesicles from Malassezia sympodialis and host exosomes induce cytokine responses - novel mechanisms for host-microbe interactions in atopic eczema. PLoS ONE 2011, 6:e21480.
37. Oliveira D.L., Nakayasu E.S., Joffe L.S., Guimaraes A.J., Sobreira T.J., Nosanchuk J.D., Cordero R.J., Frases S., Casadevall A., Almeida I.C., et al. Biogenesis of extracellular vesicles in yeast: many questions with few answers. Commun Integr Biol 2010, 3:533-535.
38. Oliveira D.L., Nimrichter L., Miranda K., Frases S., Faull K.F., Casadevall A., Rodrigues M.L. Cryptococcus neoformans cryoultramicrotomy and vesicle fractionation reveals an intimate association between membrane lipids and glucuronoxylomannan. Fungal Genet Biol 2009, 46:956-963.
39. Eisenman H.C., Frases S., Nicola A.M., Rodrigues M.L., Casadevall A. Vesicle-associated melanization in Cryptococcus neoformans. Microbiology 2009, 155:3860-3867.
40. Casadevall A., Nosanchuk J.D., Williamson P., Rodrigues M.L. Vesicular transport across the fungal cell wall. Trends Microbiol 2009, 17:158-162.
41. Panepinto J., Komperda K., Frases S., Park Y.D., Djordjevic J.T., Casadevall A., Williamson P.R. Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol Microbiol 2009, 71:1165-1176.
42. Nicola A.M., Frases S., Casadevall A. Lipophilic dye staining of Cryptococcus neoformans extracellular vesicles and capsule. Eukaryot Cell 2009, 8:1373-1380.
43. Nosanchuk J.D., Nimrichter L., Casadevall A., Rodrigues M.L. A role for vesicular transport of macromolecules across cell walls in fungal pathogenesis. Commun Integr Biol 2008, 1:37-39.
44. Rodrigues M.L., Nimrichter L., Oliveira D.L., Nosanchuk J.D., Casadevall A. Vesicular trans-cell wall transport in fungi: a mechanism for the delivery of virulence-associated macromolecules?. Lipid Insights 2008, 2:27-40.
45. Rodrigues M.L., Nimrichter L., Oliveira D.L., Frases S., Miranda K., Zaragoza O., Alvarez M., Nakouzi A., Feldmesser M., Casadevall A. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell 2007, 6:48-59.
46. Kmetzsch L., Joffe L.S., Staats C.C., de Oliveira D.L., Fonseca F.L., Cordero R.J., Casadevall A., Nimrichter L., Schrank A., Vainstein M.H., et al. Role for Golgi reassembly and stacking protein (GRASP) in polysaccharide secretion and fungal virulence. Mol Microbiol 2011, 81:206-218.
47. De Jesus M., Nicola A.M., Rodrigues M.L., Janbon G., Casadevall A. Capsular localization of the Cryptococcus neoformans polysaccharide component galactoxylomannan. Eukaryot Cell 2009, 8:96-103.
48. Hu G., Kronstad J.W. A putative P-type ATPase, Apt1, is involved in stress tolerance and virulence in Cryptococcus neoformans. Eukaryot Cell 2010, 9:74-83.
49. Kukulski W., Schorb M., Kaksonen M., Briggs J.A. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 2012, 150:508-520.
50. Lim J.P., Gleeson P.A. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol Cell Biol 2011, 89:836-843.
51. Dubois J.M., Rouzaire-Dubois B. Roles of cell volume in molecular and cellular biology. Prog Biophys Mol Biol 2012, 108:93-97.
52. 2+-induced biochemical changes in human erythrocytes and their relation to microvesiculation. Biochem J 1981, 198:433-440.