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PNAS 104 (5): 1604-1609

Copyright © 2007 by the National Academy of Sciences.

BIOLOGICAL SCIENCES / IMMUNOLOGY

MicroRNA-155 is induced during the macrophage inflammatory response

Ryan M. O'Connell*, Konstantin D. Taganov*, Mark P. Boldin*, Genhong Cheng{dagger}, and David Baltimore*,{ddagger}

*Department of Biology, California Institute of Technology, 330 Braun, 1200 East California Boulevard, Pasadena, CA 91125; and {dagger}Departments of Microbiology, Immunology, and Molecular Genetics, University of California, 650 Charles East Young Drive South, Los Angeles, CA 90095

Contributed by David Baltimore, December 4, 2006

Received for publication November 10, 2006.

Abstract: The mammalian inflammatory response to infection involves the induction of several hundred genes, a process that must be carefully regulated to achieve pathogen clearance and prevent the consequences of unregulated expression, such as cancer. Recently, microRNAs (miRNAs) have emerged as a class of gene expression regulators that has also been linked to cancer. However, the relationship between inflammation, innate immunity, and miRNA expression is just beginning to be explored. In the present study, we use microarray technology to identify miRNAs induced in primary murine macrophages after exposure to polyriboinosinic:polyribocytidylic acid or the cytokine IFN-beta. miR-155 was the only miRNA of those tested that was substantially up-regulated by both stimuli. It also was induced by several Toll-like receptor ligands through myeloid differentiation factor 88- or TRIF-dependent pathways, whereas up-regulation by IFNs was shown to involve TNF-{alpha} autocrine signaling. Pharmacological inhibition of the kinase JNK blocked induction of miR-155 in response to either polyriboinosinic:polyribocytidylic acid or TNF-{alpha}, suggesting that miR-155-inducing signals use the JNK pathway. Together, these findings characterize miR-155 as a common target of a broad range of inflammatory mediators. Importantly, because miR-155 is known to function as an oncogene, these observations identify a potential link between inflammation and cancer.

Key Words: cancer • inflammation • innate immunity • cytokines

Freely available online through the PNAS open access option.

Author contributions: R.M.O. and K.D.T. designed research; R.M.O. and K.D.T. performed research; R.M.O., M.P.B., G.C., and D.B. contributed new reagents/analytic tools; R.M.O., K.D.T., M.P.B., G.C., and D.B. analyzed data; and R.M.O. and D.B. wrote the paper.

The authors declare no conflict of interest.

This article contains supporting information online at www.pnas.org/cgi/content/full/0610731104/DC1.

{ddagger}To whom correspondence should be addressed. E-mail: baltimo{at}caltech.edu

© 2007 by The National Academy of Sciences of the USA

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IL-10 Inhibits miR-155 Induction by Toll-like Receptors.
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J. Biol. Chem. 285, 20492-20498
   Abstract »    Full Text »    PDF »
CCL8/MCP-2 is a target for mir-146a in HIV-1-infected human microglial cells.
S. Rom, I. Rom, G. Passiatore, M. Pacifici, S. Radhakrishnan, L. Del Valle, S. Pina-Oviedo, K. Khalili, D. Eletto, and F. Peruzzi (2010)
FASEB J 24, 2292-2300
   Abstract »    Full Text »    PDF »
MicroRNA-98 and let-7 Regulate Expression of Suppressor of Cytokine Signaling 4 in Biliary Epithelial Cells in Response to Cryptosporidium parvum Infection.
G. Hu, R. Zhou, J. Liu, A.-Y. Gong, and X.-M. Chen (2010)
The Journal of Infectious Disease 202, 125-135
   Abstract »    Full Text »    PDF »
MicroRNA-155 Regulates Cell Survival, Growth, and Chemosensitivity by Targeting FOXO3a in Breast Cancer.
W. Kong, L. He, M. Coppola, J. Guo, N. N. Esposito, D. Coppola, and J. Q. Cheng (2010)
J. Biol. Chem. 285, 17869-17879
   Abstract »    Full Text »    PDF »
Binding of NF-kappaB p65 subunit to the promoter elements is involved in LPS-induced transactivation of miRNA genes in human biliary epithelial cells.
R. Zhou, G. Hu, A.-Y. Gong, and X.-M. Chen (2010)
Nucleic Acids Res. 38, 3222-3232
   Abstract »    Full Text »    PDF »
Small RNAs Guide Hematopoietic Cell Differentiation and Function.
F. Navarro and J. Lieberman (2010)
J. Immunol. 184, 5939-5947
   Abstract »    Full Text »    PDF »
MicroRNA-155 Functions as an OncomiR in Breast Cancer by Targeting the Suppressor of Cytokine Signaling 1 Gene.
S. Jiang, H. W. Zhang, M. H. Lu, X. H. He, Y. Li, H. Gu, M. F. Liu, and E. D. Wang (2010)
Cancer Res. 70, 3119-3127
   Abstract »    Full Text »    PDF »
Translation Control: A Multifaceted Regulator of Inflammatory Response.
B. Mazumder, X. Li, and S. Barik (2010)
J. Immunol. 184, 3311-3319
   Abstract »    Full Text »    PDF »
MicroRNAs: a complex regulatory network drives the acquisition of malignant cell phenotype.
L. Santarpia, M. Nicoloso, and G. A Calin (2010)
Endocr. Relat. Cancer 17, F51-F75
   Abstract »    Full Text »    PDF »
Development of Monocytes, Macrophages, and Dendritic Cells.
F. Geissmann, M. G. Manz, S. Jung, M. H. Sieweke, M. Merad, and K. Ley (2010)
Science 327, 656-661
   Abstract »    Full Text »    PDF »
Post-transcriptional regulation of miR-27 in murine cytomegalovirus infection.
A. H. Buck, J. Perot, M. A. Chisholm, D. S. Kumar, L. Tuddenham, V. Cognat, L. Marcinowski, L. Dolken, and S. Pfeffer (2010)
RNA 16, 307-315
   Abstract »    Full Text »    PDF »

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