Exosomes as new diagnostic tools in CNS diseases

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1862, Issue 3, 2016, Pages 403-410

  Kanninen, Katja M ^a   Bister, Nea ^a   Koistinaho, Jari ^a   Malm, Tarja ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Alzheimer's disease; Exosomes; MicroRNA; Multiple sclerosis; Stroke

Indexed keywords

BIOLOGICAL MARKER;

ALZHEIMER DISEASE; ARTICLE; CENTRAL NERVOUS SYSTEM DISEASE; CEREBROVASCULAR ACCIDENT; ENDOTHELIUM CELL; EXOSOME; HUMAN; MOLECULAR DIAGNOSIS; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 84957849324     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.09.020     Document Type: Article

References (116)

1. Fruhbeis C., Frohlich D., Kuo W.P., Amphornrat J., Thilemann S., Saab A.S., Kirchhoff F., Mobius W., Goebbels S., Nave K.A., Schneider A., Simons M., Klugmann M., Trotter J., Kramer-Albers E.M. Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol. 2013, 11.
2. Kramer-Albers E.M., Bretz N., Tenzer S., Winterstein C., Mobius W., Berger H., Nave K.A., Schild H., Trotter J. Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons?. Proteomics Clin. Appl. 2007, 1:1446-1461.
3. Looze C., Yui D., Leung L., Ingham M., Kaler M., Yao X., Wu W.W., Shen R.F., Daniels M.P., Levine S.J. Proteomic profiling of human plasma exosomes identifies PPARgamma as an exosome-associated protein. Biochem. Biophys. Res. Commun. 2009, 378:433-438.
4. Street J.M., Barran P.E., Mackay C.L., Weidt S., Balmforth C., Walsh T.S., Chalmers R.T., Webb D.J., Dear J.W. Identification and proteomic profiling of exosomes in human cerebrospinal fluid. J. Transl. Med. 2012, 10. (5-5876-10-5).
5. Vojtech L., Woo S., Hughes S., Levy C., Ballweber L., Sauteraud R.P., Strobl J., Westerberg K., Gottardo R., Tewari M., Hladik F. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res. 2014, 42:7290-7304.
6. Michael A., Bajracharya S.D., Yuen P.S., Zhou H., Star R.A., Illei G.G., Alevizos I. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2010, 16:34-38.
7. 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.
8. Admyre C., Johansson S.M., Qazi K.R., Filen J.J., Lahesmaa R., Norman M., Neve E.P., Scheynius A., Gabrielsson S. Exosomes with immune modulatory features are present in human breast milk. J. Immunol. 2007, 179:1969-1978.
9. Urbanelli L., Magini A., Buratta S., Brozzi A., Sagini K., Polchi A., Tancini B., Emiliani C. Signaling pathways in exosomes biogenesis, secretion and fate. Genes (Basel) 2013, 4:152-170.
10. Aryani A., Denecke B. Exosomes as a nanodelivery system: a key to the future of neuromedicine?. Mol. Neurobiol. Dec. 15 2014, 1-17.
11. Friand V., David G., Zimmermann P. Syntenin and syndecan in the biogenesis of exosomes. Biol. Cell. 2015, 107(10):331-341.
12. Kosaka N., Iguchi H., Yoshioka Y., Takeshita F., Matsuki Y., Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J. Biol. Chem. 2010, 285:17442-17452.
13. Bellingham S.A., Coleman B.M., Hill A.F. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res. 2012, 40:10937-10949.
14. Wubbolts R., Leckie R.S., Veenhuizen P.T., Schwarzmann G., Mobius W., Hoernschemeyer J., Slot J.W., Geuze H.J., Stoorvogel W. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J. Biol. Chem. 2003, 278:10963-10972.
15. 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:D1241-D1244.
16. Yang J.M., Gould S.J. The cis-acting signals that target proteins to exosomes and microvesicles. Biochem. Soc. Trans. 2013, 41:277-282.
17. Zarovni N., Corrado A., Guazzi P., Zocco D., Lari E., Radano G., Muhhina J., Fondelli C., Gavrilova J., Chiesi A. Integrated isolation and quantitative analysis of exosome shuttled proteins and nucleic acids using immunocapture approaches. Methods Jun 2 2015, pii: S1046-2023(15)00234-0.
18. Lotvall J., Hill A.F., Hochberg F., Buzas E.I., Di Vizio D., Gardiner C., Gho Y.S., Kurochkin I.V., Mathivanan S., Quesenberry P., Sahoo S., Tahara H., Wauben M.H., Witwer K.W., Thery C. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J. Extracell. Vesicles 2014, 3:26913.
19. Shi M., Liu C., Cook T.J., Bullock K.M., Zhao Y., Ginghina C., Li Y., Aro P., Dator R., He C., Hipp M.J., Zabetian C.P., Peskind E.R., Hu S.C., Quinn J.F., Galasko D.R., Banks W.A., Zhang J. Plasma exosomal alpha-synuclein is likely CNS-derived and increased in Parkinson's disease. Acta Neuropathol. 2014, 128:639-650.
20. Fiandaca M.S., Kapogiannis D., Mapstone M., Boxer A., Eitan E., Schwartz J.B., Abner E.L., Petersen R.C., Federoff H.J., Miller B.L., Goetzl E.J. Identification of preclinical Alzheimer's disease by a profile of pathogenic proteins in neurally derived blood exosomes: a case-control study. Alzheimers Dement. 2015, 11(6):600-607.
21. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
22. Montecalvo A., Larregina A.T., Shufesky W.J., Stolz D.B., Sullivan M.L., Karlsson J.M., Baty C.J., Gibson G.A., Erdos G., Wang Z., Milosevic J., Tkacheva O.A., Divito S.J., Jordan R., Lyons-Weiler J., Watkins S.C., Morelli A.E. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood Jan 19 2012, 119(3):756-766.
23. Okoye I.S., Coomes S.M., Pelly V.S., Czieso S., Papayannopoulos V., Tolmachova T., Seabra M.C., Wilson M.S. MicroRNA-containing T-regulatory-cell-derived exosomes suppress pathogenic T helper 1 cells. Immunity 2014, 41:89-103.
24. Banigan M.G., Kao P.F., Kozubek J.A., Winslow A.R., Medina J., Costa J., Schmitt A., Schneider A., Cabral H., Cagsal-Getkin O., Vanderburg C.R., Delalle I. Differential expression of exosomal microRNAs in prefrontal cortices of schizophrenia and bipolar disorder patients. PLoS One 2013, 8.
25. Von Bartheld C.S., Altick A.L. Multivesicular bodies in neurons: distribution, protein content, and trafficking functions. Prog. Neurobiol. 2011, 93:313-340.
26. Faure J., Lachenal G., Court M., Hirrlinger J., Chatellard-Causse C., Blot B., Grange J., Schoehn G., Goldberg Y., Boyer V., Kirchhoff F., Raposo G., Garin J., Sadoul R. Exosomes are released by cultured cortical neurones. Mol. Cell. Neurosci. 2006, 31:642-648.
27. Lachenal G., Pernet-Gallay K., Chivet M., Hemming F.J., Belly A., Bodon G., Blot B., Haase G., Goldberg Y., Sadoul R. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol. Cell. Neurosci. 2011, 46:409-418.
28. Gosselin R.D., Meylan P., Decosterd I. Extracellular microvesicles from astrocytes contain functional glutamate transporters: regulation by protein kinase C and cell activation. Front. Cell. Neurosci. 2013, 7:251.
29. Guescini M., Genedani S., Stocchi V., Agnati L.F. Astrocytes and glioblastoma cells release exosomes carrying mtDNA. J. Neural Transm. 2010, 117:1-4.
30. Potolicchio I., Carven G.J., Xu X., Stipp C., Riese R.J., Stern L.J., Santambrogio L. Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J. Immunol. 2005, 175:2237-2243.
31. Chivet M., Javalet C., Hemming F., Pernet-Gallay K., Laulagnier K., Fraboulet S., Sadoul R. Exosomes as a novel way of interneuronal communication. Biochem. Soc. Trans. 2013, 41:241-244.
32. Tsunemi T., Hamada K., Krainc D. ATP13A2/PARK9 regulates secretion of exosomes and alpha-synuclein. J. Neurosci. 2014, 34:15281-15287.
33. Yuyama K., Sun H., Mitsutake S., Igarashi Y. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia. J. Biol. Chem. 2012, 287:10977-10989.
34. Goldie B.J., Dun M.D., Lin M., Smith N.D., Verrills N.M., Dayas C.V., Cairns M.J. Activity-associated miRNA are packaged in Map1b-enriched exosomes released from depolarized neurons. Nucleic Acids Res. 2014, 42:9195-9208.
35. Glebov K., Lochner M., Jabs R., Lau T., Merkel O., Schloss P., Steinhauser C., Walter J. Serotonin stimulates secretion of exosomes from microglia cells. Glia 2015, 63:626-634.
36. Hooper C., Sainz-Fuertes R., Lynham S., Hye A., Killick R., Warley A., Bolondi C., Pocock J., Lovestone S. Wnt3a induces exosome secretion from primary cultured rat microglia. BMC Neurosci. 2012, 13. (144-2202-13-144).
37. Grapp M., Wrede A., Schweizer M., Huwel S., Galla H.J., Snaidero N., Simons M., Buckers J., Low P.S., Urlaub H., Gartner J., Steinfeld R. Choroid plexus transcytosis and exosome shuttling deliver folate into brain parenchyma. Nat. Commun. 2013, 4:2123.
38. Lakhal S., Wood M.J. Exosome nanotechnology: an emerging paradigm shift in drug delivery: exploitation of exosome nanovesicles for systemic in vivo delivery of RNAi heralds new horizons for drug delivery across biological barriers. BioEssays 2011, 33:737-741.
39. Kalani A., Tyagi A., Tyagi N. Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics. Mol. Neurobiol. 2014, 49:590-600.
40. Haqqani A.S., Delaney C.E., Tremblay T.L., Sodja C., Sandhu J.K., Stanimirovic D.B. Method for isolation and molecular characterization of extracellular microvesicles released from brain endothelial cells. Fluids Barriers CNS 2013, 10. (4-8118-10-4).
41. Fitzner D., Schnaars M., van Rossum D., Krishnamoorthy G., Dibaj P., Bakhti M., Regen T., Hanisch U.K., Simons M. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J. Cell Sci. 2011, 124:447-458.
42. Morel L., Regan M., Higashimori H., Ng S.K., Esau C., Vidensky S., Rothstein J., Yang Y. Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. J. Biol. Chem. 2013, 288:7105-7116.
43. Smalheiser N.R. Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol. Direct 2007, 2:35.
44. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 2013, 200:373-383.
45. Simons M., Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 2009, 21:575-581.
46. van Balkom B.W., de Jong O.G., Smits M., Brummelman J., den Ouden K., de Bree P.M., van Eijndhoven M.A., Pegtel D.M., Stoorvogel W., Wurdinger T., Verhaar M.C. Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood 2013, 121:3997-4006. (S1-15).
47. Gutzeit C., Nagy N., Gentile M., Lyberg K., Gumz J., Vallhov H., Puga I., Klein E., Gabrielsson S., Cerutti A., Scheynius A. Exosomes derived from Burkitt's lymphoma cell lines induce proliferation, differentiation, and class-switch recombination in B cells. J. Immunol. 2014, 192:5852-5862.
48. Zhang B., Yin Y., Lai R.C., Tan S.S., Choo A.B., Lim S.K. Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells Dev. 2014, 23:1233-1244.
49. van der Pol E., Boing A.N., Harrison P., Sturk A., Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol. Rev. 2012, 64:676-705.
50. Rajendran L., Bali J., Barr M.M., Court F.A., Kramer-Albers E.M., Picou F., Raposo G., van der Vos K.E., van Niel G., Wang J., Breakefield X.O. Emerging roles of extracellular vesicles in the nervous system. J. Neurosci. 2014, 34:15482-15489.
51. Antonucci F., Turola E., Riganti L., Caleo M., Gabrielli M., Perrotta C., Novellino L., Clementi E., Giussani P., Viani P., Matteoli M., Verderio C. Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism. EMBO J. 2012, 31:1231-1240.
52. Wang S., Cesca F., Loers G., Schweizer M., Buck F., Benfenati F., Schachner M., Kleene R. Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes. J. Neurosci. 2011, 31:7275-7290.
53. Pusic A.D., Pusic K.M., Clayton B.L., Kraig R.P. IFNgamma-stimulated dendritic cell exosomes as a potential therapeutic for remyelination. J. Neuroimmunol. 2014, 266:12-23.
54. Pusic A.D., Kraig R.P. Youth and environmental enrichment generate serum exosomes containing miR-219 that promote CNS myelination. Glia 2014, 62:284-299.
55. Williams J.L., Gatson N.N., Smith K.M., Almad A., McTigue D.M., Whitacre C.C. Serum exosomes in pregnancy-associated immune modulation and neuroprotection during CNS autoimmunity. Clin. Immunol. 2013, 149:236-243.
56. Gatson N.N., Williams J.L., Powell N.D., McClain M.A., Hennon T.R., Robbins P.D., Whitacre C.C. Induction of pregnancy during established EAE halts progression of CNS autoimmune injury via pregnancy-specific serum factors. J. Neuroimmunol. 2011, 230:105-113.
57. Lopez-Verrilli M.A., Picou F., Court F.A. Schwann cell-derived exosomes enhance axonal regeneration in the peripheral nervous system. Glia 2013, 61:1795-1806.
58. Zhang Y., Chopp M., Meng Y., Katakowski M., Xin H., Mahmood A., Xiong Y. Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J. Neurosurg. 2015, 122:856-867.
59. Chivet M., Hemming F., Pernet-Gallay K., Fraboulet S., Sadoul R. Emerging role of neuronal exosomes in the central nervous system. Front. Physiol. 2012, 3:145.
60. Tsilioni I., Panagiotidou S., Theoharides T.C. Exosomes in neurologic and psychiatric disorders. Clin. Ther. 2014, 36:882-888.
61. Paschon V., Takada S.H., Ikebara J.M., Sousa E., Raeisossadati R., Ulrich H., Kihara A.H. Interplay between exosomes, microRNAs and Toll-like receptors in brain disorders. Mol. Neurobiol. Apr 11 2015, 1-13.
62. Rajendran L., Honsho M., Zahn T.R., Keller P., Geiger K.D., Verkade P., Simons K. Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:11172-11177.
63. Saman S., Kim W., Raya M., Visnick Y., Miro S., Saman S., Jackson B., McKee A.C., Alvarez V.E., Lee N.C., Hall G.F. Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. J. Biol. Chem. 2012, 287:3842-3849.
64. Emmanouilidou E., Melachroinou K., Roumeliotis T., Garbis S.D., Ntzouni M., Margaritis L.H., Stefanis L., Vekrellis K. Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci. 2010, 30:6838-6851.
65. Gomes C., Keller S., Altevogt P., Costa J. Evidence for secretion of Cu,Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci. Lett. 2007, 428:43-46.
66. Fevrier B., Vilette D., Archer F., Loew D., Faigle W., Vidal M., Laude H., Raposo G. Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9683-9688.
67. Yuyama K., Sun H., Usuki S., Sakai S., Hanamatsu H., Mioka T., Kimura N., Okada M., Tahara H., Furukawa J., Fujitani N., Shinohara Y., Igarashi Y. A potential function for neuronal exosomes: sequestering intracerebral amyloid-beta peptide. FEBS Lett. 2015, 589:84-88.
68. Danzer K.M., Kranich L.R., Ruf W.P., Cagsal-Getkin O., Winslow A.R., Zhu L., Vanderburg C.R., McLean P.J. Exosomal cell-to-cell transmission of alpha synuclein oligomers. Mol. Neurodegener. 2012, 7. (42-1326-7-42).
69. Basso M., Pozzi S., Tortarolo M., Fiordaliso F., Bisighini C., Pasetto L., Spaltro G., Lidonnici D., Gensano F., Battaglia E., Bendotti C., Bonetto V. Mutant copper-zinc superoxide dismutase (SOD1) induces protein secretion pathway alterations and exosome release in astrocytes: implications for disease spreading and motor neuron pathology in amyotrophic lateral sclerosis. J. Biol. Chem. 2013, 288:15699-15711.
70. Perez-Gonzalez R., Gauthier S.A., Kumar A., Levy E. The exosome secretory pathway transports amyloid precursor protein carboxyl-terminal fragments from the cell into the brain extracellular space. J. Biol. Chem. 2012, 287:43108-43115.
71. Xiao H., Wong D.T. Proteomic analysis of microvesicles in human saliva by gel electrophoresis with liquid chromatography-mass spectrometry. Anal. Chim. Acta 2012, 723:61-67.
72. Witwer K.W., Buzas E.I., Bemis L.T., Bora A., Lasser C., Lotvall J., Nolte-'t Hoen E.N., Piper M.G., Sivaraman S., Skog J., Thery C., Wauben M.H., Hochberg F. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J. Extracell. Vesicles 2013, 2. (eCollection 2013). 10.3402/jev.v2i0.20360.
73. Zeringer E., Barta T., Li M., Vlassov A.V. Strategies for isolation of exosomes. Cold Spring Harb. Protoc. 2015, 2015. (pdb.top074476.).
74. Lasser C., Eldh M., Lotvall J. Isolation and characterization of RNA-containing exosomes. J. Vis. Exp. 2012, (59). (e3037).
75. Van Deun J., Mestdagh P., Sormunen R., Cocquyt V., Vermaelen K., Vandesompele J., Bracke M., De Wever O., Hendrix A. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J. Extracell. Vesicles 2014, 3. (eCollection 2014). 10.3402/jev.v3.24858.
76. Tauro B.J., Greening D.W., Mathias R.A., Ji H., Mathivanan S., Scott A.M., Simpson R.J. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods 2012, 56:293-304.
77. Zhou H., Yuen P.S., Pisitkun T., Gonzales P.A., Yasuda H., Dear J.W., Gross P., Knepper M.A., Star R.A. Collection, storage, preservation, and normalization of human urinary exosomes for biomarker discovery. Kidney Int. 2006, 69:1471-1476.
78. Ge Q., Zhou Y., Lu J., Bai Y., Xie X., Lu Z. miRNA in plasma exosome is stable under different storage conditions. Molecules 2014, 19:1568-1575.
79. Thery C., Boussac M., Veron 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.
80. Lasser C. Identification and analysis of circulating exosomal microRNA in human body fluids. Methods Mol. Biol. 2013, 1024:109-128.
81. Kapogiannis D., Boxer A., Schwartz J.B., Abner E.L., Biragyn A., Masharani U., Frassetto L., Petersen R.C., Miller B.L., Goetzl E.J. Dysfunctionally phosphorylated type 1 insulin receptor substrate in neural-derived blood exosomes of preclinical Alzheimer's disease. FASEB J. 2015, 29:589-596.
82. Inglis H., Norris P., Danesh A. Techniques for the analysis of extracellular vesicles using flow cytometry. J. Vis. Exp. 2015, (97). 10.3791/52484.
83. Dragovic R.A., Collett G.P., Hole P., Ferguson D.J., Redman C.W., Sargent I.L., Tannetta D.S. Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence nanoparticle tracking analysis. Methods Apr 3 2015, pii: S1046-2023(15)00145-0.
84. Pospichalova V., Svoboda J., Dave Z., Kotrbova A., Kaiser K., Klemova D., Ilkovics L., Hampl A., Crha I., Jandakova E., Minar L., Weinberger V., Bryja V. Simplified protocol for flow cytometry analysis of fluorescently labeled exosomes and microvesicles using dedicated flow cytometer. J. Extracell. Vesicles 2015, 4:25530.
85. van der Vlist E.J., Nolte-'t Hoen E.N., Stoorvogel W., Arkesteijn G.J., Wauben M.H. Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution flow cytometry. Nat. Protoc. 2012, 7:1311-1326.
86. Boukouris S., Mathivanan S. Exosomes in bodily fluids are a highly stable resource of disease biomarkers. Proteomics Clin. Appl. Apr 2015, 9(3-4):358-3567.
87. Lin J., Li J., Huang B., Liu J., Chen X., Chen X.M., Xu Y.M., Huang L.F., Wang X.Z. Exosomes: novel biomarkers for clinical diagnosis. ScientificWorldJournal 2015, 2015:657086.
88. Kawikova I., Askenase P.W. Diagnostic and therapeutic potentials of exosomes in CNS diseases. Brain Res. Aug. 18 2015, 1617:63-71.
89. Manterola L., Guruceaga E., Gallego Perez-Larraya J., Gonzalez-Huarriz M., Jauregui P., Tejada S., Diez-Valle R., Segura V., Sampron N., Barrena C., Ruiz I., Agirre A., Ayuso A., Rodriguez J., Gonzalez A., Xipell E., Matheu A., Lopez de Munain A., Tunon T., Zazpe I., Garcia-Foncillas J., Paris S., Delattre J.Y., Alonso M.M. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro-Oncology 2014, 16:520-527.
90. Manterola L., Guruceaga E., Gállego Pérez-Larraya J., González-Huarriz M., Jauregui P., Tejada S., Diez-Valle R., Segura V., Samprón N., Barrena C., Ruiz I., Agirre A., Ayuso A., Rodríguez J., González A., Xipell E., Matheu A., López de Munain A., Tuñón T., Zazpe I., García-Foncillas J., Paris S., Delattre J.Y., Alonso M.M. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro. Oncol Apr 2014, 16(4):520-527.
91. Jia H.L., He C.H., Wang Z.Y., Xu Y.F., Yin G.Q., Mao L.J., Liu C.W., Deng L. MicroRNA expression profile in exosome discriminates extremely severe infections from mild infections for hand, foot and mouth disease. BMC Infect. Dis Sep. 17 2014, 14:506.
92. Bellingham S.A., Guo B.B., Coleman B.M., Hill A.F. Exosomes: vehicles for the transfer of toxic proteins associated with neurodegenerative diseases?. Front. Physiol. 2012, 3:124.
93. Seubert P., Oltersdorf T., Lee M.G., Barbour R., Blomquist C., Davis D.L., Bryant K., Fritz L.C., Galasko D., Thal L.J. Secretion of beta-amyloid precursor protein cleaved at the amino terminus of the beta-amyloid peptide. Nature 1993, 361:260-263.
94. Hardy J. Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci. 1997, 20:154-159.
95. Esch F.S., Keim P.S., Beattie E.C., Blacher R.W., Culwell A.R., Oltersdorf T., McClure D., Ward P.J. Cleavage of amyloid beta peptide during constitutive processing of its precursor. Science 1990, 248:1122-1124.
96. Dubois B., Feldman H.H., Jacova C., Dekosky S.T., Barberger-Gateau P., Cummings J., Delacourte A., Galasko D., Gauthier S., Jicha G., Meguro K., O'brien J., Pasquier F., Robert P., Rossor M., Salloway S., Stern Y., Visser P.J., Scheltens P. Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS-ADRDA criteria. Lancet Neurol. 2007, 6:734-746.
97. Vingtdeux V., Hamdane M., Loyens A., Gele P., Drobeck H., Begard S., Galas M.C., Delacourte A., Beauvillain J.C., Buee L., Sergeant N. Alkalizing drugs induce accumulation of amyloid precursor protein by-products in luminal vesicles of multivesicular bodies. J. Biol. Chem. 2007, 282:18197-18205.
98. Sharples R.A., Vella L.J., Nisbet R.M., Naylor R., Perez K., Barnham K.J., Masters C.L., Hill A.F. Inhibition of gamma-secretase causes increased secretion of amyloid precursor protein C-terminal fragments in association with exosomes. FASEB J. 2008, 22:1469-1478.
99. Chiasserini D., van Weering J.R., Piersma S.R., Pham T.V., Malekzadeh A., Teunissen C.E., de Wit H., Jimenez C.R. Proteomic analysis of cerebrospinal fluid extracellular vesicles: a comprehensive dataset. J. Proteome 2014, 106:191-204.
100. Goetzl E.J., Boxer A., Schwartz J.B., Abner E.L., Petersen R.C., Miller B.L., Kapogiannis D. Altered lysosomal proteins in neural-derived plasma exosomes in preclinical Alzheimer disease. Neurology Jul 7 2015, 85(1):40-47.
101. Cheng L., Doecke J.D., Sharples R.A., Villemagne V.L., Fowler C.J., Rembach A., Martins R.N., Rowe C.C., Macaulay S.L., Masters C.L., Hill A.F. Prognostic serum miRNA biomarkers associated with Alzheimer's disease shows concordance with neuropsychological and neuroimaging assessment. Mol. Psychiatry 2015, 20(10):1188-1196.
102. Bevan C., Gelfand J.M. Therapeutic management of severe relapses in multiple sclerosis. Curr. Treat. Options Neurol. 2015, 17. (345-015-0345-6).
103. Gelfand J.M. Multiple sclerosis: diagnosis, differential diagnosis, and clinical presentation. Handb. Clin. Neurol. 2014, 122:269-290.
104. Scolding N.J., Morgan B.P., Houston W.A., Linington C., Campbell A.K., Compston D.A. Vesicular removal by oligodendrocytes of membrane attack complexes formed by activated complement. Nature 1989, 339:620-622.
105. Minagar A., Jy W., Jimenez J.J., Sheremata W.A., Mauro L.M., Mao W.W., Horstman L.L., Ahn Y.S. Elevated plasma endothelial microparticles in multiple sclerosis. Neurology 2001, 56:1319-1324.
106. Langer-Gould A., Garren H., Slansky A., Ruiz P.J., Steinman L. Late pregnancy suppresses relapses in experimental autoimmune encephalomyelitis: evidence for a suppressive pregnancy-related serum factor. J. Immunol. 2002, 169:1084-1091.
107. McClain M.A., Gatson N.N., Powell N.D., Papenfuss T.L., Gienapp I.E., Song F., Shawler T.M., Kithcart A., Whitacre C.C. Pregnancy suppresses experimental autoimmune encephalomyelitis through immunoregulatory cytokine production. J. Immunol. 2007, 179:8146-8152.
108. Giovannelli I., Martelli F., Repice A., Massacesi L., Azzi A., Giannecchini S. Detection of JCPyV microRNA in blood and urine samples of multiple sclerosis patients under natalizumab therapy. J. Neurovirol. Feb 13 2015, 1-5.
109. Donnan G.A., Fisher M., Macleod M., Davis S.M. Stroke. Lancet 2008, 371:1612-1623.
110. Roth J.M. Recombinant tissue plasminogen activator for the treatment of acute ischemic stroke. Proc. (Baylor Univ. Med. Cent.) 2011, 24:257-259.
111. Generalized efficacy of t-PA for acute stroke. Subgroup analysis of the NINDS t-PA Stroke Trial. Stroke 1997, 28:2119-2125.
112. Jickling G.C., Sharp F.R. Blood biomarkers of ischemic stroke. Neurotherapeutics 2011, 8:349-360.
113. Xin H., Li Y., Cui Y., Yang J.J., Zhang Z.G., Chopp M. Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. J. Cereb. Blood Flow Metab. 2013, 33:1711-1715.
114. Levine D.A., Galecki A.T., Langa K.M., Unverzagt F.W., Kabeto M.U., Giordani B., Wadley V.G. Trajectory of cognitive decline after incident stroke. JAMA 2015, 314:41-51.
115. Liu Y., Zhang J., Han R., Liu H., Sun D., Liu X. Downregulation of serum brain specific microRNA is associated with inflammation and infarct volume in acute ischemic stroke. J. Clin. Neurosci. 2015, 22:291-295.
116. Laskowitz D.T., Kasner S.E., Saver J., Remmel K.S., Jauch E.C., BRAIN Study Group Clinical usefulness of a biomarker-based diagnostic test for acute stroke: the Biomarker Rapid Assessment in Ischemic Injury (BRAIN) study. Stroke 2009, 40:77-85.