Microvescicles derived from mesenchymal stromal cells are not as effective as their cellular counterpart in the ability to modulate immune responses in vitro

Stem Cells and Development

Volumn 23, Issue 21, 2014, Pages 2591-2599

  Conforti, Antonella ^a   Scarsella, Marco ^a   Starc, Nadia ^a,b   Giorda, Ezio ^a   Biagini, Simone ^a   Proia, Alessandra ^a   Carsetti, Rita ^a   Locatelli, Franco ^a,c   Bernardo, Maria Ester ^a  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; PHYTOHEMAGGLUTININ; TRANSFORMING GROWTH FACTOR BETA; GALECTIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MICROSOMAL AMINOPEPTIDASE; SIGNAL PEPTIDE;

ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; BONE MARROW; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; MEMBRANE VESICLE; MESENCHYMAL STROMA CELL; MICROVESCICLE; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROSPECTIVE STUDY; T LYMPHOCYTE; ULTRACENTRIFUGATION; CELL CULTURE; CELL PROLIFERATION; COCULTURE; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE; MEMBRANE MICROPARTICLE; METABOLISM; MONONUCLEAR CELL;

ANTIGENS, CD13; B-LYMPHOCYTES; CELL PROLIFERATION; CELL-DERIVED MICROPARTICLES; CELLS, CULTURED; COCULTURE TECHNIQUES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GALECTIN 1; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERFERON-GAMMA; INTERLEUKIN-10; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTES; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MESENCHYMAL STROMAL CELLS; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84913605925     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0091     Document Type: Article

References (46)

1. Jiang Y, BN Jahagirdar, RL Reinhardt, RE Schwartz, CD Keene, XR Ortiz-Gonzalez, M Reyes, T Lenvik, T Lund, et al. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49.
2. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
3. Deans RJ and AB Moseley. (2000). Mesenchymal stem cells: Biology and potential clinical use. Exp Hematol 28: 875-884.
4. Nauta AJ and WE Fibbe. (2007). Immunomodulatory properties of mesenchymal stromal cells. Blood 110:3499-3506.
5. Le Blanc K and D Mougiakakos. (2012). Multipotent mesenchymal stromal cells and the innate immune system. Nat Rev Immunol 12:383-396.
6. Di Nicola M, C Carlo-Stella, M Magni, M Milanesi, PD Longoni, P Matteucci, S Grisanti and AM Gianni. (2002). Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99:3838-3843.
7. Rasmusson I, O Ringden, B Sundberg and K Le Blanc. (2003). Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 76:1208-1213.
8. Maccario R, M Podesta, A Moretta, A Cometa, P Comoli, D Montagna, L Daudt, A Ibatici, G Piaggio, et al. (2005). Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favours the differentiation of CD4 + T-cell subsets ex pressing regulatory/suppressive phenotype. Haematologica 90:516-525.
9. Corcione A, F Benvenuto, E Ferretti, D Giunti, V Cappiello, F Cazzanti, M Risso, F Gualandi, GL Mancardi, V Pistoia and A Uccelli. (2006). Human mesenchymal stem cells modulate B-cell functions. Blood 107:367-372.
10. Krampera M, L Cosmi, R Angeli, A Pasini, F Liotta, A Andreini, V Santarlasci, B Mazzinghi, G Pizzolo, et al. (2006). Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 24:386-398.
11. Traggiai E, S Volpi, F Schena, M Gattorno, F Ferlito, L Moretta and A Martini. (2008). Bone marrow-derived mesenchymal stem cells induce both polyclonal expansion and differentiation of B cells isolated from healthy donors and systemic lupus erythematosus patients. Stem Cells 26:562-569.
12. Le Blanc K, F Frassoni, L Ball, F Locatelli, H Roelofs, I Lewis, E Lanino, B Sundberg, ME Bernardo, et al. (2008). Mesenchymal stem cells for treatment of steroid-resistant severe, acute graft-versus-host disease: A phase II study. Lancet 371:1579-1586.
13. Ball LM, ME Bernardo, H Roelofs, MJ van Tol, B Contoli, JJ Zwaginga, MA Avanzini, A Conforti, A Bertaina, et al. (2013). Multiple infusions of mesenchymal stromal cells induce sustained remission in children with steroidrefractory, grade III-IV acute graft-versus-host disease. Br J Haematol 163:501-509.
14. Ball LM, ME Bernardo, H Roelofs, A Lankester, A Cometa, RM Egeler, F Locatelli and WE Fibbe. (2007). Cotransplantation of ex vivo expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stemcell transplantation. Blood 110:2764-2767.
15. Bernardo ME, D Pagliara and F Locatelli. (2012). Mesenchymal stromal cell therapy: A revolution in regenerative medicine?. Bone Marrow Transplant 47:164-171.
16. Frenette PS, S Pinho, D Lucas and C Scheiermann. (2013). Mesenchymal stem cell: Keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Annu Rev Immunol 31:285-316.
17. Krampera M. (2011). Mesenchymal stromal cell licensing: A multistep process. Leukemia 25:1408-1414.
18. Waterman RS, SL Tomchuck, SL Henkle and AM Betancourt. (2010). A new mesenchymal stem cell (MSC) paradigm: Polarization into a pro-inflammatory MSC1 or an immunosuppressive MSC2 phenotype. PLoS One 5: E10088.
19. Muralidharan-Chari V, JW Clancy, A Sedgwick and C DSouza-Schorey. (2010). Microvesicles: Mediators of extracellular communication during cancer progression. J Cell Sci 123:1603-1611.
20. Thery C, M Ostrowski and E Segura. (2009). Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9:581-593.
21. Gyorgy B, TG Szabo, M Paszto i, Z Pal, P Misjak, B Aradi, V Laszlo, E Pallinger, E Pap, et al. (2011). Membrane vesicles, current state-of-The-Art: Emerging role of extracellular vesicles. Cell Mol Life Sci 68:2667-2688.
22. Cocucci E, G Racchetti and J Meldolesi. (2008). Shedding microvesicles: Artefacts no more. Trends Cell Biol 19: 43-51.
23. Lai RC, TS Chen and SK Lim. (2011). Mesenchymal stem cell exosome: A novel stem cell-based therapy for cardiovascular disease. Regen Med 6:481-492.
24. Biancone L, S Bruno, MC Deregibus, C Tetta and G Camussi. (2012). Therapeutic potential of mesenchymal stem cell-derived microvesicles. Nephrol Dial Transplant 27:3037-3042.
25. Bernardo ME, N Zaffaroni, F Novara, AM Cometa, MA Avanzini, A Moretta, D Montagna, R Maccario, R Villa, et al. (2007). Human bone marrow-derived mesenchymal stem cells do not undergo transformation after long-Term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res 67:9142-9149.
26. Muralidharan-Chari V, J Clancy, C Plou, M Romao, P Chavrier, G Raposo and C DSouza-Schorey. (2009). ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 19:1875-1885.
27. Thery C, S Amigorena, G Raposo and A Clayton. (2006). Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3:Unit 3.22.
28. Capolunghi F, S Cascioli, E Giorda, MM Rosado, A Plebani, C Auriti, G Seganti, R Zuntini, S Ferrari, et al. (2008). CpG drives human transitional B cells to terminal differentiation and production of natural antibodies. J Immunol 180:800-808.
29. Neuss S, E Becher, M Woltje, L Tietze and W Jahnen-Dechent. (2004). Functional expression of HGF and HGF receptor/c-met in adult human mesenchymal stem cells suggest a role in cell mobilization, tissue repair, and wound healing. Stem Cells 22:405-414.
30. Solchaga LA and EA Zale. (2012). Prostaglandin E2: A putative potency indicator of the immunosuppressive activity of human mesenchymal stem cells. Am J Stem Cells 1:138-145.
31. Gieseke F, J Bohringer, R Bussolari, M Dominici, R Handgretinger and I Mu ller. (2010). Human multipotent mesenchymal stromal cells use galectin-1 to inhibit immune effector cells. Blood 116:3770-3779.
32. Camussi G, MC Deregibus, S Bruno, V Cantaluppi and L Biancone. (2010). Exosomes/microvesicles as a mechanism of cell-To-cell communication. Kidney Int 78:838-848.
33. Thery C, L Duban, E Segura, P Veron, O Lantz and S Amigorena. (2002). Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 3: 1156-1162.
34. Liu C, S Yu, K Zinn, J Wang, L Zhang, Y Jia, JC Kappes, S Barnes, RP Kimberly, WE Grizzle and HG Zhang. (2006). Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol 176:1375-1385.
35. Koppler B, C Cohen, D Schlondorff and M Mack. (2006). Differential mechanisms of microparticle transfer to B cells and monocytes: Anti-inflammatory properties of microparticles. Eur J Immunol 36:648-660.
36. Yu s, C Liu, K Su, J Wang, Y Liu, L Zhang, C Li, Y Cong, R Kimberly, et al. (2007). Tumor exosomes inhibit differentiation of bone marrow dendritic cells. J Immunol 178: 6867-6875.
37. Wang GJ, Y Liu, A Qin, SV Shah, ZB Deng, X Xiang, Z Cheng, C Liu, J Wang, et al. Thymus exosomes-like particles induce regulatory T cells. J Immunol 181:5242-5248.
38. Bruno S, C Grange, F Collino, MC Deregibus, V Cantaluppi, L Biancone, C Tetta and G Camussi. (2012). Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS One 7:e33115.
39. Bruno S, C Grange, MC Deregibus, RA Calogero, S Saviozzi, F Collino, L Morando, A Busca, M Falda, et al. (2009). Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol 20:1053-1067.
40. Gatti S, S Bruno, MC Deregibus, A Sordi, V Cantaluppi, C Tetta and G Camussi. (2011). Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant 26:1474-1483.
41. Morigi M and A Benigni. (2013). Mesenchymal stem cells and kidney repair. Nephrol Dial Transplant 28:788-793.
42. Lai RC, RW Yeo, KH Tan and SK Lim. (2013). Mesenchymal stem cell exosome ameliorates reperfusion injury through proteomic complementation. Regen Med 8: 197-209.
43. Bruno S, F Collino, MC Deregibus, C Grange, C Tetta and G Camussi. (2013). Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells Dev 22:758-771.
44. Bruno S and G Camussi. (2013). Role of mesenchymal stem cell-derived microvesicles in tissue repair. Pediatr Nephrol 28:2249-2254.
45. Tarte K, J Gaillard, JJ Lataillade, L Fouillard, M Becker, H Mossafa, A Tchirkov, H Rouard, C Henry, et al. (2010). Clinical-grade production of human mesenchymal stromal cells: Occurrence of aneuploidy without transformation. Blood 115:1549-1553.
46. Ben-David U, Y Mayshar and N Benvenisty. (2011). Largescale analysis reveals acquisition of lineage-specific chromosomal aberrations in human adult stem cells. Cell Stem Cell 9:97-102.