Characterisation of extracellular vesicle-subsets derived from brain endothelial cells and analysis of their protein cargo modulation after TNF exposure

Journal of Extracellular Vesicles

Volumn 6, Issue 1, 2017, Pages

  Dozio, Vito ^a,b   Sanchez, Jean Charles ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Swiss Centre for Applied Human Toxicology   (Switzerland)

Author keywords

Biomarker; Blood brain barrier; Inflammation; Massspectrometry; Parallel reaction monitoring; Proteomics

Indexed keywords

CELL PROTEIN; CYTOSKELETON PROTEIN; HISTONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOCHONDRIAL PROTEIN; RIBOSOME PROTEIN; TUMOR NECROSIS FACTOR;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN CELL; BRAIN ENDOTHELIUM CELL; CONTROLLED STUDY; ENDOTHELIUM CELL; EXOSOME; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MEMBRANE MICROPARTICLE; PROTEIN EXPRESSION; PROTEOMICS; VASCULAR ENDOTHELIUM;

EID: 85018464968     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.1080/20013078.2017.1302705     Document Type: Article

References (66)

1. Kalra H, Simpson RJ, Ji H, et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. Plos Biol. 2012;10:e1001450.
2. El Andaloussi S, Mager I, Breakefield XO, et al. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 2013;12:347-357.
3. Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci. 2016;113:E968-E977.
4. Crescitelli R, Lässer C, Szabó TG, et al. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles. 2013;2.
5. Lorincz áM, Schütte M, Timár CI, et al. Functionally and morphologically distinct populations of extracellular vesicles produced by human neutrophilic granulocytes. J Leukoc Biol. 2015;98:583-589.
6. Valadi H, Ekstrom K, Bossios A, et al. Exosomemediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654-659.
7. Tkach M, Théry C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164:1226-1232.
8. Alexander M, Hu R, Runtsch MC, et al. Exosome-delivered microRNAs modulate the inflammatory response to endotoxin. Nat Commun. 2015;6:7321.
9. Budnik V, Ruiz-Canada C, Wendler F. Extracellular vesicles round off communication in the nervous system. Nat Rev Neurosci. 2016;17:160-172.
10. Raposo G, Théry C, Colombo M. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255-289.
11. Février B, Raposo G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol. 2004;16:415-421.
12. Kanada M, Bachmann MH, Hardy JW, et al. Differential fates of biomolecules delivered to target cells via extracellular vesicles. Proc Natl Acad Sci. 2015;112:E1433-E1442.
13. Verhaar MC, Van Balkom BWM, Schiffelers RM, et al. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J Extracell Vesicles. 2012;1:569.
14. Kucharzewska P, Christianson HC, Welch JE, et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci. 2013;110:7312-7317.
15. Akers JC, Ramakrishnan V, Kim R, et al. miR-21 in the extracellular vesicles (EVs) of cerebrospinal fluid (CSF): a platform for glioblastoma biomarker development. Plos ONE. 2013;8:e78115.
16. Cheow ESH, Cheng WC, Lee CN, et al. Plasma-derived extracellular vesicles contain predictive biomarkers and potential therapeutic targets for myocardial ischemic injury. Mol Cell Proteomics. 2016;15:2628-2640.
17. Chiasserini D, Van Weering JRT, Piersma SR, et al. Proteomic analysis of cerebrospinal fluid extracellular vesicles: A comprehensive dataset. J Proteomics. 2014;106:191-204.
18. Fiandaca MS, Kapogiannis D, Mapstone M, et al. Identification of preclinical Alzheimer's disease by a profile of pathogenic proteins in neurally derived blood exosomes: A case-control study. Alzheimer's Dementia. 2015;11:600-7.e1.
19. Shi M, Liu C, Cook TJ, et al. Plasma exosomal a-synuclein is likely CNS-derived and increased in Parkinson's disease. Acta Neuropathol. 2014;128:639-650.
20. Haqqani AS, Delaney CE, Tremblay T-L, et al. Method for isolation and molecular characterization of extracellular microvesicles released from brain endothelial cells. Fluids Barriers CNS. 2013;10:1-13.
21. Daneman R. The blood-brain barrier in health and disease. Ann Neurol. 2012;72:648-672.
22. Minagar A, Alexander JS. Blood-brain barrier disruption in multiple sclerosis. Mult Scler. 2003;9:540-549.
23. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron. 2008;57:178-201.
24. Erickson MA, Banks WA. Blood-brain barrier dysfunction as a cause and consequence of Alzheimer's disease. J Cereb Blood Flow Metab. 2013;33:1500-1513.
25. Heneka MT, Carson MJ, Khoury JE, et al. Neuroinflammation in Alzheimer's disease. Lancet Neurol. 2015;14:388-405.
26. Lyman M, Lloyd DG, Ji X, et al. Neuroinflammation: the role and consequences. Neurosci Res. 2014;79:1-12.
27. Brenner D, Blaser H, Mak TW. Regulation of tumour necrosis factor signalling: live or let die. Nat Rev Immunol. 2015;15:362-374.
28. Park KM, Bowers WJ. Tumor necrosis factor-alpha mediated signaling in neuronal homeostasis and dysfunction. Cell Signal. 2010;22:977-983.
29. Bhaskar K, Maphis N, Xu G, et al. Microglial derived tumor necrosis factor-a drives Alzheimer's diseaserelated neuronal cell cycle events. Neurobiol Dis. 2014;62:273-285.
30. Cannella B, Raine CS. The adhesion molecule and cytokine profile of multiple sclerosis lesions. Ann Neurol. 1995;37:424-435.
31. Lindoso RS, Collino F, Camussi G. Extracellular vesicles derived from renal cancer stem cells induce a pro-tumorigenic phenotype in mesenchymal stromal cells. Oncotarget. 2015;6:7959-7969.
32. Combes V, Simon A-C, Grau G-E, et al. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J Clin Investig. 1999;104:93-102.
33. Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255-289.
34. MacLean B, Tomazela DM, Shulman N, et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics. 2010;26:966-968.
35. Bindea G, Mlecnik B, Hackl H, et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25:1091-1093.
36. Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. Journal of Extracellular Vesicles. 2013;2013. Epub 2013-01-14.
37. Visner G, Chesrown SE, Monnier J, et al. Regulation of manganese superoxide dismutase: IL-1 and TNF induction in pulmonary artery and microvascular endothelial cells. Biochem Biophys Res Commun. 1992;188:453-462.
38. Venkatesh D, Ernandez T, Rosetti F, et al. Endothelial TNF receptor 2 induces IRF1 transcription factordependent interferon-ß autocrine signaling to promote monocyte recruitment. Immunity. 2013;38:1025-1037.
39. Loeb KR, Haas AL. The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J Biol Chem. 1992;267:7806-7813.
40. Yang S, Zhan Y, Zhou Y, et al. Interferon regulatory factor 3 is a key regulation factor for inducing the expression of SAMHD1 in antiviral innate immunity. Sci Rep. 2016;6:29665.
41. Wang Y, Wu TR, Cai S, et al. Stat1 as a component of tumor necrosis factor alpha receptor 1-TRADD signaling complex to inhibit NF-?B activation. Mol Cell Biol. 2000;20:4505-4512.
42. Sanz L, Diaz-Meco MT, Nakano H, et al. The atypical PKC-interacting protein p62 channels NF-?B activation by the IL-1-TRAF6 pathway. EMBO J. 2000;19:1576-1586.
43. Zhou Z, Connell MC, MacEwan DJ. TNFR1-induced NF-?B, but not ERK, p38MAPK or JNK activation, mediates TNF-induced ICAM-1 and VCAM-1 expression on endothelial cells. Cell Signal. 2007;19:1238-1248.
44. Yoo J, Perez CER, Nie W, et al. TNF-a induces upregulation of EGFR expression and signaling in human colonic myofibroblasts. Am J Physiol Gastrointest Liver Physiol. 2012;302:G805-G814.
45. Krämer A, Green J, Pollard J, et al. Causal analysis approaches in ingenuity pathway analysis. Bioinformatics. 2013;30:523-530.
46. Haraszti RA, Didiot M-C, Sapp E, et al. High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources. J Extracell Vesicles. 2016;5:32570. DOI:10.3402/jev.v5.32570
47. Lázaro-Ibáñez E, Sanz-Garcia A, Visakorpi T, et al. Different gDNA content in the subpopulations of prostate cancer extracellular vesicles: apoptotic bodies, microvesicles, and exosomes. Prostate. 2014;74:1379-1390.
48. Robert J, Ménoret A, Cohen N. Cell surface expression of the endoplasmic reticular heat shock protein gp96 is phylogenetically conserved. J Immunol. 1999;163:4133-4139.
49. Li X, Sun L, Hou J, et al. Cell membrane gp96 facilitates HER2 dimerization and serves as a novel target in breast cancer. Int J Cancer. 2015;137:512-524.
50. Mayr M, Grainger D, Mayr U, et al. Proteomics, metabolomics, and immunomics on microparticles derived from human atherosclerotic plaques. Circ Cardiovasc Genet. 2009;2:379-388.
51. Xu R, Greening DW, Rai A, et al. Highly-purified exosomes and shed microvesicles isolated from the human colon cancer cell line LIM1863 by sequential centrifugal ultrafiltration are biochemically and functionally distinct. Methods. 2015;87:11-25.
52. Koumangoye R, Delpire E. The Ste20 kinases SPAK and OSR1 travel between cells through exosomes. Am J Physiol Physiol. 2016;311:C43-C53.
53. Choi D-S, Kim D-K, Kim Y-K, et al. Proteomics of extracellular vesicles: exosomes and ectosomes. Mass Spectrom Rev. 2015;34:474-490.
54. Lunavat TR, Cheng L, Kim D-K, et al. Small RNA deep sequencing discriminates subsets of extracellular vesicles released by melanoma cells -Evidence of unique microRNA cargos. RNA Biol. 2015;12:810-823.
55. Phinney DG, Di Giuseppe M, Njah J, et al. Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs. Nat Commun. 2015;6:8472.
56. Dobbie MS, Hurst RD, Klein NJ, et al. Upregulation of intercellular adhesion molecule-1 expression on human endothelial cells by tumour necrosis factor-a in an in vitro model of the blood-brain barrier. Brain Res. 1999;830:330-336.
57. Strazza M, Pirrone V, Wigdahl B, et al. Prolonged morphine exposure induces increased firm adhesion in an in vitro model of the blood-brain barrier. Int J Mol Sci. 2016;17:916.
58. Peterson DB, Sander T, Kaul S, et al. Comparative proteomic analysis of PAI-1 and TNF-alpha-derived endothelial microparticles. Proteomics. 2008;8:2430-2446.
59. Madge LA, Pober JS. TNF Signaling in Vascular Endothelial Cells. Experimental and Molecular Pathology. 2001;70:317-325.
60. He F, Peng J, Deng XL, et al. RhoA and NF-?B are involved in lipopolysaccharide-induced brain microvascular cell line hyperpermeability. Neuroscience. 2011;188:35-47.
61. Yarilina A, Park-Min K-H, Antoniv T, et al. TNF activates an IRF1-dependent autocrine loop leading to sustained expression of chemokines and STAT1-dependent type I interferon-response genes. Nat Immunol. 2008;9:378-387.
62. Lee HD, Koo B-H, Kim YH, et al. Exosome release of ADAM15 and the functional implications of human macrophage-derived ADAM15 exosomes. Faseb J. 2012;26:3084-3095.
63. Zhang H-G, Liu C, Su K, et al. A membrane form of TNF-a presented by exosomes delays T cell activation-induced cell death. J Immunol. 2006;176:7385-7393.
64. Yarilina A, Ivashkiv LB. Type I interferon: a new player in TNF signaling. Curr Dir Autoimmun. 2010;11:94-104.
65. Meckes DG, Gunawardena HP, Dekroon RM, et al. Modulation of B-cell exosome proteins by gamma herpesvirus infection. Proc Natl Acad Sci U S A. 2013;110: E2925-E2933.
66. Ge M, Ke R, Cai T, et al. Identification and proteomic analysis of osteoblast-derived exosomes. Biochem Biophys Res Commun. 2015;467:27-32.