Retinal pigment epithelium (RPE) exosomes contain signaling phosphoproteins affected by oxidative stress

Experimental Cell Research

Volumn 319, Issue 13, 2013, Pages 2113-2123

  Biasutto, Lucia ^a,b   Chiechi, Antonella ^c   Couch, Robin ^c   Liotta, Lance A ^c   Espina, Virginia ^c  

^a CNR   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c GEORGE MASON UNIVERSITY   (United States)

Author keywords

Age related macular degeneration; ARPE 19 cells; Exosomes; Oxidative stress; Reverse phase protein arrays

Indexed keywords

ACETYL COENZYME A; CARBOXYLASE; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOPROTEIN; PROTEIN KINASE B; PROTEIN KINASE P60; TRANSCRIPTION FACTOR ELK 1;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL METABOLISM; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; EXOSOME; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MICROARRAY; PROTEIN SECRETION; SIGNAL TRANSDUCTION; UPREGULATION; VITREOUS BODY;

EID: 84879880971     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.05.005     Document Type: Article

References (69)

1. Ahmed K., Xiang J. Mechanisms of cellular communication through intercellular protein transfer. J. Cell. Mol. Med. 2011, 15:1458-1473.
2. Alcazar O., Hawkridge A.M., Collier T.S., Cousins S.W., Bhattacharya S.K., Muddiman D.C., Marin-Castano M.E. Proteomics characterization of cell membrane blebs in human retinal pigment epithelium cells. Mol. Cell. Proteomics 2009, 8:2201-2211.
3. Andersen C.L., Jensen J.L., Ørntoft T.F. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004, 64:5245-5250.
4. Barton G.M., Kagan J.C. A cell biological view of toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 2009, 9:535-542.
5. Bejjani R.A., BenEzra D., Cohen H., Rieger J., Andrieu C., Jeanny J.C., Gollomb G., Behar-Cohen F.F. Nanoparticles for gene delivery to retinal pigment epithelial cells. Mol. Vis. 2005, 11:124-132.
6. Belting M., Nanotubes Wittrup A. exosomes, and nucleic acid-binding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease. J. Cell Biol. 2008, 183:1187-1191.
7. Birch D.G., Liang F.Q. Age-related macular degeneration: a target for nanotechnology derived medicines. Int. J. Nanomed. 2007, 2:65-77.
8. Boulton M., Dayhaw-Barker P. The role of the retinal pigment epithelium: topographical variation and ageing changes. Eye (London) 2001, 15:384-389.
9. Bourges J.L., Gautier S.E., Delie F., Bejjani R.A., Jeanny J.C., Gurny R., BenEzra D., Behar-Cohen F.F. Ocular drug delivery targeting the retina and retinal pigment epithelium using polylactide nanoparticles. Invest. Ophthalmol. Vis. Sci. 2003, 44:3562-3569.
10. Charboneau L., Tory H., Chen T., Winters M., Petricoin E.F., Liotta L., Paweletz C. Utility of reverse phase protein arrays: applications to signalling pathways and human body arrays. Brief Funct. Genomic Proteomic 2002, 1:305-315.
11. Chiechi A., Mueller C., Boehm K.M., Romano A., Benassi M.S., Picci P., Liotta L.A., Espina V. Improved data normalization methods for reverse phase protein microarray analysis of complex biological samples. BioTechniques 2012, 0:1-7.
12. Cho W.G., Albuquerque R.J., Kleinman M.E., Tarallo V., Greco A., Nozaki M., Green M.G., Baffi J.Z., Ambati B.K., De Falco M., Alexander J.S., Brunetti A., De Falco S., Ambati J. Small interfering RNA-induced TLR3 activation inhibits blood and lymphatic vessel growth. Proc. Nat. Acad. Sci. USA 2009, 106:7137-7142.
13. Circu M.L., Aw T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radical Biol. Med. 2010, 48:749-762.
14. Davuluri G., Espina V., Er Petricoin, Ross M., Deng J., Liotta L., Glaser B. Activated VEGF receptor shed into the vitreous in eyes with wet AMD: a new class of biomarkers in the vitreous with potential for predicting the treatment timing and monitoring response. Arch. Ophthalmol. 2009, 127:613-621.
15. Ding X., Patel M., Chan C. Molecular pathology of age-related macular degeneration. Prog. Retin. Eye Res. 2009, 28:1-18.
16. Dorey C., Wu G., Ebenstein D., Garsd A., Weiter J. Cell loss in the aging retina. Relationship to lipofuscin accumulation and macular degeneration. Invest. Ophthalmol. Vis. Sci. 1989, 30:1691-1699.
17. Dunn K., Aotaki-Keen A., Putkey F., Hjelmeland L. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 1996, 62:155-169.
18. Février B., Raposo G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 2004, 16:415-421.
19. Finnemann S. Focal adhesion kinase signaling promotes phagocytosis of integrin-bound photoreceptors. EMBO J. 2003, 22:4143-4154.
20. Gehrs K., Anderson D., Johnson L., Hageman G. Age-related macular degeneration-emerging pathogenetic and therapeutic concepts. Ann. Med. 2006, 38:450-471.
21. Gonzales P.A., Pisitkun T., Hoffert J.D., Tchapyjnikov D., Star R.A., Kleta R., Wang N.S., Knepper M.A. Large-scale proteomics and phosphoproteomics of urinary exosomes. J. Am. Soc. Nephrol. 2009, 20:363-379.
22. Gough D.R., Cotter T.G. Hydrogen peroxide: a Jekyll and Hyde signalling molecule. Cell Death Dis. 2011, 2:e213.
23. Groeger G., Quiney C., Cotter T.G. Hydrogen peroxide as a cell-survival signaling molecule. Antioxid. Redox Signaling 2009, 11:2655-2671.
24. Ha J., Daniel S., Broyles S.S., Kim K.H. Critical phosphorylation sites for acetyl-CoA carboxylase activity. J. Biol. Chem. 1994, 269:22162-22168.
25. Jager R., Mieler W., Miller J. Age-related macular degeneration. N. Engl. J. Med. 2008, 358:2606-2617.
26. Johnson E. Age-related macular degeneration and antioxidant vitamins: recent findings. Curr. Opin. Clin. Nutr. Metab. Care 2010, 13:28-33.
27. Kaarniranta K., Salminen A. Age-related macular degeneration: activation of innate immunity system via pattern recognition receptors. J. Mol. Med. 2009, 87:117-123.
28. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat. Immunol. 2010, 11:373-384.
29. Kevany B., Palczewski K. Phagocytosis of retinal rod and cone photoreceptors. Physiology (Bethesda) 2010, 25:8-15.
30. Kleinman M.E., Kaneko H., Cho W.G., Dridi S., Fowler B.J., Blandford A.D., Albuquerque R.J., Hirano Y., Terasaki H., Kondo M., Fujita T., Ambati B.K., Tarallo V., Gelfand B.D., Bogdanovich S., Baffi J.Z., Ambati J. Short-interfering RNAs induce retinal degeneration via TLR3 and IRF3. Mol. Ther. 2012, 20:101-108.
31. Kleinman M.E., Yamada K., Takeda A., Chandrasekaran V., Nozaki M., Baffi J.Z., Albuquerque R.J., Yamasaki S., Itaya M., Pan Y., Appukuttan B., Gibbs D., Yang Z., Karikó K., Ambati B.K., Wilgus T.A., DiPietro L.A., Sakurai E., Zhang K., Smith J.R., Taylor E.W., Ambati J. Sequence- and target-independent angiogenesis suppression by siRNA via TLR3. Nature 2008, 452:591-597.
32. Koopman W., Nijtmans L., Dieteren C., Roestenberg P., Valsecchi F., Smeitink J., Willems P. Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid. Redox Signaling 2010, 12:1431-1470.
33. Lu L., Hackett S.F., Mincey A., Lai H., Campochiaro P.A. Effects of different types of oxidative stress in RPE cells. J. Cell Physiol. 2006, 206:119-125.
34. Maa M.C., Leu T.H. Vanadate-dependent FAK activation is accomplished by the sustained FAK Tyr-576/577 phosphorylation. Biochem. Biophys. Res. Commun. 1998, 251:344-349.
35. Maloney S.C., Antecka E., Orellana M.E., Fernandes B.F., Odashiro A.N., Eghtedari M., Burnier M.N. Choroidal neovascular membranes express toll-like receptor 3. Ophthalmic Res. 2010, 44:237-241.
36. Mathivanan S., Fahner C.J., Reid G.E., Simpson R.J. ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 2012, 40(Database issue):D1241-D1244.
37. Mathivanan S., Simpson R. ExoCarta: a compendium of exosomal proteins and RNA. Proteomics 2009, 9:4997-5000.
38. Miceli M., Liles M., Newsome D. Evaluation of oxidative processes in human pigment epithelial cells associated with retinal outer segment phagocytosis. Exp. Cell Res. 1994, 214:242-249.
39. Mueller C., Liotta L.A., Espina V. Reverse phase protein microarrays advance to use in clinical trials. Mol. Oncol. 2010, 4:461-481.
40. Nandrot E., Kim Y., Brodie S., Huang X., Sheppard D., Finnemann S. Loss of synchronized retinal phagocytosis and age-related blindness in mice lacking alphavbeta5 integrin. J. Exp. Med. 2004, 200:1539-1545.
41. Ng K., Gugiu B., Renganathan K., Davies M., Gu X., Crabb J., Kim S., Rózanowska M., Bonilha V., Rayborn M., Salomon R., Sparrow J., Boulton M., Hollyfield J., Crabb J. Retinal pigment epithelium lipofuscin proteomics. Mol. Cell Proteomics 2008, 7:1397-1405.
42. Oliver F.J., de la Rubia G., Rolli V., Ruiz-Ruiz M.C., de Murcia G., Murcia J.M. Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J. Biol. Chem. 1998, 273:33533-33539.
43. Palanisamy V., Sharma S., Deshpande A., Zhou H., Gimzewski J., Wong D. Nanostructural and transcriptomic analyses of human saliva derived exosomes. PLoS One 2010, 5:e8577.
44. Palmisano G., Jensen S.S., Le Bihan M.C., Laine J., McGuire J.N., Pociot F., Larsen M.R. Characterization of membrane-shed micro-vesicles from cytokine-stimulated beta-cells using proteomics strategies. Mol. Cell Proteomics 2012, 11:230-243.
45. Pant S., Hilton H., Burczynski M.E. The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem. Pharmacol. 2012, 83:1484-1494.
46. Plafker S. Oxidative stress and the ubiquitin proteolytic system in age-related macular degeneration. Adv. Exp. Med. Biol. 2010, 664:447-456.
47. Qin S. Oxidative damage of retinal pigment epithelial cells and age-related macular degeneration. Drug Dev.. Res. 2007, 68:213-225.
48. Schlaepfer D.D., Hauck C.R., Sieg D.J. Signaling through focal adhesion kinase. Prog. Biophys. Mol. Biol. 1999, 71:435-478.
49. Sharma S., Rasool H., Palanisamy V., Mathisen C., Schmidt M., Wong D., Gimzewski J. Structural-mechanical characterization of nanoparticle exosomes in human saliva, using correlative AFM, FESEM, and force spectroscopy. ACS Nano 2010, 4:1921-1926.
50. Simpson R., Jensen S., Lim J. Proteomic profiling of exosomes: current perspectives. Proteomics 2008, 8:4083-4099.
51. Speer R., Wulfkuhle J., Espina V., Aurajo R., Edmiston K., Liotta L., Petricoin E.F. Development of reverse phase protein microarrays for clinical applications and patient-tailored therapy. Cancer Genomics Proteomics 2007, 4:157-164.
52. Suntres Z. Role of antioxidants in paraquat toxicity. Toxicology 2002, 180:65-77.
53. Tamburro D., Facchiano F., Petricoin E.F., Liotta L.A., Zhou W. Mass spectrometry-based characterization of the vitreous phosphoproteome. Proteomics Clin. Appl. 2010, 4:839-846.
54. Théry 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:Unit 3.22.
55. Théry C., Boussac M., Véron P., Ricciardi-Castagnoli P., Raposo G., Garin J., Amigorena S. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 2001, 166:7309-7318.
56. Théry C., Zitvogel L., Amigorena S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2002, 2:569-579.
57. Tschopp J. Mitochondria: sovereign of inflammation?. Eur. J. Immunol. 2011, 41:1196-1202.
58. van Niel G., Porto-Carreiro I., Simoes S., Raposo G. Exosomes: a common pathway for a specialized function. J. Biochem. 2006, 140:13-21.
59. Vanlangenakker N., Vanden Berghe T., Krysko D.V., Festjens N., Vandenabeele P. Molecular mechanisms and pathophysiology of necrotic cell death. Curr. Mol. Med. 2008, 8:207-220.
60. VanMeter A., Rodriguez A., Bowman E., Jen J., Harris C., Deng J., Calvert V., Silvestri A., Fredolini C., Chandhoke V., Petricoin E.F., Liotta L., Espina V. Laser capture microdissection and protein microarray analysis of human non-small cell lung cancer: differential epidermal growth factor receptor (EGPR) phosphorylation events associated with mutated EGFR compared with wild type. Mol. Cell Proteomics 2008, 7:1902-1924.
61. VanMeter A., Signore M., Pierobon M., Espina V., Liotta L., Petricoin E.F. Reverse-phase protein microarrays: application to biomarker discovery and translational medicine. Expert Rev. Mol. Diagn. 2007, 7:625-633.
62. Wang A., Lukas T., Yuan M., Du N., Tso M., Neufeld A. Autophagy and exosomes in the aged retinal pigment epithelium: possible relevance to drusen formation and age-related macular degeneration. PLoS One 2009, 4:e4160.
63. Weigel A., Handa J., Hjelmeland L. Microarray analysis of H2O2-, HNE-, or tBH-treated ARPE-19 cells. Free Radical Biol. Med. 2002, 33:1419-1432.
64. Wilson B., Liotta L., Petricoin E.F. Monitoring proteins and protein networks using reverse phase protein arrays. Dis. Markers 2010, 28:225-232.
65. Wolf G. Lipofuscin and macular degeneration. Nutr. Rev. 2003, 61:342-346.
66. Wu S.B., Wei Y.H. AMPK-mediated increase of glycolysis as an adaptive response to oxidative stress in human cells: implication of the cell survival in mitochondrial diseases. Biochim. Biophys. Acta 2012, 1822:233-247.
67. Wu Y., Yanase E., Feng X., Siegel M., Sparrow J. Structural characterization of bisretinoid A2E photocleavage products and implications for age-related macular degeneration. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:7275-7280.
68. Yu D., Cringle S. Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog. Retin. Eye Res. 2001, 20:175-208.
69. Zarbin M. Current concepts in the pathogenesis of age-related macular degeneration. Arch. Ophthalmol. 2004, 122:598-614.