Identifying Functional MicroRNAs in Macrophages with Polarized Phenotypes
Open accessAbstract
Macrophages respond to external stimuli with rapid changes in expression of many genes. Different combinations of external stimuli lead to distinct polarized activation patterns, resulting in a spectrum of possible macrophage activation phenotypes. MicroRNAs (miRNAs) are small, noncoding RNAs that can repress the expression of many target genes. We hypothesized that miRNAs play a role in macrophage polarization. miRNA expression profiles were determined in monocyte-derived macrophages (MDMs) incubated in conditions causing activation toward M1, M2a, M2b, or M2c phenotypes. One miRNA guide strand and seven miRNA passenger strands were significantly altered. Changes were confirmed in MDMs from six separate donors. The amplitude of miRNA expression changes in MDMs was smaller than described studies of monocytes responding to inflammatory stimuli. Further investigation revealed this correlated with higher basal miRNA expression in MDMs compared with monocytes. The regulation of M1- and M2b-responsive miRNAs (miR-27a, miR-29b, miR-125a, miR-146a, miR-155, and miR-222) was similar in differentiated THP-1 cells and primary MDMs. Studies in this model revealed cross-talk between IFNγ- and LPS-associated pathways regulating miRNA expression. Furthermore, expression of M1-associated transcripts was increased in THP-1 cells transfected with mimics of miR-29b, miR-125a-5p, or miR-155. The apparent inflammatory property of miR-29b and miR-125a-5p can be at least partially explained by repression of TNFAIP3, a negative regulator of NF-κB signaling. Overall, these data suggest miRNAs can contribute to changes in macrophage gene expression that occur in different exogenous activating conditions. Macrophages respond to external stimuli with rapid changes in expression of many genes. Different combinations of external stimuli lead to distinct polarized activation patterns, resulting in a spectrum of possible macrophage activation phenotypes. MicroRNAs (miRNAs) are small, noncoding RNAs that can repress the expression of many target genes. We hypothesized that miRNAs play a role in macrophage polarization. miRNA expression profiles were determined in monocyte-derived macrophages (MDMs) incubated in conditions causing activation toward M1, M2a, M2b, or M2c phenotypes. One miRNA guide strand and seven miRNA passenger strands were significantly altered. Changes were confirmed in MDMs from six separate donors. The amplitude of miRNA expression changes in MDMs was smaller than described studies of monocytes responding to inflammatory stimuli. Further investigation revealed this correlated with higher basal miRNA expression in MDMs compared with monocytes. The regulation of M1- and M2b-responsive miRNAs (miR-27a, miR-29b, miR-125a, miR-146a, miR-155, and miR-222) was similar in differentiated THP-1 cells and primary MDMs. Studies in this model revealed cross-talk between IFNγ- and LPS-associated pathways regulating miRNA expression. Furthermore, expression of M1-associated transcripts was increased in THP-1 cells transfected with mimics of miR-29b, miR-125a-5p, or miR-155. The apparent inflammatory property of miR-29b and miR-125a-5p can be at least partially explained by repression of TNFAIP3, a negative regulator of NF-κB signaling. Overall, these data suggest miRNAs can contribute to changes in macrophage gene expression that occur in different exogenous activating conditions.
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Graff et al. found increases of miR-125a-3p, miR-155-5p, miR-155-3p in M1, miR-193b in M2a, miR-27a-5p, miR-155-5p, miR-155-3p in M2b and decreases of miR-26a-2-3p and miR-29b-1-5p in both M1 and M2a.
“They noticed increases of miR-125a-3p, miR-155-5p, miR-155-3p in M1, miR-193b in M2a, miR-27a-5p, miR-155-5p, miR-155-3p in M2b and decreases of miR-26a-2-3p, and miR-29b-1-5p in both M1 and M2a.”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [195]
The Results report increased miR-125a-3p in M1, miR-193b in M2a, and miR-27a* in M2b; they also report miR-155* induction in M1 and M2b. But the Results place co-regulation of miR-26a-2* and miR-29b-1* in M1 and M2b, not M1 and M2a as claimed. The paper also cautions that most corresponding guide-strand changes in macrophages did not reach statistical significance. (LLM, conf=0.88)
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Cites
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714 · see citing works
Exploring the full spectrum of macrophage activation
Mosser, D. M., & Edwards, J. P. (2008) · Nature Reviews Immunology · doi:10.1038/nri2448 · Cited by 9,144 · see citing works
Most mammalian mRNAs are conserved targets of microRNAs
Friedman, R. C., Farh, K. K.-H., Burge, C. B., & Bartel, D. P. (2009) · Genome Research · doi:10.1101/gr.082701.108 · Cited by 8,462 · see citing works
The chemokine system in diverse forms of macrophage activation and polarization
MANTOVANI, A., SICA, A., SOZZANI, S., ALLAVENA, P., VECCHI, A., & LOCATI, M. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.09.015 · Cited by 6,534 · see citing works
Taganov, K. D., Boldin, M. P., Chang, K.-J., & Baltimore, D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605298103 · Cited by 4,317 · see citing works
The impact of microRNAs on protein output
Baek, D., Villén, J., Shin, C., Camargo, F. D., Gygi, S. P., & Bartel, D. P. (2008) · Nature · doi:10.1038/nature07242 · Cited by 3,592 · see citing works
Widespread changes in protein synthesis induced by microRNAs
Selbach, M., Schwanhäusser, B., Thierfelder, N., Fang, Z., Khanin, R., & Rajewsky, N. (2008) · Nature · doi:10.1038/nature07228 · Cited by 3,429 · cited 1× · see citing works
“Indeed, there is evidence that some evolutionarily conserved miRNAs target hundreds of transcripts (8, 9).”
BackgroundMacrophage activation and polarization
Martinez, F. O. (2008) · Frontiers in Bioscience · doi:10.2741/2692 · Cited by 3,160 · see citing works
Functional siRNAs and miRNAs exhibit strand bias
Khvorova, A., Reynolds, A., & Jayasena, S. D. (2003) · Cell · doi:10.1016/s0092-8674(03)00801-8 · Cited by 2,645 · see citing works
Griffiths-Jones, S. (2004) · Nucleic Acids Res. · doi:10.1093/nar/gkh023 · Cited by 2,446 · see citing works
Martínez, F. O., Gordon, S., Locati, M., & Mantovani, A. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.10.7303 · Cited by 2,336 · see citing works
Asymmetry in the Assembly of the RNAi Enzyme Complex
Schwarz, D. S., Hutvágner, G., Du, T., Xu, Z., Aronin, N., & Zamore, P. D. (2003) · Cell · doi:10.1016/s0092-8674(03)00759-1 · Cited by 2,323 · see citing works
Stein, M., Keshav, S., Harris, N., & Gordon, S. (1992) · The Journal of experimental medicine · doi:10.1084/jem.176.1.287 · Cited by 1,960 · see citing works
The many faces of macrophage activation
Mosser, D. M. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0602325 · Cited by 1,902 · see citing works
MicroRNA-155 is induced during the macrophage inflammatory response
O'Connell, R. M., Taganov, K. D., Boldin, M. P., Cheng, G., & Baltimore, D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610731104 · Cited by 1,866 · see citing works
Tili, E., Michaille, J.-J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., Fabbri, M., Alder, H., Liu, C. G., Calin, G. A., et al. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.8.5082 · Cited by 1,304 · see citing works
Biochemical and functional characterization of three activated macrophage populations
Edwards, J. P., Zhang, X., Frauwirth, K. A., & Mosser, D. M. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0406249 · Cited by 863 · see citing works
THE IMMUNOLOGICAL BASIS OF ACQUIRED CELLULAR RESISTANCE
Mackaness, G. B. (1964) · The Journal of Experimental Medicine · doi:10.1084/jem.120.1.105 · Cited by 806 · see citing works
Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester.
Tsuchiya, S., Kobayashi, Y., Goto, Y., Okumura, H., Nakae, S., Konno, T., & Tada, K. (1982) · PubMed · Cited by 803 · see citing works
MicroRNA functions in stress responses
Leung, A. K. L., & Sharp, P. A. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.027 · Cited by 765 · see citing works
Tang, Y., Luo, X., Cui, H., Xu-ming, N., Yuan, M., Guo, Y., Huang, X., Zhou, H., de Vries, N., Tak, P. P., et al. (2009) · Arthritis & Rheumatism · doi:10.1002/art.24436 · Cited by 735 · see citing works
The Kinase Akt1 Controls Macrophage Response to Lipopolysaccharide by Regulating MicroRNAs
Androulidaki, A., Iliopoulos, D., Arranz, A., Doxaki, C., Schworer, S., Zacharioudaki, V., Margioris, A. N., Tsichlis, P. N., & Tsatsanis, C. (2009) · Immunity · doi:10.1016/j.immuni.2009.06.024 · Cited by 581 · see citing works
Bazzoni, F., Rossato, M., Fabbri, M., Gaudiosi, D., Mirolo, M., Mori, L., Tamassia, N., Mantovani, A., Cassatella, M. A., & Locati, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810909106 · Cited by 548 · see citing works
Okamura, K., Phillips, M. D., Tyler, D. M., Duan, H., Chou, Y.-T., & Lai, E. C. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1409 · Cited by 461 · see citing works
Liu, G., Friggeri, A., Yang, Y., Park, Y.-J., Tsuruta, Y., & Abraham, E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901216106 · Cited by 438 · see citing works
Artificial MicroRNAs as siRNA Shuttles: Improved Safety as Compared to shRNAs In vitro and In vivo
Boudreau, R. L., Martins, I., & Davidson, B. L. (2008) · Molecular Therapy · doi:10.1038/mt.2008.231 · Cited by 359 · see citing works
A novel phenotype for an activated macrophage: the type 2 activated macrophage
Anderson, C. F., & Mosser, D. M. (2002) · Journal of Leukocyte Biology · doi:10.1189/jlb.72.1.101 · Cited by 334 · see citing works
Reversal of Proinflammatory Responses by Ligating the Macrophage Fcγ Receptor Type I
Sutterwala, F. S., Noel, G. J., Salgame, P. R., & Mosser, D. M. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.1.217 · Cited by 327 · see citing works
Regulation of MicroRNA Expression and Abundance during Lymphopoiesis
Kuchen, S., Resch, W., Yamane, A., Kuo, N., Li, Z., Chakraborty, T., Wei, L., Laurence, A. D. J., Yasuda, T., Peng, S., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.05.009 · Cited by 324 · see citing works
Schulte, L. N., Eulalio, A., Mollenkopf, H., Reinhardt, R., & Vogel, J. (2011) · EMBO Journal · doi:10.1038/emboj.2011.94 · Cited by 316 · see citing works
Chen, T., Huang, Z., Wang, L., Wang, Y., Wu, F., Meng, S., & Wang, C. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp121 · Cited by 297 · see citing works
Forrest, A., Kanamori-Katayama, M., Tomaru, Y., Lassmann, T., Ninomiya, N., Takahashi, Y., de Hoon, M. D., Kubosaki, A., Ai, K.-H., Suzuki, M., et al. (2010) · Leukemia · doi:10.1038/leu.2009.246 · Cited by 270 · see citing works
Ruggiero, T., Trabucchi, M., Santa, F. D., Zupo, S., Harfe, B. D., McManus, M. T., Rosenfeld, M. G., Briata, P., & Gherzi, R. (2009) · The FASEB Journal · doi:10.1096/fj.09-131342 · Cited by 203 · see citing works
Activation of TGF-β by Leishmania chagasi : Importance for Parasite Survival in Macrophages
Gantt, K. R., Schultz‐Cherry, S., Rodríguez, N. E., Jerônimo, S. M. B., Nascimento, E. T., Goldman, T. L., Recker, T. J., Miller, M. A., & Wilson, M. E. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.5.2613 · Cited by 171 · see citing works
Self-citationMinimizing variables among hairpin-based RNAi vectors reveals the potency of shRNAs
Boudreau, R. L., Mas, A., & Davidson, B. L. (2008) · RNA · doi:10.1261/rna.1062908 · Cited by 165 · see citing works
Tserel, L., Runnel, T., Kisand, K., Pihlap, M., Bakhoff, L., Kolde, R., Peterson, H., Vilo, J., Peterson, P., & Rebane, A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.213561 · Cited by 136 · see citing works
Regulation of miRNA Transcription in Macrophages in Response to Candida albicans
Monk, C. E., Hutvágner, G., & Arthur, J. S. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013669 · Cited by 126 · see citing works
Absence of DICER in Monocytes and Its Regulation by HIV-1
Coley, W., Duyne, R. V., Carpio, L., Guendel, I., Kehn‐Hall, K., Chevalier, S. A., Narayanan, A., Luu, T. V., Lee, N., Klase, Z. A., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.101709 · Cited by 88 · see citing works
Chen, A., Luo, M., Yuan, G., Yu, J., Deng, T., Zhang, L., Zhou, Y., Mitchelson, K. R., & Cheng, J. (2008) · Biotechnology Letters · doi:10.1007/s10529-008-9800-8 · Cited by 45 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The M1 and M2 paradigm of macrophage activation: Time for reassessment
Martinez, F. O., & Gordon, S. (2014) · F1000Prime Reports · doi:10.12703/p6-13 · Cited by 4,689 · see citing works
Molecular Mechanisms That Influence the Macrophage M1–M2 Polarization Balance
Wang, N., Liang, H., & Zen, K. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00614 · Cited by 1,997 · see citing works
Microglial and macrophage polarization—new prospects for brain repair
Hu, X., Leak, R. K., Shi, Y., Suenaga, J., Gao, Y., Zheng, P., & Chen, J. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.207 · Cited by 1,456 · see citing works
Akt Signaling Pathway in Macrophage Activation and M1/M2 Polarization
Vergadi, E., Ieronymaki, E., Lyroni, K., Vaporidi, K., & Tsatsanis, C. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601515 · Cited by 1,148 · see citing works
M2b macrophage polarization and its roles in diseases
Wang, L., Zhang, S.-X., Wu, H., Rong, X., & Guo, J. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.3ru1018-378rr · Cited by 889 · see citing works
Functions and mechanisms of microglia/macrophages in neuroinflammation and neurogenesis after stroke
Xiong, X., Liu, L., & Yang, Q. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.05.001 · Cited by 703 · see citing works
Macrophage phenotypes in atherosclerosis
Colin, S., Chinetti‐Gbaguidi, G., & Staels, B. (2014) · Immunological Reviews · doi:10.1111/imr.12218 · Cited by 657 · see citing works
Dixon, L. J., Barnes, M., Tang, H., Pritchard, M. T., & Nagy, L. E. (2013) · Comprehensive Physiology · doi:10.1002/cphy.c120026 · Cited by 628 · see citing works
Essandoh, K., Li, Y., Huo, J., & Fan, G. (2016) · Shock · doi:10.1097/shk.0000000000000604 · Cited by 603 · see citing works
A20: linking a complex regulator of ubiquitylation to immunity and human disease
Ma, A. I., & Malynn, B. A. (2012) · Nature reviews. Immunology · doi:10.1038/nri3313 · Cited by 550 · see citing works
MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages
Nazari-Jahantigh, M., Wei, Y., Noels, H., Akhtar, S., Zhou, Z., Koenen, R. R., Heyll, K., Gremse, F., Kiessling, F. M., Grommes, J., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci61716 · Cited by 529 · see citing works
Macrophage Polarization in Chronic Inflammatory Diseases: Killers or Builders?
Parisi, L., Gini, E., Baci, D., Tremolati, M., Fanuli, M., Bassani, B., Farronato, G., Bruno, A., & Mortara, L. (2018) · Journal of Immunology Research · doi:10.1155/2018/8917804 · Cited by 508 · see citing works
Turning 21: Induction of miR-21 as a Key Switch in the Inflammatory Response
Sheedy, F. J. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00019 · Cited by 496 · see citing works
Macrophages and the Recovery from Acute and Chronic Inflammation
Hamidzadeh, K., Christensen, S. M., Dalby, E., Chandrasekaran, P., & Mosser, D. M. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034348 · Cited by 439 · see citing works
Macrophage polarization and allergic asthma
Saradna, A., Do, D. C., Kumar, S. A., Fu, Q.-L., & Gao, P. (2017) · Translational research · doi:10.1016/j.trsl.2017.09.002 · Cited by 428 · see citing works
Macrophage Activation and Polarization as an Adaptive Component of Innate Immunity
Locati, M., Mantovani, A., & Sica, A. (2013) · Advances in immunology · doi:10.1016/b978-0-12-417028-5.00006-5 · Cited by 405 · see citing works
Molecular and epigenetic basis of macrophage polarized activation
Porta, C., Riboldi, E., Ippolito, A., & Sica, A. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2015.10.003 · Cited by 319 · see citing works
MicroRNA let-7c Regulates Macrophage Polarization
Banerjee, S., Xie, N., Cui, H., Tan, Z., Yang, S., Icyuz, M., Abraham, E., & Liu, G. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202496 · Cited by 320 · see citing works
Tumor-Associated Macrophages as a Paradigm of Macrophage Plasticity, Diversity, and Polarization
Mantovani, A., & Locati, M. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.113.300168 · Cited by 291 · see citing works
Malyshev, I. Y., & Malyshev, Y. (2015) · BioMed Research International · doi:10.1155/2015/341308 · Cited by 276 · see citing works
Tiedt, S., Prestel, M., Malik, R., Schieferdecker, N., Duering, M., Kautzky, V., Stoycheva, I., Böck, J., Northoff, B. H., Klein, M., et al. (2017) · Circulation Research · doi:10.1161/circresaha.117.311572 · Cited by 274 · see citing works
Njock, M., Cheng, H. S., Dang, L. T. H., Nazari-Jahantigh, M., Lau, A. C., Boudreau, É., Roufaiel, M., Cybulsky, M. I., Schober, A., & Fish, J. E. (2015) · Blood · doi:10.1182/blood-2014-11-611046 · Cited by 270 · see citing works
miR-146 and miR-155: Two Key Modulators of Immune Response and Tumor Development
Testa, U., Pelosi, E., Castelli, G., & Labbaye, C. (2017) · Non-Coding RNA · doi:10.3390/ncrna3030022 · Cited by 270 · see citing works
Parayath, N. N., Parikh, A. B., & Amiji, M. M. (2018) · Nano Letters · doi:10.1021/acs.nanolett.8b00689 · Cited by 263 · see citing works
Baer, C., Squadrito, M. L., Laoui, D., Thompson, D., Hansen, S. K., Kiialainen, A., Hoves, S., Ries, C. H., Ooi, C.-H., & De Palma, M. (2016) · Nature Cell Biology · doi:10.1038/ncb3371 · Cited by 259 · see citing works
Functional polarization of neuroglia: Implications in neuroinflammation and neurological disorders
Jha, M. K., Lee, W., & Suk, K. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.11.003 · Cited by 260 · see citing works
miR-125a-5p Regulates Differential Activation of Macrophages and Inflammation
Banerjee, S., Cui, H., Xie, N., Tan, Z., Yang, S., Icyuz, M., Thannickal, V. J., Abraham, E., & Liu, G. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.426866 · Cited by 258 · see citing works
MicroRNAs in Immune Response and Macrophage Polarization
Liu, G., & Abraham, E. H. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.112.300068 · Cited by 243 · see citing works
Saha, B., Momen-Heravi, F., Kodys, K., & Szabo, G. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.694133 · Cited by 229 · see citing works
Macrophage Polarization in Leishmaniasis: Broadening Horizons
Tomiotto‐Pellissier, F., Bortoleti, B. T. D. S., Assolini, J. P., Gonçalves, M. D., Carloto, A. C. M., Miranda-Sapla, M. M., Costa, I. C., Bordignon, J., & Pavanelli, W. R. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02529 · Cited by 225 · see citing works
miR‐155 as a multiple sclerosis–relevant regulator of myeloid cell polarization
Moore, C. S., Rao, V. T. S., Durafourt, B. A., Bedell, B. J., Ludwin, S. K., Bar‐Or, A., & Antel, J. P. (2013) · Annals of Neurology · doi:10.1002/ana.23967 · Cited by 219 · see citing works
Ying, H., Kang, Y., Zhang, H., Zhao, D., Xia, J., Lü, Z., Wang, H., Xu, F., & Shi, L. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1402088 · Cited by 216 · see citing works
Wei, Y., Nazari-Jahantigh, M., Neth, P., Weber, C., & Schober, A. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.112.300279 · Cited by 209 · see citing works
Transcriptional Regulation of Macrophages Polarization by MicroRNAs
Li, H., Jiang, T., Li, M., Zheng, X., & Zhao, G.-J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01175 · Cited by 204 · see citing works
Bone regeneration is mediated by macrophage extracellular vesicles
Kang, M., Huang, C.-C., Lu, Y., Shirazi, S., Gajendrareddy, P., Ravindran, S., & Cooper, L. F. (2020) · Bone · doi:10.1016/j.bone.2020.115627 · Cited by 197 · see citing works
Su, M.-J., Aldawsari, H. M., & Amiji, M. M. (2016) · Scientific Reports · doi:10.1038/srep30110 · Cited by 194 · see citing works
Molecular Mechanisms Modulating the Phenotype of Macrophages and Microglia
Amici, S. A., Dong, J., & Guerau‐de‐Arellano, M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01520 · Cited by 192 · see citing works
Expression profiles of miRNAs in polarized macrophages
Zhang, Y., Zhang, M., Zhong, M., Suo, Q., & Lv, K. (2013) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2013.1260 · Cited by 192 · see citing works
Wu, S., He, L., Li, Y., Wang, T.-L., Feng, L., Jiang, L., Zhang, P., & Huang, X. (2013) · Journal of Infection · doi:10.1016/j.jinf.2013.05.003 · Cited by 190 · see citing works
Cockroach allergen exposure and risk of asthma
Do, D. C., Zhao, Y., & Gao, P. (2015) · Allergy · doi:10.1111/all.12827 · Cited by 190 · see citing works
Sedighzadeh, S. S., Khoshbin, A. P., Razi, S., Keshavarz‐Fathi, M., & Rezaei, N. (2021) · Translational Lung Cancer Research · doi:10.21037/tlcr-20-1241 · Cited by 188 · see citing works
MicroRNA-mediated control of macrophages and its implications for cancer
Squadrito, M. L., Etzrodt, M., Palma, M. D., & Pittet, M. J. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.02.003 · Cited by 188 · see citing works
Melatonin in macrophage biology: Current understanding and future perspectives
Xia, Y., Chen, S., Zeng, S., Zhao, Y., Zhu, C., Deng, B., Zhu, G., Yin, Y., Wang, W., Hardeland, R., et al. (2018) · Journal of Pineal Research · doi:10.1111/jpi.12547 · Cited by 188 · see citing works
Kapoor, N., Niu, J., Saad, Y., Kumar, S., Sirakova, T. D., Becerra, E., Li, X., & Kolattukudy, P. E. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402797 · Cited by 179 · see citing works
Macrophage activation and polarization in post-infarction cardiac remodeling
Энхэевна, Г. А., Rogovskaya, Y. V., Сергеевич, Ш. В., Ребенкова, М. С., Kzhyshkowska, J. G., Popov, S. V., Karpov, R. S., & Ryabov, V. V. (2017) · Journal of Biomedical Science · doi:10.1186/s12929-017-0322-3 · Cited by 174 · see citing works
Mycobacterium tuberculosis limits host glycolysis and IL-1β by restriction of PFK-m via microRNA-21
Hackett, E. E., Charles-Messance, H., O'Leary, S., Gleeson, L. E., Muñoz‐Wolf, N., Case, S., Wedderburn, A., Johnston, D. G. W., Williams, M. A., Smyth, A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.015 · Cited by 152 · see citing works
Wang, Z., Brandt, S., Medeiros, A., Wang, S., Wu, H., Dent, A., & Serezani, C. H. (2015) · PLOS ONE · doi:10.1371/journal.pone.0115855 · Cited by 169 · see citing works
Hao, J., Yan, F., Zhang, Y., Triplett, A., Zhang, Y., Schultz, D. A., Sun, Y., Zeng, J., Silverstein, K. A. T., Zheng, Q., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-17-2465 · Cited by 169 · see citing works
MiR-146a modulates macrophage polarization by inhibiting Notch1 pathway in RAW264.7 macrophages
Huang, C., Liu, X.-J., QunZhou, Xie, J., Ma, T.-T., Meng, X.-M., & Li, J. (2016) · International Immunopharmacology · doi:10.1016/j.intimp.2016.01.009 · Cited by 160 · see citing works
Immune Modulatory microRNAs Involved in Tumor Attack and Tumor Immune Escape
Eichmüller, S. B., Osen, W., Mandelboim, O., & Seliger, B. (2017) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djx034 · Cited by 155 · see citing works
Control of the Inflammatory Macrophage Transcriptional Signature by miR-155
Jablonski, K., Gaudet, A. D., Amici, S. A., Popovich, P. G., & Guerau‐de‐Arellano, M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0159724 · Cited by 152 · see citing works
Wang, J., Huang, R., Xu, Q., Zheng, G., Qiu, G., Ge, M., Shu, Q., & Xu, J. (2020) · Critical Care Medicine · doi:10.1097/ccm.0000000000004315 · Cited by 152 · see citing works
Microglial Polarization: Novel Therapeutic Strategy against Ischemic Stroke
Xue, Y., Nie, D., Wang, L.-J., Qiu, H., Ma, L., Dong, M., Tu, W., & Zhao, J. (2021) · Aging and Disease · doi:10.14336/ad.2020.0701 · Cited by 140 · see citing works
Macrophages with regulatory functions, a possible new therapeutic perspective in autoimmune diseases
Benedetto, P. D., Ruscitti, P., Vadasz, Z., Toubi, E., & Giacomelli, R. (2019) · Autoimmunity Reviews · doi:10.1016/j.autrev.2019.102369 · Cited by 139 · see citing works
Mantuano, E., Brifault, C., Lam, M. S., Azmoon, P., Gilder, A. S., & Gonias, S. L. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515480113 · Cited by 141 · see citing works
A Regulatory Role for MicroRNA 33* in Controlling Lipid Metabolism Gene Expression
Goedeke, L., Vales-Lara, F. M., Fenstermaker, M., Cirera-Salinas, D., Chamorro-Jorganes, A., Ramírez, C. M., Mattison, J. A., de Cabo, R., Suárez, Y., & Fernández-Hernando, C. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01714-12 · Cited by 140 · see citing works
MicroRNA-125 in immunity and cancer
Wang, J. K., Wang, Z., & Li, G. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.04.015 · Cited by 137 · see citing works
How to reprogram microglia toward beneficial functions
Fumagalli, M., Lombardi, M., Gressèns, P., & Verderio, C. (2018) · Glia · doi:10.1002/glia.23484 · Cited by 134 · see citing works
Mannose receptor modulates macrophage polarization and allergic inflammation through miR-511-3p
Zhou, Y., Do, D. C., Ishmael, F. T., Squadrito, M. L., Tang, H. M., Tang, H. L., Hsu, M.-H., Qiu, L., Li, C., Zhang, Y., et al. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.04.049 · Cited by 124 · see citing works
MicroRNA Targeting to Modulate Tumor Microenvironment
Kuninty, P. R., Schnittert, J., Storm, G., & Prakash, J. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2016.00003 · Cited by 123 · see citing works
Macrophage-targeted nanomedicine for chronic diseases immunotherapy
Song, Y., Huang, Y., Zhou, F., Ding, J., & Zhou, W. (2021) · Chinese Chemical Letters · doi:10.1016/j.cclet.2021.08.090 · Cited by 126 · see citing works
Dixon, L. J., Barnes, M. A., Tang, H., Pritchard, M., & Nagy, L. E. (2013) · Comprehensive Physiology · doi:10.1002/j.2040-4603.2013.tb00510.x · Cited by 633 · see citing works
The microRNA-221/-222 cluster balances the antiviral and inflammatory response in viral myocarditis
Corsten, M. F., Heggermont, W., Papageorgiou, A., Deckx, S., Tijsma, A. S. L., Verhesen, W., van Leeuwen, R. E. W., Carai, P., Thibaut, H. J., Custers, K., et al. (2015) · European Heart Journal · doi:10.1093/eurheartj/ehv321 · Cited by 119 · see citing works
MicroRNAs in vascular aging and atherosclerosis
Menghini, R., Stöhr, R., & Federici, M. (2014) · Ageing Research Reviews · doi:10.1016/j.arr.2014.03.005 · Cited by 117 · see citing works
MicroRNA-24 Regulates Macrophage Behavior and Retards Atherosclerosis
Gregoli, K. D., Jenkins, N., Salter, R., White, S., Newby, A., & Johnson, J. L. (2014) · Arteriosclerosis, Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.304088 · Cited by 112 · see citing works
Ma, S., Liu, M., Xu, Z., Li, Y., Guo, H., Ge, Y., Liu, Y., Zheng, D., & Shi, J. (2015) · Oncotarget · doi:10.18632/oncotarget.6284 · Cited by 117 · see citing works
Wu, X., Dai, Y., Yang, Y., Huang, C. Z., Meng, X., Wu, B., & Li, J. (2016) · Immunology · doi:10.1111/imm.12608 · Cited by 116 · see citing works
Sinha, S., Boila, L. D., Chatterjee, S. S., & Sengupta, A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-811022-5.00002-4 · Cited by 116 · see citing works
Role of Macrophages and Related Cytokines in Kidney Disease
Cantero‐Navarro, E., Rayego‐Mateos, S., Orejudo, M., Tejedor-Santamaria, L., Tejera‐Muñoz, A., Sanz, A. B., Márquez‐Expósito, L., Marchant, V. A., Santos‐Sanchez, L., Egido, J., et al. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.688060 · Cited by 115 · see citing works
Zhao, J.-L., Huang, F., He, F., Gao, C.-C., Liang, S.-Q., Ma, P., Dong, G.-Y., Han, H., & Qin, H.-Y. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-2019 · Cited by 111 · see citing works
Functional Immune Anatomy of the Liver—As an Allograft
Demetris, A. J., Bellamy, C. O. C., Gandhi, C. R., Prost, S., Nakanuma, Y., & Stolz, D. B. (2016) · American Journal of Transplantation · doi:10.1111/ajt.13749 · Cited by 115 · see citing works
Pathogenic arterial remodeling: the good and bad of microRNAs
Wei, Y., Schober, A., & Weber, C. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00267.2012 · Cited by 114 · see citing works
Modulation of Immune Function by Polyphenols: Possible Contribution of Epigenetic Factors
Cuevas, A., Saavedra, N., Salazar, L. A., & Abdalla, D. S. P. (2013) · Nutrients · doi:10.3390/nu5072314 · Cited by 117 · see citing works
MicroRNA-mediated mechanisms of the cellular stress response in atherosclerosis
Schober, A., Nazari-Jahantigh, M., & Weber, C. (2015) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2015.38 · Cited by 113 · see citing works
Bai, J., Adriani, G., Dang, T.-M., Tu, T.-Y., Leong Penny, H.-X., Wong, S.-C., Kamm, R. D., & Thiery, J.-P. (2015) · Oncotarget · doi:10.18632/oncotarget.4716 · Cited by 110 · see citing works
Kapellos, T. S., & Iqbal, A. J. (2016) · Mediators of Inflammation · doi:10.1155/2016/6591703 · Cited by 104 · see citing works
miRNAs in Tuberculosis: New Avenues for Diagnosis and Host-Directed Therapy
Sabir, N., Hussain, T. A., Shah, S. Z. A., Peramo, A., Zhao, D., & Zhou, X. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00602 · Cited by 105 · see citing works
Thounaojam, M. C., Kaushik, D. K., Kundu, K., & Basu, A. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12609 · Cited by 101 · see citing works
Next-generation sequencing of microRNAs uncovers expression signatures in polarized macrophages
Cobos Jiménez, V., Bradley, E. J., Willemsen, A. M., van Kampen, A. H. C., Baas, F., & Kootstra, N. A. (2014) · Physiological Genomics · doi:10.1152/physiolgenomics.00140.2013 · Cited by 103 · see citing works
Functional regulation of decidual macrophages during pregnancy
Sun, F., Wang, S., & Du, M. (2020) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2020.103264 · Cited by 104 · see citing works
NF-κB: Governing Macrophages in Cancer
Cornice, J., Verzella, D., Arboretto, P., Vecchiotti, D., Capece, D., Zazzeroni, F., & Franzoso, G. (2024) · Genes · doi:10.3390/genes15020197 · Cited by 104 · see citing works
Xu, H.-T., Zhu, Y.-L., Hsiao, A. W.-T., Xu, J.-K., Tong, W.-X., Chang, L., Zhang, X., Chen, Y.-F., Li, J., Chen, W., et al. (2023) · Biomaterials · doi:10.1016/j.biomaterials.2023.121998 · Cited by 95 · see citing works
Sisino, G., Bouckenooghe, T., Aurientis, S., Fontaine, P., Storme, L., & Vambergue, A. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.07.009 · Cited by 99 · see citing works
Tumor Immune Microenvironment and Its Related miRNAs in Tumor Progression
Xing, Y., Ruan, G., Ni, H., Qin, H., Chen, S., Gu, X., Shang, J., Zhou, Y., Xi, T., & Zheng, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.624725 · Cited by 96 · see citing works
The Role of MiRNA in Cancer: Pathogenesis, Diagnosis, and Treatment
Uzuner, E., Ulu, G. T., Gürler, S. B., & Baran, Y. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1170-8_18 · Cited by 96 · see citing works
MicroRNAs in the Atherosclerotic Plaque
Raitoharju, E., Oksala, N., & Lehtimäki, T. J. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2013.204917 · Cited by 93 · see citing works
Saha, B., Bruneau, J. C., Kodys, K., & Szabó, G. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402190 · Cited by 93 · see citing works
microRNA control of HDL Metabolism and Function
Rayner, K. J., & Moore, K. (2014) · Circulation Research · doi:10.1161/circresaha.114.300645 · Cited by 89 · see citing works
Schulert, G. S., Fall, N., Harley, J. B., Shen, N., Lovell, D. J., Thornton, S., & Grom, A. A. (2016) · Arthritis & Rheumatology · doi:10.1002/art.39694 · Cited by 88 · see citing works
miRNA in Macrophage Development and Function
Roy, S. (2016) · Antioxidants and Redox Signaling · doi:10.1089/ars.2016.6728 · Cited by 87 · see citing works
Lu, L., McCurdy, S., Huang, S., Zhu, X., Peplowska, K., Tiirikainen, M., Boisvert, W. A., & Garmire, L. X. (2016) · Scientific Reports · doi:10.1038/srep37446 · Cited by 83 · see citing works
Inflammation-related microRNA expression level in the bovine milk is affected by mastitis
Lai, Y., FUJIKAWA, T., Maemura, T., Takaaki, A. N. D. O., Kitahara, G., Endo, Y., Yamato, O., Koiwa, M., Kubota, C., & Miura, N. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177182 · Cited by 87 · see citing works
Smoking alters circulating plasma microvesicle pattern and microRNA signatures
Badrnya, S., Assinger, A., & Baumgartner, R. (2014) · Thrombosis and Haemostasis · doi:10.1160/th13-11-0977 · Cited by 87 · see citing works
Gaudet, A. D., Mandrekar-Colucci, S., Hall, J. C. E., Sweet, D. R., Schmitt, P., Xu, X., Guan, Z., Mo, X. M., Guerau‐de‐Arellano, M., & Popovich, P. G. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0735-16.2016 · Cited by 87 · see citing works
miR-125b controls monocyte adaptation to inflammation through mitochondrial metabolism and dynamics
Duroux-Richard, I., Roubert, C., Ammari, M., Présumey, J., Grün, J. R., Häupl, T., Grützkau, A., Lecellier, C., Boitez, V., Codogno, P., et al. (2016) · Blood · doi:10.1182/blood-2016-02-697003 · Cited by 86 · see citing works
Colangelo, T., Polcaro, G., Ziccardi, P., Pucci, B., Muccillo, L., Galgani, M., Fucci, A., Milone, M. R., Budillon, A., Santopaolo, M., et al. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.28 · Cited by 87 · see citing works
MicroRNAs and Cardiovascular Diseases
Nishiguchi, T., Imanishi, T., & Akasaka, T. (2015) · BioMed Research International · doi:10.1155/2015/682857 · Cited by 83 · see citing works
Endothelial cell dysfunction as a novel therapeutic target in atherosclerosis
Jensen, H., & Mehta, J. L. (2016) · Expert Review of Cardiovascular Therapy · doi:10.1080/14779072.2016.1207527 · Cited by 85 · see citing works
Macrophages in tumor: An inflammatory perspective
Goswami, K. K., Bose, A., & Baral, R. (2021) · Clinical Immunology · doi:10.1016/j.clim.2021.108875 · Cited by 86 · see citing works
The Macrophage Response Is Driven by Mesenchymal Stem Cell-Mediated Metabolic Reprogramming
Luque-Campos, N., Bustamante-Barrientos, F. A., Pradenas, C., García, C., Araya, M. J., Bohaud, C., Contreras-López, R., Elizondo-Vega, R., Djouad, F., Luz-Crawford, P., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.624746 · Cited by 82 · see citing works
- Authors
- Graff, J. W., Dickson, A. M., Clay, G., McCaffrey, A. P., & Wilson, M. E.
- Affiliations
- University of Iowa (US)
- Corresponding author
- Wilson, Mary E.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2012-06
- Volume
- 287
- Issue
- 26
- Pages
- 21816-21825
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3381144
- OpenAlex
- W2077124851
- Cited by
- 367
- References
- 39
- Citations by year
- 2026: 2 · 2025: 14 · 2024: 18 · 2023: 20 · 2022: 26 · 2021: 31 · 2020: 29 · 2019: 25 · 2018: 23 · 2017: 33 · 2016: 48 · 2015: 36 · 2014: 28 · 2013: 28 · 2012: 6
- FWCI
- 10.41
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (T32GM007337)
- National Institute of Allergy and Infectious Diseases (R01AI076233, R01AI045540, T32AI007343, R01AI067874, R21AI080801, T32AI007511)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- macrophage polarization, microRNA, monocyte-derived macrophages, M1 macrophages, M2 macrophages, miR-29b, miR-125a-5p, miR-155, miR-27a, miR-222, miR-146a, miR-296, interferon-gamma signaling, LPS signaling, A20, NF-κB signaling, THP-1 cells, miRNA mimics
- MeSH terms
- Cell Differentiation, Humans, Inflammation, Interferon-gamma, Leukocytes, Lipopolysaccharides, Macrophages, Monocytes, Phenotype, Gene Expression Regulation, Neoplastic, Cytokines, Chemokines, MicroRNAs, Cell Line, Tumor, HEK293 Cells
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