TGF-β-inducible microRNA-183 silences tumor-associated natural killer cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 11, 2014, Pages 4203-4208

  Donatelli, Sarah S ^a   Zhou, Jun Min ^a   Gilvary, Danielle L ^a   Eksioglu, Erika A ^a   Chen, Xianghong ^a   Cress, W Douglas ^a   Haura, Eric B ^a   Schabath, Matthew B ^a   Coppola, Domenico ^a   Wei, Sheng ^a   Djeu, Julie Y ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Immune suppression; Non small cell lung cancer; Posttranscriptional silencing

Indexed keywords

KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; MICRORNA; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL KILLER CELL RECEPTOR; PERFORIN; TRANSFORMING GROWTH FACTOR BETA;

3' UNTRANSLATED REGION; ARTICLE; CANCER CELL; CELL POLARITY; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; LUNG CANCER; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL DESTRUCTION; TUMOR MICROENVIRONMENT;

IMMUNE SUPPRESSION; NON-SMALL CELL LUNG CANCER; POSTTRANSCRIPTIONAL SILENCING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; FLOW CYTOMETRY; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KILLER CELLS, NATURAL; LUCIFERASES; MEMBRANE PROTEINS; MICRORNAS; MICROSCOPY, FLUORESCENCE; NEOPLASMS; RECEPTORS, NATURAL KILLER CELL; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84896538538     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1319269111     Document Type: Article

References (42)

1. Djeu JY, Jiang K, Wei S (2002) A view to a kill: Signals triggering cytotoxicity. Clin Cancer Res 8(3):636-640. (Pubitemid 34745987)
2. Graef T, et al. (2009) KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C. J Exp Med 206(11):2557-2572.
3. Yokoyama WM, Plougastel BF (2003) Immune functions encoded by the natural killer gene complex. Nat Rev Immunol 3(4):304-316. (Pubitemid 37328683)
4. Vitale M, et al. (1998) NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J Exp Med 187(12):2065-2072. (Pubitemid 28285576)
5. Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63(1): 11-30.
6. Carrega P, et al. (2008) Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(-) cells and display an impaired capability to kill tumor cells. Cancer 112(4):863-875. (Pubitemid 351240580)
7. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144(5):646-674.
8. Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limón P (2010) The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol 10(8):554-567.
9. Ikushima H, Miyazono K (2010) TGFbeta signalling: A complex web in cancer progression. Nat Rev Cancer 10(6):415-424.
10. Friese MA, et al. (2004) RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo. Cancer Res 64(20): 7596-7603. (Pubitemid 39372105)
11. Trotta R, et al. (2008) TGF-beta utilizes SMAD3 to inhibit CD16-mediated IFN-gamma production and antibody-dependent cellular cytotoxicity in human NK cells. J Immunol 181(6):3784-3792.
12. Baltimore D, Boldin MP, O'Connell RM, Rao DS, Taganov KD (2008) MicroRNAs: New regulators of immune cell development and function. Nat Immunol 9(8):839-845. (Pubitemid 352038302)
13. Calin GA, et al. (2004) Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101(9):2999-3004. (Pubitemid 38327724)
14. Giebel S, et al. (2008) Association of KIR2DS4 and its variant KIR1D with leukemia. Leukemia 22(11):2129-2130, discussion 2130-2131.
15. Katz G, et al. (2004) MHC class I-independent recognition of NK-activating receptor KIR2DS4. J Immunol 173(3):1819-1825. (Pubitemid 38971615)
16. Busche A, Goldmann T, Naumann U, Steinle A, Brandau S (2006) Natural killer cellmediated rejection of experimental human lung cancer by genetic overexpression of major histocompatibility complex class I chain-related gene A. Hum Gene Ther 17(2): 135-146. (Pubitemid 43262029)
17. Landi MT, et al. (2008) Gene expression signature of cigarette smoking and its role in lung adenocarcinoma development and survival. PLoS ONE 3(2):e1651.
18. Bhattacharjee A, et al. (2001) Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci USA 98(24):13790-13795. (Pubitemid 33115977)
19. Hou J, et al. (2010) Gene expression-based classification of non-small cell lung carcinomas and survival prediction. PLoS ONE 5(4):e10312.
20. Geller MA, et al. (2011) A phase II study of allogeneic natural killer cell therapy to treat patients with recurrent ovarian and breast cancer. Cytotherapy 13(1):98-107.
21. Saji H, et al. (2003) Significance of expression of TGF-beta in pulmonary metastasis in non-small cell lung cancer tissues. Ann Thorac Cardiovasc Surg 9(5):295-300.
22. Garber ME, et al. (2001) Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci USA 98(24):13784-13789. (Pubitemid 33115976)
23. Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: Contributions of translational repression and mRNA decay. Nat Rev Genet 12(2):99-110.
24. Pillai RS, et al. (2005) Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309(5740):1573-1576. (Pubitemid 41266485)
25. Bartel DP (2009) MicroRNAs: Target recognition and regulatory functions. Cell 136(2): 215-233.
26. Su LJ, et al. (2007) Selection of DDX5 as a novel internal control for Q-RT-PCR from microarray data using a block bootstrap re-sampling scheme. BMC Genomics 8:140.
27. Narni-Mancinelli E, et al. (2012) Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 335(6066):344-348.
28. Platonova S, et al. (2011) Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res 71(16):5412-5422.
29. Didiano D, Hobert O (2006) Perfect seed pairing is not a generally reliable predictor for miRNA-target interactions. Nat Struct Mol Biol 13(9):849-851. (Pubitemid 44338780)
30. Saetrom P, et al. (2007) Distance constraints between microRNA target sites dictate efficacy and cooperativity. Nucleic Acids Res 35(7):2333-2342. (Pubitemid 47073716)
31. Yu J, et al. (2006) Pro- and antiinflammatory cytokine signaling: Reciprocal antagonism regulates interferon-gamma production by human natural killer cells. Immunity 24(5):575-590. (Pubitemid 43728149)
32. Arnon TI, et al. (2001) Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol 31(9):2680-2689. (Pubitemid 32898735)
33. Baychelier F, et al. (2013) Identification of a cellular ligand for the natural cytotoxicity receptor NKp44. Blood 122(17):2935-2942.
34. Turnbull IR, Colonna M (2007) Activating and inhibitory functions of DAP12. Nat Rev Immunol 7(2):155-161. (Pubitemid 46174861)
35. Park YP, et al. (2011) Complex regulation of human NKG2D-DAP10 cell surface expression: Opposing roles of the γc cytokines and TGF-β1. Blood 118(11): 3019-3027.
36. Lanier LL (2009) DAP10- and DAP12-associated receptors in innate immunity. Immunol Rev 227(1):150-160.
37. Snyder MR, Nakajima T, Leibson PJ, Weyand CM, Goronzy JJ (2004) Stimulatory killer Ig-like receptors modulate T cell activation through DAP12-dependent and DAP12- independent mechanisms. J Immunol 173(6):3725-3731. (Pubitemid 39280733)
38. Tridandapani S, et al. (2003) TGF-beta 1 suppresses [correction of supresses] myeloid Fc gamma receptor function by regulating the expression and function of the common gamma-subunit. J Immunol 170(9):4572-4577. (Pubitemid 36519963)
39. Lin Q, et al. (2012) A cluster of specified microRNAs in peripheral blood as biomarkers for metastatic non-small-cell lung cancer by stem-loop RT-PCR. J Cancer Res Clin Oncol 138(1):85-93.
40. Sarver AL, Li L, Subramanian S (2010) MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res 70(23):9570-9580.
41. Mulrooney TJ, Posch PE, Hurley CK (2013) DAP12 impacts trafficking and surface stability of killer immunoglobulin-like receptors on natural killer cells. J Leukoc Biol 94(2):301-313.
42. Soroosh P, et al. (2013) Lung-resident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance. J Exp Med 210(4):775-788.