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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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MicroRNA 9 Is a Regulator of Endothelial to Mesenchymal Transition in Diabetic Retinopathy
Wang, E., Feng, B., & Chakrabarti, S. (2023) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.64.7.13 · Cited by 18
“37,39,40 41–44 MiR-9 has been reported to regulate TGF-β signaling via regulation of the type II TGF-β receptor, 45,46 and NF-κ B-mediated inflammatory signaling via regulation of the NF-κ B subunit 1, 47–49 making it a molecule of interest with respect to EndMT.”
Li, H.-F., Wu, Y.-L., Tseng, T.-L., Chao, S.-W., Lin, H., & Chen, H.-H. (2020) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.00116.2020 · Cited by 18
miR-636: A Newly-Identified Actor for the Regulation of Pulmonary Inflammation in Cystic Fibrosis
Bardin, P., Foussignière, T., Rousselet, N., Rebeyrol, C., Porter, J. C., Corvol, H., & Tabary, O. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02643 · Cited by 18
“It has also been shown that TLR4-activated NF-κB rapidly increases the expression of miR-9 that fine-tunes NF-κBdependent responses (49).”
BackgroundMinhas, G., Mathur, D., Balakrishnan, R., Sharma, N. K., Paanu, V., & Anand, A. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00386 · Cited by 20
“Several other miRNAs such as miR-9, miR-21, and miR-147 are induced by TLR signaling and are expressed considerably and hence regulate immune responses in response to microbial invasion (Bazzoni et al., 2009; Liu et al., 2009; Sheedy et al., 2010).”
BackgroundToxicology study with microRNA
An, Y. R., & Hwang, S. Y. (2014) · Molecular & Cellular Toxicology · doi:10.1007/s13273-014-0014-y · Cited by 17
Non-coding RNAs in cardiac inflammation: key drivers in the pathophysiology of heart failure
Sansonetti, M., & Windt, L. J. D. (2021) · Cardiovascular Research · doi:10.1093/cvr/cvab192 · Cited by 17
Small Non-coding RNAs: Do They Encode Answers for Controlling SARS-CoV-2 in the Future?
Bhattacharyya, P., & Biswas, S. C. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.571553 · Cited by 17
“miR-9 is known to negatively regulate NFKB1, involved in the NF-kβ pathway (Bazzoni et al., 2009), and under stimulus and/or OC43 infection, expression of both miR-9 and NFKB1 increases.”
BackgroundImmunopathologic Processes in Sympathetic Ophthalmia as Signified by MicroRNA Profiling
Kaneko, Y., Wu, G. S., Saraswathy, S., Vasconcelos-Santos, D. V., & Rao, N. A. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-9465 · Cited by 18
“With the luciferase reporter assay, NFjB1 mRNA is also found to be directly regulated by hsa-miR-9 in human peripheral monocytes and polymorphonuclear neutrophils.(26) These results indicate that TNF-a and NFjB1 are validated targets of hsa-miR-9.”
BackgroundHost miRNA and immune cell interactions: relevance in nano-therapeutics for human health
Sharma, Y., Saini, A. K., Kashyap, S., Chandan, G., Kaur, N., Gupta, V. K., Thakur, V. K., Saini, V., & Saini, R. V. (2021) · Immunologic Research · doi:10.1007/s12026-021-09247-8 · Cited by 22
“Innate immune system response to macrophage infection comprises the upregulation of various miRNAs such as miR-9, miR-21, and miR147 [35, 45].”
BackgroundNon-coding RNA regulators of diabetic polyneuropathy
Meydan, C., Üçeyler, N., & Soreq, H. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135058 · Cited by 20
Garrido‐Mesa, J., Algieri, F., Rodríguez‐Nogales, A., Vezza, T., Utrilla, M. P., García, F., Chueca, N., Rodríguez‐Cabezas, M. E., Garrido‐Mesa, N., & Gálvez, J. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.07.044 · Cited by 17
He, J., He, Y., Chen, D.-W., Yu, B., Mao, X., Zheng, P., Yu, J., Huang, Z.-Q., & Luo, J.-Q. (2015) · Scientific Reports · doi:10.1038/srep12226 · Cited by 16
Williamson, V. S., Mamdani, M., McMichael, G. O., Kim, A. H., Lee, D., Bacanu, S., & Vladimirov, V. I. (2015) · Psychological Medicine · doi:10.1017/s0033291715000483 · Cited by 16
“relationship between the host and the miRNA gene and instances of FFLs involving these same miRNAs (Wilfred et al. 2007; Bazzoni et al. 2009; Lize et al. 2010; Fish et al. 2011).”
BackgroundXi, J. (2013) · Cancer treatment and research · doi:10.1007/978-3-642-31659-3_5 · Cited by 16
Shokati, E., & Safari, E. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110267 · Cited by 16
Intersections between innate immune response and gastric cancer development
Villarroel‐Espíndola, F., Ejsmentewicz, T., González‐Stegmaier, R., Jorquera, R., & Salinas, E. (2023) · World Journal of Gastroenterology · doi:10.3748/wjg.v29.i15.2222 · Cited by 15
Ülker, Ö. C., Panieri, E., Süzen, S., Jaganjac, M., Žarković, N., & Saso, L. (2021) · Journal of Pharmacy and Pharmacology · doi:10.1093/jpp/rgab045 · Cited by 16
Interactions between immune response to fungal infection and microRNAs: The pioneer tuners
Pakshir, K., Badali, H., Nami, S., Mirzaei, H., Ebrahimzadeh, V., & Morovati, H. (2019) · Mycoses · doi:10.1111/myc.13017 · Cited by 20
Zhao, Y., Zou, M., Sun, Y., Zhang, K., & Peng, X. (2019) · Veterinary Microbiology · doi:10.1016/j.vetmic.2019.108407 · Cited by 18
Ding, J., Guo, J., Wang, L., Chen, Y., Hu, B., Li, Y., Huang, R., Cao, J., Zhao, Y., Geiser, M., et al. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.9b00399 · Cited by 19
Shukla, S., Levine, C., Sripathi, R. P., Elson, G., Lutz, C. S., & Leibovich, S. J. (2018) · Mediators of Inflammation · doi:10.1155/2018/7852742 · Cited by 18
Popp, N. A., Yu, D., Green, B., Chew, E. Y., Ning, B., Chan, C., & Tuo, J. (2015) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21982 · Cited by 16
“…convincing evidence for miRNA involve- ment in inflammation, angiogenesis, and ocular disease, their role in AMD has not been explored to a great extent [Shen et al., 2008; Sonkoly et al., 2008; Bazzoni et al., 2009; Lin et al., 2011; Sabatel et al., 2011; Wang et al., 2012; Tuo et al., 2014].”
BackgroundMicroRNA Function in Mast Cell Biology: Protocols to Characterize and Modulate MicroRNA Expression
Maltby, S., Plank, M. W., Ptaschinski, C., Mattes, J., & Foster, P. S. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1568-2_18 · Cited by 11
Cui, X.-R., Bi, X., Zhang, X.-P., Zhang, Z.-P., Yan, Q., Wang, Y., Huang, X., Wu, X.-Q., Jing, X., & Wang, H.-W. (2024) · Immunity, Inflammation and Disease · doi:10.1002/iid3.1140 · Cited by 14
Nascimento, D. D. Q., da Silva, I. I. F. G., Lima, C., Cavalcanti, A. R. D. S., Roberti, L., Queiroz, R. G. D. P., Ferriani, V., Crovella, S., de Carvalho, L. D., & Sandrin-Garcia, P. (2022) · Autoimmunity · doi:10.1080/08916934.2022.2128781 · Cited by 14
“To emphasize the important role of miR-9 in the immune system and its correlation with target genes, Bazzoni et al [13] conducted a study on polymorphonuclear monocytes and neutrophils humans; the authors demonstrated that miR-9 is directly induced by lipopolysaccharides via the MyD88/NF-κB, being NF-κB a key regulato…”
BackgroundRaia, N. M. A., Shaker, O., Hassan, Z., & Elrahim, T. A. A. (2021) · Experimental Dermatology · doi:10.1111/exd.14487 · Cited by 14
Cordeiro, B., Jeon, P., Boukhaled, G. M., Corrado, M., Lapohos, O., Roy, D. G., Williams, K. S., Jones, R. G., Gruenheid, S., Sagan, S. M., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107585 · Cited by 13
MiR‐9 promotes multiple myeloma progression by regulating TRIM56/NF‐κB pathway
Huang, G.-Q., Liu, X.-P., Zhao, X.-Y., Zhao, J., Hao, J., Ren, J., & Chen, Y. (2019) · Cell Biology International · doi:10.1002/cbin.11104 · Cited by 14
“Moreover, overexpression of miR‐9 led to a reduced expression of the endogenous NF‐κB1/p105 protein by targeting NFKB1 in LPS‐induced monocytes and neutrophils (Bazzoni et al., 2009).”
Dai, M., Feng, M., Xie, T., & Zhang, X. (2019) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2019.103414 · Cited by 13
Limited differential expression of miRNAs and other small RNAs in LPS-stimulated human monocytes
Lu, D., Yamawaki, T., Zhou, H., Chou, W.-Y., Chhoa, M., Lamas, E., Escobar, S. M., Arnett, H. A., Ge, H., Juan, T., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0214296 · Cited by 13
“Bazzoni and colleagues also report that hsa-mir-99b, hsa-mir-125a and hsa-mir-187 are induced after 8 hours of LPS treatment[11], while our study finds that these miRNA genes are upregulated after 24 hours but not after 6 hours of LPS treatment.”
InfluentialAyyar, K. K., & Reddy, K. V. R. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.26665 · Cited by 15
Liu, K., Beck, D., Thoms, J. A. I., Liu, L., Zhao, W., Pimanda, J. E., & Zhou, X. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx280 · Cited by 14
Epigenetic Regulation of Innate Immunity by microRNAs
Boosani, C. S., & Agrawal, D. K. (2016) · Antibodies · doi:10.3390/antib5020008 · Cited by 13
“In PAMP-challenged monocytes, miRNAs, such as miR-9, miR-21, miR-132, miR-146, and miR-155, have been reported to regulate cellular homeostasis [1,9–15].”
BackgroundMicroRNAs Involved in Anti-Tumour Immunity
Yu, H., Sze, D., & Cho, W. C. S. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14035587 · Cited by 14
“In addition, LPS will regulate miR-9 expression via the myeloid differentiation primary response gene 88 through the NF-κB pathway in human macrophages and neutrophils [16].”
BackgroundLiu, T. C., Liu, Y., Wei, E.-X., & Fanghui, L. (2012) · International Journal of Photoenergy · doi:10.1155/2012/628649 · Cited by 25
“Inflammation involves a coordinated, sequential, and self-limiting sequence of events controlled by positive and negative regulatory mechanisms [20].”
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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