Exosome and Microvesicle-Enriched Fractions Isolated from Mesenchymal Stem Cells by Gradient Separation Showed Different Molecular Signatures and Functions on Renal Tubular Epithelial Cells

Stem Cell Reviews and Reports

Volumn 13, Issue 2, 2017, Pages 226-243

  Collino, Federica ^a,b   Pomatto, Margherita ^b   Bruno, Stefania ^c   Lindoso, Rafael Soares ^a   Tapparo, Marta ^b   Sicheng, Wen ^d   Quesenberry, Peter ^d   Camussi, Giovanni ^b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d BROWN UNIVERSITY   (United States)

Author keywords

Acute kidney injury; Exosomes; Extracellular vesicles; Kidney regeneration; Mesenchymal stem cells; Microvesicles

Indexed keywords

ALPHA5 INTEGRIN; BETA1 INTEGRIN; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CD63 ANTIGEN; CD81 ANTIGEN; EPHRIN RECEPTOR A5; MICRORNA; MICRORNA 100; MICRORNA 10B; MICRORNA 125B; MICRORNA 127; MICRORNA 17; MICRORNA 21; MICRORNA 214; MICRORNA 24; MICRORNA 29A; MICRORNA 30C; MICRORNA 34A; MICRORNA 99A; SECRETED FRIZZLED RELATED PROTEIN 1; TETRASPANIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; PROTEOME;

ANIMAL CELL; APOPTOSIS; ARTICLE; CAPILLARY ELECTROPHORESIS; CELL COMPARTMENTALIZATION; CELL PROLIFERATION; CELL SEPARATION; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; EXOSOME; FATTY ACID SYNTHESIS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE MICROSCOPY; GENE ONTOLOGY; IMMUNE RESPONSE; KIDNEY TUBULE EPITHELIUM; MEMBRANE MICROPARTICLE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MICROARRAY; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL LINE; CYTOLOGY; ELECTRON MICROSCOPY; EPITHELIUM CELL; GENETICS; KIDNEY TUBULE; MESENCHYMAL STROMA CELL; METABOLISM; PROCEDURES; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE; CELL PROLIFERATION; CELL SEPARATION; CELL-DERIVED MICROPARTICLES; CELLS, CULTURED; CENTRIFUGATION, DENSITY GRADIENT; EPITHELIAL CELLS; EXOSOMES; KIDNEY TUBULES; MESENCHYMAL STROMAL CELLS; MICE; MICRORNAS; MICROSCOPY, ELECTRON; PROTEOME; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 85008618874     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-016-9713-1     Document Type: Article

References (59)

1. Ratajczak, J., Miekus, K., Kucia, M., et al. (2006). Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia, 20(5), 847–856.
2. Bruno, S., Grange, C., Deregibus, M. C., et al. (2009). Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. Journal of the American Society of Nephrology, 20(5), 1053–1067.
3. Tan, C. Y., Lai, R. C., Wong, W., Dan, Y. Y., Lim, S. K., & Ho, H. K. (2014). Mesenchymal stem cell-derived exosomes promote hepatic regeneration in drug-induced liver injury models. Stem Cell Research & Therapy, 5(3), 76–89.
4. Zhu, Y. J., Sun, J., & Du, T. (2015). Microvesicles derived from human umbilical cord mesenchymal stem cells facilitate tubular epithelial cell dedifferentiation and growth via hepatocyte growth factor induction. PloS One, 10(3), e0121534.
5. Nakamura, Y., Miyaki, S., Ishitobi, H., et al. (2015). Mesenchymal-stem-cell-derived exosomes accelerate skeletal muscle regeneration. FEBS Letters, 589(11), 1257–1265.
6. Deregibus, M. C., Cantaluppi, V., Calogero, R., et al. (2007). Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood, 110(7), 2440–2448.
7. Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., & Lötvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology, 9(6), 654–659.
8. Collino, F., Deregibus, M. C., Bruno, S., et al. (2010). Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PloS One, 5(7), e11803.
9. Lai, R. C., Tan, S. S., Teh, B. J., et al. (2012). Proteolytic potential of the MSCS exosome proteome: implications for an exosome-mediated delivery of therapeutic proteasome. The International Journal of Prosthodontics. doi:10.1155/2012/971907.
10. Nolte-'t Hoen, E.N., Buermans, H.P., Waasdorp, M., Stoorvogel, W., Wauben, M.H., 't Hoen, P.A. (2012) Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Research, 40(18), 9272–9285.
11. Konala, V. B., Mamidi, M. K., Bhonde, R., Das, A. K., Pochampally, R., & Pal, R. (2016). The current landscape of the mesenchymal stromal cell secretome: a new paradigm for cell-free regeneration. Cytotherapy, 18(1), 13–24.
12. Chiasserini, D., Mazzoni, M., Bordi, F., et al. (2015). Identification and partial characterization of two populations of Prostasomes by a combination of dynamic light scattering and proteomic analysis. The Journal of Membrane Biology, 248(6), 991–1004.
13. Guduric-Fuchs, J., O'Connor, A., Camp, B., O'Neill, C. L., Medina, R. J., & Simpson, D. A. (2012). Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics, 13, 357. doi:10.1186/1471-2164-13-357.
14. Ji, H., Chen, M., Greening, D. W., et al. (2014). Deep sequencing of RNA from three different extracellular vesicle (EV) subtypes released from the human LIM1863 colon cancer cell line uncovers distinct miRNA-enrichment signatures. PloS One, 9(10), e110314.
15. Lenassi, M., Cagney, G., Liao, M., et al. (2010). HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells. Traffic, 11(1), 110–122.
16. Lai, R. C., Arslan, F., Lee, M. M., et al. (2010). Exosome secreted by MSCs reduces myocardial ischemia/reperfusion injury. Stem Cell Research, 4(3), 214–222.
17. Greening, D. W., Xu, R., Ji, H., Tauro, B. J., & Simpson, R. J. (2015). A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods in Molecular Biology, 1295, 179–209.
18. Taylor, D. D. (2015). Isolation and molecular characterization of extracellular vesicles. Methods, 87, 1–2. doi:10.1016/j.ymeth.2015.08.006.
19. Tomasoni, S., Longaretti, L., Rota, C., et al. (2013). Transfer of growth factor receptor mRNA via exosomes unravels the regenerative effect of mesenchymal stem cells. Stem Cells and Development, 22(5), 772–780.
20. Collino, F., Bruno, S., Incarnato, D., et al. (2015). AKI recovery induced by mesenchymal stromal cell-derived extracellular vesicles carrying MicroRNAs. Journal of the American Society of Nephrology, 26(10), 2349–2360.
21. Herrera, M. B., Fonsato, V., Bruno, S., et al. (2013). Human liver stem cells improve liver injury in a model of fulminant liver failure. Hepatology, 57(1), 311–319.
22. Tauro, B. J., Greening, D. W., Mathias, R. A., et al. (2012). Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods, 56(2), 293–304.
23. Kowal, J., Arras, G., Colombo, M., et al. (2016). Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proceedings of the National Academy of Sciences of the United States of America, 113(8), E968–E977.
24. Mestdagh, P., Van Vlierberghe, P., De Weer, A., et al. (2009). A novel and universal method for microRNA RT-qPCR data normalization. Genome Biology, 10(6), R64. doi:10.1186/gb-2009-10-6-r64.
25. Vlachos, I. S., Zagganas, K., Paraskevopoulou, M. D., et al. (2015). DIANA-miRPath v3.0: deciphering microRNA function with experimental support. Nucleic Acids Research, 43(W1), W460–W466.
26. Pathan, M., Keerthikumar, S., Ang, C. S., et al. (2015). FunRich: a standalone tool for functional enrichment analysis. Proteomics, 15, 2597–2601.
27. Bhatt, K., Zhou, L., Mi, Q. S., Huang, S., She, J. X., & Dong, Z. (2010). MicroRNA-34a is induced via p53 during cisplatin nephrotoxicity and contributes to cell survival. Molecular Medicine, 16, 409–416.
28. Godwin, J. G., Geb, X., Stephana, K., Jurischb, A., Tulliusb, S. G., & Iacominia, J. (2010). Identification of a microRNA signature of renal ischemia reperfusion injury. Proceedings of the National Academy of Sciences, 107(32), 14339–14344.
29. Aguado-Fraile, E., Ramos, E., Saenz-Morales, D., et al. (2012). miR-127 protects proximal tubule cells against ischemia/reperfusion: identification of kinesin family member 3B as miR-127 target. PloS One, 7, e44305.
30. Patel, V., & Noureddine, L. (2012). MicroRNAs and fibrosis. Current Opinion in Nephrology and Hypertension, 21(4), 410–416.
31. Joo, M. S., Lee, C. G., Koo, J. H., & Kim, S. G. (2013). miR-125b transcriptionally increased by Nrf2 inhibits AhR repressor, which protects kidney from cisplatin-induced injury. Cell Death & Disease, 4, e899.
32. Kaucsár, T., Révész, C., & Godó, M. (2013). Activation of the miR-17 family and miR-21 during murine kidney ischemia-reperfusion injury. Nucleic Acid Therapeutics, 23(5), 344–354.
33. Chiabotto, G., Bruno, S., Collino, F., & Camussi, G. (2016). Mesenchymal stromal cells epithelial transition induced by renal tubular cells-derived extracellular vesicles. PloS One, 11(7), e0159163.
34. Gatti, S., Bruno, S., Deregibus, M. C., et al. (2011). Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrology, Dialysis, Transplantation, 26(5), 1474–1483.
35. Zhang, Y., Chopp, M., Meng, Y., et al. (2015). Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. Journal of Neurosurgery, 122(4), 856–867.
36. Mitsialis, S. A., & Kourembanas, S. (2016). Stem cell-based therapies for the newborn lung and brain: possibilities and challenges. Seminars in Perinatology, 40(3), 138–151.
37. Lai, R. C., Yeo, R. W., & Lim, S. K. (2015). Mesenchymal stem cell exosomes. Seminars in Cell & Developmental Biology, 40, 82–88.
38. Hagiwara, K., Katsuda, T., Gailhouste, L., Kosaka, N., & Ochiya, T. (2015). Commitment of annexin A2 in recruitment of microRNAs into extracellular vesicles. FEBS Letters, 589(24 Pt B), 4071–4078.
39. Palma, J., Yaddanapudi, S. C., Pigati, L., et al. (2012). MicroRNAs are exported from malignant cells in customized particles. Nucleic Acids Research, 40(18), 9125–9138.
40. Xu, R., Greening, D. W., Rai, A., Ji, H., & Simpson, R. J. (2015). Highly-purified exosomes and shed microvesicles isolated from the human colon cancer cell line LIM1863 by sequential centrifugal ultrafiltration are biochemically and functionally distinct. Methods, 87, 11–25.
41. Aliotta, J. M., Pereira, M., Wen, S., et al. (2016). Exosomes induce and reverse monocrotaline-induced pulmonary hypertension in mice. Cardiovascular Research, 110(3), 319–330.
42. Wen, S., Dooner, M., Cheng, Y., et al. (2016). Mesenchymal stromal cell-derived extracellular vesicles rescue radiation damage to murine marrow hematopoietic cells. Leukemia. doi:10.1038/leu.2016.107.
43. Lindoso, R. S., Collino, F., Bruno, S., et al. (2014). Extracellular vesicles released from mesenchymal stromal cells modulate miRNA in renal tubular cells and inhibit ATP depletion injury. Stem Cells and Development, 23(15), 1809–1819.
44. Momen-Heravi, F., Bala, S., Kodys, K., & Szabo, G. (2015). Exosomes derived from alcohol-treated hepatocytes horizontally transfer liver specific miRNA-122 and sensitize monocytes to LPS. Scientific Reports, 5, 9991.
45. Wang, B., Yao, K., & Huuskes, B. M. (2016). Mesenchymal stem cells deliver exogenous MicroRNA-let7c via exosomes to attenuate renal fibrosis. Molecular Therapy. doi:10.1038/mt.2016.90.
46. Zhang, X., Wang, X., & Zhu, H. (2010). Synergistic effects of the GATA-4-mediated miR-144/451 cluster in protection against simulated ischemia/reperfusion-induced cardiomyocyte death. Journal of Molecular and Cellular Cardiology, 49(5), 841–850.
47. Simon, N., & Hertig, A. (2015). Alteration of fatty acid oxidation in tubular epithelial cells: from acute kidney injury to renal Fibrogenesis. Frontiers in Medicine (Lausanne), 2, 52. doi:10.3389/fmed.2015.00052.
48. Zhou, D., Tan, R. J., Fu, H., & Liu, Y. (2016). Wnt/β-catenin signaling in kidney injury and repair: a double-edged sword. Laboratory Investigation, 96(2), 156–167.
49. Kalra, H., Simpson, R. J., Ji, H., et al. (2012). Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biology, 10(12), e1001450.
50. Kim, H. S., Choi, D. Y., Yun, S. J., et al. (2012). Proteomic analysis of microvesicles derived from human mesenchymal stem cells. Journal of Proteome Research, 11(2), 839–849.
51. Du, T., & Zhu, Y. J. (2014). The regulation of inflammatory mediators in acute kidney injury via exogenous mesenchymal stem cells. Mediators of Inflammation, 2014, 261697. doi:10.1155/2014/261697.
52. Arthur, A., Zannettino, A., Panagopoulos, R., et al. (2011). EphB/ephrin-B interactions mediate human MSCS attachment, migration and osteochondral differentiation. Bone, 48(3), 533–542.
53. Nguyen, T. M., Arthur, A., Hayball, J. D., & Gronthos, S. (2013). EphB and ephrin-B interactions mediate human mesenchymal stem cell suppression of activated T-cells. Stem Cells and Development, 22(20), 2751–2764.
54. Lin, K. C., Yip, H. K., & Shao, P. L. (2016). Combination of adipose-derived mesenchymal stem cells (ADMSCS) and ADMSCS-derived exosomes for protecting kidney from acute ischemia-reperfusion injury. International Journal of Cardiology, 216, 173–185.
55. Gao, J., Zhou, X. L., Kong, R. N., Ji, L. M., He, L. L., & Zhao, D. B. (2016). microRNA-126 targeting PIK3R2 promotes rheumatoid arthritis synovial fibroblasts proliferation and resistance to apoptosis by regulating PI3K/AKT pathway. Experimental and Molecular Pathology, 100(1), 192–198.
56. Tanaka, T. (2016) A mechanistic link between renal ischemia and fibrosis. Medical Molecular Morphology, 2016 Jul 20. [Epub ahead of print].
57. Ricardo, S. D., van Goor, H., & Eddy, A. A. (2008). Macrophage diversity in renal injury and repair. Journal of Clinical Investigation, 118(11), 3522–3530.
58. Geng, Y., Zhang, L., & Fu, B. (2014). Mesenchymal stem cells ameliorate rhabdomyolysis-induced acute kidney injury via the activation of M2 macrophages. Stem Cell Research & Therapy, 5(3), 80–94.
59. Kilpinen, L., Impola, U., & Sankkila, L. (2013). Extracellular membrane vesicles from umbilical cord blood-derived MSCS protect against ischemic acute kidney injury, a feature that is lost after inflammatory conditioning. Journal of Extracellular Vesicles. doi:10.3402/jev.v2i0.21927.