miR-24, miR-30b, and miR-142-3p Regulate Phagocytosis in Myeloid Inflammatory Cells
Open accessAbstract
Micro-RNAs (miRNAs) are small noncoding RNAs that regulate various biological pathways. As their role in phagocytosis remains poorly understood, we investigated their impact on phagocytosis in myeloid inflammatory cells. Seven miRNAs (miR-24, -30b, -101, 142-3p, -652-3p, -652-5p, and -1275) that were differentially expressed during monocyte to macrophage (Mφ) and monocyte to dendritic cell (DC) differentiation were screened for their potential role in phagocytosis. Among these, overexpression of miR-24, miR-30b, and miR-142-3p in human monocyte-derived Mφ, DC, monocytes, and PBMCs significantly attenuate phagocytosis of Escherichia coli and Staphylococcus aureus, as well as the secretion of inflammatory mediators, including TNF-α, IL-6, and IL-12p40. miRNA-mediated changes in cytokine profiles were observed at transcriptional and/or posttranscriptional levels and importantly exhibit miRNA-specific impact. To examine the underlying mechanism, we monitored the expression of phagocytosis pathway-associated genes and identified several genes that were altered in Mφ and DC transfected with miR-24, miR-30b, and miR-142-3p mimics. Some of these genes with altered expression also harbor putative miRNA binding sites. We show that miR-142-3p directly regulates protein kinase Cα (PKCα), a key gene involved in phagocytosis. Interestingly, miR-142-3p and PKCα exhibit antagonistic expression during Mφ and DC differentiation. Short interfering RNA-mediated knockdown of PKCα in Mφ leads to reduced bacterial uptake, further highlighting the role of the gene in phagocytosis. Overall, these results demonstrate that miR-24, miR-30b, and miR-142-3p regulate phagocytosis and associated cytokine production in myeloid inflammatory cells through modulation of various genes involved in the pathway.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
miR-142-3p and PKCα exhibit antagonistic expression during monocyte differentiation.
“Interestingly, miR-142-3p and PKCα exhibit antagonistic expression during monocyte differentiation.”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [125]
miR-142-3p directly regulates PKCα.
“Naqvi et al. confirmed that miR-142-3p directly regulates protein kinase Cα (PKCα), a key gene involved in phagocytosis.”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [125]
miR-24, miR-30b, and miR-142-3p regulate cytokine production associated with phagocytosis stimulation.
“The authors also demonstrated that miR-24, miR-30b, and miR-142-3p regulate cytokine production associated with phagocytosis stimulation [125].”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [125]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Protective and pathogenic functions of macrophage subsets
Murray, P. J., & Wynn, T. A. (2011) · Nature Reviews Immunology · doi:10.1038/nri3073 · Cited by 5,269 · see citing works
The history of toll-like receptors - redefining innate immunity
O'Neill, L. A. J., Golenbock, D., & Bowie, A. G. (2013) · Nature reviews. Immunology · doi:10.1038/nri3446 · Cited by 1,765 · see citing works
Phagocyte partnership during the onset and resolution of inflammation
Soehnlein, O., & Lindbom, L. (2010) · Nature Reviews Immunology · doi:10.1038/nri2779 · Cited by 1,054 · see citing works
Flagged first, then by citations
Research works printed but not linked: 39
- [2]Kubach J Becker C Schmitt E Steinbrink K Huter E Tuettenberg A Jonuleit H Dendritic Cells: Sentinels of immunity and tolerance. Int. J. Hemat 2005 81 197 203 15814330
- [3]Matt U Sharif O Martins R Furtner T Langeberg L Gawish R Elbau I Zivkovic A Lakovits K Oskolkova O Doninger B Vychytil A Perkmann T Schabbauer G Binder CJ Bochkov VN Scott JD Knapp S WAVE1 mediates suppression of phagocytosis by phospholipid-derived DAMPs. J. Cli. Invest 2013 123 3014 3024 PMC3696563 23934128
- [4]Mosser DM Edwards JP Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol 2008 8 958 969 19029990 PMC2724991
- [5]Auffray C Sieweke MH Geissmann F Blood Monocytes: Development, heterogeneity, and relationship with dendritic cells. Ann. Rev. Immunol 2009 27 669 692 19132917
- [6]Bartel DP MicroRNAs: Target recognition and regulatory functions. Cell 2009 136 215 233 19167326 PMC3794896
- [7]Didiano D Hobert O Molecular architecture of a miRNA-regulated 3′ UTR. RNA 2008 14 1297 1317 18463285 PMC2441980
- [8]Makeyev EV Maniatis T Multilevel Regulation of Gene Expression by MicroRNAs. Science 2008 319 1789 1790 18369137 PMC3139454
- [9]O'Connell RM Rao DS Chaudhuri AA Baltimore D Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol 2010 10 111 122 20098459
- [10]Lodish HF Zhou B Liu G Chen CZ Micromanagement of the immune system by microRNAs. Nat. Rev. Immunol 2008 8 120 130 18204468
- [11]O'Connell RM Rao DS Baltimore D microRNA regulation of inflammatory responses. Ann. Rev. Immunol 2012 30 295 312 22224773
- [12]O'Connell RM Taganov KD Boldin MP Cheng G Baltimore D MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA 2007 104 1604 1609 17242365 PMC1780072
- [13]Jurkin J Schichl YM Koeffel R Bauer T Richter S Konradi S Gesslbauer B Strobl H miR-146a is differentially expressed by myeloid dendritic cell subsets and desensitizes cells to TLR2-dependent activation. J. Immunol 2010 184 4955 4965 20375304
- [14]Croce CM MicroRNA dysregulation in acute myeloid leukemia. J. Clin. Onco 2013 31 2065 2066 23650415
- [15]Wang XS Gong JN Yu J Wang F Zhang XH Yin XL Tan ZQ Luo ZM Yang GH Shen C Zhang JW MicroRNA-29a and microRNA-142-3p are regulators of myeloid differentiation and acute myeloid leukemia. Blood 2012 119 4992 5004 22493297
- [16]Sharbati J Lewin A Kutz-Lohroff B Kamal E Einspanier R Sharbati S Integrated microRNA-mRNA-analysis of human monocyte derived macrophages upon Mycobacterium avium subsp. hominissuis infection. PLoS One 2011 6 e20258 21629653 PMC3101234
- [17]Singh Y Kaul V Mehra A Chatterjee S Tousif S Dwivedi VP Suar M Van Kaer L Bishai WR Das G Mycobacterium tuberculosis controls miR-99b expression in infected murine dendritic cells to modulate host immunity. J. Biol. Chem 2012 288 5056 5061 23233675 PMC3576108
- [18]Nares S Moutsopoulos NM Angelov N Rangel ZG Munson PJ Sinha N Wahl SM Rapid myeloid cell transcriptional and proteomic responses to periodontopathogenic Porphyromonas gingivalis. Am. J. Path 2009 174 1400 1414 19264901 PMC2671371
- [19]Naqvi AR Fordham JB Khan A Nares S MicroRNAs responsive to Aggregatibacter actinomycetemcomitans and Porphyromonas gingivalis LPS modulate expression of genes regulating innate immunity in human macrophages. Inn. Imm 2013 20 540 551 PMC3962801 24062196
- [21]Murray RZ Kay JG Sangermani DG Stow JL A role for the phagosome in cytokine secretion. Science 2005 310 1492 1495 16282525
- [22]Dweep H Sticht C Pandey P Gretz N miRWalk-database: prediction of possible miRNA binding sites by “walking” the genes of three genomes. J. Biomed. Inform 2011 44 839 847 21605702
- [23]Bettencourt P Marion S Pires D Santos LF Lastrucci C Carmo N Blake J Benes V Griffiths G Neyrolles O Lugo-Villarino G Anes E Actin-binding protein regulation by microRNAs as a novel microbial strategy to modulate phagocytosis by host cells: the case of N-Wasp and miR-142-3p. Front. Cell Infect. Microbiol 2013 3 19 23760605 PMC3672780
- [24]Jiang A Zhang S Li Z Liang R Ren S Li J Pu Y Yang J miR-615-3p promotes the phagocytic capacity of splenic macrophages by targeting ligand-dependent nuclear receptor corepressor in cirrhosis-related portal hypertension. Exp. Biol. Med 2012 236 672 680 21565892
- [25]Ma F Xu S Liu X Zhang Q Xu X Liu M Hua M Li N Yao H Cao X The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-[gamma]. Nat. Immunol 2011 12 861 869 21785411
- [26]Liu H Sidiropoulos P Song G Pagliari LJ Birrer MJ Stein B Anrather J Pope RM TNF-alpha gene expression in macrophages: regulation by NF-kappa B is independent of c-Jun or C/EBP beta. J. Immunol 2000 164 4277 4285 10754326
- [27]Ajizian SJ English BK Meals EA Specific inhibitors of p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways block inducible nitric oxide synthase and tumor necrosis factor accumulation in murine macrophages stimulated with lipopolysaccharide and interferon-γ. J. Infect. Dis 1999 179 939 944 10068590
- [28]Craig R Larkin A Mingo AM Thuerauf DJ Andrews C McDonough PM Glembotski CC p38 MAPK and NF-κB collaborate to induce Interleukin-6 gene expression and release: evidence for a cytoprotective autocrine signaling pathway in a cardiac myocyte model system. J. Biol. Chem 2000 275 23814 23824 10781614
- [29]Goodridge HS Simmons RM Underhill DM Dectin-1 stimulation by Candida albicans yeast or zymosan triggers NFAT activation in macrophages and dendritic cells. J. Immunol 2007 178 3107 3115 17312158
- [31]MacLeod H Wetzler LM T cell activation by TLRs: a role for TLRs in the adaptive immune response. Sci STKE 2007 402 pe48 17785715
- [32]Thoma-Uszynski S Stenger S Takeuchi O Ochoa MT Engele M Sieling PA Barnes PF Rollinghoff M Bolcskei PL Wagner M Akira S Norgard MV Belisle JT Godowski PJ Bloom BR Modlin RL Induction of direct antimicrobial activity through mammalian toll-like receptors. Science 2001 291 1544 1547 11222859
- [33]Anderson CL Guyre PM Whitin JC Ryan DH Looney RJ Fanger M Monoclonal antibodies to Fc receptors for IgG on human mononuclear phagocytes. Antibody characterization and induction of superoxide production in a monocyte cell line. J. Biol. Chem 1986 261 12856 12864 3017990
- [34]van Spriel AB van den Herik-Oudijk IE van Sorge NM Vilé HA van Strijp JA van de Winkel JG Effective phagocytosis and killing of Candida albicans via targeting FcγRI (CD64) or FcαRI (CD89) on neutrophils. J. Infect. Dis 1999 179 661 669 9952373
- [35]Dekker LV Parker PJ Protein kinase C – a question of specificity. Trends Biochem. Sci 1994 19 73 77 8160269
- [36]Nakashima S Protein kinase C alpha (PKC alpha): regulation and biological function. J. Biochem 2002 132 669 675 12417014
- [37]St-Denis A Caouras V Gervais F Descoteaux. Role of protein kinase C-alpha in the control of infection by intracellular pathogens in macrophages. J. Immunol 1999 163 5505 5511 10553077
- [38]Ng Yan Hing JD Desjardins M Descoteaux A Proteomic analysis reveals a role for protein kinase C-alpha in phagosome maturation. Biochem. Biophys. Res. Commun 2004 319 810 816 15184055
- [39]Holm A Tejle K Magnusson KE Descoteaux A Rasmusson B Leishmania donovani lipophosphoglycan causes periphagosomal actin accumulation: correlation with impaired translocation of PKCalpha and defective phagosome maturation. Cell Microbiol 2001 3 439 447 11437830
- [40]St-Denis A Chano F Tremblay P St-Pierre Y Descoteaux A Protein kinase C-alpha modulates lipopolysaccharide-induced functions in a murine macrophage cell line. J. Biol. Chem 1998 273 32787 32792 9830023
- [41]Langlet C Springael C Johnson J Thomas S Flamand V Leitges M Goldman M Aksoy E Willems F PKC-alpha controls MYD88-dependent TLR/IL-1R signaling and cytokine production in mouse and human dendritic cells. Eur. J. Immunol 2010 40 505 515 19950169
- [42]Johnson J Albarani V Nguyen M Goldman M Willems F Aksoy E Protein kinase C alpha is involved in interferon regulatory factor 3 activation and type I interferon-beta synthesis. J. Biol. Chem 2007 282 15022 15032 17296604
Cited by
Sorted by citations
Prata, J., Santos, S. G., Almeida, M. I., Coelho, R., & Barbosa, M. A. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0938-y · Cited by 115 · see citing works
miRNAs in immune responses to Mycobacterium tuberculosis infection
Yang, T., & Ge, B. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.05.028 · Cited by 78 · see citing works
miR-24 Regulates Macrophage Polarization and Plasticity
Afsar R. Naqvi, J. B. F., & Nares, S. (2015) · Journal of Clinical & Cellular Immunology · doi:10.4172/2155-9899.1000362 · Cited by 65 · see citing works
“html) [21] as we previously described [9,19]; targets identified by 3 or more of the 8 predictive algorithms were considered as putative targets.”
BackgroundMethodSelf-citationHuman infrapatellar fat pad mesenchymal stem cells show immunomodulatory exosomal signatures
Kouroupis, D., Kaplan, L. D., & Best, T. M. (2022) · Scientific Reports · doi:10.1038/s41598-022-07569-7 · Cited by 50 · see citing works
MicroRNAs as Regulators of Phagocytosis
Gierlikowski, W., & Gierlikowska, B. (2022) · Cells · doi:10.3390/cells11091380 · Cited by 25 · see citing works
- Authors
- Naqvi, A. R., Fordham, J. B., & Nares, S.
- Affiliations
- University of Illinois Chicago (US)
- Corresponding author
- Nares, Salvador
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-02
- Volume
- 194
- Issue
- 4
- Pages
- 1916-1927
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC4323870
- OpenAlex
- W2168590981
- Cited by
- 124
- References
- 3
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 7 · 2023: 11 · 2022: 14 · 2021: 12 · 2020: 11 · 2019: 11 · 2018: 15 · 2017: 11 · 2016: 17 · 2015: 4
- FWCI
- 5.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- University of Illinois at Urbana-Champaign
- University of Illinois at Chicago
- National Institute of Dental and Craniofacial Research (DE021052, R01DE021052)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- miR-24, miR-30b, miR-142-3p, monocyte-derived macrophages, dendritic cells, monocyte differentiation, protein kinase C alpha, bacterial internalization, Escherichia coli, Staphylococcus aureus, cytokine production, TNF-α, interleukin-6, IL-12
- MeSH terms
- Flow Cytometry, Fluorescent Antibody Technique, Humans, Inflammation, Phagocytosis, Transfection, Blotting, Western, Cytokines, Reverse Transcriptase Polymerase Chain Reaction, Myeloid Cells, MicroRNAs
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review