MicroRNA let-7i regulates dendritic cells maturation targeting interleukin-10 via the Janus kinase 1-signal transducer and activator of transcription 3 signal pathway subsequently induces prolonged cardiac allograft survival in rats

Journal of Heart and Lung Transplantation

Volumn 35, Issue 3, 2016, Pages 378-388

  Sun, Yong ^a,b   Jin, Xiangyuan ^b   Liu, Xianglan ^a,b   Zhang, Maomao ^a,b   Liu, Wei ^a,b   Li, Zhenchao ^b   Han, Na ^b   Tan, Miaoxin ^c   Chi, Di ^a,b   Zhu, Jingyi ^b   Zhang, Bo ^b   Yu, Bo ^a,b   Wu, Jian ^a,b  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b HARBIN MEDICAL UNIVERSITY   (China)

^c First Hospital of Fangshan District   (China)

Author keywords

dendritic cell; heart transplantation; IL 10; JAK1 STAT3; MicroRNA let 7i; rat; tolerance

Indexed keywords

INTERLEUKIN 10; JANUS KINASE 1; MICRORNA; MICRORNA LET 7I; STAT3 PROTEIN; UNCLASSIFIED DRUG; MIRNLET7 MICRORNA, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CELL MATURATION; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEART GRAFT; HEART TRANSPLANTATION; IMMUNOHISTOCHEMISTRY; MALE; MIXED LYMPHOCYTE REACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ALLOGRAFT; ANIMAL; LEWIS RAT; PHYSIOLOGY;

ALLOGRAFTS; ANIMALS; DENDRITIC CELLS; HEART TRANSPLANTATION; INTERLEUKIN-10; JANUS KINASE 1; MALE; MICRORNAS; RATS; RATS, INBRED LEW; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84951916656     PISSN: 10532498     EISSN: 15573117     Source Type: Journal    
DOI: 10.1016/j.healun.2015.10.041     Document Type: Article

References (50)

1. A. O'Garra, and P. Vieira T(H)1 cells control themselves by producing interleukin-10 Nat Rev Immunol 7 2007 425 428
2. C.A. Akdis, T. Blesken, M. Akdis, B. Wuthrich, and K. Blaser Role of interleukin 10 in specific immunotherapy J Clin Invest 102 1998 98 106
3. Y.Y. Wan, and R.A. Flavell The roles for cytokines in the generation and maintenance of regulatory T cells Immunol Rev 212 2006 114 130
4. M. Hara, C.I. Kingsley, M. Niimi, and et al. IL-10 is required for regulatory T cells to mediate tolerance to alloantigens in vivo J Immunol 166 2001 3789 3796
5. A. O'Garra, P.L. Vieira, P. Vieira, and A.E. Goldfeld IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage J Clin Invest 114 2004 1372 1378
6. A.F. Heneghan, J.F. Pierre, and K.A. Kudsk JAK-STAT and intestinal mucosal immunology JAKSTAT 2 2013 e25530
7. Y. Laouar, T. Welte, X.Y. Fu, and R.A. Flavell STAT3 is required for Flt3L-dependent dendritic cell differentiation Immunity 19 2003 903 912
8. K. Takeda, B.E. Clausen, T. Kaisho, and et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils Immunity 10 1999 39 49
9. A. Chaudhry, D. Rudra, P. Treuting, and et al. CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner Science 326 2009 986 991
10. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
11. C.Z. Chen, L. Li, H.F. Lodish, and D.P. Bartel MicroRNAs modulate hematopoietic lineage differentiation Science 303 2004 83 86
12. M.A. Nahid, M. Satoh, and E.K. Chan Mechanistic role of microRNA-146a in endotoxin-induced differential cross-regulation of TLR signaling J Immunol 186 2011 1723 1734
13. A. Rodriguez, E. Vigorito, S. Clare, and et al. Requirement of bic/microRNA-155 for normal immune function Science 316 2007 608 611
14. M. Zhang, F. Liu, H. Jia, and et al. Inhibition of microRNA let-7i depresses maturation and functional state of dendritic cells in response to lipopolysaccharide stimulation via targeting suppressor of cytokine signaling 1 J Immunol 187 2011 1674 1683
15. M. Niimi The technique for heterotopic cardiac transplantation in mice: experience of 3000 operations by one surgeon J Heart Lung Transplant 20 2001 1123 1128
16. S. Stewart, G.L. Winters, M.C. Fishbein, and et al. Revision of the 1990 working formulation for the standardization of nomenclature in the diagnosis of heart rejection J Heart Lung Transplant 24 2005 1710 1720
17. H.C. Probst, S. Muth, and H. Schild Regulation of the tolerogenic function of steady-state DCs Eur J Immunol 44 2014 927 933
18. G. Huang, Y. Wang, and H. Chi Control of T cell fates and immune tolerance by p38α signaling in mucosal CD103+ dendritic cells J Immunol 191 2013 650 659
19. M.L. Turner, F.M. Schnorfeil, and T. Brocker MicroRNAs regulate dendritic cell differentiation and function J Immunol 187 2011 3911 3917
20. M.M. Tiao, L. Lu, R. Tao, L. Wang, J.J. Fung, and S. Qian Prolongation of cardiac allograft survival by systemic administration of immature recipient dendritic cells deficient in NF-kappaB activity Ann Surg 241 2005 497 505
21. L. Chen, L. Zheng, W. He, and et al. Cotransfection with IL-10 and TGF-β1 into immature dendritic cells enhances immune tolerance in a rat liver transplantation model Am J Physiol Gastrointest Liver Physiol 306 2014 G575 G581
22. X.W. Gao, Y. Fu, W.J. Li, A.J. Du, X. Li, and X.D. Zhao Mechanism of immune tolerance induced by donor derived immature dendritic cells in rat high-risk corneal transplantation Int J Ophthalmol 6 2013 269 275
23. F. Huang, M.L. Li, Z.F. Fang, and et al. Overexpression of MicroRNA-1 improves the efficacy of mesenchymal stem cell transplantation after myocardial infarction Cardiology 125 2013 18 30
24. H. Huang, J. He, X. Teng, and et al. Combined intrathymic and intravenous injection of mesenchymal stem cells can prolong the survival of rat cardiac allograft associated with decrease in miR-155 expression J Surg Res 185 2013 896 903
25. J. Li, J. Gong, P. Li, and et al. Knockdown of microRNA-155 in Kupffer cells results in immunosuppressive effects and prolongs survival of mouse liver allografts Transplantation 97 2014 626 635
26. B.J. Reinhart, F.J. Slack, M. Basson, and et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans Nature 403 2000 901 906
27. A.E. Pasquinelli, B.J. Reinhart, F. Slack, and et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA Nature 408 2000 86 89
28. N. Yang, S. Kaur, S. Volinia, and et al. MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer Cancer Res 68 2008 10307 10314
29. X.M. Chen, P.L. Splinter, S.P. O'Hare, and N.F. LaRusso A cellular micro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection J Biol Chem 282 2007 28929 28938
30. M. Satoh, Y. Minami, Y. Takahashi, T. Tabuchi, and M. Nakamura A cellular microRNA, let-7i, is a novel biomarker for clinical outcome in patients with dilated cardiomyopathy J Card Fail 17 2011 923 929
31. M. Saraiva, and A. O'Garra The regulation of IL-10 production by immune cells Nat Rev Immunol 10 2010 170 181
32. D. De Kouchkovsky, J.H. Esensten, W.L. Rosenthal, M.M. Morar, J.A. Bluestone, and L.T. Jeker microRNA-17-92 regulates IL-10 production by regulatory T cells and control of experimental autoimmune encephalomyelitis J Immunol 191 2013 1594 1605
33. Y. Liu, Q. Chen, Y. Song, and et al. MicroRNA-98 negatively regulates IL-10 production and endotoxin tolerance in macrophages after LPS stimulation FEBS Lett 585 2011 1963 1968
34. A. Sharma, M. Kumar, T. Ahmad, and et al. Antagonism of mmu-mir-106a attenuates asthma features in allergic murine model J Appl Physiol 113 1985 459 464
35. A. Qin, Z. Wen, Y. Zhou, and et al. MicroRNA-126 regulates the induction and function of CD4(+) Foxp3(+) regulatory T cells through PI3K/AKT pathway J Cell Mol Med 17 2013 252 264
36. Q. Zhou, X. Xiao, C. Wang, and et al. Decreased microRNA-155 expression in ocular Behcet's disease but not in Vogt Koyanagi Harada syndrome Invest Ophthalmol Vis Sci 53 2012 5665 5674
37. F. Ma, X. Liu, D. Li, and et al. MicroRNA-4661 upregulates IL-10 expression in TLR-triggered macrophages by antagonizing RNA-binding protein tristetraprolin-mediated IL-10 mRNA degradation J Immunol 184 2010 6053 6059
38. P.J. Murray The JAK-STAT signaling pathway: input and output integration J Immunol 178 2007 2623 2629
39. M. Yeganegi, C.G. Leung, A. Martins, and et al. Lactobacillus rhamnosus GR-1-induced IL-10 production in human placental trophoblast cells involves activation of JAK/STAT and MAPK pathways Reprod Sci 17 2010 1043 1051
40. N. Hirata, Y. Yanagawa, K. Iwabuchi, and K. Onoe Selective regulation of interleukin-10 production via Janus kinase pathway in murine conventional dendritic cells Cell Immunol 258 2009 9 17
41. Y. Nefedova, P. Cheng, D. Gilkes, and et al. Activation of dendritic cells via inhibition of Jak2/STAT3 signaling J Immunol 175 2005 4338 4346
42. Y. Nefedova, M. Huang, S. Kusmartsev, and et al. Hyperactivation of STAT3 is involved in abnormal differentiation of dendritic cells in cancer J Immunol 172 2004 464 474
43. L.W. Collison, and D.A. Vignali Interleukin-35: odd one out or part of the family? Immunol Rev 226 2008 248 262
44. L.W. Collison, C.J. Workman, T.T. Kuo, and et al. The inhibitory cytokine IL-35 contributes to regulatory T-cell function Nature 450 2007 566 569
45. L.W. Collison, M.R. Pillai, V. Chaturvedi, and D.A. Vignali Regulatory T cell suppression is potentiated by target T cells in a cell contact, IL-35- and IL- 10-dependent manner J Immunol 182 2009 121 128
46. L.W. Collison, V. Chaturvedi, A.L. Henderson, and et al. IL-35-mediated induction of a potent regulatory T cell population Nat Immunol 11 2010 1093 1101
47. R.X. Wang, C.R. Yu, I.M. Dambuza, and et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease Nat Med 20 2014 633 641
48. B.M. Olson, J.A. Sullivan, and W.J. Burlingham Interleukin 35: a key mediator of suppression and the propagation of infectious tolerance Front Immunol 4 2013 315
49. M.L. Belladonna, and U. Grohmann Bioengineering heterodimeric cytokines: turning promiscuous proteins into therapeutic agents Biotechnol Genet Eng Rev 29 2013 149 174
50. J. Bai, S.L. Qiu, X.N. Zhong, and et al. Erythromycin enhances CD4+Foxp3+ regulatory T-cell responses in a rat model of smoke-induced lung inflammation Mediators Inflamm 2012 2012 410232