Mesenchymal stromal cell-derived microvesicles regulate an internal pro-inflammatory program in activated macrophages

Frontiers in Immunology

Volumn 8, Issue JUL, 2017, Pages

  Henao Agudelo, Juan S ^a   Braga, Tarcio T ^b   Amano, Mariane T ^b   Cenedeze, Marcos A ^a   Cavinato, Regiane A ^a   Peixoto Santos, Amandda R ^a   Muscará, Marcelo N ^b   Teixeira, Simone A ^b   Cruz, Mario C ^a   Castoldi, Angela ^b   Sinigaglia Coimbra, Rita ^a   Pacheco Silva, Alvaro ^a,c   De Almeida, Danilo C ^b   Saraiva Camara, Niels Olsen ^a,b  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

Author keywords

Acute peritonitis; Immunomodulation; Macrophages; Mesenchymal stromal cells; Microvesicles

Indexed keywords

5' NUCLEOTIDASE; ARGINASE; CD206 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; CD9 ANTIGEN; CELL ANTIGEN; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CX3CR1; ENDOGLIN; GAMMA INTERFERON; HERMES ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOCORTIN 5; MICRORNA; MICRORNA 155; MICRORNA 21; NITRIC OXIDE; SUPPRESSOR OF CYTOKINE SIGNALING 3; THIOGLYCOLIC ACID; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; COCULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; EXOSOME; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE FUNCTION TEST; IMMUNOMODULATION; INFLAMMATION; MACROPHAGE; MALE; MEMBRANE MICROPARTICLE; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PERITONEAL CAVITY; PERITONITIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; TISSUE REGENERATION; TISSUE REPAIR; TRANSMISSION ELECTRON MICROSCOPY;

EID: 85026650771     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00881     Document Type: Article

References (44)

1. Nombela-Arrieta C, Ritz J, Silberstein LE. The elusive nature and function of mesenchymal stem cells. Nat Rev Mol Cell Biol (2011) 12(2):126-31. doi:10.1038/nrm3049
2. Murphy MB, Moncivais K, Caplan AI. Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine. Exp Mol Med (2013) 45:e54. doi:10.1038/emm.2013.94
3. Liang X, Ding Y, Zhang Y, Tse HF, Lian Q. Paracrine mechanisms of mesenchymal stem cell-based therapy: current status and perspectives. Cell Transplant (2014) 23(9):1045-59. doi:10.3727/096368913X667709
4. Alagesan S, Griffin MD. Autologous and allogeneic mesenchymal stem cells in organ transplantation: what do we know about their safety and efficacy? Curr Opin Organ Transplant (2014) 19(1):65-72. doi:10.1097/MOT.0000000000000043
5. Wise AF, Ricardo SD. Mesenchymal stem cells in kidney inflammation and repair. Nephrology (Carlton) (2012) 17(1):1-10. doi:10.1111/j.1440-1797.2011.01501.x
6. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood (2005) 105(4):1815-22. doi:10.1182/blood-2004-04-1559
7. Klyushnenkova E, Mosca JD, Zernetkina V, Majumdar MK, Beggs KJ, Simonetti DW, et al. T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci (2005) 12(1):47-57. doi:10.1007/s11373-004-8183-7
8. Bassi EJ, Aita CA, Camara NO. Immune regulatory properties of multipotent mesenchymal stromal cells: where do we stand? World J Stem Cells (2011) 3(1):1-8. doi:10.4252/wjsc.v3.i1.1
9. Kim J, Hematti P. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp Hematol (2009) 37(12):1445-53. doi:10.1016/j.exphem.2009.09.004
10. Prockop DJ, Oh JY. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol Ther (2012) 20(1):14-20. doi:10.1038/mt.2011.211
11. English K. Mechanisms of mesenchymal stromal cell immunomodulation. Immunol Cell Biol (2013) 91(1):19-26. doi:10.1038/icb.2012.56
12. Cho DI, Kim MR, Jeong HY, Jeong HC, Jeong MH, Yoon SH, et al. Mesenchymal stem cells reciprocally regulate the M1/M2 balance in mouse bone marrow-derived macrophages. Exp Mol Med (2014) 46:e70. doi:10.1038/emm.2013.135
13. Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol (2009) 20(5):1053-67. doi:10.1681/ASN.2008070798
14. 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(8):1664-73. doi:10.1007/s00125-014-3262-4
15. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol (2013) 200(4):373-83. doi:10.1083/jcb.201211138
16. Gyorgy B, Szabo TG, Pasztoi M, Pal Z, Misjak P, Aradi B, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci (2011) 68(16):2667-88. doi:10.1007/s00018-011-0689-3
17. Arslan F, Lai RC, Smeets MB, Akeroyd L, Choo A, Aguor EN, et al. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res (2013) 10(3):301-12. doi:10.1016/j.scr.2013.01.002
18. Xin H, Li Y, Chopp M. Exosomes/miRNAs as mediating cell-based therapy of stroke. Front Cell Neurosci (2014) 8:377. doi:10.3389/fncel.2014.00377
19. Chen W, Huang Y, Han J, Yu L, Li Y, Lu Z, et al. Immunomodulatory effects of mesenchymal stromal cells-derived exosome. Immunol Res (2016) 64(4):831-40. doi:10.1007/s12026-016-8798-6
20. Bassi EJ, Moraes-Vieira PM, Moreira-Sa CS, Almeida DC, Vieira LM, Cunha CS, et al. Immune regulatory properties of allogeneic adipose-derived mesenchymal stem cells in the treatment of experimental autoimmune diabetes. Diabetes (2012) 61(10):2534-45. doi:10.2337/db11-0844
21. Semedo P, Correa-Costa M, Antonio Cenedeze M, Maria Avancini Costa Malheiros D, Antonia dos Reis M, Shimizu MH, et al. Mesenchymal stem cells attenuate renal fibrosis through immune modulation and remodeling properties in a rat remnant kidney model. Stem Cells (2009) 27(12):3063-73. doi:10.1002/stem.214
22. Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Current Protocols in Cell Biology. John Wiley & Sons, Inc (2006) Chapter 3:Unit 3.22. doi:10.1002/0471143030.cb0322s30
23. Deryugina EI, Ratnikov BI, Bourdon MA, Gilmore GL, Shadduck RK, Muller-Sieburg CE. Identification of a growth factor for primary murine stroma as macrophage colony-stimulating factor. Blood (1995) 86(7):2568-78.
24. Albesiano E, Messmer BT, Damle RN, Allen SL, Rai KR, Chiorazzi N. Activation-induced cytidine deaminase in chronic lymphocytic leukemia B cells: expression as multiple forms in a dynamic, variably sized fraction of the clone. Blood (2003) 102(9):3333-9. doi:10.1182/blood-2003-05-1585
25. Ylostalo JH, Bartosh TJ, Coble K, Prockop DJ. Human mesenchymal stem/stromal cells cultured as spheroids are self-activated to produce prostaglandin E2 that directs stimulated macrophages into an anti-inflammatory phenotype. Stem Cells (2012) 30(10):2283-96. doi:10.1002/stem.1191
26. Biancone L, Bruno S, Deregibus MC, Tetta C, Camussi G. Therapeutic potential of mesenchymal stem cell-derived microvesicles. Nephrol Dial Transplant (2012) 27(8):3037-42. doi:10.1093/ndt/gfs168
27. Zhai A, Qian J, Kao W, Li A, Li Y, He J, et al. Borna disease virus encoded phosphoprotein inhibits host innate immunity by regulating miR-155. Antiviral Res (2013) 98(1):66-75. doi:10.1016/j.antiviral.2013.02.009
28. Wang Z, Brandt S, Medeiros A, Wang S, Wu H, Dent A, et al. MicroRNA 21 is a homeostatic regulator of macrophage polarization and prevents prostaglandin E2-mediated M2 generation. PLoS One (2015) 10(2):e0115855. doi:10.1371/journal.pone.0115855
29. Lam D, Harris D, Qin Z. Inflammatory mediator profiling reveals immune properties of chemotactic gradients and macrophage mediator production inhibition during thioglycollate elicited peritoneal inflammation. Mediators Inflamm (2013) 2013:931562. doi:10.1155/2013/931562
30. Misharin AV, Saber R, Perlman H. Eosinophil contamination of thioglycollate-elicited peritoneal macrophage cultures skews the functional readouts of in vitro assays. J Leukoc Biol (2012) 92(2):325-31. doi:10.1189/jlb.1111560
31. Auffray C, Sieweke MH, Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol (2009) 27:669-92. doi:10.1146/annurev.immunol.021908.132557
32. Ghosn EE, Cassado AA, Govoni GR, Fukuhara T, Yang Y, Monack DM, et al. Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc Natl Acad Sci U S A (2010) 107(6):2568-73. doi:10.1073/pnas.0915000107
33. Lener T, Gimona M, Aigner L, Borger V, Buzas E, Camussi G, et al. Applying extracellular vesicles based therapeutics in clinical trials-an ISEV position paper. J Extracell Vesicles (2015) 4:30087. doi:10.3402/jev.v4.30087
34. Lai RC, Yeo RW, Lim SK. Mesenchymal stem cell exosomes. Semin Cell Dev Biol (2015) 40:82-8. doi:10.1016/j.semcdb.2015.03.001
35. Kordelas L, Rebmann V, Ludwig AK, Radtke S, Ruesing J, Doeppner TR, et al. MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus-host disease. Leukemia (2014) 28(4):970-3. doi:10.1038/leu.2014.41
36. Konala VB, Mamidi MK, Bhonde R, Das AK, Pochampally R, Pal R. The current landscape of the mesenchymal stromal cell secretome: a new paradigm for cell-free regeneration. Cytotherapy (2016) 18(1):13-24. doi:10.1016/j.jcyt.2015.10.008
37. Allaire MA, Tanne B, Cote SC, Dumais N. Prostaglandin E 2 does not modulate CCR7 expression and functionality after differentiation of blood monocytes into macrophages. Int J Inflam (2013) 2013:918016. doi:10.1155/2013/918016
38. Harris NL, Ronchese F. The role of B7 costimulation in T-cell immunity. Immunol Cell Biol (1999) 77(4):304-11. doi:10.1046/j.1440-1711.1999.00835.x
39. Lindoso RS, Collino F, Bruno S, Araujo DS, Sant'Anna JF, Tetta C, et al. Extracellular vesicles released from mesenchymal stromal cells modulate miRNA in renal tubular cells and inhibit ATP depletion injury. Stem Cells Dev (2014) 23(15):1809-19. doi:10.1089/scd.2013.0618
40. Leung AK. The whereabouts of microRNA actions: cytoplasm and beyond. Trends Cell Biol (2015) 25(10):601-10. doi:10.1016/j.tcb.2015.07.005
41. Roszer T. Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediators Inflamm (2015) 2015:816460. doi:10.1155/2015/816460
42. Yang Z, Ming XF. Functions of arginase isoforms in macrophage inflammatory responses: impact on cardiovascular diseases and metabolic disorders. Front Immunol (2014) 5:533. doi:10.3389/fimmu.2014.00533
43. Carow B, Rottenberg ME. SOCS3, a major regulator of infection and inflammation. Front Immunol (2014) 5:58. doi:10.3389/fimmu.2014.00058
44. Bain CC, Scott CL, Uronen-Hansson H, Gudjonsson S, Jansson O, Grip O, et al. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol (2013) 6(3):498-510. doi:10.1038/mi.2012.89