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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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ResultA Primary Study on Down-Regulated miR-9-1 and Its Biological Significances in Methylmalonic Acidemia
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BackgroundMicroRNAs as potential biomarkers and therapeutic targets in age-related macular degeneration
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Inhibition of SIRT1 by microRNA-9, the key point in process of LPS-induced severe inflammation
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“Initially identified as brain-specific, miRNA-9 is a highly functional miRNA in brain development, which has been involved in the fine-tuning of nuclear factor Kappa-B- (NFκB-) dependent inflammatory response [35].”
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“On the other hand, expression of NF- itself in monocytes or neutrophils is regulated by several miRNAs, such as miR-9, whose expression is in its turn regulated by NF-, thus establishing a feedback loop that may control the degree of inflammation (Bazzoni et al., 2009).”
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Miguel, M. M. V., & Shaddox, L. (2024) · Pathogens · doi:10.3390/pathogens13070580 · Cited by 7
“…levels were previously found in inflamed gingival tissue from patients diagnosed with periodontitis [54] and also in neutrophils and monocytes post-TLR2-4 activation [57], and both miR155-5 and 147a have also been found elevated post-LPS stimulation, promoting further inflammatory cascade [58–60].”
BackgroundBollati, V., Monti, P., Biganzoli, D., Marano, G., Favero, C., Iodice, S., Ferrari, L., Dioni, L., Bianchi, F., Pesatori, A. C., et al. (2023) · Cancers · doi:10.3390/cancers15174317 · Cited by 7
“Moreover, miR-9-5p has been associated with the regulation of inflammatory processes [48,49]; given that obesity is characterized by chronic low-grade inflammation in adipose tissue [50], the dysregulation of miR-9-5p in obesity may contribute to adipose tissue inflammation and insulin resistance.”
BackgroundTavakoli, S., Gholami, M. H., Ghorban, K., Nojoumi, F., Faghihloo, E., Dadmanesh, M., & Rouzbahani, N. H. (2021) · Gene Reports · doi:10.1016/j.genrep.2021.101025 · Cited by 6
Mercy, C. S. A., Natarajaseenivasan, S. M., Velusamy, P., Bothammal, P., Sumaiya, K., Saranya, P., Langford, D., Shanmughapriya, S., & Natarajaseenivasan, K. (2020) · mSphere · doi:10.1128/msphere.00409-20 · Cited by 8
“Despite differences in cell type, both oligonucleotide-based microarray technology (21, 37, 38) and next-generation sequencing (NGS) technologies (23) indicated that the classic miRNAs hsa-mir-155, hsa-mir-9, and hsa-mir-146a are upregulated in LPS-treated monocytes, suggesting that these miRNAs are critical for promo…”
Micro-RNA Feedback Loops Modulating the Calcineurin/NFAT Signaling Pathway
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“In humans, miR-155 expression was shown to be associated with transcription factor NF-κB; however, in mice, miR-155 was shown to be activated via the NFAT pathway [81,82].”
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“Several miRNAs, including miR-155 [13], miR-125b [14], miR-21 [15], miR-146 [16], miR-9 [17], and miR-132 [18] have been identified to be involved in infectious diseases.”
BackgroundZhang, L., Long, K.-L., Wang, C.-X., Zhang, X., Yang, H.-J., Chen, J., Li, X., Gao, P.-Y., & Zhang, S. (2020) · Medicine · doi:10.1097/md.0000000000021066 · Cited by 6
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“[44] Six studies in this inclusion examined the relationship between miR-124 and infarct volume.”
Zhang, J., Zheng, K., Wu, Y., Zhang, S., Guo, A., & Sui, C. (2024) · Immunity Inflammation and Disease · doi:10.1002/iid3.1211 · Cited by 5
“18 These studies provide a theoretical basis for the understanding and intervention of innate immune ‐ related diseases.”
BackgroundLi, H.-Y., Lin, L., Chong, L., Gu, S., Wen, S.-H., Yu, G., Hu, X.-G., Dong, L., Zhang, H., & Li, C.-C. (2020) · Immunology and Cell Biology · doi:10.1111/imcb.12371 · Cited by 5
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“Intensity of staining was scored as strong, moderate, weak, and no for evaluation of IL-1β and TNF-α.”
BackgroundInfluentialPolarized Activation of Macrophages
Galdiero, M. R., Biswas, S. K., & Mantovani, A. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1311-4_2 · Cited by 4
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Khidr, E. G., El-Sayyad, G. S., Abulsoud, A. I., Rizk, N. I., Zaki, M. B., Raouf, A. A., Elrebehy, M. A., Hady, M. M. M. A., Elballal, M. S., Mohammed, O. A., et al. (2025) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.70156 · Cited by 5
“LPS also stimulates miR ‐ 9 in neutrophils and monocytes, which suppresses nuclear factor ‐ κ B1 transcript expression to adversely regulate inflammatory responses that are dependent on nuclear factor ‐ κ B [59].”
The role of microRNA in regulation of the body’s immune responses
Nizyaeva, N. V., Kulikova, G. V., Shchyogolev, A. I., & Zemskov, V. M. (2016) · Biology Bulletin Reviews · doi:10.1134/s2079086416060050 · Cited by 5
“MicroRNA-9 exhibits a pro-inflammatory effect, suppresses NFκB1, and ensures a constant level of protein NFκB1 expression in TLR4-mediated activation of monocytes and neutrophils (Bazzoni et al., 2009).”
BackgroundMacrophage Polarization in Metabolism and Metabolic Disease
Meiliana, A., & Wijaya, A. (2013) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v5i2.56 · Cited by 4
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How Noncoding RNAs Contribute to Macrophage Polarization
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Targeting the microbiota‐ miRNA ‐protease axis: A new therapeutic avenue in melanoma
Katsoulieris, E. N., Ioannou, P., & Afratis, N. A. (2026) · FEBS Journal · doi:10.1111/febs.70386 · Cited by 4
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“…an upregulation of miR-155 expression during L. major infection, providing valuable insights into the complex interplay between miR-155 and Leishmania infection, shedding light on the intricate mechanisms employed by the parasites to establish and maintain infection within the host [35–37].”
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“, miR9, miR132, miR-146a, miR-155 and miR-187, are well known to control TLR-receptor signaling in monocytes [27,50,51].”
BackgroundNuevos conocimientos en genética y enfermedad inflamatoria intestinal. ¿alguna utilidad práctica?
Iborra, M., Beltrán, B., & Nos, P. (2011) · Gastroenterología y Hepatología · doi:10.1016/j.gastrohep.2011.08.003 · Cited by 3
Circulating microRNAs in Inflammatory Bowel Diseases.
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Nuclear factor-κB1 expression levels in human gastric adenocarcinoma
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Hamad, R. S., Doghish, A. S., Mageed, S. S. A., Rizk, N. I., Mohammed, O. A., Alam-ElDein, K. M., Abuelhaded, K., Fahmy, H. A., Saad, H. A., Elhadad, G., et al. (2026) · IUBMB Life · doi:10.1002/iub.70117 · Cited by 2
“Together, our results demonstrate that miRNAs are active regulators of HPV-driven carcinogenic pathways rather than just passive indicators, enhancing their biological significance and potential therapeutic use [122].”
Microribonucleic acid-9 (miRNA-9) as a potential diagnostic marker in Behҫet’s syndrome patients
Saad, M. A., Gendy, H. I. E., Behiry, M. E., Shaker, O. G., & Laymouna, A. H. (2024) · The Egyptian Rheumatologist · doi:10.1016/j.ejr.2024.07.004 · Cited by 3
Differentiated expressed miRNAs in splenic monocyte induced by burn injury in mice
Liu, H., Li, L. G., Wang, M., Liu, D., Su, Q., & Zhang, Q. (2023) · International Wound Journal · doi:10.1111/iwj.14288 · Cited by 2
“7 macrophage and in human autologous monocytes both in the response to LPS, 26,27 miR-146a was downregulated by morphine, contributing to the development of tolerance to endotoxin by morphine.”
BackgroundmiR-9 Does Not Regulate Lamin A Expression in Metastatic Cells from Lung Adenocarcinoma
Guinde, J., Benoit, A., Frankel, D., Robert, S., Ostacolo, K., Lévy, N., Astoul, P., Roll, P., & Kaspi, É. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051599 · Cited by 2
“As metastatic pleural effusions often contain hematopoietic reactional cells (macrophages and neutrophils) highly expressing miR-9 [37,38], we analyzed miR-9 expression specifically on carcinoma cells to confirm these results.”
ResultThe epigenetic landscape of innate immunity
Luca, M. D., Pels, K., Moleirinho, S., & Curtale, G. (2017) · AIMS molecular science · doi:10.3934/molsci.2017.1.110 · Cited by 2
“Indeed, miR-155 and miR-9 promote the inflammatory signal by targeting negative regulators of inflammation, such as SOCS1 and NFκBp50 (p50), respectively [91,92].”
Zhao, Y.-G., Shi, B., Qian, Y., Bai, H., Xiao, L., & He, X.-Y. (2014) · Tumori · doi:10.1700/1778.19294 · Cited by 2
KATO, Y. O., Kusakabe, R., Inoue, K., & Tochinai, S. (2013) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.30.891 · Cited by 2
“The three miR-9 genes in humans, on chromosomes 1, 5, and 15, are separately transcribed from different promoters and regulate the expression of different genes (Bazzoni et al., 2009; Laneve et al., 2010; Hsu et al., 2009).”
BackgroundEndotoxin Tolerance as a Key Mechanism for Immunosuppression
Subhra, K., & Irina, N. (2012) · InTech eBooks · doi:10.5772/27368 · Cited by 3
“(p105/p50NF-κB) transcript thereby serving as a possible negative feedback mechanism on the inflammation (Bazzoni et al., 2009).”
BackgroundOxidative Stress-Mediated miRNA Regulation in Cancer
Datta, D., & Bhattacharyya, S. N. (2022) · Handbook of Oxidative Stress in Cancer: Therapeutic Aspects · doi:10.1007/978-981-16-1247-3_67-1
LPS Induces microRNAs -9, -192, and -205 Overexpression in Colorectal Cell Lines SW480, HCT116
Tavakolian, S., Goudarzi, H., & Faghihloo, E. (2020) · doi:10.30476/mejc.2019.81423.1001 · Cited by 2
MicroRNAs in Respiratory Diseases
Mondéjar‐Parreño, G., Callejo, M., Cogolludo, A. L., & Pérez‐Vizcaíno, F. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-814470-1.00004-6 · Cited by 5
MicroRNA Profiles of HPV-Associated Oropharyngeal Squamous Cell Carcinoma (OPSCC)
Miller, D. L., & Stack, M. S. (2015) · Springer eBooks · doi:10.1007/978-3-319-21100-8_6 · Cited by 1
Besta, S., Roupakia, E., Kanaki, Z., Vatsellas, G., Samuels, M., Foutadakis, S., Tokamani, M., Barbon, A., Sandaltzopoulos, R., Kanellis, D. C., et al. (2026) · Cell Death Discovery · doi:10.1038/s41420-026-03195-8 · Cited by 1
“Overall, these data identify a novel IKK α -regulated miRNA and demonstrate how miR-9-5p contributes to EMT and transcriptomic changes in lung cancer.”
The emergence of mRNA therapeutics: A new era in precision medicine
Sakat, S., Jyotishi, A., Ram, B. L., Kharche, A., Mutha, S. S., Chaudhari, V., Dhonde, S., & Dhage, S. S. (2025) · Journal of Applied Pharmaceutical Sciences · doi:10.7324/japs.2025.234438 · Cited by 1
“…for effective translation; the 5’ Untranslated Region, reading frame, coding for the viral antigen, i.e., the spike protein, to be translated into protein in host cells; the 3’ Untranslated Region, which ensures mRNA stability and protein production life of the mRNA by preventing degradation [5,6].”
The critical role of miRNA in bacterial zoonosis
Chen, S., Lei, Z., & Sun, T. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.113267
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“miR-9 was induced by LPS in human monocytes and neutrophils, and increased miR-9 acts as a feedback control of NF-κB dependent inflammatory response by inhibiting the expression of NFκB1 [51].”
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“PPARδ has been shown to drive transcriptional programming of M1 phenotype macrophages (35,40).”
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Tripp, R. A., & Bakre, A. A. (2017) · Current topics in microbiology and immunology · doi:10.1007/82_2017_32
MicroRNAs as Novel Biomarkers in IBD: Characterization and Current Status
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“Specific miRNAs such as miR-132, miR-146 and miR-155 can be regulated by inflammatory mediators (NF-κβ, TNF-α, IFN-β), microbial components (lipopolysaccharides and flagelin) and a variety of Toll-like receptors ligands (TLR), led to physiological granulocyte/ monocyte diffusion and growth during inflammation [29,30].”
BackgroundMicroRNAs in Normal and Malignant Myelopoiesis
Alemdehy, M. F., & Erkeland, S. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405544-5.00008-3
Role of MicroRNA in Macrophage Activation and Polarization
Curtale, G., & Locati, M. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1311-4_27 · Cited by 1
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Li, H., Yang, W., Liu, M.-W., Wan, L., & Wang, Y.-Q. (2022) · Brazilian Journal of Pharmaceutical Sciences · doi:10.1590/s2175-97902022e19791 · Cited by 1
microRNAs in Pregnancy: Implications for Basic Research and Clinical Management
Liu, M. R., Bian, X., Wang, H., & Wang, Y. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813570-9.00014-0
Exploiting MicroRNA (miRNA) Profiles for Diagnostics
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MicroRNA Regulation of Neutrophil Function
Cowland, J. B. (2014) · Springer eBooks · doi:10.1007/978-3-319-13689-9_3 · Cited by 2
“Stimulation of PMNs with LPS, IL-1β ,or TNF-α, all activators of NF-κB, but not IFN-γ or IFN-β, that do not induce NF-κB activity, caused a prominent increase of miR-9-1 [64].”
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Abraham, C., Vogel, S. N., & Perkins, D. J. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-415847-4.00030-6 · Cited by 2
Long Non-Coding RNA, Like NEAT1 and MALAT1, in Asthma: Mechanisms and Therapeutic Potential.
Poole, A., Laing, I., Mead-Hunter, R., Souëf, P. L., & Zhang, G. (2026) · Clinical and Experimental Allergy · doi:10.1111/cea.70427
Zheng, Z., Tian, R., Chen, Y., Li, Y., Pan, T., & Pan, T. (2026) · Journal of Translational Medicine · doi:10.1186/s12967-026-08626-9
“In human neutrophils and monocytes, LPS and other pro-inflammatory stimuli induce miR-9 through a MyD88-and NF-κB-dependent pathway; miR-9 then targets NFKB1 , forming a negative feedback loop that fine-tunes NF-κB-dependent responses [81].”
Zhou, J., Zhū, L., Wang, Y., Wu, Y., Yang, M., Xu, W., Ma, X., Qiu, C., Bian, X., Yi, F., et al. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1786162 · Cited by 1
Malikides, O., Sallo, A., Papazachariou, A., Kopidakis, I., Alifragki, A., Kontaraki, J., Fragkiadakis, K., Chlouverakis, G., Kallergis, E., Simantirakis, E., et al. (2026) · Genes · doi:10.3390/genes17010103
“MiR-9 suppresses key inflammatory pathways, including NF-κ B activation [40,41] and downstream cytokine release (TNF-α , IL-1 β , IL-6) [42].”
Jiang, Q., Zhang, H., Cai, Y., Meng, F., Wu, H., Liu, W., Zhang, F., Chen, H., Chen, Z., Shen, X., et al. (2025) · Cellular Oncology · doi:10.1007/s13402-025-01116-y
“Additionally, miR-9 and miR-21 are upregulated in various cells following TLR-NFκB signaling [28 –32 ].”
da Silva, I. I. F. G., Nascimento, D. D. Q., Barbosa, A. D., Souto, F. O., Maia, M. D. M. D., Crovella, S., de Souza, P. R. E., & Sandrin‐Garcia, P. (2024) · Genetics and Molecular Biology · doi:10.1590/1678-4685-gmb-2023-0235
Novel Mechanism of Lowering Blood Pressure by Electroacupuncture:MicroRNA9/P2RX7Preprint
Yue, B., Sun, J., Zhou, Z., Li, X., Liu, X., & Liu, Q. (2022) · Research Square · doi:10.21203/rs.3.rs-1266362/v1
Post-transcriptional regulation of miRNA biogenesis
Downie, A. (2019) · doi:10.7488/era/55
“Both pre-let-7a-1 and pre-miR-9 were able to pull down full length Lin28a as well as Lin28a with truncated C and N termini but containing both the CSD and the zinc fingers (24-190).”
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MicroRNA-9 represses sirtuin 1 (SIRT1) in human keratinocytes
Farrer, D., Jc, R., & Ross, K. (2016) · Liverpool John Moores University · doi:10.21276/sb.2016.2.9.2
“These mechanisms may be augmented by other pathways known to contribute to the expression of miR-9, such as Toll-like receptor, IL-1β and TNF-α signalling [24].”
Characterisation of novel therapies to mitigate inflammation in retinal degenerations
Saxena, K. (2015) · ANU Open Research (Australian National University) · doi:10.25911/5d78d614a6941
“MiR9 negatively regulates NF-κB-dependent inflammatory responses by suppressing expression of NFKB1 transcripts in LPS-stimulated neutrophils and monocytes [190].”
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“MiR-9 has also been shown to be a pro-inflammatory miRNA and is involved in modulating the nuclear factor Kappa-B (NF-κB)-dependent inflammatory response [39] .”
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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