Home LiteratureArticle Details
PMID: 22210182 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

MicroRNAs and STAT interplay.

Seminars in cancer biology ·Vol. 22 ·No. 1 ·2012-02-00 ·Pages 70-5

Kohanbash G, Okada H

Abstract

MicroRNA (miR) are emerging as important gene expression regulators often involved in a variety of pathogenesis such as cancers and autoimmunity. Signal transducers and activators of transcription (STAT) proteins are the principle signaling proteins for many cytokines and growth factors, thereby play a critical role in regulating immune cell homeostasis, differentiation and cellular functions. In this review, we discuss recent advances in the field demonstrating active interactions between STATs and miRs, with our primary focus on the promotion and inhibition of immune cells and cancer. Additionally, we review the reciprocal regulations between STATs and miR, and discuss how we can use this knowledge in the context of diseases. For example, recent findings related to STAT1 and miR-155 support the presence of a positive feedback loop of miR-155 and STAT1 in response to inflammatory signals or infection. STAT3 is known to play critical roles in tumorigenesis and cancer-induced immunosuppression. There is a growing body of evidence demonstrating that STAT3 directly activates miR-21, one of miRs that promote cancer cell survival and proliferation. While some miRs directly regulate STATs, there are findings demonstrating indirect STAT regulation by miRs also mediate important biological mechanisms. Therefore, further research is warranted to elucidate significant contributions made by direct and indirect miR-STAT mechanisms. As we learn more about miR pathways, we gain the opportunity to manipulate them in cancer cells to slow down growth or increase their susceptibility anti-tumor immunity.

MeSH Terms
Gene Expression Regulation Humans Immunotherapy Interferons/immunology MicroRNAs/physiology Neoplasms/genetics,immunology,therapy STAT Transcription Factors/immunology,physiology,therapeutic use
Chemicals
MicroRNAs STAT Transcription Factors Interferons
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Kohanbash Gary
Department of Infectious Diseases and Microbiology, University of Pittsburgh Graduate School of Public Health, Pittsburgh, PA 15261, USA.
Okada Hideho
References (76)
76 references, click to expand
  1. The miR-17-92 cluster of microRNAs confers tumorigenicity by inhibiting oncogene-induced senescence.
    Cancer Res. 2010 Nov 1;70(21):8547-57 PMID: 20851997
  2. Oncogenic microRNAs (OncomiRs) as a new class of cancer biomarkers.
    Bioessays. 2010 Oct;32(10):894-904 PMID: 21105295
  3. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein.
    Immunity. 2009 Jan 16;30(1):80-91 PMID: 19144316
  4. The JAK/STAT signaling pathway.
    J Cell Sci. 2004 Mar 15;117(Pt 8):1281-3 PMID: 15020666
  5. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway.
    Cell. 1996 Feb 9;84(3):431-42 PMID: 8608597
  6. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells.
    Cancer Res. 2005 Jul 15;65(14):6029-33 PMID: 16024602
  7. microRNA-222 controls neovascularization by regulating signal transducer and activator of transcription 5A expression.
    Arterioscler Thromb Vasc Biol. 2010 Aug;30(8):1562-8 PMID: 20489169
  8. How cells respond to interferons.
    Annu Rev Biochem. 1998;67:227-64 PMID: 9759489
  9. IL-4 suppresses very late antigen-4 expression which is required for therapeutic Th1 T-cell trafficking into tumors.
    J Immunother. 2009 Oct;32(8):793-802 PMID: 19752754
  10. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3539-43 PMID: 8097319
  11. Enforced expression of miR-125b affects myelopoiesis by targeting multiple signaling pathways.
    Blood. 2011 Apr 21;117(16):4338-48 PMID: 21368288
  12. Global changes of mRNA expression reveals an increased activity of the interferon-induced signal transducer and activator of transcription (STAT) pathway by repression of miR-221/222 in glioblastoma U251 cells.
    Int J Oncol. 2010 Jun;36(6):1503-12 PMID: 20428775
  13. miR-20a and miR-290, multi-faceted players with a role in tumourigenesis and senescence.
    J Cell Mol Med. 2010 Nov;14(11):2633-40 PMID: 21114763
  14. MicroRNA let-7a inhibits proliferation of human prostate cancer cells in vitro and in vivo by targeting E2F2 and CCND2.
    PLoS One. 2010 Apr 14;5(4):e10147 PMID: 20418948
  15. The Stat family in cytokine signaling.
    Curr Opin Cell Biol. 2001 Apr;13(2):211-7 PMID: 11248555
  16. A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development.
    Blood. 2011 Feb 3;117(5):1565-73 PMID: 21127177
  17. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells.
    Immunity. 1996 Mar;4(3):313-9 PMID: 8624821
  18. Lethal-7 is down-regulated by the hepatitis B virus x protein and targets signal transducer and activator of transcription 3.
    J Hepatol. 2010 Jul;53(1):57-66 PMID: 20447714
  19. MicroRNAs and prostate cancer.
    Acta Biochim Biophys Sin (Shanghai). 2010 Jun 15;42(6):363-9 PMID: 20539944
  20. Immunotherapeutic approaches for glioma.
    Crit Rev Immunol. 2009;29(1):1-42 PMID: 19348609
  21. Regulation of the germinal center response by microRNA-155.
    Science. 2007 Apr 27;316(5824):604-8 PMID: 17463289
  22. Functional roles of STAT family proteins: lessons from knockout mice.
    Stem Cells. 1999;17(3):138-46 PMID: 10342556
  23. MicroRNAs (miR)-221 and miR-222, both overexpressed in human thyroid papillary carcinomas, regulate p27Kip1 protein levels and cell cycle.
    Endocr Relat Cancer. 2007 Sep;14(3):791-8 PMID: 17914108
  24. Dicer-regulated microRNAs 222 and 339 promote resistance of cancer cells to cytotoxic T-lymphocytes by down-regulation of ICAM-1.
    Proc Natl Acad Sci U S A. 2009 Jun 30;106(26):10746-51 PMID: 19520829
  25. Regulation of macrophage production of vascular endothelial growth factor (VEGF) by hypoxia and transforming growth factor beta-1.
    Ann Surg Oncol. 1998 Apr-May;5(3):271-8 PMID: 9607631
  26. Viruses and interferon: a fight for supremacy.
    Nat Rev Immunol. 2002 Sep;2(9):675-87 PMID: 12209136
  27. Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer.
    Blood. 2007 Aug 15;110(4):1330-3 PMID: 17496199
  28. A microRNA polycistron as a potential human oncogene.
    Nature. 2005 Jun 9;435(7043):828-33 PMID: 15944707
  29. Requirement of bic/microRNA-155 for normal immune function.
    Science. 2007 Apr 27;316(5824):608-11 PMID: 17463290
  30. IFN induces miR-21 through a signal transducer and activator of transcription 3-dependent pathway as a suppressive negative feedback on IFN-induced apoptosis.
    Cancer Res. 2010 Oct 15;70(20):8108-16 PMID: 20813833
  31. MicroRNA-146a modulates human bronchial epithelial cell survival in response to the cytokine-induced apoptosis.
    Biochem Biophys Res Commun. 2009 Feb 27;380(1):177-82 PMID: 19167348
  32. STAT proteins and transcriptional responses to extracellular signals.
    Trends Biochem Sci. 2000 Oct;25(10):496-502 PMID: 11050435
  33. Interpretation and applicability of microRNA data to the context of Alzheimer's and age-related diseases.
    Aging (Albany NY). 2010 Mar 31;2(3):166-9 PMID: 20375468
  34. MicroRNA biogenesis: coordinated cropping and dicing.
    Nat Rev Mol Cell Biol. 2005 May;6(5):376-85 PMID: 15852042
  35. Fibroblast growth factors in development and cancer: insights from the mammary and prostate glands.
    Curr Drug Targets. 2009 Jul;10(7):632-44 PMID: 19601767
  36. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters.
    Cell. 2008 Mar 7;132(5):875-86 PMID: 18329372
  37. miR-20b modulates VEGF expression by targeting HIF-1 alpha and STAT3 in MCF-7 breast cancer cells.
    J Cell Physiol. 2010 Jul;224(1):242-9 PMID: 20232316
  38. miR-17-92 expression in differentiated T cells - implications for cancer immunotherapy.
    J Transl Med. 2010 Feb 18;8:17 PMID: 20167088
  39. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice.
    Nature. 1996 Jul 11;382(6587):174-7 PMID: 8700209
  40. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells.
    Immunity. 1999 Feb;10(2):249-59 PMID: 10072077
  41. Bone morphogenetic proteins in bone tumors.
    J Orthop Sci. 2004;9(3):334-40 PMID: 15168194
  42. The antitumor effects of IFN-alpha are abrogated in a STAT1-deficient mouse.
    J Clin Invest. 2003 Jul;112(2):170-80 PMID: 12865406
  43. Formation of STAT1-STAT2 heterodimers and their role in the activation of IRF-1 gene transcription by interferon-alpha.
    J Biol Chem. 1996 Mar 8;271(10):5790-4 PMID: 8621447
  44. MicroRNAs and cancer--new paradigms in molecular oncology.
    Curr Opin Cell Biol. 2009 Jun;21(3):470-9 PMID: 19411171
  45. Bone morphogenetic protein receptors and signal transduction.
    J Biochem. 2010 Jan;147(1):35-51 PMID: 19762341
  46. Ectopic expression of microRNA-155 enhances innate antiviral immunity against HBV infection in human hepatoma cells.
    Virol J. 2011 Jul 18;8:354 PMID: 21762537
  47. The modulation of microRNAs by type I IFN through the activation of signal transducers and activators of transcription 3 in human glioma.
    Mol Cancer Res. 2009 Dec;7(12):2022-30 PMID: 19934272
  48. MicroRNA-145 targets YES and STAT1 in colon cancer cells.
    PLoS One. 2010 Jan 21;5(1):e8836 PMID: 20098684
  49. Inflammatory cytokines regulate microRNA-155 expression in human retinal pigment epithelial cells by activating JAK/STAT pathway.
    Biochem Biophys Res Commun. 2010 Nov 12;402(2):390-5 PMID: 20950585
  50. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer.
    Gastroenterology. 2007 Aug;133(2):647-58 PMID: 17681183
  51. Intron-mediated RNA interference and microRNA biogenesis.
    Methods Mol Biol. 2009;487:387-413 PMID: 19301658
  52. MicroRNAs in breast cancer pathogenesis.
    Minerva Ginecol. 2010 Dec;62(6):559-71 PMID: 21079577
  53. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice.
    Nat Immunol. 2007 Feb;8(2):191-7 PMID: 17136045
  54. Interferon-alpha in tumor immunity and immunotherapy.
    Cytokine Growth Factor Rev. 2002 Apr;13(2):119-34 PMID: 11900988
  55. NF-κB and STAT3 - key players in liver inflammation and cancer.
    Cell Res. 2011 Jan;21(1):159-68 PMID: 21187858
  56. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation.
    Cancer Res. 2005 Nov 1;65(21):9628-32 PMID: 16266980
  57. miR-17 family of microRNAs controls FGF10-mediated embryonic lung epithelial branching morphogenesis through MAPK14 and STAT3 regulation of E-Cadherin distribution.
    Dev Biol. 2009 Sep 15;333(2):238-50 PMID: 19559694
  58. Regulation of JAK-STAT signalling in the immune system.
    Nat Rev Immunol. 2003 Nov;3(11):900-11 PMID: 14668806
  59. miR-17-92 cluster microRNAs confers tumorigenicity in multiple myeloma.
    Cancer Lett. 2011 Oct 1;309(1):62-70 PMID: 21664042
  60. Signal transducer and activator of transcription 3-mediated regulation of miR-199a-5p links cardiomyocyte and endothelial cell function in the heart: a key role for ubiquitin-conjugating enzymes.
    Eur Heart J. 2011 May;32(10):1287-97 PMID: 20965886
  61. Interleukin-6 modulates the expression of the bone morphogenic protein receptor type II through a novel STAT3-microRNA cluster 17/92 pathway.
    Circ Res. 2009 May 22;104(10):1184-91 PMID: 19390056
  62. Mechanisms of type-I- and type-II-interferon-mediated signalling.
    Nat Rev Immunol. 2005 May;5(5):375-86 PMID: 15864272
  63. Discrete roles of STAT4 and STAT6 transcription factors in tuning epigenetic modifications and transcription during T helper cell differentiation.
    Immunity. 2010 Jun 25;32(6):840-51 PMID: 20620946
  64. Characterization of the human STAT5A and STAT5B promoters: evidence of a positive and negative mechanism of transcriptional regulation.
    FEBS Lett. 2004 Mar 26;562(1-3):27-34 PMID: 15043997
  65. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer.
    Mol Cell. 2010 Aug 27;39(4):493-506 PMID: 20797623
  66. MicroRNA-21 expression in CD4+ T cells is regulated by STAT3 and is pathologically involved in Sézary syndrome.
    J Invest Dermatol. 2011 Mar;131(3):762-8 PMID: 21085192
  67. STAT3 in CD4+ T helper cell differentiation and inflammatory diseases.
    Cytokine. 2009 Sep;47(3):149-56 PMID: 19648026
  68. MicroRNAs in immune regulation--opportunities for cancer immunotherapy.
    Int J Biochem Cell Biol. 2010 Aug;42(8):1256-61 PMID: 20144731
  69. STAT5 requires the N-domain for suppression of miR15/16, induction of bcl-2, and survival signaling in myeloproliferative disease.
    Blood. 2010 Feb 18;115(7):1416-24 PMID: 20008792
  70. The biology of Stat4 and Stat6.
    Oncogene. 2000 May 15;19(21):2577-84 PMID: 10851056
  71. The interleukin 13 (IL-13) pathway in human macrophages is modulated by microRNA-155 via direct targeting of interleukin 13 receptor alpha1 (IL13Ralpha1).
    J Biol Chem. 2011 Jan 21;286(3):1786-94 PMID: 21097505
  72. RNAi, microRNAs, and human disease.
    Cancer Chemother Pharmacol. 2006 Nov;58 Suppl 1:s63-8 PMID: 17093929
  73. Recombinant human granulocyte macrophage-colony stimulating factor (rhGM-CSF) and autologous melanoma vaccine mediate tumor regression in patients with metastatic melanoma.
    J Immunother. 1999 Mar;22(2):166-74 PMID: 10093041
  74. microRNAs at the regulatory frontier: an investigation into how microRNAs impact the development and effector functions of CD4 T cells.
    Immunol Res. 2011 Apr;49(1-3):87-96 PMID: 21191665
  75. Many roads to maturity: microRNA biogenesis pathways and their regulation.
    Nat Cell Biol. 2009 Mar;11(3):228-34 PMID: 19255566
  76. Role of type 1 IFNs in antiglioma immunosurveillance--using mouse studies to guide examination of novel prognostic markers in humans.
    Clin Cancer Res. 2010 Jul 1;16(13):3409-19 PMID: 20472682
Article Info
Journal
Seminars in cancer biology
Abbr.
Semin Cancer Biol
ISSN
1096-3650
Published
2012-02-00
Epub
2011-00-24
Pages
70-5
Language
English
Region
England
NLM ID
9010218
PMCID
PMC3288787
Subset
IM
Grants
NCI NIH HHS · P30 CA047904-24 · United States
NINDS NIH HHS · R01 NS055140-05 · United States
NINDS NIH HHS · [2R01NS055140 · United States
NCI NIH HHS · 1P01CA132714 · United States
NINDS NIH HHS · 2P01NS40923 · United States
NCI NIH HHS · P01 CA132714 · United States
NCI NIH HHS · P3CA047904 · United States
NINDS NIH HHS · P01 NS040923-09 · United States
NCI NIH HHS · P30 CA047904 · United States
NINDS NIH HHS · R01 NS055140 · United States
NINDS NIH HHS · P01 NS040923 · United States
NCI NIH HHS · P01 CA132714-04 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com