Umbilical cord-derived mesenchymal stem cells instruct dendritic cells to acquire tolerogenic phenotypes through the IL-6-mediated upregulation of SOCS1

Stem Cells and Development

Volumn 23, Issue 17, 2014, Pages 2080-2092

  Deng, Yinan ^a,b   Yi, Shuhong ^a   Wang, Guoying ^a   Cheng, Jintao ^a,b   Zhang, Yingcai ^a,b   Chen, Wenjie ^a,b   Tai, Yan ^b   Chen, Shaohong ^a   Chen, Guihua ^a,b   Liu, Wei ^b   Zhang, Qi ^a,b   Yang, Yang ^a,b  

^a THE THIRD AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^b Guangdong Provincial Key Laboratory of Liver Disease Research   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 6; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR 4; IL6 PROTEIN, HUMAN; JANUS KINASE; SOCS1 PROTEIN, HUMAN; STAT3 PROTEIN; STAT3 PROTEIN, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING; TLR4 PROTEIN, HUMAN;

ARTICLE; CD3+ T LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; MESENCHYMAL STEM CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; UMBILICAL CORD; UPREGULATION; CELL COMMUNICATION; CELL CULTURE; CELL DIFFERENTIATION; COCULTURE; CYTOLOGY; GENE EXPRESSION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; TRANSCRIPTION INITIATION;

CELL COMMUNICATION; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; GENE EXPRESSION; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-6; JANUS KINASES; MESENCHYMAL STROMAL CELLS; PHENOTYPE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TOLL-LIKE RECEPTOR 4; TRANSCRIPTIONAL ACTIVATION; UMBILICAL CORD; UP-REGULATION;

EID: 84906545300     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0559     Document Type: Article

References (49)

1. 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.
2. Prockop DJ. (1997). Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74.
3. Jorgensen C, F Djouad, F Apparailly and D Noel. (2003). Engineering mesenchymal stem cells for immunotherapy. Gene Ther 10:928-931.
4. Uccelli A, L Moretta and V Pistoia. (2008). Mesenchymal stem cells in health and disease. Nat Rev Immunol 8:726-736.
5. Zhao RC, L Liao and Q Han. (2004). Mechanisms of and perspectives on the mesenchymal stem cell in immunotherapy. J Lab Clin Med 143:284-291.
6. Spaggiari GM, A Capobianco, S Becchetti, MC Mingari and L Moretta. (2006). Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 107:1484-1490.
7. 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.
8. Krampera M, S Glennie, J Dyson, D Scott, R Laylor, E Simpson and F Dazzi. (2003). Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101: 3722-3729.
9. Bartholomew A, C Sturgeon, M Siatskas, K Ferrer, K McIntosh, S Patil, W Hardy, S Devine, D Ucker, et al. (2002). mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 30:42-48.
10. Le Blanc K, I Rasmusson, B Sundberg, C Gotherstrom, M Hassan, M Uzunel and O Ringden. (2004). Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363:1439-1441.
11. Meisel R, A Zibert, M Laryea, U Gobel, W Daubener and D Dilloo. (2004). Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenasemediated tryptophan degradation. Blood 103:4619-4621.
12. Ren, G, L Zhang, X Zhao,G Xu, Y Zhang, AI Roberts, RC Zhao and Y Shi. (2008). Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2:141-150.
13. Potian JA, H Aviv, NM Ponzio, JS Harrison and P Rameshwar. (2003). Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol 171:3426-3434.
14. Tse WT, JD Pendleton, WM Beyer, MC Egalka and EC Guinan. (2003). Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 75:389-397.
15. Djouad F, P Plence, C Bony, P Tropel, F Apparailly, J Sany, D Noel and C Jorgensen. (2003). Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102:3837-3844.
16. Beyth S, Z Borovsky, D Mevorach, M Liebergall, Z Gazit, H Aslan, E Galun and J Rachmilewitz. (2005). Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 105:2214-2219.
17. Zeddou M, A Briquet, B Relic, C Josse, MG Malaise, A Gothot, C Lechanteur and YM Beguin. (2010). The umbilical cord matrix is a better source of mesenchymal stem cells (MSC) than the umbilical cord blood. Cell Biol Int 34:693-701.
18. Banas A, T Teratani, Y Yamamoto, M Tokuhara, F Takeshita, G Quinn, H Okochi and T Ochiya. (2007). Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology 46:219-228.
19. Jin JD, HX Wang, FJ Xiao, JS Wang, X Lou, LD Hu, LS Wang and ZK Guo. (2008). A novel rich source of human mesenchymal stem cells from the debris of bone marrow samples. Biochem Biophys Res Commun 376: 191-195.
20. Lu LL, YJ Liu, SG Yang, QJ Zhao, X Wang, W Gong, ZB Han, ZS Xu, YX Lu, et al. (2006). Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica 91:1017-1026.
21. Cho PS, DJ Messina, EL Hirsh, N Chi, SN Goldman, DP Lo, IR Harris, SH Popma, DH Sachs and CA Huang. (2008). Immunogenicity of umbilical cord tissue derived cells. Blood 111:430-438.
22. Steinman RM. (2003). The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9:271-296.
23. Steinman RM, D Hawiger and MC Nussenzweig. (2003). Tolerogenic dendritic cells. Annu Rev Immunol 21:685-711.
24. Thomson AW and PD Robbins. (2008). Tolerogenic dendritic cells for autoimmune disease and transplantation. Ann Rheum Dis 67 (Suppl. 3):iii90-iii96.
25. Chorny, A, E Gonzalez-Rey and D Ganea. (2006). Vasoactive intestinal peptide generates CD4 +CD25 + regulatory T cells in vivo: therapeutic applications in autoimmunity and transplantation. Ann N Y Acad Sci 1070:190-195.
26. Benkhoucha M, ML Santiago-Raber, G Schneiter, M Chofflon, H Funakoshi, T Nakamura and PH Lalive. (2010). Hepatocyte growth factor inhibits CNS autoimmunity by inducing tolerogenic dendritic cells and CD25 + Foxp3 + regulatory T cells. Proc Natl Acad Sci U S A 107:6424-6429.
27. Farquhar CA, AM Paterson, SP Cobbold, H Garcia Rueda, PJ Fairchild, SF Yates, E Adams, NJ Saunders, H Waldmann and KF Nolan. (2010). Tolerogenicity is not an absolute property of a dendritic cell. Eur J Immunol 40: 1728-1737.
28. Boks MA, JR Kager-Groenland, MS Haasjes, JJ Zwaginga, SM van Ham and A ten Brinke. (2012). IL-10-generated tolerogenic dendritic cells are optimal for functional regulatory T cell induction - a comparative study of human clinical-applicable DC. Clin Immunol 142:332-342.
29. Chen L, W Zhang, H Yue, Q Han, B Chen, M Shi, J Li, B Li, S You, Y Shi and RC Zhao. (2007). Effects of human mesenchymal stem cells on the differentiation of dendritic cells from CD34 + cells. Stem Cells Dev 16:719-731.
30. Chiesa S, S Morbelli, S Morando, M Massollo, C Marini, A Bertoni, F Frassoni, ST Bartolome, G Gambuceti, E Traggiai and A Uccelli. (2011). Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells. Proc Natl Acad Sci U S A 108:17384-17389.
31. Zhang B, R Liu, D Shi, X Liu, Y Chen, X Dou, X Zhu, C Lu, W Liang, et al. (2009). Mesenchymal stem cells induce mature dendritic cells into a novel Jagged-2- dependent regulatory dendritic cell population. Blood 113: 46-57.
32. Zhang W, W Ge, C Li, S You, L Liao, Q Han, W Deng and RC Zhao. (2004). Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte- derived dendritic cells. Stem Cells Dev 13:263-271.
33. Li YP, S Paczesny, E Lauret, S Poirault, P Bordigoni, F Mekhloufi, O Hequet, Y Bertrand, JP Ou-Yang, et al. (2008). Human mesenchymal stem cells license adult CD34 + hemopoietic progenitor cells to differentiate into regulatory dendritic cells through activation of the Notch pathway. J Immunol 180:1598-1608.
34. O'Shea JJ, M Gadina and RD Schreiber. (2002). Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109 (Suppl.):S121-S131.
35. Starr R, TA Willson, EM Viney, LJ Murray, JR Rayner, BJ Jenkins, TJ Gonda, WS Alexander, D Metcalf, NA Nicola and DJ Hilton. (1997). A family of cytokineinducible inhibitors of signalling. Nature 87:917-921.
36. Starr R, D Metcalf, AG Elefanty, M Brysha, TA Willson, NA Nicola, DJ Hilton and WS Alexander. (1998). Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc Natl Acad Sci U S A 95:14395-14399.
37. Henson SM, R Macaulay, S Kiani-Alikhan and AN Akbar. The use of the inhibitory receptors for modulating the immune responses. Curr Pharm Des 14:2643-2650.
38. Tanaka K. (2008). Loss of suppressor of cytokine signaling- 1 in helper T cells leads to defective Th17 differentiation by enhancing antagonistic effects of IFN on STAT3 and Smads. J Immunol 180:3746-3756.
39. Hanada T, H Yoshida, S Kato, K Tanaka, K Masutani, J Tsukada, Y Nomura, H Mimata, M Kubo and A Yoshimura. (2003). Suppressor of cytokine signaling-1 is essential for suppressing dendritic cell activation and systemic autoimmunity. Immunity 19:437-450.
40. Jackson SH, CR Yu, RM Mahdi, S Ebong and CE Egwuagu. (2004). Dendritic cell maturation requires STAT1 and is under feedback regulation by suppressors of cytokine signaling. J Immunol 172:2307-2315.
41. Shen L, K Evel-Kabler, R Strube and SY Chen. (2004). Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific anti-tumor immunity. Nat Biotechnol 22:1546-1553.
42. Satou R, K Miyata, RA Gonzalez-Villalobos, JR Ingelfinger, LG Navar and H Kobori. (2012). Interferongamma biphasically regulates angiotensinogen expression via a JAK-STAT pathway and suppressor of cytokine signaling 1 (SOCS1) in renal proximal tubular cells. FASEB J 26:1821-1830.
43. Tamiya T, I Kashiwagi, R Takahashi, H Yasukawa and A Yoshimura. (2011). Suppressors of cytokine signaling (SOCS) proteins and JAK/STAT pathways: regulation of T-cell inflammation by SOCS1 and SOCS3. Arterioscler Thromb Vasc Biol 31:980-985.
44. Kubo M, T Hanada and A Yoshimura. (2003). Suppressors of cytokine signaling and immunity. Nat Immunol 4:1169-1176.
45. Alexander WS and DJ Hilton. (2004). The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu Rev Immunol 22:503-529.
46. Subramanya S, M Armant, JR Salkowitz, AM Nyakeriga, V Haridas, M Hasan, A Bansal, PA Goepfert, KK Wynn, et al. (2010). Enhanced induction of HIV-specific cytotoxic T lymphocytes by dendritic cell-targeted delivery of SOCS-1 siRNA. Mol Ther 18:2028-2037.
47. Manetti R, F Gerosa, MG Giudizi, R Biagiotti, P Parronchi, MP Piccinni, S Sampognaro, E Maggi, S Romagnani and G Trinchieri. (1994). Interleukin 12 induces stable priming for interferon gamma (IFN-gamma) production during differentiation of human T helper (Th) cells and transient IFN-gamma production in established Th2 cell clones. J Exp Med 179:1273-1283.
48. Kinjyo I, T Hanada, K Inagaki-Ohara, H Mori, D Aki, M Ohishi, H Yoshida, M Kubo and A Yoshimura. (2002). SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 17:583-591.
49. Nakagawa R, T Naka, H Tsutsui, M Fujimoto, A Kimura, T Abe, E Seki, S Sato, O Takeuchi, et al. (2002). SOCS-1 participates in negative regulation of LPS responses. Immunity 17:677-687.