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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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The Interleukin 13 (IL-13) Pathway in Human Macrophages Is Modulated by MicroRNA-155 via Direct Targeting of Interleukin 13 Receptor {alpha}1 (IL13R{alpha}1).
R. T. Martinez-Nunez, F. Louafi, and T. Sanchez-Elsner (2011)
J. Biol. Chem. 286, 1786-1794
   Abstract »    Full Text »    PDF »
Up-regulation of MicroRNA-155 in Macrophages Contributes to Increased Tumor Necrosis Factor {alpha} (TNF{alpha}) Production via Increased mRNA Half-life in Alcoholic Liver Disease.
S. Bala, M. Marcos, K. Kodys, T. Csak, D. Catalano, P. Mandrekar, and G. Szabo (2011)
J. Biol. Chem. 286, 1436-1444
   Abstract »    Full Text »    PDF »
MicroRNA-155 Targets SMAD2 and Modulates the Response of Macrophages to Transforming Growth Factor-{beta}.
F. Louafi, R. T. Martinez-Nunez, and T. Sanchez-Elsner (2010)
J. Biol. Chem. 285, 41328-41336
   Abstract »    Full Text »    PDF »
miR-155 and its star-form partner miR-155* cooperatively regulate type I interferon production by human plasmacytoid dendritic cells.
H. Zhou, X. Huang, H. Cui, X. Luo, Y. Tang, S. Chen, L. Wu, and N. Shen (2010)
Blood 116, 5885-5894
   Abstract »    Full Text »    PDF »
MicroRNA-101 Targets MAPK Phosphatase-1 To Regulate the Activation of MAPKs in Macrophages.
Q.-Y. Zhu, Q. Liu, J.-X. Chen, K. Lan, and B.-X. Ge (2010)
J. Immunol. 185, 7435-7442
   Abstract »    Full Text »    PDF »
MicroRNA-148/152 Impair Innate Response and Antigen Presentation of TLR-Triggered Dendritic Cells by Targeting CaMKII{alpha}.
X. Liu, Z. Zhan, L. Xu, F. Ma, D. Li, Z. Guo, N. Li, and X. Cao (2010)
J. Immunol. 185, 7244-7251
   Abstract »    Full Text »    PDF »
Inducible microRNA-155 Feedback Promotes Type I IFN Signaling in Antiviral Innate Immunity by Targeting Suppressor of Cytokine Signaling 1.
P. Wang, J. Hou, L. Lin, C. Wang, X. Liu, D. Li, F. Ma, Z. Wang, and X. Cao (2010)
J. Immunol. 185, 6226-6233
   Abstract »    Full Text »    PDF »
Noncanonical cytoplasmic processing of viral microRNAs.
J. S. Shapiro, A. Varble, A. M. Pham, and B. R. tenOever (2010)
RNA 16, 2068-2074
   Abstract »    Full Text »    PDF »
Characterization of the Alpha Interferon-Induced Postentry Block to HIV-1 Infection in Primary Human Macrophages and T Cells.
C. Goujon and M. H. Malim (2010)
J. Virol. 84, 9254-9266
   Abstract »    Full Text »    PDF »
miRNA-based mechanism for the commitment of multipotent progenitors to a single cellular fate.
M. Mann, O. Barad, R. Agami, B. Geiger, and E. Hornstein (2010)
PNAS 107, 15804-15809
   Abstract »    Full Text »    PDF »
Circulating MicroRNAs As Potential Biomarkers of Coronary Artery Disease: A Promise to Be Fulfilled?.
R. Contu, M. V. G. Latronico, and G. Condorelli (2010)
Circ. Res. 107, 573-574
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Resveratrol decreases the levels of miR-155 by upregulating miR-663, a microRNA targeting JunB and JunD.
E. Tili, J.-J. Michaille, B. Adair, H. Alder, E. Limagne, C. Taccioli, M. Ferracin, D. Delmas, N. Latruffe, and C. M. Croce (2010)
Carcinogenesis 31, 1561-1566
   Abstract »    Full Text »    PDF »

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