Quantitative proteomics of extracellular vesicles released from human monocyte-derived macrophages upon β-glucan stimulation

Journal of Proteome Research

Volumn 13, Issue 5, 2014, Pages 2468-2477

  Cypryk, Wojciech ^a   Öhman, Tiina ^a   Eskelinen, Eeva Liisa ^b   Matikainen, Sampsa ^c   Nyman, Tuula A ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c FINNISH INSTITUTE OF OCCUPATIONAL HEALTH   (Finland)

Author keywords

Dectin 1; extracellular vesicle; macrophage; quantitative proteomics; glucan

Indexed keywords

BETA GLUCAN; INTEGRIN; INTERLEUKIN 1BETA; MEMBRANE PROTEIN; PURINERGIC P2X7 RECEPTOR; SCAVENGER RECEPTOR; SOMATOMEDIN B RECEPTOR; PROTEIN; PROTEOME;

ARTICLE; BIOINFORMATICS; CELL DIFFERENTIATION; CELL STIMULATION; CELL VACUOLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOPLASM; FUNGAL CELL WALL; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROPHAGE; MASS SPECTROMETRY; MEMBRANE STRUCTURE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; PROTEOMICS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; ELECTRON MICROSCOPY; LIQUID CHROMATOGRAPHY; METABOLISM; MONOCYTE; PROCEDURES; SECRETION (PROCESS); SECRETORY VESICLE; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; ULTRASTRUCTURE; WESTERN BLOTTING;

BETA-GLUCANS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; HUMANS; MACROPHAGES; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MONOCYTES; PROTEINS; PROTEOME; PROTEOMICS; SECRETORY VESICLES; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 84899844127     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4012552     Document Type: Article

References (48)

1. Auberger, J.; Lass-Flörl, C.; Aigner, M.; Clausen, J.; Gastl, G.; Nachbaur, D. Invasive fungal breakthrough infections, fungal colonization and emergence of resistant strains in high-risk patients receiving antifungal prophylaxis with posaconazole: real-life data from a single-centre institutional retrospective observational study J. Antimicrob. Chemother. 2012, 67 (9) 2268-73
2. Romani, L. Immunity to fungal infections Nat. Rev. Immunol. 2011, 11, 275-88
3. Means, T. K.; Mylonakis, E.; Tampakakis, E.; Colvin, R. A.; Seung, E.; Puckett, L.; Tai, M. F.; Stewart, C. R.; Pukkila-Worley, R.; Hickman, S. E.; Moore, K. J.; Calderwood, S. B.; Hacohen, N.; Luster, A. D.; Khoury, J. E. Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36 J. Exp Med. 2009, 206 (3) 637-53
4. Thornton, B. P.; Vetvicka, V.; Pitman, M.; Goldman, R. C.; Ross, G. D. Analysis of the sugar specificity and molecular location of β-glucan- binding lectin site of complement receptor type 3 (CD11D/CD18) J. Immunol. 1996, 156, 1235-46
5. Zhu, L.-L.; Zhao, X.-Q.; Jiang, C.; You, Y.; Chen, X.-P.; Jiang, Y.-Y.; Jia, X.-M.; Lin, X. C-type lectin receptors dectin-3 and dectin-2 form a heterodimeric pattern-recognition receptor for defense against fungal infection Immunity 2013, 39, 324-34
6. Lam, J. S.; Huang, H.; Levitz, S. M. Effect of differential N-linked and O-linked mannosylation on recognition of fungal antigens by dendritic cells PLoS One 2007, 2, e33297 10.1371/journal.pone.0001009
7. Cambi, A.; Netea, M. G.; Mora-Montes, H. M.; Gow, N. A. R.; Hato, S. V.; Lowman, D. W.; Kullberg, B.-J.; Torensma, R.; Williams, D. L.; Figdor, C. G. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan J. Biol. Chem. 2008, 283, 20590-9
8. Record, M.; Carayon, K.; Poirot, M.; Silvente-Poirot, S. Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2014, 1841, 108-20
9. Robbins, P. D.; Morelli, A. E. Regulation of immune responses by extracellular vesicles Nat. Rev. Immunol. 2014, 14, 195-208
10. Raposo, G.; Stoorvogel, W. Extracellular vesicles: exosomes, microvesicles and friends J. Cell. Biol. 2013, 200, 373-83
11. Pan, B. T.; Teng, K.; Wu, C.; Adam, M.; Johnstone, R. M. Electron microscopic evidence for externalization of the transferring receptor in vesicular form in sheep reticulocytes J. Cell. Biol. 1985, 101, 942-8
12. Chaput, N.; Théry, C. Exosomes: immune properties and potential clinical implementations Semin. Immunopathol. 2011, 33, 419-40
13. Lässer, C.; Aikhani, V. S.; Ekström, K.; Eldh, M.; Parredes, P. T.; Bossios, A.; Sjörstrand, M.; Gabrielsson, S.; Lötvall, J.; Valadi, H. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages J. Transl. Med. 2011, 9, 1-8
14. Ross, P. L.; Huang, Y. N.; Marchese, J. N.; Williamson, B.; Parker, K.; Hattan, S.; Khainovski, N.; Pillai, S.; Dey, S.; Daniels, S.; Purkayastha, S.; Juhasz, P.; Martin, S.; Bartlet-Jones, M.; He, F.; Jacobson, A.; Pappin, D. J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents Mol. Cell. Proteomics 2004, 3, 1154-69
15. Pirhonen, J.; Sareneva, T.; Kurimoto, M.; Julkunen, I.; Matikainen, S. Virus infection activates IL-1 β and IL-18 production in human macrophages by a caspase-1-dependent pathway J. Immunol. 1999, 162, 7322-9
16. Théry, C.; Clayton, A.; Amigorena, S.; Raposo, G. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. In Current Protocols in Cell Biology; Bonifacino, J. S.; Dasson, M.; Harford, J. B.; Lippincott-Schwartz, J.; Yamada, K. M., Eds.; Wiley: Hoboken, NJ, 2006; Unit 3.22, pp 1-29
17. Lietzén, N.; Öhman, T.; Rintahaka, J.; Julkunen, I.; Aittokallio, T.; Matikainen, S.; Nyman, T. A. Quantitative subcellular proteome and secretome profiling of influenza A virus-infected human primary macrophages PLoS Pathog. 2011, 7, e1001340 10.1371/journal.ppat.1001340
18. Öhman, T.; Lietzén, N.; Välimäki, E.; Melchjorsen, J.; Matikainen, S.; Nyman, T. A. Cytosolic RNA recognition pathway activates 14-3-3 protein mediated signaling and caspase-dependent disruption of cytokeratin network in human keratinocytes J. Proteome Res. 2010, 9, 1549-64
19. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4, 207-14
20. Vizcaíno, J. A.; Côté, R. G.; Csordas, A.; Dianes, J. A.; Fabregat, A.; Foster, J. M.; Griss, J.; Alpi, E.; Birim, M.; Contell, J.; O'Kelly, J.; Schoenegger, A.; Ovelleiro, D.; Pérez-Riverol, Y.; Reisinger, F.; Ríos, D.; Wang, R.; Hermjakob, H. The Proteomics Identifications (PRIDE) database and associated tools: status in 2013 Nucleic Acids Res. 2013, 41 (D1) D1063-9
21. Mathivanan, S.; Simpson, R. J. ExoCarta: a compendium of exosomal proteins and RNA Proteomics 2009, 9, 4997-5000
22. Mathivanan, S.; Fahner, C. J.; Reis, G. E.; Simpson, R. J. ExoCarta 2012: database of exosomal proteins, RNA and lipids Nucleic Acids Res. 2012, 40, D1241-4
23. Nordahl, T.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions Nat. Methods 2011, 8, 785-786
24. Zhang, B.; Kirov, S. A.; Snoddy, J. R. WebGestalt: an integrated system for exploring gene sets in various biological contexts Nucleic Acids Res. 2005, 33, W741-8
25. Wang, J.; Duncan, D.; Shi, Z.; Zhang, B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013 Nucleic Acids Res. 2013, 41, W77-83
26. Becker, L.; Liu, N.-C.; Averill, M. M.; Yuan, W.; Pamir, M.; Peng, Y.; Irwin, A. D.; Fu, X.; Bornfeldt, K. E.; Heinecke, J. W. Unique proteomic signature distinguish macrophages and dendritic cells PLoS One 2012, 7, e33297 10.1371/journal.pone.0033297
27. Kim, C.; Ye, F.; Ginsberg, M. H. Regulation of intregrin activation Annu. Rev. Cell Dev. Biol. 2011, 27, 321-45
28. Underhill, D. M.; Rossnagle, E.; Lowell, C. A.; Simmons, R. M. Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production Blood 2005, 106, 2543-2550
29. Lee, Y.; Andaloussi, S. E. L.; Wood, M. J. A. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy Hum. Mol. Genet. 2012, 21, R125-34 10.1093/hmg/dds317
30. MacKenzie, A.; Wilson, A. L.; Kiss-Toth, E.; Dower, S. K.; North, R. A.; Suprenant, A. Rapid secretion of interleukin-1β by microvesicle shedding Immunity 2001, 15, 825-35
31. Feng, Y. H.; Wang, L.; Wang, Q.; Li, X.; Zeng, R.; Gorodeski, G. I. ATP stimulates GRK-3 phosphorylation and β-arrestin-2-dependent internalization of P2X7 receptor Am. J. Physiol.: Cell Physiol. 2005, 288, C1342-56 10.1152/ajpcell.00315.2004
32. Kankkunen, P.; Teirilä, L.; Rintahaka, J.; Alenius, H.; Wolff, H.; Matikainen, S. 1,3)-β-glucans activate both Dectin-1 and NLRP3 inflammasome in human macrophages J. Immunol. 2010, 184, 6335-42
33. Théry, C.; Ostrowski, M.; Segura, E. Membrane vesicles as conveyors of immune responses Nat. Rev. Immunol. 2009, 9, 581-93
34. Clayton, A.; Turkes, A.; Dewitt, S.; Steadman, R.; Mason, M. D.; Hallett, M. B. Adhesion and signaling by B cell-derived exosomes: the role of integrins FASEB J. 2004, 18, 977-9
35. Rieu, S.; Géminard, C.; Rabesandratana, H.; Sainte-Marie, J.; Vidal, M. Exosomes released during reticulocyte maturation bind to fibronectin via integrin α4β1 Eur. J. Biochem. 2000, 267, 583-90
36. Skog, J.; Würdinger, T.; van Rijn, S.; Meijer, D. H.; Gainche, L.; Curry, W. T.; Carter, B. S.; Krichevsky, A. M.; Breakefield, X. O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers Nat. Cell Biol. 2008, 10, 1470-6
37. Valadi, H.; Ekström, K.; Bossios, A.; Sjöstrand, M.; Lee, J. J.; Lötvall, J. O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat. Cell Biol. 2007, 9, 654-9
38. Al-Nedawi, K.; Meehan, B.; Micallef, J.; Lhotak, V.; May, L.; Guha, A.; Rak, J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells Nat. Cell Biol. 2008, 10, 619-24
39. Bouvard, D.; Pouwels, J.; De Franceschi, N.; Ivaska, J. Integrin inactivators: balancing cellular functions in vitro and in vivo Nat. Rev. Mol. Cell Biol. 2013, 14, 430-42
40. Jawhara, S.; Pluskota, E.; Verbovetskiy, D.; Skomorovska-Prokvolit, O.; Plow, E. F.; Soloview, D. A. Integrin αXβ2 is a leukocyte receptor for Candida albicans and is essential for protection against fungal infections J. Immunol. 2012, 189, 2468-77
41. Solovjov, D.; Pluskota, E.; Plow, E. Distinct roles for the α and β subunits in the functions of integrin αMβ2 J. Biol. Chem. 2005, 280, 1336-45
42. Ross, G. D.; Cain, J. A.; Myones, B. L.; Newman, S. L.; Lachmann, P. J. Specificity of membrane complement receptor type three (CR3) for β-glucans Complement 1987, 4, 61-74
43. Schlesinger, L. S.; Bellinger-Kawahara, C. G.; Payne, N. R.; Horwitz, M. A. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3 J. Immunol. 1990, 144, 2771-80
44. Forsyth, C. B.; Mathews, H. L. Lymphocytes utilize CD11b/CD18 for adhesion to Candida albicans Cell. Immunol. 1996, 170, 91-100
45. Forsyth, C. B.; Plow, E. F.; Zhang, L. Interaction of the fungal pathogen Candida albicans with integrin CD11b/CD18: recognition by the I domain is modulated by the lectin-like domain and the CD18 subunit J. Immunol. 1998, 161, 6198-205
46. Qu, Y.; Franchi, L.; Nunez, G.; Dubyak, G. R. Nonclassical IL-1 β secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated J. Immunol. 2007, 179, 1913-25
47. Qu, Y.; Ramachandra, L.; Mohr, S.; Franchi, L.; Harding, C. V.; Nunez, G.; Dubyak, G. R. P2X7 receptor-stimulated secretion of MHC class II-containing exosomes requires the ASC/NLRP3 inflammasome but is independent of caspase-1 J. Immunol. 2009, 182, 5052-62
48. Buzas, E. I.; György, B.; Nagy, G.; Falus, A.; Gay, S. Emerging role of extracellular vesicles in inflammatory diseases Nat. Rev. Rheumatol. 2014, 10.1038/nrrheum.2014.19