Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes

Journal of Extracellular Vesicles

Volumn 1, Issue 1, 2012, Pages

  de Jong, Olivier G ^a   Verhaar, Marianne C ^a   Chen, Yong ^b   Vader, Pieter ^a   Gremmels, Hendrik ^a   Posthuma, George ^a   Schiffelers, Raymond M ^a   Gucek, Marjan ^b   van Balkom, Bas W M ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Exosomes; Extracellular vesicles; Hypoxia; Proteomics; RNA; Tumor necrosis factor alpha

Indexed keywords

GLUCOSE; MANNOSE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL ACTIVATION; CELL HYPOXIA; CELL ISOLATION; CELLULAR STRESS RESPONSE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOTHELIUM CELL; EXOSOME; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEOMICS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA TRANSPORT;

EID: 85013156831     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.3402/jev.v1i0.18396     Document Type: Article

References (64)

1. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G. The biogenesis and functions of exosomes. Traffic. 2002;3:321-30.
2. Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA. Structural heterogeneity and protein composition of exosomelike vesicles (prostasomes) in human semen. Prostate. 2009; 69:159-67.
3. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569-610.
4. Fevrier B, Raposo G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol. 2004;16: 415-21.
5. Ohshima K, Inoue K, Fujiwara A, Hatekeyama K, Kanto K, Watanabe Y, et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One. 2010;5:e13247.
6. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654-9.
7. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze H. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem. 1998;273:20121-7.
8. Clayton A, Mitchell JP, Court J, Linnane S, Mason MD, Tabi Z. Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol. 2008;180:7249-58.
9. Lotvall J, Valadi H. Cell to cell signalling via exosomes through esRNA. Cell Adh Migr. 2007;1:156-8.
10. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA. 2010;107:6328-33.
11. Zhan R, Leng X, Liu X, Wang X, Gong J, Yan L, et al. Heat shock protein 70 is secreted from endothelial cells by a nonclassical pathway involving exosomes. Biochem Biophys Res Commun. 2009;387:229-33.
12. Taylor AR, Robinson MB, Gifondorwa DJ, Tytell M, Milligan CE. Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases. Dev Neurobiol. 2007;67: 1815-29.
13. Lancaster GI, Febbraio MA. Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem. 2005;280:23349-55.
14. Clayton A, Turkes A, Navabi H, Mason MD, Tabi Z. Induction of heat shock proteins in B-cell exosomes. J Cell Sci. 2005;118:3631-8.
15. Gupta S, Knowlton AA. HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway. Am J Physiol Heart Circ Physiol. 2007;292:H3052-6.
16. Gastpar R, Gehrmann M, Bausero MA, Asea A, Gross C, Schroeder JA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 2005;65:5238-47.
17. Eldh M, Ekstrom K, Valadi H, Sjostrand M, Olsson B, Jernas M, et al. Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA. PLoS One. 2010;5:e15353.
18. Goligorsky MS, Kuo MC, Patschan D, Verhaar MC. Review article: endothelial progenitor cells in renal disease. Nephrology (Carlton). 2009;14:291-7.
19. Sheldon H, Heikamp E, Turley H, Dragovic R, Thomas P, Oon CE, et al. New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood. 2010;116:2385-94.
20. Al-Nedawi K, Szemraj J, Cierniewski CS. Mast cell-derived exosomes activate endothelial cells to secrete plasminogen activator inhibitor type 1. Arterioscler Thromb Vasc Biol. 2005;25:1744-9.
21. Basile DP. The endothelial cell in ischemic acute kidney injury: implications for acute and chronic function. Kidney Int. 2007;72:151-6.
22. Fagan SC, Hess DC, Hohnadel EJ, Pollock DM, Ergul A. Targets for vascular protection after acute ischemic stroke. Stroke. 2004;35:2220-5.
23. Fisher M. Injuries to the vascular endothelium: vascular wall and endothelial dysfunction. Rev Neurol Dis. 2008;5(Suppl 1): S4-11.
24. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, Bosse DC, et al. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol. 1992;99:683-90.
25. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, et al. B lymphocytes secrete antigenpresenting vesicles. J Exp Med. 1996;183:1161-72.
26. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;Chapter 3: 3.22.1-3.22.29.
27. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002;74:5383-92.
28. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003;75:4646-58.
29. Huber W, von HA, Sultmann H, Poustka A, Vingron M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics. 2002;18(Suppl 1):S96-104.
30. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:Article 3.
31. Wang X, Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res. 2003;31:e154.
32. Bauer S, Grossmann S, Vingron M, Robinson PN. Ontologizer 2.0-a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics. 2008;24:1650-1.
33. Grossmann S, Bauer S, Robinson PN, Vingron M. Improved detection of overrepresentation of Gene-Ontology annotations with parent child analysis. Bioinformatics. 2007;23:3024-31.
34. Slot JW, Geuze HJ. Cryosectioning and immunolabeling. Nat Protoc. 2007;2:2480-91.
35. Brodsky SV, Zhang F, Nasjletti A, Goligorsky MS. Endothelium-derived microparticles impair endothelial function in vitro. Am J Physiol Heart Circ Physiol. 2004;286: H1910-5.
36. Mezentsev A, Merks RM, O'Riordan E, Chen J, Mendelev N, Goligorsky MS, et al. Endothelial microparticles affect angiogenesis in vitro: role of oxidative stress. Am J Physiol Heart Circ Physiol. 2005;289:H1106-14.
37. Wiese S, Reidegeld KA, Meyer HE, Warscheid B. Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics. 2007;7:340-50.
38. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics. 2004;3:1154-69.
39. Buschow SI, van Balkom BW, Aalberts M, Heck AJ, Wauben M, Stoorvogel W. MHC class II-associated proteins in B-cell exosomes and potential functional implications for exosome biogenesis. Immunol Cell Biol. 2010;88:851-6.
40. Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: current perspectives. Proteomics. 2008;8:4083-99.
41. van Niel G, Raposo G, Candalh C, Boussac M, Hershberg R, Cerf-Bensussan N, et al. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology. 2001;121:337-49.
42. Brillard-Bourdet M, Rehault S, Juliano L, Ferrer M, Moreau T, Gauthier F. Amidolytic activity of prostatic acid phosphatase on human semenogelins and semenogelin-derived synthetic substrates. Eur J Biochem. 2002;269:390-5.
43. Jonsson M, Lundwall A, Linse S, Frohm B, Malm J. Truncated semenogelin I binds zinc and is cleaved by prostate-specific antigen. J Androl. 2006;27:542-7.
44. Wang XL, Fu A, Spiro C, Lee HC. Proteomic analysis of vascular endothelial cells-effects of laminar shear stress and high glucose. J Proteomics Bioinform. 2009;2:445.
45. Cooper JT, Stroka DM, Brostjan C, Palmetshofer A, Bach FH, Ferran C. A20 blocks endothelial cell activation through a NF-kappaB-dependent mechanism. J Biol Chem. 1996;271:18068-73.
46. Opipari AW Jr, Boguski MS, Dixit VM. The A20 cDNA induced by tumor necrosis factor alpha encodes a novel type of zinc finger protein. J Biol Chem. 1990;265:14705-8.
47. Sluiter W, Pietersma A, Lamers JM, Koster JF. Leukocyte adhesion molecules on the vascular endothelium: their role in the pathogenesis of cardiovascular disease and the mechanisms underlying their expression. J Cardiovasc Pharmacol. 1993; 22(Suppl 4):S37-44.
48. Peterson DB, Sander T, Kaul S, Wakim BT, Halligan B, Twigger S, et al. Comparative proteomic analysis of PAI-1 and TNF-alpha-derived endothelial microparticles. Proteomics. 2008;8:2430-46.
49. Gu L, Tseng SC, Rollins BJ. Monocyte chemoattractant protein-1. Chem Immunol. 1999;72:7-29.
50. Gerszten RE, Garcia-Zepeda EA, Lim YC, Yoshida M, Ding HA, Gimbrone Jr MA, et al. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature. 1999;398:718-23.
51. Kim SH, Han SY, Azam T, Yoon DY, Dinarello CA. Interleukin-32: a cytokine and inducer of TNFalpha. Immunity. 2005;22:131-42.
52. Carlos T, Kovach N, Schwartz B, Rosa M, Newman B,Wayner E, et al. Human monocytes bind to two cytokine-induced adhesive ligands on cultured human endothelial cells: endothelial-leukocyte adhesion molecule-1 and vascular cell adhesion molecule-1. Blood. 1991;77:2266-71.
53. Curran JE, Weinstein SR, Griffiths LR. Polymorphic variants of NFKB1 and its inhibitory protein NFKBIA, and their involvement in sporadic breast cancer. Cancer Lett. 2002;188: 103-7.
54. Heyninck K, Kreike MM, Beyaert R. Structure-function analysis of the A20-binding inhibitor of NF-kappa B activation, ABIN-1. FEBS Lett. 2003;536:135-40.
55. Ostergaard L, Simonsen U, Eskildsen-Helmond Y, Vorum H, Uldbjerg N, Honore B, et al. Proteomics reveals lowering oxygen alters cytoskeletal and endoplasmatic stress proteins in human endothelial cells. Proteomics. 2009;9:4457-67.
56. Kovacevic Z, Sivagurunathan S, Mangs H, Chikhani S, Zhang D, Richardson DR. The metastasis suppressor, N-myc downstream regulated gene 1 (NDRG1), upregulates p21 via p53-independent mechanisms. Carcinogenesis. 2011; 32:732-40.
57. De LF, Zhang T, Wauquier C, Huez G, Kruys V, Gueydan C. The cold-inducible RNA-binding protein migrates from the nucleus to cytoplasmic stress granules by a methylationdependent mechanism and acts as a translational repressor. Exp Cell Res. 2007;313:4130-44.
58. Zeng Y, Kulkarni P, Inoue T, Getzenberg RH. Downregulating cold shock protein genes impairs cancer cell survival and enhances chemosensitivity. J Cell Biochem. 2009;107: 179-88.
59. Sowter HM, Ratcliffe PJ, Watson P, Greenberg AH, Harris AL. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 2001;61:6669-73.
60. van Balkom BW, Pisitkun T, Verhaar MC, Knepper MA. Exosomes and the kidney: prospects for diagnosis and therapy of renal diseases. Kidney Int. 2011;80:1138-45.
61. Zhou H, Yuen PS, Pisitkun T, Gonzales PA, Yasuda H, Dear JW, et al. Collection, storage, preservation, and normalization of human urinary exosomes for biomarker discovery. Kidney Int. 2006;69:1471-6.
62. Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer. 2009;10:42-6.
63. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470-6.
64. Simpson RJ, Lim JW, Moritz RL, Mathivanan S. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics. 2009;6:267-83.