Candida albicans Modifies the Protein Composition and Size Distribution of THP1 macrophages-derived Extracellular Vesicles.
Loading...
Official URL
Full text at PDC
Publication date
2016
Advisors (or tutors)
Editors
Journal Title
Journal ISSN
Volume Title
Publisher
American Chemical Society
Citation
1) Brown, G. D.; Denning, D. W.; Gow, N. A.; Levitz, S. M.; Netea,
M. G.; White, T. C. Hidden killers: human fungal infections. Sci.
Transl. Med. 2012, 4 (165), 165rv13.
(2) Netea, M. G.; Joosten, L. A. Master and commander: epigenetic
regulation of macrophages. Cell Res. 2016, 26 (2), 145−6.
(3) Bourgeois, C.; Majer, O.; Frohner, I. E.; Tierney, L.; Kuchler, K.
Fungal attacks on mammalian hosts: pathogen elimination requires
sensing and tasting. Curr. Opin. Microbiol. 2010, 13 (4), 401−8.
(4) Denzer, K.; Kleijmeer, M. J.; Heijnen, H. F.; Stoorvogel, W.;
Geuze, H. J. Exosome: from internal vesicle of the multivesicular body
to intercellular signaling device. J. Cell Sci. 2000, 113 (Pt 19), 3365−
74.
(5) Raposo, G.; Stoorvogel, W. Extracellular vesicles: Exosomes,
microvesicles, and friends. J. Cell Biol. 2013, 200 (4), 373−383.
(6) Reales-Calderon, J. A.; Corona, F.; Monteoliva, L.; Gil, C.;
Martinez, J. L. Quantitative proteomics unravels that the posttranscriptional
regulator Crc modulates the generation of vesicles and
secreted virulence determinants of Pseudomonas aeruginosa. J.
Proteomics 2015, 127 (Pt B), 352−64.
(7) Gil-Bona, A.; Llama-Palacios, A.; Parra, C. M.; Vivanco, F.;
Nombela, C.; Monteoliva, L.; Gil, C. Proteomics unravels extracellular
vesicles as carriers of classical cytoplasmic proteins in Candida albicans.
J. Proteome Res. 2015, 14 (1), 142−53.
(8) Brown, L.; Wolf, J. M.; Prados-Rosales, R.; Casadevall, A.
Through the wall: extracellular vesicles in Gram-positive bacteria,
mycobacteria and fungi. Nat. Rev. Microbiol. 2015, 13 (10), 620−630.
(9) Hassani, K.; Olivier, M. Immunomodulatory impact of
Leishmania-induced macrophage exosomes: a comparative proteomic
and functional analysis. PLoS Neglected Trop. Dis. 2013, 7 (5), e2185.
(10) Keerthikumar, S.; Chisanga, D.; Ariyaratne, D.; Al Saffar, H.;
Anand, S.; Zhao, K.; Samuel, M.; Pathan, M.; Jois, M.; Chilamkurti, N.;
Gangoda, L.; Mathivanan, S. ExoCarta: A Web-Based Compendium of
Exosomal Cargo. J. Mol. Biol. 2016, 428 (4), 688−92.
(11) Singh, P. P.; Smith, V. L.; Karakousis, P. C.; Schorey, J. S.
Exosomes isolated from mycobacteria-infected mice or cultured
macrophages can recruit and activate immune cells in vitro and in
vivo. J. Immunol. 2012, 189 (2), 777−85.
(12) Wang, J.; Yao, Y.; Xiong, J.; Wu, J.; Tang, X.; Li, G. Evaluation
of the inflammatory response in macrophages stimulated with
exosomes secreted by Mycobacterium avium-infected macrophages.
BioMed Res. Int. 2015, 2015, 658421.
(13) Cronemberger-Andrade, A.; Aragao-Franca, L.; de Araujo, C. F.;
Rocha, V. J.; Borges-Silva, M. d. C.; Figueiras, C. P.; Oliveira, P. R.; de
Freitas, L. A.; Veras, P. S.; Pontes-de-Carvalho, L. Extracellular vesicles
from Leishmania-infected macrophages confer an anti-infection
cytokine-production profile to naive macrophages. PLoS Neglected
Trop. Dis. 2014, 8 (9), e3161.
(14) Zhu, Y.; Chen, X.; Pan, Q.; Wang, Y.; Su, S.; Jiang, C.; Li, Y.; Xu,
N.; Wu, L.; Lou, X.; Liu, S. A Comprehensive Proteomics Analysis
Reveals a Secretory Path- and Status-Dependent Signature of
Exosomes Released from Tumor-Associated Macrophages. J. Proteome
Res. 2015, 14 (10), 4319−31.
(15) Wang, J. J.; Chen, C.; Xie, P. F.; Pan, Y.; Tan, Y. H.; Tang, L. J.
Proteomic analysis and immune properties of exosomes released by
macrophages infected with Mycobacterium avium. Microbes Infect.
2014, 16 (4), 283−91.
(16) Cypryk, W.; Ohman, T.; Eskelinen, E. L.; Matikainen, S.;
Nyman, T. A. Quantitative proteomics of extracellular vesicles released
from human monocyte-derived macrophages upon beta-glucan
stimulation. J. Proteome Res. 2014, 13 (5), 2468−77.
(17) Reales-Calderon, J. A.; Sylvester, M.; Strijbis, K.; Jensen, O. N.;
Nombela, C.; Molero, G.; Gil, C. Candida albicans induces proinflammatory
and anti-apoptotic signals in macrophages as revealed by
quantitative proteomics and phosphoproteomics. J. Proteomics 2013,
91, 106−35.
(18) Reales-Calderon, J. A.; Aguilera-Montilla, N.; Corbi, A. L.;
Molero, G.; Gil, C. Proteomic characterization of human proinflammatory
M1 and anti-inflammatory M2 macrophages and their
response to Candida albicans. Proteomics 2014, 14 (12), 1503−18.
(19) 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 (1), 179−82.
(20) 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 transcell
wall transport. Eukaryotic Cell 2007, 6 (1), 48−59.
Journal of Proteome Research Article
DOI: 10.1021/acs.jproteome.6b00605
J. Proteome Res. XXXX, XXX, XXX−XXX
Q
(21) 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.; Nimrichter, L.; Rodrigues, M. L. Characterization of
yeast extracellular vesicles: evidence for the participation of different
pathways of cellular traffic in vesicle biogenesis. PLoS One 2010, 5 (6),
e11113.
(22) Eisenman, H. C.; Frases, S.; Nicola, A. M.; Rodrigues, M. L.;
Casadevall, A. Vesicle-associated melanization in Cryptococcus neoformans.
Microbiology 2009, 155 (Pt 12), 3860−7.
(23) Wessel, D.; Flugge, U. I. A method for the quantitative recovery
of protein in dilute solution in the presence of detergents and lipids.
Anal. Biochem. 1984, 138 (1), 141−3.
(24) Vizcaino, J. A.; Cote, R. G.; Csordas, A.; Dianes, J. A.; Fabregat,
A.; Foster, J. M.; Griss, J.; Alpi, E.; Birim, M.; Contell, J.; O’Kelly, G.;
Schoenegger, A.; Ovelleiro, D.; Perez-Riverol, Y.; Reisinger, F.; Rios,
D.; Wang, R.; Hermjakob, H. The PRoteomics IDEntifications
(PRIDE) database and associated tools: status in 2013. Nucleic Acids
Res. 2013, 41 (Database issue), D1063−9.
(25) Ramos-Fernandez, A.; Paradela, A.; Navajas, R.; Albar, J. P.
Generalized method for probability-based peptide and protein
identification from tandem mass spectrometry data and sequence
database searching. Mol. Cell. Proteomics 2008, 7 (9), 1748−54.
(26) Lopez-Serra, P.; Marcilla, M.; Villanueva, A.; Ramos-Fernandez,
A.; Palau, A.; Leal, L.; Wahi, J. E.; Setien-Baranda, F.; Szczesna, K.;
Moutinho, C.; et al. A DERL3-associated defect in the degradation of
SLC2A1 mediates the Warburg effect. Nat. Commun. 2014, 5, 5.
(27) Bhatia, V. N.; Perlman, D. H.; Costello, C. E.; McComb, M. E.
Software tool for researching annotations of proteins: open-source
protein annotation software with data visualization. Anal. Chem. 2009,
81 (23), 9819−23.
(28) Benito-Martin, A.; Peinado, H. FunRich proteomics software
analysis, let the fun begin! Proteomics 2015, 15 (15), 2555−6.
(29) Petersen, T. N.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP
4.0: discriminating signal peptides from transmembrane regions. Nat.
Methods 2011, 8 (10), 785−786.
(30) Bendtsen, J. D.; Kiemer, L.; Fausboll, A.; Brunak, S. Nonclassical
protein secretion in bacteria. BMC Microbiol. 2005, 5, 58.
(31) Keerthikumar, S.; Chisanga, D.; Ariyaratne, D.; Al Saffar, H.;
Anand, S.; Zhao, K.; Samuel, M.; Pathan, M.; Jois, M.; Chilamkurti, N.;
Gangoda, L.; Mathivanan, S. ExoCarta: A Web-Based Compendium of
Exosomal Cargo. J. Mol. Biol. 2016, 428, 688.
(32) Diez-Orejas, R.; Molero, G.; Moro, M. A.; Gil, C.; Nombela, C.;
Sanchez-Perez, M. Two different NO-dependent mechanisms account
for the low virulence of a non-mycelial morphological mutant of
Candida albicans. Med. Microbiol. Immunol. 2001, 189 (3), 153−160.
(33) Thery, C.; Regnault, A.; Garin, J.; Wolfers, J.; Zitvogel, L.;
Ricciardi-Castagnoli, P.; Raposo, G.; Amigorena, S. Molecular
characterization of dendritic cell-derived exosomes: Selective accumulation
of the heat shock protein hsc73. J. Cell Biol. 1999, 147 (3), 599−
610.
(34) Ung, T. H.; Madsen, H. J.; Hellwinkel, J. E.; Lencioni, A. M.;
Graner, M. W. Exosome proteomics reveals transcriptional regulator
proteins with potential to mediate downstream pathways. Cancer Sci.
2014, 105 (11), 1384−92.
(35) Martínez-Solano, L.; Reales-Calderón, J. A.; Nombela, C.;
Molero, G.; Gil, C. Proteomics of RAW 264.7 macrophages upon
interaction with heat-inactivated Candida albicans cells unravel an antiinflammatory
response. Proteomics 2009, 9 (11), 2995−3010.
(36) Reales-Calderon, J. A.; Martinez-Solano, L.; Martinez-Gomariz,
M.; Nombela, C.; Molero, G.; Gil, C. Sub-proteomic study on
macrophage response to Candida albicans unravels new proteins
involved in the host defense against the fungus. J. Proteomics 2012, 75
(15), 4734−46.
(37) Mizoguchi, E. Chitinase 3-like-1 exacerbates intestinal
inflammation by enhancing bacterial adhesion and invasion in colonic
epithelial cells. Gastroenterology 2006, 130 (2), 398−411.
(38) Volck, B.; Price, P. A.; Johansen, J. S.; Sorensen, O.; Benfield, T.
L.; Nielsen, H. J.; Calafat, J.; Borregaard, N. YKL-40, a mammalian
member of the Chitinase family, is a matrix protein of specific granules
in human neutrophils. Proc. Assoc. Am. Physicians 1998, 110 (4), 351−
360.
(39) Rehli, M.; Niller, H. H.; Ammon, C.; Langmann, S.;
Schwarzfischer, L.; Andreesen, R.; Krause, S. W. Transcriptional
regulation of CHI3L1, a marker gene for late stages of macrophage
differentiation. J. Biol. Chem. 2003, 278 (45), 44058−67.
(40) Lee, J. H.; Kim, S. S.; Kim, I. J.; Song, S. H.; Kim, Y. K.; In Kim,
J.; Jeon, Y. K.; Kim, B. H.; Kwak, I. S. Clinical implication of plasma
and urine YKL-40, as a proinflammatory biomarker, on early stage of
nephropathy in type 2 diabetic patients. J. Diabetes Complications 2012,
26 (4), 308−12.
(41) Di Rosa, M.; Malaguarnera, G.; De Gregorio, C.; Drago, F.;
Malaguarnera, L. Evaluation of CHI3L-1 and CHIT-1 expression in
differentiated and polarized macrophages. Inflammation 2013, 36 (2),
482−92.
(42) Johansen, J. S. Studies on serum YKL-40 as a biomarker in
diseases with inflammation, tissue remodelling, fibroses and cancer.
Dan. Med. Bull. 2006, 53 (2), 172−209.
(43) Cario, E.; Gerken, G.; Podolsky, D. K. Toll-like receptor 2
controls mucosal inflammation by regulating epithelial barrier
function. Gastroenterology 2007, 132 (4), 1359−74.
(44) Heimesaat, M. M.; Fischer, A.; Siegmund, B.; Kupz, A.;
Niebergall, J.; Fuchs, D.; Jahn, H. K.; Freudenberg, M.;
Loddenkemper, C.; Batra, A.; Lehr, H. A.; Liesenfeld, O.; Blaut, M.;
Gobel, U. B.; Schumann, R. R.; Bereswill, S. Shift towards proinflammatory
intestinal bacteria aggravates acute murine colitis via
Toll-like receptors 2 and 4. PLoS One 2007, 2 (7), e662.
(45) Barone, R.; Simpore, J.; Malaguarnera, L.; Pignatelli, S.;
Musumeci, S. Plasma chitotriosidase activity in acute Plasmodium
falciparum malaria. Clin. Chim. Acta 2003, 331 (1−2), 79−85.
(46) Soria, G.; Ben-Baruch, A. The inflammatory chemokines CCL2
and CCL5 in breast cancer. Cancer Lett. 2008, 267 (2), 271−285.
(47) Devalaraja, M. N.; Richmond, A. Multiple chemotactic factors:
fine control or redundancy? Trends Pharmacol. Sci. 1999, 20 (4), 151−
156.
(48) Mantovani, A. The chemokine system: redundancy for robust
outputs. Immunology Today 1999, 20 (6), 254−257.
(49) Renkema, G. H.; Boot, R. G.; Muijsers, A. O.; Donkerkoopman,
W. E.; Aerts, J. M. F. G. Purification and Characterization of Human
Chitotriosidase, a Novel Member of the Chitinase Family of Proteins.
J. Biol. Chem. 1995, 270 (5), 2198−2202.
(50) Cozzarini, E.; Bellin, M.; Norberto, L.; Polese, L.; Musumeci, S.;
Lanfranchi, G.; Paoletti, M. G. CHIT1 and AMCase expression in
human gastric mucosa: correlation with inflammation and Helicobacter
pylori infection. Eur. J. Gastroenterol. Hepatol. 2009, 21 (10), 1119−26.
(51) Nair, M. G.; Gallagher, L. J.; Taylor, M. D.; Loke, P.; Coulson,
P. S.; Wilson, R. A.; Maizels, R. M.; Allen, J. E. Chitinase and Fizz
family members are a generalized feature of nematode infection with
selective Upregulation of Ym1 and F10.1 by antigen-presenting cells.
Infect. Immun. 2005, 73 (1), 385−394.
(52) Di Rosa, M.; De Gregorio, C.; Malaguarnera, G.; Tuttobene, M.;
Biazzo, F.; Malaguarnera, L. Evaluation of AMCase and CHIT-1
expression in monocyte macrophages lineage. Mol. Cell. Biochem. 2013,
374 (1−2), 73−80.
(53) Shen, C. R.; Juang, H. H.; Chen, H. S.; Yang, C. J.; Wu, C. J.;
Lee, M. H.; Hwang, Y. S.; Kuo, M. L.; Chen, Y. S.; Chen, J. K.; Liu, C.
L. The Correlation between Chitin and Acidic Mammalian Chitinase
in Animal Models of Allergic Asthma. Int. J. Mol. Sci. 2015, 16 (11),
27371−27377.
(54) Boulland, M. L.; Marquet, J.; Molinier-Frenkel, V.; M?ller, P.;
Guiter, C.; Lasoudris, F.; Copie-Bergman, C.; Baia, M.; Gaulard, P.;
Leroy, K.; Castellano, F. Human IL4I1 is a secreted L-phenylalanine
oxidase expressed by mature dendritic cells that inhibits T-lymphocyte
proliferation. Blood 2007, 110 (1), 220−227.
(55) Marquet, J.; Lasoudris, F.; Cousin, C.; Puiffe, M. L.; Martin-
Garcia, N.; Baud, V.; Chereau, F.; Farcet, J. P.; Molinier-Frenkel, V.;
Castellano, F. Dichotomy between factors inducing the immunosuppressive
enzyme IL-4-induced gene 1 (IL4I1) in B lymphocytes and
mononuclear phagocytes. Eur. J. Immunol. 2010, 40 (9), 2557−2568.
Journal of Proteome Research Article
DOI: 10.1021/acs.jproteome.6b00605
J. Proteome Res. XXXX, XXX, XXX−XXX
R
(56) Yue, Y. P.; Huang, W.; Liang, J. J.; Guo, J.; Ji, J.; Yao, Y. L.;
Zheng, M. Z.; Cai, Z. J.; Lu, L. R.; Wang, J. L. IL4I1 Is a Novel
Regulator of M2Macrophage Polarization That Can Inhibit T Cell
Activation via L-Tryptophan and Arginine Depletion and IL-10
Production. PLoS One 2015, 10 (11), e0142979.
(57) Benes, P.; Maceckova, V.; Zdrahal, Z.; Konecna, H.;
Zahradnickova, E.; Muzik, J.; Smarda, J. Role of vimentin in regulation
of monocyte/macrophage differentiation. Differentiation 2006, 74 (6),
265−276.
(58) Mor-Vaknin, N.; Punturieri, A.; Sitwala, K.; Markovitz, D. M.
Vimentin is secreted by activated macrophages. Nat. Cell Biol. 2002, 5
(1), 59−63.
(59) Perlson, E.; Michaelevski, I.; Kowalsman, N.; Ben-Yaakov, K.;
Shaked, M.; Seger, R.; Eisenstein, M.; Fainzilber, M. Vimentin binding
to phosphorylated Erk sterically hinders enzymatic dephosphorylation
of the kinase. J. Mol. Biol. 2006, 364 (5), 938−44.
(60) Mor-Vaknin, N.; Punturieri, A.; Sitwala, K.; Faulkner, N.;
Legendre, M.; Khodadoust, M. S.; Kappes, F.; Ruth, J. H.; Koch, A.;
Glass, D.; Petruzzelli, L.; Adams, B. S.; Markovitz, D. M. The DEK
nuclear autoantigen is a secreted chemotactic factor. Mol. Cell. Biol.
2006, 26 (24), 9484−9496.
(61) Saha, A. K.; Kappes, F.; Mundade, A.; Deutzmann, A.;
Rosmarin, D. M.; Legendre, M.; Chatain, N.; Al-Obaidi, Z.; Adams,
B. S.; Ploegh, H. L.; Ferrando-May, E.; Mor-Vaknin, N.; Markovitz, D.
M. Intercellular trafficking of the nuclear oncoprotein DEK. Proc. Natl.
Acad. Sci. U. S. A. 2013, 110 (17), 6847−6852.
(62) Etienne-Manneville, S.; Hall, A. Rho GTPases in cell biology.
Nature 2002, 420 (6916), 629−35.
(63) Medrano-Fernandez, I.; Reyes, R.; Olazabal, I.; Rodriguez, E.;
Sanchez-Madrid, F.; Boussiotis, V. A.; Reche, P. A.; Cabanas, C.;
Lafuente, E. M. RIAM (Rap1-interacting adaptor molecule) regulates
complement-dependent phagocytosis. Cell. Mol. Life Sci. 2013, 70
(13), 2395−410.
(64) Cammas, L.; Wolfe, J.; Choi, S. Y.; Dedhar, S.; Beggs, H. E.
Integrin-linked kinase deletion in the developing lens leads to capsule
rupture, impaired fiber migration and non-apoptotic epithelial cell
Abstract
The effectiveness of macrophages in the response to systemic candidiasis is crucial to an effective clearance of the pathogen. The secretion of proteins, mRNAs, non-coding RNAs and lipids through extracellular vesicles (EVs) is one of the mechanisms of communication between immune cells. EVs change their cargo to mediate different responses, and may play a role in the response against infections. Thus, we have undertaken the first quantitative proteomic analysis on the protein composition of THP1 macrophages-derived EVs during the interaction with Candida albicans. This study revealed changes in EVs sizes and in protein composition, and allowed the identification and quantification of 717 proteins. Of them, 133 proteins changed their abundance due to the interaction. The differentially abundant proteins were involved in functions relating to immune response, signaling, or cytoskeletal reorganization. THP1-derived EVs, both from control and from Candida-infected macrophages, had similar effector functions on other THP1-differenciated macrophages, activating ERK and p38 kinases, and increasing both the secretion of proinflammatory cytokines and the candidacidal activity; while in THP1 non-differenciated monocytes, only EVs from infected macrophages increased significantly the TNF-α secretion. Our findings provide new information on the role of macrophage-derived EVs in response to C. albicans infection and in macrophages communication.