Mesenchymal stem cells-derived exosomes are more immunosuppressive than microparticles in inflammatory arthritis

Theranostics

Volumn 8, Issue 5, 2018, Pages 1399-1410

  Cosenza, Stella ^a,b   Toupet, Karine ^a,b   Maumus, Marie ^a,b   Luz Crawford, Patricia ^c   Blanc Brude, Olivier ^d   Jorgensen, Christian ^a,b,e   Noël, Danièle ^a,b,e  

^a HÔPITAL SAINT ELOI   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSIDAD DE LOS ANDES   (Chile)

^d INSERM   (France)

^e LAPEYRONIE HOSPITAL   (France)

Author keywords

Cell therapy; Extracellular vesicles; Mesenchymal stem cells; Rheumatoid arthritis; Trophic factors

Indexed keywords

GAMMA INTERFERON; IMMUNOSUPPRESSIVE AGENT;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELL VACUOLE; COLLAGEN-INDUCED ARTHRITIS; CONTROLLED STUDY; CRYOPRESERVATION; DELAYED HYPERSENSITIVITY; EXOSOME; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; LYMPH NODE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MEMBRANE MICROPARTICLE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PLASMABLAST; REGULATORY B LYMPHOCYTE; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; ULTRACENTRIFUGATION; ANIMAL; C57BL MOUSE; EXPERIMENTAL ARTHRITIS; INFLAMMATION; METABOLISM; PATHOLOGY; ULTRASTRUCTURE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CELL-DERIVED MICROPARTICLES; CRYOPRESERVATION; EXOSOMES; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATION; MESENCHYMAL STEM CELLS; MICE, INBRED C57BL; T-LYMPHOCYTES;

EID: 85041595800     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.21072     Document Type: Article

References (38)

1. Jorgensen C, Noel D. Mesenchymal stem cells in osteoarticular diseases. Regen Med. 2011; 6: 44-51
2. Castro-Manrreza ME, Montesinos JJ. Immunoregulation by mesenchymal stem cells: biological aspects and clinical applications. J Immunol Res. 2015; 2015: 394917
3. Kavanagh DP, Robinson J, Kalia N. Mesenchymal Stem Cell Priming: Fine-tuning Adhesion and Function. Stem Cell Rev. 2014; 10: 587-99
4. Maumus M, Roussignol G, Toupet K, Penarier G, Bentz I, Teixeira S, et al. Utility of a Mouse Model of Osteoarthritis to Demonstrate Cartilage Protection by IFNgamma-Primed Equine Mesenchymal Stem Cells. Front Immunol. 2016; 7: 392
5. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003; 102: 3837-44
6. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell. 2008; 2: 141-50
7. Kannan K, Ortmann RA, Kimpel D. Animal models of rheumatoid arthritis and their relevance to human disease. Pathophysiology. 2005; 12: 167-81
8. Bouffi C, Bony C, Courties G, Jorgensen C, Noel D. IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis. PLoS One. 2010; 5: e14247
9. Luz-Crawford P, Tejedor G, Mausset-Bonnefont AL, Beaulieu E, Morand EF, Jorgensen C, et al. Gilz governs the therapeutic potential of mesenchymal stem cells by inducing a switch from pathogenic to regulatory Th17 cells. Arthritis Rheumatol. 2015; 67: 1514-24
10. Luz-Crawford P, Djouad F, Toupet K, Bony C, Franquesa M, Hoogduijn MJ, et al. Mesenchymal Stem Cell-Derived Interleukin 1 Receptor Antagonist Promotes Macrophage Polarization and Inhibits B Cell Differentiation. Stem Cells. 2016; 34: 483-92
11. Luz-Crawford P, Ipseiz N, Espinosa-Carrasco G, Caicedo A, Tejedor G, Toupet K, et al. PPARbeta/delta directs the therapeutic potential of mesenchymal stem cells in arthritis. Ann Rheum Dis. 2016; 75: 2166-74
12. Maumus M, Jorgensen C, Noel D. Mesenchymal stem cells in regenerative medicine applied to rheumatic diseases: role of secretome and exosomes. Biochimie. 2013; 95: 2229-34
13. Lotvall J, Hill AF, Hochberg F, Buzas EI, Di Vizio D, Gardiner C, et al. 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
14. Heldring N, Mager I, Wood MJ, Le Blanc K, Andaloussi SE. Therapeutic Potential of Multipotent Mesenchymal Stromal Cells and Their Extracellular Vesicles. Hum Gene Ther. 2015; 26: 506-17
15. Cosenza S, Ruiz M, Maumus M, Jorgensen C, Noel D. Pathogenic or Therapeutic Extracellular Vesicles in Rheumatic Diseases: Role of Mesenchymal Stem Cell-Derived Vesicles. Int J Mol Sci. 2017; 18: 889
16. Burrello J, Monticone S, Gai C, Gomez Y, Kholia S, Camussi G. Stem Cell-Derived Extracellular Vesicles and Immune-Modulation. Front Cell Dev Biol. 2016; 4: 83
17. Maria AT, Toupet K, Maumus M, Fonteneau G, Le Quellec A, Jorgensen C, et al. Human adipose mesenchymal stem cells as potent anti-fibrosis therapy for systemic sclerosis. J Autoimmun. 2016; 70: 31-9
18. Domergue S, Bony C, Maumus M, Toupet K, Frouin E, Rigau V, et al. Comparison between Stromal Vascular Fraction and Adipose Mesenchymal Stem Cells in Remodeling Hypertrophic Scars. PLoS One. 2016; 11: e0156161
19. Toupet K, Maumus M, Luz-Crawford P, Lombardo E, Lopez-Belmonte J, van Lent P, et al. Survival and biodistribution of xenogenic adipose mesenchymal stem cells is not affected by the degree of inflammation in arthritis. PLoS One. 2015; 10: e0114962
20. Thery 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
21. Bouffi C, Bony C, Jorgensen C, Noel D. Skin fibroblasts are potent suppressors of inflammation in experimental arthritis. Ann Rheum Dis. 2011; 70: 1671-6
22. Del Fattore A, Luciano R, Pascucci L, Goffredo BM, Giorda E, Scapaticci M, et al. Immunoregulatory Effects of Mesenchymal Stem Cell-Derived Extracellular Vesicles on T Lymphocytes. Cell Transplant. 2015; 24: 2615-27
23. Blazquez R, Sanchez-Margallo FM, de la Rosa O, Dalemans W, Alvarez V, Tarazona R, et al. Immunomodulatory Potential of Human Adipose Mesenchymal Stem Cells Derived Exosomes on in vitro Stimulated T Cells. Front Immunol. 2014; 5: 556
24. Di Trapani M, Bassi G, Midolo M, Gatti A, Kamga PT, Cassaro A, et al. Differential and transferable modulatory effects of mesenchymal stromal cell-derived extracellular vesicles on T, B and NK cell functions. Sci Rep. 2016; 6: 24120
25. Monguio-Tortajada M, Roura S, Galvez-Monton C, Pujal JM, Aran G, Sanjurjo L, et al. Nanosized UCMSC-derived extracellular vesicles but not conditioned medium exclusively inhibit the inflammatory response of stimulated T cells: implications for nanomedicine. Theranostics. 2017; 7: 270-84
26. Matula Z, Nemeth A, Lorincz P, Szepesi A, Brozik A, Buzas EI, et al. The Role of Extracellular Vesicle and Tunneling Nanotube-Mediated Intercellular Cross-Talk Between Mesenchymal Stem Cells and Human Peripheral T Cells. Stem Cells Dev. 2016; 25: 1818-32
27. Conforti A, Scarsella M, Starc N, Giorda E, Biagini S, Proia A, et al. 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 Dev. 2014; 23: 2591-9
28. Brisson AR, Tan S, Linares R, Gounou C, Arraud N. Extracellular vesicles from activated platelets: a semiquantitative cryo-electron microscopy and immuno-gold labeling study. Platelets. 2017; 28: 263-71
29. Favaro E, Carpanetto A, Lamorte S, Fusco A, Caorsi C, Deregibus MC, et al. Human mesenchymal stem cell-derived microvesicles modulate T cell response to islet antigen glutamic acid decarboxylase in patients with type 1 diabetes. Diabetologia. 2014; 57: 1664-73
30. Bony C, Cren M, Domergue S, Toupet K, Jorgensen C, Noel D. Adipose Mesenchymal Stem Cells Isolated after Manual or Water-jet-Assisted Liposuction Display Similar Properties. Front Immunol. 2016; 6: 655
31. Grange C, Tapparo M, Bruno S, Chatterjee D, Quesenberry PJ, Tetta C, et al. Biodistribution of mesenchymal stem cell-derived extracellular vesicles in a model of acute kidney injury monitored by optical imaging. Int J Mol Med. 2014; 33: 1055-63
32. Wiklander OP, Nordin JZ, O'Loughlin A, Gustafsson Y, Corso G, Mager I, et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J Extracell Vesicles. 2015; 4: 26316
33. Foussat A, Cottrez F, Brun V, Fournier N, Breittmayer JP, Groux H. A comparative study between T regulatory type 1 and CD4+CD25+ T cells in the control of inflammation. J Immunol. 2003; 171: 5018-26
34. Budoni M, Fierabracci A, Luciano R, Petrini S, Di Ciommo V, Muraca M. The immunosuppressive effect of mesenchymal stromal cells on B lymphocytes is mediated by membrane vesicles. Cell Transplant. 2013; 22: 369-79
35. Zhu Y, Wang Y, Zhao B, Niu X, Hu B, Li Q, et al. Comparison of exosomes secreted by induced pluripotent stem cell-derived mesenchymal stem cells and synovial membrane-derived mesenchymal stem cells for the treatment of osteoarthritis. Stem Cell Res Ther. 2017; 8: 64
36. Withrow J, Murphy C, Liu Y, Hunter M, Fulzele S, Hamrick MW. Extracellular vesicles in the pathogenesis of rheumatoid arthritis and osteoarthritis. Arthritis Res Ther. 2016; 18: 286
37. Headland SE, Jones HR, Norling LV, Kim A, Souza PR, Corsiero E, et al. Neutrophil-derived microvesicles enter cartilage and protect the joint in inflammatory arthritis. Sci Transl Med. 2015; 7: 315ra190
38. Cosenza S, Ruiz M, Toupet K, Jorgensen C, Noël D. Mesenchymal stem cells derived exosomes and microparticles protect cartilage and bone from degradation in osteoarthritis. Scientific reports, 2017, 7:16214