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Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals
Open accessAbstract
Inflammation involves a coordinated, sequential, and self limiting sequence of events controlled by positive and negative regulatory mechanisms. Recent studies have shown that microRNAs (miRNAs), an evolutionarily conserved class of endogenous 22-nucleotide noncoding RNAs, contribute to the regulation of inflammation by repressing gene expression at the posttranscriptional level. In this study, we characterize the profile of miRNAs induced by LPS in human polymorphonuclear neutrophils (PMN) and monocytes. In particular, we identify miR-9 as the only miRNA (among 365 analyzed) up-regulated in both cell types after TLR4 activation. miR-9 is also induced by TLR2 and TLR7/8 agonists and by the proinflammatory cytokines TNF-alpha and IL-1beta, but not by IFNgamma. Among the 3 different genes encoding miR-9 precursors in humans, we show that LPS selectively induces the transcription of miR-9-1 located in the CROC4 locus, in a MyD88- and NF-kappaB-dependent manner. In PMN and monocytes, LPS regulates NFKB1 at both the transcriptional and posttranscriptional levels, and a conserved miR-9 seed sustained a miR-9-dependent inhibition of the NFKB1 transcript. Overall, these data suggest that TLR4-activated NF-kappaB rapidly increases the expression of miR-9 that operates a feedback control of the NF-kappaB-dependent responses by fine tuning the expression of a key member of the NF-kappaB family.
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“It was shown that NF-κB, upon its activation in response to LPS, initiates transcription of miR-9-1, which subsequently downregulates NF-κB [112].”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [112]
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BackgroundRegulation of mi RNA biogenesis and turnover in the immune system
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“Interestingly, miR-9 can directly repress the NF-jB1 transcript, suggesting that this miRNA may also mediate negative feedback to dampen or limit the duration of NF-jB activation (38).”
BackgroundMicroRNAs and Multiple Sclerosis
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“The increased expression of miR-9 during the first week of life was likely related to TLR4 activation in an NFKBdependent manner, operating in a negative feedback control by exerting close control on the expression of key members of the NFKB pathway (Bazzoni et al., 2009).”
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“Another study has indicated that miR-9 was induced by lipopolysaccharide (LPS) in a MyD88- and TLR4/NF-κB-dependent manner [157].”
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“In particular, rapid increases in miR-146a and miR-155 expression have been demonstrated in immune cells following activation of members of the TLR/IL-1R family [32-37].”
BackgroundInfluentialCritical role of miR-9 in myelopoiesis and EVI1-induced leukemogenesis
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“Less information is available on the role of miR-9 in other tissues, although it was detected in normal hepatocyte differentiation (8) and retina development (9) and has been implicated in the regulation of proinflammatory response (5, 10).”
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Sulindac inhibits tumor cell invasion by suppressing NF-κB-mediated transcription of microRNAs
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BackgroundMicroRNAs and Toll-like Receptor/Interleukin-1 Receptor Signaling
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“miR-9 has also been shown to be augmented by TLR/ IL-1 activity in monocytes and granulocytes [143,144].”
Oxidative stress in atherosclerosis: The role of microRNAs in arterial remodeling
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“A conserved miR-9 binding site on the NF-κB1 transcript and a miR-9dependent inhibition were identified.”
Studying micro RNA Function and Dysfunction in Alzheimer’s Disease
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“In multiple independent studies miRNA-9 has been associated with neurogenesis, morphogenesis, developmental patterning, brain cell proliferation, and glioblastoma (Sempere et al., 2004; Singh, 2007; Bazzoni et al., 2009; Hébert and De Strooper, 2009; Tsitsiou and Lindsay, 2009; Arora et al., 2010; Kutty et al., 2010a,…”
BackgroundmiRNA in Macrophage Development and Function
Roy, S. (2016) · Antioxidants and Redox Signaling · doi:10.1089/ars.2016.6728 · Cited by 88
“miR-9 has been linked with innate immune response; the expression of this miRNA contributes to a negative feedback loop in the NFjB pathway, where miR-9 is activated by TLR4/NFjB in human PMNs and monocytes target NFjB subunit p50 (6).”
BackgroundWang, L. Q., Kwong, Y., Kho, C. S., Wong, K. F., Wong, K. Y., Ferracin, M., Călin, G. A., & Chim, C. S. (2013) · Molecular Cancer · doi:10.1186/1476-4598-12-173 · Cited by 80
“In HEK-293 cells and ovarian cancer ES-2 cells, NFκB1 has been shown to be a direct target of miR-9 by luciferase assay [24,47].”
BackgroundMicroRNAs: Emerging Regulators of Immune‐Mediated Diseases
Tománková, T., Petřek, M., Gallo, J., & Kriegová, E. (2011) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.2011.02650.x · Cited by 82
Tuli, H. S., Kaur, J., Vashishth, K., Sak, K., Sharma, U., Choudhary, R., Behl, T., Singh, T., Sharma, S., Saini, A. K., et al. (2022) · Archives of Toxicology · doi:10.1007/s00204-022-03421-z · Cited by 91
Cross, D. L., Drury, R. E., Hill, J. W., & Pollard, A. J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01363 · Cited by 83
“Elevation of miR-9 expression during sepsis is not confirmed, however it should be noted that it is inducible by LPS and several pro-inflammatory cytokines (79), making a strong case for activity during sepsis.”
BackgroundRegulation of Vascular Smooth Muscle Cell Dysfunction Under Diabetic Conditions by miR-504
Reddy, M. A., Das, S., Chen, Z., Jin, W. L., Wang, M., Lanting, L. L., & Natarajan, R. D. (2016) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.115.306770 · Cited by 86
Sen, D., Chapla, A., Walter, N. M., Daniel, V., Srivastava, A., & Jayandharan, G. R. (2012) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.12101 · Cited by 79
Epigenetic targets for reversing immune defects caused by alcohol exposure
Curtis, B. J. (2013) · Alcohol research · doi:10.35946/arcr.v35.1.11 · Cited by 65
“Several of these upregulated miRNAs created a negative feedback loop to prevent excessive production of proinflammatory cytokines, therefore contributing to immune regulation and homeostasis (Bazzoni et al. 2009; Liu et al. 2009, 2010).”
Mirzaei, R., Mahdavi, F., Badrzadeh, F., Hosseini‐Fard, S. R., Heidary, M., Jeda, A. S., Mohammadi, T., Roshani, M., Yousefimashouf, R., Keyvani, H., et al. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.107204 · Cited by 83
“Studies showed that miR-9 is overexpressed upon TLR4 activation in human monocytes and neutrophils [44,45].”
Inflammatory cells and their non-coding RNAs as targets for treating myocardial infarction
Jung, M., Dodsworth, M., & Thum, T. (2018) · Basic Research in Cardiology · doi:10.1007/s00395-018-0712-z · Cited by 73
“Monocyte activation leads to an upregulation of miR-9, miR-9*, lnc-IL7R and THRIL, which suppress several genes that serve as regulators of the inflammatory response in immunity [12, 30].”
BackgroundThe emerging role of microRNA in regulation of endotoxin tolerance
Quinn, E. M., Wang, J., & Redmond, H. P. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.1111571 · Cited by 65
Regulation of Neutrophil Senescence by MicroRNAs
Ward, J. R., Heath, P. R., Catto, J. W. F., Whyte, M. K. B., Milo, M., & Renshaw, S. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015810 · Cited by 67
“Several other recent studies have also reported microRNA expression in human neutrophils using a variety of techniques [19,20,21,45].”
BackgroundInfluentialNoncoding RNAs regulate NF-κB signaling to modulate blood vessel inflammation
Cheng, H. S., Njock, M.-S., Khyzha, N., Dang, L. T., & Fish, J. E. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00422 · Cited by 69
“…PARTICIPATES IN NEGATIVE FEEDBACK REGULATION OF NF-κB ACTIVITY AND CONTRIBUTES TO THE CONTROL OF VASCULAR INFLAMMATION Several microRNAs are induced in response to inflammatory stimuli in human monocytes (Taganov et al., 2006; Bazzoni et al., 2009) and ECs (Suarez et al., 2010; Cheng et al., 2013).”
BackgroundTranscriptional Regulation during Aberrant Activation of NF-κB Signalling in Cancer
Deka, K., & Li, Y. (2023) · Cells · doi:10.3390/cells12050788 · Cited by 75
The gut microbiota metabolite urolithin A inhibits NF-κB activation in LPS stimulated BMDMs
Abdelazeem, K. N. M., Kalo, M. Z., Beer‐Hammer, S., & Lang, F. J. W. (2021) · Scientific Reports · doi:10.1038/s41598-021-86514-6 · Cited by 81
Gomez, G., Volinia, S., Croce, C., Zanca, C., Li, M., Emnett, R. J., Gutmann, D., Brennan, C. W., Furnari, F., & Cavenee, W. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2117 · Cited by 69
“The primer sequences used to amplify hsa-pri-miR-9-1, hsa-pri-miR-9-2, and hsa-pri-miR-9-3 were as described previously (25).”
BackgroundNetworks controlling mRNA decay in the immune system
Schott, J., & Stoecklin, G. (2010) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.13 · Cited by 64
Inflammatory Diseases and Growth: Effects on the GH–IGF Axis and on Growth Plate
Cirillo, F., Lazzeroni, P., Sartori, C., & Street, M. E. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18091878 · Cited by 72
Regulatory Role of IL-1R8 in Immunity and Disease
Molgora, M., Barajon, I., Mantovani, A., & Garlanda, C. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00149 · Cited by 79
Self-citationmiRNAs as potential therapeutic targets for age-related macular degeneration
Wang, S., Koster, K. M., He, Y., & Zhou, Q. (2012) · Future Medicinal Chemistry · doi:10.4155/fmc.11.176 · Cited by 67
Tay, H. L., Kaiko, G. E., Plank, M., Li, J., Maltby, S., Essilfie, A.-T., Jarnicki, A., Yang, M., Mattes, J., Hansbro, P. M., et al. (2015) · PLOS Pathogens · doi:10.1371/journal.ppat.1004549 · Cited by 67
“Key examples of miRNAs that are known to be activated by pathogen associated molecular patterns (PAMPs) include miR-9 [13], miR-146 [14] and miR-155 [14], which are important in regulating inflammatory pathways in macrophages and neutrophils by controlling TLR signaling.”
BackgroundDecoys and Regulatory “Receptors” of the IL-1/Toll-Like Receptor Superfamily
Garlanda, C., Riva, F., Bonavita, E., Gentile, S., & Mantovani, A. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00180 · Cited by 72
Self-citationThe role of mi RNA s in mast cells and other innate immune cells
Montagner, S., Orlandi, E. M., Merante, S., & Monticelli, S. (2013) · Immunological Reviews · doi:10.1111/imr.12042 · Cited by 60
“Activation of the innate immune response has been associated with changes in expression of a number of selected miRNAs, including miR-146 (48), miR-155 (49), miR-132 (48), and miR-9 (50).”
BackgroundInflammation linking EMT and cancer stem cells
Zhou, C., Liu, J., Tang, Y., & Liang, X. (2012) · Oral Oncology · doi:10.1016/j.oraloncology.2012.06.005 · Cited by 66
Role of miR-146a in regulation of the acute inflammatory response to monosodium urate crystals
Dalbeth, N., Pool, B., Shaw, O. M., Harper, J. L., Tan, P., Franklin, C., House, M. E., Cornish, J., & Naot, D. (2015) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2014-205409 · Cited by 59
MicroRNA-155 induction by Mycobacterium bovis BCG enhances ROS production through targeting SHIP1
Wang, J., Wu, M., Wen, J., Yang, K., Li, M., Zhan, X., Feng, L., Li, M., & Huang, X. (2014) · Molecular Immunology · doi:10.1016/j.molimm.2014.05.012 · Cited by 67
The Interplay of MicroRNAs in the Inflammatory Mechanisms Following Ischemic Stroke
Khoshnam, S. E., Winlow, W., & Farzaneh, M. (2017) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlx036 · Cited by 69
Liu, W.-L., Wang, X., Zheng, Y., Shang, G., Huang, J., Tao, J., & Chen, L.-D. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4745 · Cited by 63
“miR‐9 is also induced by the proinflammatory cytokines, TNF‐α and IL-1β (34).”
InfluentialPappalardo, D., Balaraman, S., Sathyan, P., Carter, E. S., Chen, W. A., & Miranda, R. C. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12139 · Cited by 72
“Such data, in conjunction with studies showing miR-9 is important for cell growth in mesoderm (Bazzoni et al., 2009) and endoderm (Plaisance et al., 2006), suggest this miRNA may broadly mediate ethanol effects during development.”
ResultRodríguez‐Otero, P., Román‐Gómez, J., Vilas‐Zornoza, A., José‐Eneriz, E. S., Martín‐Palanco, V., Rifón, J., Torres, A., Calasanz, M. J., Agirre, X., & Prósper, F. (2011) · British Journal of Haematology · doi:10.1111/j.1365-2141.2011.08812.x · Cited by 58
“Of the 13 miRNAs regulated by epigenetic mechanisms, the current study has focused on the MIR9 family because it has been implicated in physiological processes (neuronal development) and the pathogenesis of several cancer types (Lehmann et al, 2008; Packer et al, 2008; Bazzoni et al, 2009).”
BackgroundNF-κB and STAT3 signaling hubs for lung innate immunity
Quinton, L. J., & Mizgerd, J. P. (2011) · Cell and Tissue Research · doi:10.1007/s00441-010-1044-y · Cited by 65
“…of mir-146 (which targets TRAF6 ad IRAK-1 to tune TLR signaling; Taganov et al. 2006), of mir-9 (which targets Nfkb1 to diminish NFκB p50 and p105; Bazzoni et al. 2009), of mir-147 (which limits cytokine expression by as yet unknown means; Liu et al. 2009), of mir-21 (which targets PDCD4 to…”
BackgroundHuman Coronavirus OC43 Nucleocapsid Protein Binds MicroRNA 9 and Potentiates NF-κB Activation
Lai, F. W., Stephenson, K. B., Mahony, J. B., & Lichty, B. D. (2013) · Journal of Virology · doi:10.1128/jvi.02678-13 · Cited by 72
“Additionally, miR-9 expression is inducible by TNF- as well as by the TLR2 signaling pathways (26, 27).”
BackgroundMethodInfluentialWang, J., Gu, Z., Ni, P., Qiao, Y., Chen, C., Liu, X., Lin, J., Chen, N., & Fan, Q. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr302 · Cited by 59
“Although the presence of kB motif in pri-miR-9-1 promoter has been predicted by bioinformatics previously (36), we confirmed this possibility experimentally for the first time.”
BackgroundMeseguer, S., Martínez-Zamora, A., García‐Arumí, E., Andreu, A. L., & Armengod, M. ‐. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu427 · Cited by 63
Okada, Y., Hosoi, N., Matsuzaki, Y., Fukai, Y., Hiraga, A., Nakai, J., Nitta, K., Shinohara, Y., Konno, A., & Hirai, H. (2022) · Communications Biology · doi:10.1038/s42003-022-04200-3 · Cited by 58
Driedonks, T. A. P., van der Grein, S. G., Ariyürek, Y., Buermans, H. P. J., Jekel, H., Chow, F. W., Wauben, M. H. M., Buck, A. H., Hoen, P. A. C. ’., & Hoen, E. N. M. N. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2842-8 · Cited by 67
Transcriptional determination and functional specificity of myeloid cells: making sense of diversity
Monticelli, S., & Natoli, G. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2017.51 · Cited by 63
Adyshev, D. M., Elangovan, V. R., Moldobaeva, N., Mapes, B. L., Sun, X., & Garcia, J. G. N. (2013) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2013-0292oc · Cited by 61
Metadata
- Authors
- Bazzoni, F., Rossato, M., Fabbri, M., Gaudiosi, D., Mirolo, M., Mori, L., Tamassia, N., Mantovani, A., Cassatella, M. A., & Locati, M.
- Affiliations
- University of Verona (IT)
- Humanitas University (IT)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-03-31
- Volume
- 106
- Issue
- 13
- Pages
- 5282-5287
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2664036
- OpenAlex
- W2020932061
- Cited by
- 548
- References
- 40
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 17 · 2023: 14 · 2022: 18 · 2021: 25 · 2020: 33 · 2019: 33 · 2018: 38 · 2017: 38 · 2016: 35 · 2015: 36 · 2014: 46 · 2013: 65 · 2012: 50
- FWCI
- 19.41
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Fondazione Cariplo
- Associazione Italiana per la Ricerca sul Cancro
- Fondazione Cassa di Risparmio di Verona Vicenza Belluno e Ancona
- Università degli Studi di Verona
- Alleanza Contro il Cancro
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
- Keywords
- miR-9, microRNA, monocytes, neutrophils, lipopolysaccharide, TLR4, TLR2, TLR7/8, NF-κB, NFKB1, MyD88, post-transcriptional regulation, inflammation, TNF-α, IL-1β, feedback regulation
- MeSH terms
- Humans, Inflammation, Lipopolysaccharides, Monocytes, Neutrophils, Transcriptional Activation, Cytokines, NF-kappa B, Inflammation Mediators, Gene Expression Profiling, MicroRNAs, Toll-Like Receptors, Toll-Like Receptor 4
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