More than cell dust: Microparticles isolated from cerebrospinal fluid of brain injured patients are messengers carrying mRNAs, miRNAs, and proteins

Journal of Neurotrauma

Volumn 30, Issue 14, 2013, Pages 1232-1242

  Patz, Silke ^a   Trattnig, Christa ^a   Grünbacher, Gerda ^a   Ebner, Birgit ^a   Gülly, Christian ^a   Novak, Alexandra ^a   Rinner, Beate ^a   Leitinger, Gerd ^a   Absenger, Markus ^a   Tomescu, Oana A ^b   Thallinger, Gerhard G ^b   Fasching, Ulrike ^a   Wissa, Sonja ^a   Archelos Garcia, Juan ^a   Schäfer, Ute ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

cerebrospinal fluid; microparticles; microRNA; traumatic brain injury

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 9; PROTEIN; RNA;

ADULT; ARTICLE; BRAIN INJURY; CEREBROSPINAL FLUID; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOCHEMISTRY; ELECTRON MICROSCOPY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MICROARRAY ANALYSIS; NEURAL STEM CELL; TARGET CELL; WESTERN BLOTTING;

ADULT; AGED; BLOTTING, WESTERN; BRAIN INJURIES; CELL LINE; CELL-DERIVED MICROPARTICLES; COMPUTATIONAL BIOLOGY; FEMALE; FLOW CYTOMETRY; GENE SILENCING; GLASGOW COMA SCALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICRORNAS; MICROSCOPY, ELECTRON; MIDDLE AGED; NERVE TISSUE PROTEINS; POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84880341728     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2596     Document Type: Article

References (50)

1. Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A., and Ratajczak, M.Z. (2006). Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487-1495. (Pubitemid 44264090)
2. Hunter, M.P., Ismail, N., Zhang, X., Aguda, B.D., Lee, E.J., Yu, L., Xiao, T., Schafer, J., Lee, M.L., Schmittgen, T.D., Nana-Sinkam, S.P., Jarjoura, D., and Marsh, C.B. (2008). Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 3, e3694.
3. Garcia, B.A., Smalley, D.M., Cho, H., Shabanowitz, J., Ley, K., and Hunt, D.F. (2005). The platelet microparticle proteome. J. Proteome Res. 4, 1516-1521. (Pubitemid 41464776)
4. Gibbings, D.J., Ciaudo, C., Erhardt, M., and Voinnet, O. (2009). Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol. 11, 1143-1149.
5. van der Vos, K.E., Balaj, L., Skog, J., and Breakefield, X.O. (2011). Brain tumor microvesicles: insights into intercellular communication in the nervous system. Cell Mol. Neurobiol. 31, 949-959.
6. Wolf, P. (1967). The nature and significance of platelet products in human plasma. Br. J. Haematol. 13, 269-288.
7. VanWijk, M.J., VanBavel, E., Sturk, A., and Nieuwland, R. (2003). Microparticles in cardiovascular diseases. Cardiovasc. Res. 59, 277-287. (Pubitemid 37272022)
8. Burnier, L., Fontana, P., Kwak, B.R., and Angelillo-Scherrer, A. (2009). Cell-derived microparticles in haemostasis and vascular medicine. Thromb. Haemost. 101, 439-451.
9. De Maio, A. (2011). Extracellular heat shock proteins, cellular export vesicles, and the Stress Observation System: a form of communication during injury, infection, and cell damage. It is never known how far a controversial finding will go! Cell Stress Chaperones 16, 235-249.
10. Marzesco, A.M., Janich, P., Wilsch-Bräuninger, M., Dubreuil, V., Langenfeld, K., Corbeil, D., and Huttner, H.B. (2005). Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J. Cell Sci. 118, 2849-2858. (Pubitemid 41136362)
11. Mause, S.F., and Weber, C. (2010). Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ. Res. 107, 1047-1057.
12. Simons, M., and Raposo, G. (2009). Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581.
13. Wetterberg, L., Nybom, R., Bratlid, T., Fladby, T., Olsson, B., and Wigzell, H. (2002). Micrometer-sized particles in cerebrospinal fluid (CSF) in patients with schizophrenia. Neurosci. Lett. 329, 91-95.
14. Ekelund, J., Wahlbeck, K., and Back, N. (2003). No association between micrometer-sized particles in human cerebrospinal fluid and schizophrenia. Neurosci. Lett. 349, 68-70. (Pubitemid 37289272)
15. Morel, N., Morel, O., Petit, L., Hugel, B., Cochard, J.F., Freyssinet, J.M., Sztark, F., and Dabadie, P. (2008). Generation of procoagulant microparticles in cerebrospinal fluid and peripheral blood after traumatic brain injury. J. Trauma 64, 698-704. (Pubitemid 351366895)
16. Huang, M., Hu, Y.Y., and Dong, X.Q. (2009). High concentrations of procoagulant microparticles in the cerebrospinal fluid and peripheral blood of patients with acute basal ganglia hemorrhage are associated with poor outcome. Surg. Neurol. 72, 481-489.
17. Harrington, M.G., Fonteh, A.N., Oborina, E., Liao, P., Cowan, R.P., McComb, G., Chavez, J.N., Rush, J., Biringer, R.G., and Hühmer, A.F. (2009). The morphology and biochemistry of nanostructures provide evidence for synthesis and signaling functions in human cerebrospinal fluid. Cerebrospinal Fluid Res. 6, 10.
18. Smalheiser, N.R. (2009). Do neural cells communicate with endothelial cells via secretory exosomes and microvesicles? Cardiovasc. Psychiatry Neurol. 2009, 383086.
19. Smalheiser, N.R. (2007). Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol. Direct. 2, 35.
20. Shet, A.S., Aras, O., Gupta, K., Hass, M.J., Rausch, D.J., Saba, N., Koopmeiners, L., Key, N.S., and Hebbel, R.P. (2003). Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood 102, 2678-2683. (Pubitemid 37193612)
21. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504. (Pubitemid 37428274)
22. Maere, S., Heymans, K., and Kuiper, M. (2005). BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449. (Pubitemid 41222459)
23. Collino, F., Deregibus, M.C., Bruno, S., Sterpone, L., Aghemo, G., Viltono, L., Tetta, C., and Camussi, G. (2010). Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS ONE 5, e11803.
24. Lei, P., Li, Y., Chen, X., Yang, S., and Zhang, J. (2009). Microarray based analysis of microRNA expression in rat cerebral cortex after traumatic brain injury. Brain Res. 1284, 191-201.
25. Redell, J.B., Liu, Y., and Dash, P.K. (2009). Traumatic brian injury alters expression of hippocampal microRNAs: Potential regulators of multiple pathophysiological processes. J. Neursci. Res. 87, 1435-1448.
26. Langlois, A., and Duval, D. (1997). Differentiation of the human NT2 cells into neurons and glia. Methods in Cell Sci. 19, 213-219. (Pubitemid 28142462)
27. Pleasure, S.J., and Lee, V.M. (1993). NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J. Neurosci. Res. 35, 585-602. (Pubitemid 23226712)
28. Sommer, J.B., Gaul, C., Heckmann, J., Neundörfer, B., and Erbguth, F.J. (2002). Does lumbar cerebrospinal fluid reflect ventricular cerebrospinal fluid? A prospective study in patients with external ventricular drainage. Eur. Neurol. 47, 224-232. (Pubitemid 34621588)
29. Atack, J.R., May, C., Kaye, J.A., and Rapoport, S.I. (1990). Cerebrospinal fluid gradients of acetylcholinesterase and butyrylcholinesterase activity in healthy aging. Neurochem. Int. 16, 533-538. (Pubitemid 20221681)
30. Bach, F.W., Schmidt, J.F., and Faber, T. (1992). Radioimmunoassay of beta-endorphin in ventricular and lumbar cerebrospinal fluid. Clin. Chem. 38, 847-852.
31. Facchinetti, F., Petraglia, F., Cicero, S., Nappi, G., Valentini, M., and Genazzani, A.R. (1987). No gradient exists between lumbar and ventricular cerebrospinal fluid beta-endorphin. Neurosci. Lett. 77, 349-352.
32. Faull, K.F., Rafie, R., Pascoe, N., Marsh, L., and Pfefferbaum, A. (1999). N-acetylaspartic acid (NAA) and N-acetylaspartylglutamic acid (NAAG) in human ventricular, subarachnoid, and lumbar cerebrospinal fluid. Neurochem. Res. 24, 1249-1261. (Pubitemid 29420271)
33. Tarnaris, A., Toma, A.K., Chapman, M.D., Petzold, A., Keir, G., Kitchen, N.D., and Watkins, L.D. (2011). Rostrocaudal dynamics of CSF biomarkers. Neurochem. Res. 36, 528-532.
34. Skog, J., Würdinger, T., Van Rijn, S., Meijer, D.H., Gainche, L., Sena-Esteves, M., Curry, W.T., Jr., Carter, B.S., Krichevsky, A.M., and Breakefield, X.O. (2008). Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470-1476.
35. Sadallah, S., Eken, C., and Schifferli, J.A. (2008). Erythrocyte-derived ectosomes have immunosuppressive properties. J. Leukoc. Biol. 84, 1316-1325.
36. Mrvar-Brecko, A., Sustar, V., Jansa, V., Stukelj, R., Jansa, R., Mujagic, E., Kruljc, P., Iglic, A., Hägerstrand, H., and Kralj-Iglic, V. (2010). Isolated microvesicles from peripheral blood and body fluids as observed by scanning electron microscope. Blood Cells Mol. Dis. 44, 307-312.
37. Sinauridze, E.I., Kireev, D.A., Popenko, N.Y., Pichugin, A.V., Panteleev, M.A., Krymskaya, O.V., and Ataullakhanov, F.I. (2007). Platelet microparticle membranes have 50-to 100-fold higher specific procoagulant activity than activated platelets. Thromb. Haemost. 97, 425-434. (Pubitemid 46437805)
38. Pluskota, E., Woody, N.M., Szpak, D., Ballantyne, C.M., Soloviev, D.A., Simon, D.I., and Plow, E.F. (2008). Expression, activation, and function of integrin alphaMbeta2 (Mac-1) on neutrophil-derived microparticles. Blood 112, 2327-2335.
39. Schratt, G.M., Tuebing, F., Nigh, E.A., Kane, C.G., Sabatini, M.E., Kiebler, M., and Greenberg, M.E. (2006). A brain-specific microRNA regulates dendritic spine development. Nature 439, 283-289. (Pubitemid 43128846)
40. Kiebler, M.A., and Bassell, G.J. (2006). Neuronal RNA granules: movers and makers. Neuron 51, 685-690. (Pubitemid 44374907)
41. Li, L., Zhu, D., Huang, L., Zhang, J., Bian, Z., Chen, X., Liu, Y., Zhang, C.Y., and Zen, K. (2012). Argonaute 2 complexes selectively protect the circulating microRNAs in cell-secreted microvesicles. PLoS ONE 7, e46957.
42. Diehl, P., Fricke, A., Sander, L., Stamm, J., Bassler, N., Htun, N., Ziemann, M., Helbing, T., El-Osta, A., Jowett, J.B., and Peter, K. (2012). Microparticles: major transport vehicles for distinct micro-RNAs in circulation. Cardiovasc. Res. 93, 633-644.
43. Shibata, M., Nakao, H., Kiyonari, H., Abe, T., and Aizawa, S. (2011). MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J. Neurosci. 31, 3407-3422.
44. Bonev, B., Pisco, A., and Papalopulu, N. (2011). MicroRNA-9 reveals regional diversity of neural progenitors along the anterior-posterior axis. Dev. Cell 20, 19-32.
45. Bruno, S., Collino, F., Deregibus,M.C., Grange, C., Tetta, C., and Camussi, G. (2013). Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells Dev. 22, 758-771.
46. Yuan, A., Farber, E.L., Rapoport, A.L., Tejada, D., Deniskin, R., Akhmedov, N.B., and Farber, D.B. (2009). Transfer of microRNAs by embryonic stem cell microvesicles. PLoS ONE 4, e4722.
47. Ratajczak, J., Miekus, K., Kucia, M., Zhang, J., Reca, R., Dvorak, P., and Ratajczak, M.Z. (2006). Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20, 847-856.
48. Aliotta, J.M., Pereira, M., Johnson, K.W., de Paz, N., Dooner, M.S., Puente, N., Ayala, C., Brilliant, K., Berz, D., Lee, D., Ramratnam, B., McMillan, P.N., Hixson, D.C., Josic, D., and Quesenberry, P.J. (2010). Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription. Exp. Hematol. 38, 233-245.
49. Waldenstrom, A., Gennebäck, N., Hellman, U., and Ronquist, G. (2012). Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS ONE 7, e34653.
50. Cantaluppi, V., Gatti, S., Medica, D., Figliolini, F., Bruno, S., Deregibus, M.C., Sordi, A., Biancone, L., Tetta, C., and Camussi, G. (2012). Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 82, 412-427.