Home LiteratureArticle Details
PMID: 21741842 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

miRNA response to DNA damage.

Trends in biochemical sciences ·Vol. 36 ·No. 9 ·2011-09-00 ·Pages 478-84

Wan G, Mathur R, Hu X, Zhang X, Lu X

Abstract

Faithful transmission of genetic material in eukaryotic cells requires not only accurate DNA replication and chromosome distribution but also the ability to sense and repair spontaneous and induced DNA damage. To maintain genomic integrity, cells undergo a DNA damage response using a complex network of signaling pathways composed of coordinate sensors, transducers and effectors in cell cycle arrest, apoptosis and DNA repair. Emerging evidence has suggested that miRNAs play a crucial role in regulation of DNA damage response. In this review, we discuss the recent findings on how miRNAs interact with the canonical DNA damage response and how miRNA expression is regulated after DNA damage.

MeSH Terms
Apoptosis Cell Cycle Checkpoints Cell Transformation, Neoplastic/genetics,metabolism DNA Damage DNA Repair Gene Expression Regulation, Neoplastic Humans MicroRNAs/genetics,metabolism RNA Processing, Post-Transcriptional RNA Stability Signal Transduction Transcription Factors/genetics,metabolism Transcription, Genetic Transcriptional Activation Tumor Suppressor Protein p53/genetics,metabolism
Chemicals
MicroRNAs TP53 protein, human Transcription Factors Tumor Suppressor Protein p53
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wan Guohui
Department of Cancer Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Mathur Rohit
Hu Xiaoxiao
Zhang Xinna
Lu Xiongbin
References (83)
83 references, click to expand
  1. miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors.
    Mol Cell. 2011 Jan 21;41(2):210-20 PMID: 21195000
  2. miR-15 and miR-16 induce apoptosis by targeting BCL2.
    Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13944-9 PMID: 16166262
  3. microRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells.
    Cancer Res. 2009 Oct 15;69(20):8157-65 PMID: 19826040
  4. MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc.
    Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):19678-83 PMID: 19066217
  5. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer.
    Cancer Cell. 2008 Mar;13(3):272-86 PMID: 18328430
  6. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs.
    Nature. 2010 Oct 21;467(7318):986-90 PMID: 20962848
  7. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells.
    Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15472-7 PMID: 17875987
  8. p53-Responsive micrornas 192 and 215 are capable of inducing cell cycle arrest.
    Cancer Res. 2008 Dec 15;68(24):10094-104 PMID: 19074875
  9. MicroRNAs: genomics, biogenesis, mechanism, and function.
    Cell. 2004 Jan 23;116(2):281-97 PMID: 14744438
  10. Coordinated regulation of cell cycle transcripts by p53-Inducible microRNAs, miR-192 and miR-215.
    Cancer Res. 2008 Dec 15;68(24):10105-12 PMID: 19074876
  11. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage.
    Science. 2007 May 25;316(5828):1160-6 PMID: 17525332
  12. miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42.
    Nat Struct Mol Biol. 2009 Jan;16(1):23-9 PMID: 19079265
  13. Oncogenic Wip1 phosphatase is inhibited by miR-16 in the DNA damage signaling pathway.
    Cancer Res. 2010 Sep 15;70(18):7176-86 PMID: 20668064
  14. Modulation of microRNA processing by p53.
    Nature. 2009 Jul 23;460(7254):529-33 PMID: 19626115
  15. Immunofluorescence-based screening identifies germ cell associated microRNA 302 as an antagonist to p63 expression.
    Cell Cycle. 2009 May 1;8(9):1426-32 PMID: 19342891
  16. MicroRNA miR-885-5p targets CDK2 and MCM5, activates p53 and inhibits proliferation and survival.
    Cell Death Differ. 2011 Jun;18(6):974-84 PMID: 21233845
  17. P53 and prognosis: new insights and further complexity.
    Cell. 2005 Jan 14;120(1):7-10 PMID: 15652475
  18. Substrate specificities and identification of putative substrates of ATM kinase family members.
    J Biol Chem. 1999 Dec 31;274(53):37538-43 PMID: 10608806
  19. MAPK pathways in radiation responses.
    Oncogene. 2003 Sep 1;22(37):5885-96 PMID: 12947395
  20. MicroRNA-125b is a novel negative regulator of p53.
    Genes Dev. 2009 Apr 1;23(7):862-76 PMID: 19293287
  21. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs.
    Nat Cell Biol. 2007 May;9(5):604-11 PMID: 17435748
  22. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2999-3004 PMID: 14973191
  23. p53--a Jack of all trades but master of none.
    Nat Rev Cancer. 2009 Nov;9(11):821-9 PMID: 19776747
  24. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation.
    Cell. 2005 Nov 18;123(4):621-9 PMID: 16271385
  25. Nuclear networking fashions pre-messenger RNA and primary microRNA transcripts for function.
    Trends Cell Biol. 2010 Jan;20(1):52-61 PMID: 20004579
  26. The microRNA miR-92 increases proliferation of myeloid cells and by targeting p63 modulates the abundance of its isoforms.
    FASEB J. 2009 Nov;23(11):3957-66 PMID: 19608627
  27. Processing of intronic microRNAs.
    EMBO J. 2007 Feb 7;26(3):775-83 PMID: 17255951
  28. Posttranscriptional regulation of microRNA biogenesis in animals.
    Mol Cell. 2010 May 14;38(3):323-32 PMID: 20471939
  29. miR-449a and miR-449b are direct transcriptional targets of E2F1 and negatively regulate pRb-E2F1 activity through a feedback loop by targeting CDK6 and CDC25A.
    Genes Dev. 2009 Oct 15;23(20):2388-93 PMID: 19833767
  30. Downregulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development.
    Cancer Cell. 2010 Oct 19;18(4):367-81 PMID: 20951946
  31. Regulation of cyclin dependent kinase 6 by microRNA 124 in medulloblastoma.
    J Neurooncol. 2008 Oct;90(1):1-7 PMID: 18607543
  32. ATM is down-regulated by N-Myc-regulated microRNA-421.
    Proc Natl Acad Sci U S A. 2010 Jan 26;107(4):1506-11 PMID: 20080624
  33. MicroRNA-124a is a key regulator of proliferation and monocyte chemoattractant protein 1 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis.
    Arthritis Rheum. 2009 May;60(5):1294-304 PMID: 19404929
  34. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells.
    Cell Stem Cell. 2008 Mar 6;2(3):219-29 PMID: 18371447
  35. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs.
    Nature. 2009 Jun 18;459(7249):1010-4 PMID: 19458619
  36. Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma.
    Cancer Res. 2004 May 1;64(9):3087-95 PMID: 15126345
  37. A genetic defect in exportin-5 traps precursor microRNAs in the nucleus of cancer cells.
    Cancer Cell. 2010 Oct 19;18(4):303-15 PMID: 20951941
  38. MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma.
    Oncogene. 2008 Sep 25;27(43):5651-61 PMID: 18521080
  39. Phosphorylation of the RNase III enzyme Drosha at Serine300 or Serine302 is required for its nuclear localization.
    Nucleic Acids Res. 2010 Oct;38(19):6610-9 PMID: 20554852
  40. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression.
    Cell. 2007 Dec 14;131(6):1097-108 PMID: 18083100
  41. An E2F/miR-20a autoregulatory feedback loop.
    J Biol Chem. 2007 Jan 26;282(4):2135-43 PMID: 17135249
  42. MicroRNA-mediated gene silencing modulates the UV-induced DNA-damage response.
    EMBO J. 2009 Jul 22;28(14):2090-9 PMID: 19536137
  43. Phosphoproteomic analysis of human embryonic stem cells.
    Cell Stem Cell. 2009 Aug 7;5(2):204-13 PMID: 19664994
  44. miR-181a regulates cap-dependent translation of p27(kip1) mRNA in myeloid cells.
    Mol Cell Biol. 2009 May;29(10):2841-51 PMID: 19273599
  45. MicroRNA regulation of DNA repair gene expression in hypoxic stress.
    Cancer Res. 2009 Feb 1;69(3):1221-9 PMID: 19141645
  46. Context-dependent bidirectional regulation of the MutS homolog 2 by transforming growth factor β contributes to chemoresistance in breast cancer cells.
    Mol Cancer Res. 2010 Dec;8(12):1633-42 PMID: 21047769
  47. Nuclear export of microRNA precursors.
    Science. 2004 Jan 2;303(5654):95-8 PMID: 14631048
  48. Negative regulation of tumor suppressor p53 by microRNA miR-504.
    Mol Cell. 2010 Jun 11;38(5):689-99 PMID: 20542001
  49. The ATM kinase induces microRNA biogenesis in the DNA damage response.
    Mol Cell. 2011 Feb 18;41(4):371-83 PMID: 21329876
  50. Ionizing radiation-induced oxidative stress alters miRNA expression.
    PLoS One. 2009 Jul 27;4(7):e6377 PMID: 19633716
  51. Chromatin dynamics coupled to DNA repair.
    Epigenetics. 2009 Jan;4(1):31-42 PMID: 19218832
  52. MicroRNAs: target recognition and regulatory functions.
    Cell. 2009 Jan 23;136(2):215-33 PMID: 19167326
  53. MicroRNA genes are transcribed by RNA polymerase II.
    EMBO J. 2004 Oct 13;23(20):4051-60 PMID: 15372072
  54. Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma.
    Cancer Res. 2007 Jul 1;67(13):6092-9 PMID: 17616664
  55. Emerging paradigms of regulated microRNA processing.
    Genes Dev. 2010 Jun 1;24(11):1086-92 PMID: 20516194
  56. ATM and ATR: networking cellular responses to DNA damage.
    Curr Opin Genet Dev. 2001 Feb;11(1):71-7 PMID: 11163154
  57. The nuclear RNase III Drosha initiates microRNA processing.
    Nature. 2003 Sep 25;425(6956):415-9 PMID: 14508493
  58. Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo.
    Hippocampus. 2010 Apr;20(4):492-8 PMID: 19557767
  59. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing.
    Nature. 2005 Aug 4;436(7051):740-4 PMID: 15973356
  60. The guardians of the genome (p53, TA-p73, and TA-p63) are regulators of tumor suppressor miRNAs network.
    Cancer Metastasis Rev. 2010 Dec;29(4):613-39 PMID: 20922462
  61. The DNA damage response: making it safe to play with knives.
    Mol Cell. 2010 Oct 22;40(2):179-204 PMID: 20965415
  62. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities.
    Nat Med. 2008 Nov;14(11):1271-7 PMID: 18931683
  63. MicroRNAs in Cancer.
    Annu Rev Med. 2009;60:167-79 PMID: 19630570
  64. Nucleocytoplasmic shuttling of JAZ, a new cargo protein for exportin-5.
    Mol Cell Biol. 2004 Aug;24(15):6608-19 PMID: 15254228
  65. ATP-dependent human RISC assembly pathways.
    Nat Struct Mol Biol. 2010 Jan;17(1):17-23 PMID: 19966796
  66. Stress granules: the Tao of RNA triage.
    Trends Biochem Sci. 2008 Mar;33(3):141-50 PMID: 18291657
  67. Multiple microRNAs modulate p21Cip1/Waf1 expression by directly targeting its 3' untranslated region.
    Oncogene. 2010 Apr 15;29(15):2302-8 PMID: 20190813
  68. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs.
    Genes Dev. 2003 Dec 15;17(24):3011-6 PMID: 14681208
  69. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma.
    Blood. 2010 Apr 1;115(13):2630-9 PMID: 20086245
  70. A microRNA component of the p53 tumour suppressor network.
    Nature. 2007 Jun 28;447(7148):1130-4 PMID: 17554337
  71. KSRP, many functions for a single protein.
    Front Biosci (Landmark Ed). 2011 Jan 01;16:1787-96 PMID: 21196264
  72. A quantitative atlas of mitotic phosphorylation.
    Proc Natl Acad Sci U S A. 2008 Aug 5;105(31):10762-7 PMID: 18669648
  73. microRNAs regulate human embryonic stem cell division.
    Cell Cycle. 2009 Nov 15;8(22):3729-41 PMID: 19823043
  74. The Microprocessor complex mediates the genesis of microRNAs.
    Nature. 2004 Nov 11;432(7014):235-40 PMID: 15531877
  75. A feed-forward loop involving protein kinase Calpha and microRNAs regulates tumor cell cycle.
    Cancer Res. 2009 Jan 1;69(1):65-74 PMID: 19117988
  76. Active turnover modulates mature microRNA activity in Caenorhabditis elegans.
    Nature. 2009 Sep 24;461(7263):546-9 PMID: 19734881
  77. Many roads to maturity: microRNA biogenesis pathways and their regulation.
    Nat Cell Biol. 2009 Mar;11(3):228-34 PMID: 19255566
  78. Human polynucleotide phosphorylase selectively and preferentially degrades microRNA-221 in human melanoma cells.
    Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11948-53 PMID: 20547861
  79. miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells.
    Nat Struct Mol Biol. 2009 May;16(5):492-8 PMID: 19377482
  80. Repression of the miR-17-92 cluster by p53 has an important function in hypoxia-induced apoptosis.
    EMBO J. 2009 Sep 16;28(18):2719-32 PMID: 19696742
  81. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas.
    Nat Rev Cancer. 2006 Dec;6(12):909-23 PMID: 17128209
  82. Down-regulation of the cyclin E1 oncogene expression by microRNA-16-1 induces cell cycle arrest in human cancer cells.
    BMB Rep. 2009 Nov 30;42(11):725-30 PMID: 19944013
  83. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses.
    Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12481-6 PMID: 16885212
Article Info
Journal
Trends in biochemical sciences
Abbr.
Trends Biochem Sci
ISSN
0968-0004
Published
2011-09-00
Epub
2011-00-07
Pages
478-84
Language
English
Region
England
NLM ID
7610674
PMCID
PMC3532742
Subset
IM
Grants
NCI NIH HHS · R01 CA136549 · United States
NCI NIH HHS · R01 CA136549-03 · United States
NCI NIH HHS · CA136549 · 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