Home LiteratureArticle Details
PMID: 19878981 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation.

Cell ·Vol. 139 ·No. 4 ·2009-11-13 ·Pages 693-706

Iliopoulos D, Hirsch HA, Struhl K

Abstract

Inflammation is linked clinically and epidemiologically to cancer, and NF-kappaB appears to play a causative role, but the mechanisms are poorly understood. We show that transient activation of Src oncoprotein can mediate an epigenetic switch from immortalized breast cells to a stably transformed line that forms self-renewing mammospheres that contain cancer stem cells. Src activation triggers an inflammatory response mediated by NF-kappaB that directly activates Lin28 transcription and rapidly reduces let-7 microRNA levels. Let-7 directly inhibits IL6 expression, resulting in higher levels of IL6 than achieved by NF-kappaB activation. IL6-mediated activation of the STAT3 transcription factor is necessary for transformation, and IL6 activates NF-kappaB, thereby completing a positive feedback loop. This regulatory circuit operates in other cancer cells lines, and its transcriptional signature is found in human cancer tissues. Thus, inflammation activates a positive feedback loop that maintains the epigenetic transformed state for many generations in the absence of the inducing signal.

MeSH Terms
Animals Cell Line Cell Line, Transformed Epigenesis, Genetic Feedback, Physiological Genes, src Humans Inflammation/metabolism Interleukin-6/metabolism Mice Mice, Nude MicroRNAs/metabolism NF-kappa B p50 Subunit/metabolism Neoplasm Transplantation RNA-Binding Proteins/metabolism Transplantation, Heterologous
Chemicals
Interleukin-6 Lin28A protein, human MicroRNAs NF-kappa B p50 Subunit NFKB1 protein, human RNA-Binding Proteins mirnlet7 microRNA, human
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Iliopoulos Dimitrios
Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA.
Hirsch Heather A
Struhl Kevin
References (42)
42 references, click to expand
  1. The epithelial-mesenchymal transition generates cells with properties of stem cells.
    Cell. 2008 May 16;133(4):704-15 PMID: 18485877
  2. An elaborate pathway required for Ras-mediated epigenetic silencing.
    Nature. 2007 Oct 25;449(7165):1073-7 PMID: 17960246
  3. 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
  4. Suppression of non-small cell lung tumor development by the let-7 microRNA family.
    Proc Natl Acad Sci U S A. 2008 Mar 11;105(10):3903-8 PMID: 18308936
  5. DNA methylation and gene silencing in cancer.
    Nat Clin Pract Oncol. 2005 Dec;2 Suppl 1:S4-11 PMID: 16341240
  6. Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis.
    Oncogene. 2002 Mar 27;21(13):2000-8 PMID: 11960372
  7. Rules for making human tumor cells.
    N Engl J Med. 2002 Nov 14;347(20):1593-603 PMID: 12432047
  8. Inflammation and cancer: back to Virchow?
    Lancet. 2001 Feb 17;357(9255):539-45 PMID: 11229684
  9. NF-kappaB and cancer-identifying targets and mechanisms.
    Curr Opin Genet Dev. 2008 Feb;18(1):19-26 PMID: 18440219
  10. Binding reactions: epigenetic switches, signal transduction and cancer.
    Curr Biol. 2009 Mar 24;19(6):R234-41 PMID: 19321137
  11. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties.
    Cancer Res. 2005 Jul 1;65(13):5506-11 PMID: 15994920
  12. Interleukin-6 is a potent growth factor for ER-alpha-positive human breast cancer.
    FASEB J. 2007 Nov;21(13):3763-70 PMID: 17586727
  13. Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients.
    J Clin Oncol. 2009 Jul 20;27(21):3437-44 PMID: 19470939
  14. Lin28 promotes transformation and is associated with advanced human malignancies.
    Nat Genet. 2009 Jul;41(7):843-8 PMID: 19483683
  15. Characterization of a subpopulation of colon cancer cells with stem cell-like properties.
    Int J Cancer. 2009 Mar 15;124(6):1312-21 PMID: 19072981
  16. STAT3 as a central mediator of neoplastic cellular transformation.
    Cancer Lett. 2007 Jun 28;251(2):199-210 PMID: 17129668
  17. Selective blockade of microRNA processing by Lin28.
    Science. 2008 Apr 4;320(5872):97-100 PMID: 18292307
  18. Src tyrosine kinases mediate activations of NF-kappaB and integrin signal during lipopolysaccharide-induced acute lung injury.
    J Immunol. 2007 Nov 15;179(10):7001-11 PMID: 17982091
  19. MicroRNAs and cancer: short RNAs go a long way.
    Cell. 2009 Feb 20;136(4):586-91 PMID: 19239879
  20. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation.
    Science. 2007 Mar 16;315(5818):1576-9 PMID: 17322030
  21. Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis.
    Cancer Cell. 2008 Aug 12;14(2):156-65 PMID: 18691550
  22. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis.
    Cancer Cell. 2009 Feb 3;15(2):91-102 PMID: 19185844
  23. IKK/NF-kappaB signaling: balancing life and death--a new approach to cancer therapy.
    J Clin Invest. 2005 Oct;115(10):2625-32 PMID: 16200195
  24. HLXB9 activates IL6 in Hodgkin lymphoma cell lines and is regulated by PI3K signalling involving E2F3.
    Leukemia. 2005 May;19(5):841-6 PMID: 15772702
  25. RAS is regulated by the let-7 microRNA family.
    Cell. 2005 Mar 11;120(5):635-47 PMID: 15766527
  26. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells.
    Breast Cancer Res. 2008;10(3):R52 PMID: 18541018
  27. Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells.
    Mol Cell. 2006 Nov 17;24(4):593-602 PMID: 17188034
  28. Cancer genes and the pathways they control.
    Nat Med. 2004 Aug;10(8):789-99 PMID: 15286780
  29. Interleukin-6 activates PI3K/Akt pathway and regulates cyclin A1 to promote prostate cancer cell survival.
    Int J Cancer. 2008 Apr 1;122(7):1521-9 PMID: 18027847
  30. Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA.
    Mol Cell. 2008 Oct 24;32(2):276-84 PMID: 18951094
  31. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10.
    Cancer Res. 1990 Sep 15;50(18):6075-86 PMID: 1975513
  32. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer.
    Cancer Cell. 2009 Feb 3;15(2):103-13 PMID: 19185845
  33. Enrichment of a population of mammary gland cells that form mammospheres and have in vivo repopulating activity.
    Cancer Res. 2007 Sep 1;67(17):8131-8 PMID: 17804725
  34. Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma.
    Cancer Cell. 2007 Feb;11(2):119-32 PMID: 17292824
  35. MicroRNA expression profiles classify human cancers.
    Nature. 2005 Jun 9;435(7043):834-8 PMID: 15944708
  36. MicroRNAs: target recognition and regulatory functions.
    Cell. 2009 Jan 23;136(2):215-33 PMID: 19167326
  37. MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells.
    Cancer Res. 2007 Oct 15;67(20):9762-70 PMID: 17942906
  38. Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis.
    Genes Dev. 2007 Jul 15;21(14):1714-9 PMID: 17639077
  39. Metformin selectively targets cancer stem cells, and acts together with chemotherapy to block tumor growth and prolong remission.
    Cancer Res. 2009 Oct 1;69(19):7507-11 PMID: 19752085
  40. Tumor necrosis factor-alpha activation of nuclear transcription factor-kappaB in marrow macrophages is mediated by c-Src tyrosine phosphorylation of Ikappa Balpha.
    J Biol Chem. 1998 Nov 6;273(45):29417-23 PMID: 9792645
  41. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells.
    Genes Dev. 2003 May 15;17(10):1253-70 PMID: 12756227
  42. Autocrine generation and requirement of BSF-2/IL-6 for human multiple myelomas.
    Nature. 1988 Mar 3;332(6159):83-5 PMID: 3258060
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
Published
2009-11-13
Epub
2009-00-29
Pages
693-706
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC2783826
Subset
IM
Grants
NCI NIH HHS · R01 CA107486 · United States
NCI NIH HHS · R01 CA107486-03 · United States
NCI NIH HHS · CA 107486 · United States
Corrections
CommentIn
CommentIn
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: [email protected]