Tumor-secreted miR-214 induces regulatory T cells: A major link between immune evasion and tumor growth

Cell Research

Volumn 24, Issue 10, 2014, Pages 1164-1180

  Yin, Yuan ^a   Cai, Xing ^a   Chen, Xi ^a   Liang, Hongwei ^a   Zhang, Yujing ^a   Li, Jing ^a   Wang, Zuoyun ^b   Chen, Xiulan ^c   Zhang, Wen ^a   Yokoyama, Seiji ^d   Wang, Cheng ^a   Li, Liang ^a   Li, Limin ^a   Hou, Dongxia ^a   Dong, Lei ^a   Xu, Tao ^e,f   Hiroi, Takachika ^d   Yang, Fuquan ^c   Ji, Hongbin ^b   Zhang, Junfeng ^a   Zen, Ke ^a   Zhang, Chen Yu ^a   more..

^a NANJING UNIVERSITY   (China)

^b INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^e INSTITUTE OF BIOPHYSICS   (China)

^f JIANGNAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MUS; MUS MUSCULUS;

ANTISENSE OLIGONUCLEOTIDE; INTERLEUKIN 10; MICRORNA; MIRN214 MICRORNA, HUMAN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CYTOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; MALE; METABOLISM; MOUSE; NEOPLASM; NUDE MOUSE; PATHOLOGY; REGULATORY T LYMPHOCYTE; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; HEK293 CELLS; HUMANS; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; MICRORNAS; NEOPLASMS; OLIGONUCLEOTIDES, ANTISENSE; PTEN PHOSPHOHYDROLASE; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HETEROLOGOUS;

EID: 84926151514     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2014.121     Document Type: Article

References (47)

1. Algarra I, Garcia-Lora A, Cabrera T, Ruiz-Cabello F, Garrido F. The selection of tumor variants with altered expression of classical and nonclassical MHC class I molecules: implications for tumor immune escape. Cancer Immunol Immunother 2004; 53:904-910.
2. Clark RA, Huang SJ, Murphy GF, et al. Human squamous cell carcinomas evade the immune response by down-regulation of vascular E-selectin and recruitment of regulatory T cells. J Exp Med 2008; 205:2221-2234.
3. Bach JF. Regulatory T cells under scrutiny. Nat Rev Immunol 2003; 3:189-198.
4. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004; 22:531-562.
5. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008; 133:775-787.
6. Fu J, Xu D, Liu Z, et al. Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology 2007; 132:2328-2339.
7. Gallimore A, Godkin A. Regulatory T cells and tumour immunity ? observations in mice and men. Immunology 2008; 123:157-163.
8. Quezada SA, Peggs KS, Simpson TR, Shen Y, Littman DR, Allison JP. Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. J Exp Med 2008; 205:2125-2138.
9. Zhou Q, Bucher C, Munger ME, et al. Depletion of endogenous tumor-associated regulatory T cells improves the efficacy of adoptive cytotoxic T-cell immunotherapy in murine acute myeloid leukemia. Blood 2009; 114:3793-3802.
10. Malek TR, Yu A, Vincek V, Scibelli P, Kong L. CD4 regulatory T cells prevent lethal autoimmunity in IL-2Rbeta-deficient mice. Implications for the nonredundant function of IL-2. Immunity 2002; 17:167-178.
11. Andersson J, Tran DQ, Pesu M, et al. CD4+FoxP3+ regulatory T cells confer infectious tolerance in a TGF-beta-dependent manner. J Exp Med 2008; 205:1975-1981.
12. Lohr J, Knoechel B, Abbas AK. Regulatory T cells in the periphery. Immunol Rev 2006; 212:149-162.
13. Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004; 303:83-86.
14. Lindsay MA. microRNAs and the immune response. Trends Immunol 2008; 29:343-351.
15. Rouas R, Fayyad-Kazan H, El Zein N, et al. Human natural Treg microRNA signature: role of microRNA-31 and microRNA-21 in FOXP3 expression. Eur J Immunol 2009; 39:1608-1618.
16. Divekar AA, Dubey S, Gangalum PR, Singh RR. Dicer insufficiency and microRNA-155 overexpression in lupus regulatory T cells: an apparent paradox in the setting of an inflammatory milieu. J Immunol 2011; 186:924-930.
17. Kohlhaas S, Garden OA, Scudamore C, Turner M, Okkenhaug K, Vigorito E. Cutting edge: the Foxp3 target miR-155 contributes to the development of regulatory T cells. J Immunol 2009; 182:2578-2582.
18. Zhang Y, Liu D, Chen X, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010; 39:133-144.
19. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103:2257-2261.
20. Al-Nedawi K, Meehan B, Rak J. Microvesicles: messengers and mediators of tumor progression. Cell Cycle 2009; 8:2014-2018.
21. Qin YJ, Buermans HPJ, van Kester MS, et al. Deep-sequencing analysis reveals that the miR-199a2/214 cluster within DNM3os represents the vast majority of aberrantly expressed microRNAs in Sezary syndrome. J Investig Dermatol 2012; 132:1520-1522.
22. Flynt AS, Li N, Thatcher EJ, Solnica-Krezel L, Patton JG. Zebrafish miR-214 modulates Hedgehog signaling to specify muscle cell fate. Nat Genet 2007; 39:259-263.
23. Narducci MG, Arcelli D, Picchio MC, et al. MicroRNA profiling reveals that miR-21, miR486 and miR-214 are upregulated and involved in cell survival in Sezary syndrome. Cell Death Dis; 2:e151.
24. Cobb BS, Hertweck A, Smith J, et al. A role for Dicer in immune regulation. J Exp Med 2006; 203:2519-2527.
25. Jindra PT, Bagley J, Godwin JG, Iacomini J. Costimulation-dependent expression of microRNA-214 increases the ability of T cells to proliferate by targeting Pten. J Immunol 2010; 185:990-997.
26. Ha TY. The role of microRNAs in regulatory T Cells and in the immune response. Immune Netw; 11:11-41.
27. Iborra M, Bernuzzi F, Invernizzi P, Danese S. MicroRNAs in autoimmunity and inflammatory bowel disease: crucial regulators in immune response. Autoimmun Rev 2012; 11:305-14
28. Walsh PT, Buckler JL, Zhang J, et al. PTEN inhibits IL-2 receptor-mediated expansion of CD4+CD25+ Tregs. J Clin Invest 2006; 116:2521-2531.
29. Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 2007; 8:191-197.
30. Lahl K, Loddenkemper C, Drouin C, et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med 2007; 204:57-63.
31. Tuveson DA, Shaw AT, Willis NA, et al. Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 2004; 5:375-387.
32. Wang Y, Zhang Z, Lubet RA, You M. A mouse model for tumor progression of lung cancer in ras and p53 transgenic mice. Oncogene 2006; 25:1277-1280.
33. Gao Y, Xiao Q, Ma H, et al. LKB1 inhibits lung cancer progression through lysyl oxidase and extracellular matrix remodeling. Proc Natl Acad Sci USA 2010; 107:18892-18897.
34. Wang Z, Feng Y, Bardeesy N, Wong KK, Liu XY, Ji H. Temporal dissection of K-ras(G12D) mutant in vitro and in vivo using a regulatable K-ras(G12D) mouse allele. PLoS One 2012; 7:e37308.
35. Zhou W, Fong MY, Min Y, et al. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell 2014; 25:501-515.
36. He WA, Calore F, Londhe P, Canella A, Guttridge DC, Croce CM. Microvesicles containing miRNAs promote muscle cell death in cancer cachexia via TLR7. Proc Natl Acad Sci USA 2014; 111:4525-4529.
37. Bar-Eli M. Searching for the 'melano-miRs': miR-214 drives melanoma metastasis. EMBO J 2011; 30:1880-1881.
38. Chan E, Patel R, Nallur S, et al. MicroRNA signatures differentiate melanoma subtypes. Cell Cycle 2011; 10:1845-1852.
39. Miyara M, Sakaguchi S. Natural regulatory T cells: mechanisms of suppression. Trends Mol Med 2007; 13:108-116.
40. Joffre O, Gorsse N, Romagnoli P, Hudrisier D, van Meerwijk JP. Induction of antigen-specific tolerance to bone marrow allografts with CD4+CD25+ T lymphocytes. Blood 2004; 103:4216-4221.
41. von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol 2005; 6:338-344.
42. Huang B, Pan PY, Li Q, et al. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res 2006; 66:1123-1131.
43. Valzasina B, Piconese S, Guiducci C, Colombo MP. Tumor-induced expansion of regulatory T cells by conversion of CD4+CD25? lymphocytes is thymus and proliferation independent. Cancer Res 2006; 66:4488-4495.
44. Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res 1999; 59:3128-3133.
45. Dannull J, Su Z, Rizzieri D, et al. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 2005; 115:3623-3633.
46. Liu Y, Tuve S, Persson J, et al. Adenovirus-mediated intratumoral expression of immunostimulatory proteins in combination with systemic Treg inactivation induces tumor-destructive immune responses in mouse models. Cancer Gene Ther 2011; 18:407-418.
47. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 2009; 11:1143-1149.