Human urinary exosome proteome unveils its aerobic respiratory ability

Journal of Proteomics

Volumn 136, Issue , 2016, Pages 25-34

  Bruschi, Maurizio ^a   Santucci, Laura ^a   Ravera, Silvia ^b   Candiano, Giovanni ^a   Bartolucci, Martina ^a   Calzia, Daniela ^b   Lavarello, Chiara ^a   Inglese, Elvira ^a   Ramenghi, Luca A ^a   Petretto, Andrea ^a   Ghiggeri, Gian Marco ^a   Panfoli, Isabella ^b  

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

Exosomes; FoF1 ATP synthase; Mass spectrometry; Oxidative phosphorylation; Proteomics; Respiratory complexes; Urinoma

Indexed keywords

ADENOSINE TRIPHOSPHATE; PROTEOME;

ARTICLE; BIOENERGY; CONTROLLED STUDY; EXOSOME; FEMALE; HUMAN; MALE; MASS SPECTROMETRY; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN URINE LEVEL; PROTEOMICS; URINOMA; ADULT; METABOLISM; OXYGEN CONSUMPTION; URINE;

ADULT; EXOSOMES; FEMALE; HUMANS; MALE; OXYGEN CONSUMPTION; PROTEOME; URINOMA;

EID: 84957927521     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2016.02.001     Document Type: Article

References (58)

1. Mathivanan S., Ji H., Simpson R.J. Exosomes: extracellular organelles important in intercellular communication. J. Proteome 2010, 73:1907-1920. 10.1016/j.jprot.2010.06.006.
2. Camussi G., Deregibus M.C., Bruno S., Cantaluppi V., Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 2010, 78:838-848. 10.1038/ki.2010.278.
3. 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. 10.1016/j.bcp.2011.12.037.
4. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 2013, 200:373-383. 10.1083/jcb.201211138.
5. Conde-Vancells J., Rodriguez-Suarez E., Embade N., Gil D., Matthiesen R., Valle M., et al. Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J. Proteome Res. 2008, 7:5157-5166.
6. Pan B.T., Teng K., Wu C., Adam M., Johnstone R.M. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J. Cell Biol. 1985, 101:942-948.
7. Wollert T., Hurley J.H. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 2010, 464:864-869. 10.1038/nature08849.
8. Kowal J., Tkach M., Théry C. Biogenesis and secretion of exosomes. Curr. Opin. Cell Biol. 2014, 29C:116-125. 10.1016/j.ceb.2014.05.004.
9. Wang D., Sun W. Urinary extracellular microvesicles: isolation methods and prospects for urinary proteome. Proteomics 2014, 14:1922-1932. 10.1002/pmic.201300371.
10. Lässer C., Alikhani V.S., Ekström K., Eldh M., Paredes P.T., Bossios A., et al. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J. Transl. Med. 2011, 9:9. 10.1186/1479-5876-9-9.
11. Pisitkun T., Shen R.-F., Knepper M.A. Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. 2004, 101:13368-13373. 10.1073/pnas.0403453101.
12. Dear J.W., Street J.M., Bailey M.A. Urinary exosomes: a reservoir for biomarker discovery and potential mediators of intrarenal signalling. Proteomics 2013, 13:1572-1580. 10.1002/pmic.201200285.
13. GÃmez-Valero A., Lozano-Ramos S.I., Bancu I., Lauzurica-Valdemoros R., BorrÃs F.E. Urinary extracellular vesicles as source of biomarkers in kidney diseases. Front. Immunol. 2015, 6:6. 10.3389/fimmu.2015.00006.
14. Bourderioux M., Nguyen-Khoa T., Chhuon C., Jeanson L., Tondelier D., Walczak M., et al. A new workflow for proteomic analysis of urinary exosomes and assessment in cystinuria patients. J. Proteome Res. 2015, 14:567-577. 10.1021/pr501003q.
15. Conde-Vancells J., Rodriguez-Suarez E., Embade N., Gil D., Matthiesen R., Valle M., et al. Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J. Proteome Res. 2008, 7:5157-5166. (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2696236&tool=pmcentrez&rendertype=abstract, accessed May 29, 2014).
16. Lin J., Li J., Huang B., Liu J., Chen X., Chen X.-M., et al. Exosomes: novel biomarkers for clinical diagnosis. ScientificWorldJournal 2015, 2015:657086. 10.1155/2015/657086.
17. Kharaziha P., Ceder S., Li Q., Panaretakis T. Tumor cell-derived exosomes: a message in a bottle. Biochim. Biophys. Acta 2012, 1826:103-111. 10.1016/j.bbcan.2012.03.006.
18. Rabinowits G., Gerçel-Taylor C., Day J.M., Taylor D.D., Kloecker G.H. Exosomal microRNA: a diagnostic marker for lung cancer. Clin. Lung Cancer 2009, 10:42-46. 10.3816/CLC.2009.n.006.
19. Hiemstra T.F., Charles P.D., Gracia T., Hester S.S., Gatto L., Al-Lamki R., et al. Human urinary exosomes as innate immune effectors. J. Am. Soc. Nephrol. 2014, 25:2017-2027. 10.1681/ASN.2013101066.
20. Bruschi M., Ravera S., Santucci L., Candiano G., Bartolucci M., Calzia D., et al. Human urinary exosome as a metabolic effector cargo. Expert Rev. Proteomics 2015, (in press).
21. Arslan F., Lai R.C., Smeets M.B., Akeroyd L., Choo A., Aguor E.N.E., et al. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res. 2013, 10:301-312. 10.1016/j.scr.2013.01.002.
22. Islam M.N., Das S.R., Emin M.T., Wei M., Sun L., Westphalen K., et al. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat. Med. 2012, 18:759-765. 10.1038/nm.2736.
23. Lai R.C., Yeo R.W.Y., Lim S.K. Mesenchymal stem cell exosomes. Semin. Cell Dev. Biol. 2015, 10.1016/j.semcdb.2015.03.001.
24. Vishnubhatla I., Corteling R., Stevanato L., Hicks C., Sinden J. The development of stem cell-derived exosomes as a cell-free regenerative medicine. J. Circ. Biomarkers 2014, 3:2.
25. Panfoli I., Ravera S., Podestà M., Cossu C., Santucci L., Bartolucci M., et al. Exosomes from human mesenchymal stem cells conduct aerobic metabolism in term and preterm newborn infants. FASEB J. 2015, (fj.15-279679-). 10.1096/fj.15-279679.
26. Candiano G., Santucci L., Bruschi M., Petretto A., D'Ambrosio C., Scaloni A., et al. "Cheek-to-cheek" urinary proteome profiling via combinatorial peptide ligand libraries: A novel, unexpected elution system. J. Proteome 2012, 75:796-805. 10.1016/j.jprot.2011.09.018.
27. Santucci L., Candiano G., Bruschi M., D'Ambrosio C., Petretto A., Scaloni A., et al. Combinatorial peptide ligand libraries for the analysis of low-expression proteins: validation for normal urine and definition of a first protein MAP. Proteomics 2012, 12:509-515. 10.1002/pmic.201100404.
28. 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). 10.1002/0471143030.cb0322s30.
29. Bruschi M., Musante L., Candiano G., Ghiggeri G.M., Herbert B., Antonucci F., et al. Soft immobilized pH gradient gels in proteome analysis: a follow-up. Proteomics 2003, 3:821-825. 10.1002/pmic.200300361.
30. Ravera S., Panfoli I., Calzia D., Aluigi M.G., Bianchini P., Diaspro A., et al. Evidence for aerobic ATP synthesis in isolated myelin vesicles. Int. J. Biochem. Cell Biol. 2009, 41:1581-1591. (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19401152).
31. Panfoli I., Calzia D., Bianchini P., Ravera S., Diaspro A., Candiano G., et al. Evidence for aerobic metabolism in retinal rod outer segment disks. Int. J. Biochem. Cell Biol. 2009, 41:2555-2565. (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19715769).
32. Ravera S., Aluigi M.G., Calzia D., Ramoino P., Morelli A., Panfoli I. Evidence for ectopic aerobic ATP production on C6 glioma cell plasma membrane. Cell. Mol. Neurobiol. 2011, 31:313-321. (http://www.scopus.com/inward/record.url?eid=2-s2.0-79959759025&partnerID=40&md5=f63374526f565976e02a847b9ef3453a).
33. Dell R.B., Holleran S., Ramakrishnan R. Sample size determination. ILAR J. 2002, 43:207-213. (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3275906&tool=pmcentrez&rendertype=abstract, accessed November 14, 2015).
34. Ravera S., Panfoli I., Aluigi M.G., Calzia D., Morelli A. Characterization of myelin sheath F(o)F(1)-ATP synthase and its regulation by IF(1). Cell Biochem. Biophys. 2011, 59:63-70.
35. Panfoli I., Calzia D., Ravera S., Morelli A.M., Traverso C.E. Extra-mitochondrial aerobic metabolism in retinal rod outer segments: new perspectives in retinopathies. Med. Hypotheses 2012, 78:423-427. (http://www.scopus.com/inward/record.url?eid=2-s2.0-84858153319&partnerID=40&md5=e56a4cae83f471c9fe61a328513de4bf).
36. Ravera S., Bartolucci M., Calzia D., Aluigi M.G., Ramoino P., Morelli A., et al. Tricarboxylic acid cycle-sustained oxidative phosphorylation in isolated myelin vesicles. Biochimie 2013, 95:1991-1998. (S0300-9084(13)00212-[pii]). 10.1016/j.biochi.2013.07.003.
37. Panfoli I., Calzia D., Ravera S., Bruschi M., Tacchetti C., Candiani S., et al. Extramitochondrial tricarboxylic acid cycle in retinal rod outer segments. Biochimie 2011, 93:1565-1575. (http://www.scopus.com/inward/record.url?eid=2-s2.0-79960835049&partnerID=40&md5=721b8dbb62d8fcb2ee51cccbe6d10273).
38. Panfoli I., Ravera S., Bruschi M., Candiano G., Morelli A. Proteomics unravels the exportability of mitochondrial respiratory chains. Expert Rev Proteomics 2011, 8:231-239. (http://www.scopus.com/inward/record.url?eid=2-s2.0-79955062150&partnerID=40&md5=58ccccc6a47132d53dfee7838c7ecefc).
39. Shao C., Wang Y., Gao Y. Applications of urinary proteomics in biomarker discovery. Sci. China Life Sci. 2011, 54:409-417. 10.1007/s11427-011-4162-1.
40. Santucci L., Candiano G., Petretto A., Bruschi M., Lavarello C., Inglese E., et al. From hundreds to thousands: widening the normal human urinome (1). J. Proteome 2015, 112:53-62. 10.1016/j.jprot.2014.07.021.
41. Adachi J., Kumar C., Zhang Y., Olsen J.V., Mann M. The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins. Genome Biol. 2006, 7:R80. 10.1186/gb-2006-7-9-R80.
42. Marimuthu A., O'Meally R.N., Chaerkady R., Subbannayya Y., Nanjappa V., Kumar P., et al. A comprehensive map of the human urinary proteome. J. Proteome Res. 2011, 10:2734-2743. 10.1021/pr2003038.
43. Nagaraj N., Wisniewski J.R., Geiger T., Cox J., Kircher M., Kelso J., et al. Deep proteome and transcriptome mapping of a human cancer cell line. Mol. Syst. Biol. 2011, 7:548. 10.1038/msb.2011.81.
44. Zerefos P.G., Aivaliotis M., Baumann M., Vlahou A. Analysis of the urine proteome via a combination of multi-dimensional approaches. Proteomics 2012, 12:391-400. 10.1002/pmic.201100212.
45. Farrah T., Deutsch E.W., Omenn G.S., Sun Z., Watts J.D., Yamamoto T., et al. State of the human proteome in 2013 as viewed through PeptideAtlas: comparing the kidney, urine, and plasma proteomes for the biology- and disease-driven Human Proteome Project. J. Proteome Res. 2014, 13:60-75. 10.1021/pr4010037.
46. Keerthikumar S., Chisanga D., Ariyaratne D., Al Saffar H., Anand S., Zhao K., et al. ExoCarta: a web-based compendium of exosomal cargo. J. Mol. Biol. 2015, 10.1016/j.jmb.2015.09.019.
47. Prunotto M., Farina A., Lane L., Pernin A., Schifferli J., Hochstrasser D.F., et al. Proteomic analysis of podocyte exosome-enriched fraction from normal human urine. J. Proteome 2013, 82:193-229. 10.1016/j.jprot.2013.01.012.
48. Genova M.L., Baracca A., Biondi A., Casalena G., Faccioli M., Falasca A.I., et al. Is supercomplex organization of the respiratory chain required for optimal electron transfer activity?. Biochim. Biophys. Acta 2008, 1777:740-746. 10.1016/j.bbabio.2008.04.007.
49. Lebiedzinska M., Szabadkai G., Jones A.W.E., Duszynski J., Wieckowski M.R. Interactions between the endoplasmic reticulum, mitochondria, plasma membrane and other subcellular organelles. Int. J. Biochem. Cell Biol. 2009, 41:1805-1816. 10.1016/j.biocel.2009.02.017.
50. Wiedemann N., Meisinger C., Pfanner N. Cell biology. Connecting organelles. Science 2009, 325:403-404. 10.1126/science.1178016.
51. Vance J.E. Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 1990, 265:7248-7256.
52. A.Raturi T.Simmen Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochim. Biophys. Acta 2013, 1833:213-224. 10.1016/j.bbamcr.2012.04.013.
53. Giorgi C., De Stefani D., Bononi A., Rizzuto R., Pinton P. Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int. J. Biochem. Cell Biol. 2009, 41:1817-1827. 10.1016/j.biocel.2009.04.010.
54. Ravera S., Nobbio L., Visigalli D., Bartolucci M., Calzia D., Fiorese F., et al. Oxydative phosphorylation in sciatic nerve myelin and its impairment in a model of dysmyelinating peripheral neuropathy. J. Neurochem. 2013, 126:82-92. 10.1111/jnc.12253.
55. Taylor D.D., Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods 2015, 10.1016/j.ymeth.2015.02.019.
56. Alvarez M.L. Isolation of urinary exosomes for RNA biomarker discovery using a simple, fast, and highly scalable method. Methods Mol. Biol. 2014, 1182:145-170. 10.1007/978-1-4939-1062-5_13.
57. Dragovic R.A., Collett G.P., Hole P., Ferguson D.J.P., Redman C.W., Sargent I.L., et al. Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence nanoparticle tracking analysis. Methods 2015, 10.1016/j.ymeth.2015.03.028.
58. Pisitkun T., Johnstone R., Knepper M.A. Discovery of urinary biomarkers. Mol. Cell. Proteomics 2006, 5:1760-1771. 10.1074/mcp.R600004-MCP200.