Cited by 153Neuroinflammation and Neurodegeneration MechanismsInflammasome and immune disordersExtracellular vesicles in disease

Exploring New Inflammatory Biomarkers and Pathways during LPS-Induced M1 Polarization

Open access
Cunha, Carolina, Gomes, Cátia, Vaz, Ana Rita, Brites, Dora·2016·Mediators of Inflammation

Abstract

Identification of mediators triggering microglia activation and transference of noncoding microRNA (miRNA) into exosomes are critical to dissect the mechanisms underlying neurodegeneration. We used lipopolysaccharide- (LPS-) induced N9 microglia activation to explore new biomarkers/signaling pathways and to identify inflammatory miRNA (inflamma-miR) in cells and their derived exosomes. Upregulation of iNOS and MHC-II (M1-markers) and downregulation of arginase 1, FIZZ1 (M2-markers), and CX3CR1 (M0/M2 polarization) confirmed the switch of N9 LPS-treated cells into the M1 phenotype, as described for macrophages/microglia. Cells showed increased proliferation, activated TLR4/TLR2/NF-κ B pathway, and enhanced phagocytosis, further corroborated by upregulated MFG-E8. We found NLRP3-inflammasome activation in these cells, probably accounting for the increased extracellular content of the cytokine HMGB1 and of the MMP-9 we have observed. We demonstrate for the first time that the inflamma-miR profiling (upregulated miR-155 and miR-146a plus downregulated miR-124) in M1 polarized N9 cells, noticed by others in activated macrophages/microglia, was replicated in their derived exosomes, likely regulating the inflammatory response of recipient cells and dissemination processes. Data show that LPS-treated N9 cells behave like M1 polarized microglia/macrophages, while providing new targets for drug discovery. In particular, the study yields novel insights into the exosomal circulating miRNA during neuroinflammation important for emerging therapeutic approaches targeting microglia activation.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1155/2016/6986175

Cites

15 of 15 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Upon LPS stimulation, upregulation of miR-155 and miR-146a and downregulation of miR-124 (typical for M1 polarization) is accompanied by increased phagocytic activity.

    “It was demonstrated that, typical for M1 polarization, upregulation of miR-155 and miR-146a, along with downregulation of miR-124 upon LPS stimulation, is accompanied with increased phagocytic activity.”

    From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [242]

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

Flagged first, then by citations

Research works printed but not linked: 75

  1. [1]Vilhardt F. Microglia: phagocyte and glia cell International Journal of Biochemistry and Cell Biology 2005 37 1 17 21 10.1016/j.biocel.2004.06.010 2-s2.0-4644308783 15381143 · DOI
  2. [4]McKimmie C. S. Roy D. Forster T. Fazakerley J. K. Innate immune response gene expression profiles of N9 microglia are pathogen-type specific Journal of Neuroimmunology 2006 175 1-2 128 141 10.1016/j.jneuroim.2006.03.012 2-s2.0-33646813652 16697053 16697053 · DOI · Paper page
  3. [5]Perry V. H. O'Connor V. The role of microglia in synaptic stripping and synaptic degeneration: a revised perspective ASN Neuro 2010 2 5 e00047 2-s2.0-84855718087 PMC2954441 20967131
  4. [6]Graeber M. B. Streit W. J. Microglia: biology and pathology Acta Neuropathologica 2010 119 1 89 105 10.1007/s00401-009-0622-0 2-s2.0-77649184973 20012873 · DOI
  5. [7]Brites D. Vaz A. R. Microglia centered pathogenesis in ALS: insights in cell interconnectivity Frontiers in Cellular Neuroscience 2014 8 MAY, article 117 10.3389/fncel.2014.00117 2-s2.0-84901445351 PMC4033073 24904276 · DOI
  6. [8]Fernandes A. Miller-Fleming L. Pais T. F. Microglia and inflammation: conspiracy, controversy or control? Cellular and Molecular Life Sciences 2014 71 20 3969 3985 10.1007/s00018-014-1670-8 2-s2.0-84909987977 25008043 PMC11113719 · DOI
  7. [9]Ohsawa K. Kohsaka S. Dynamic motility of microglia: purinergic modulation of microglial movement in the normal and pathological brain GLIA 2011 59 12 1793 1799 10.1002/glia.21238 2-s2.0-80053575339 21901756 · DOI
  8. [10]Sheridan G. K. Murphy K. J. Neuron-glia crosstalk in health and disease: fractalkine and CX3CR1 take centre stage Open Biology 2013 3 12 130181 10.1098/rsob.130181 2-s2.0-84897478440 PMC3877844 24352739 · DOI
  9. [12]Durafourt B. A. Moore C. S. Zammit D. A. Comparison of polarization properties of human adult microglia and blood-derived macrophages Glia 2012 60 5 717 727 10.1002/glia.22298 2-s2.0-84858072878 22290798 · DOI
  10. [13]Chhor V. Le Charpentier T. Lebon S. Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia In vitro Brain, Behavior, and Immunity 2013 32 70 85 10.1016/j.bbi.2013.02.005 2-s2.0-84891373720 23454862 23454862 PMC3694309 · DOI
  11. [14]Liu H.-C. Zheng M.-H. Du Y.-L. N9 microglial cells polarized by LPS and IL4 show differential responses to secondary environmental stimuli Cellular Immunology 2012 278 1-2 84 90 10.1016/j.cellimm.2012.06.001 2-s2.0-84868288704 23121979 23121979 · DOI
  12. [15]Zhu H.-T. Bian C. Yuan J.-C. Curcumin attenuates acute inflammatory injury by inhibiting the TLR4/MyD88/NF-κB signaling pathway in experimental traumatic brain injury Journal of Neuroinflammation 2014 11, article 59 10.1186/1742-2094-11-59 2-s2.0-84899574914 PMC3986937 24669820 · DOI
  13. [17]Lu B. Wang H. Andersson U. Tracey K. J. Regulation of HMGB1 release by inflammasomes Protein and Cell 2013 4 3 163 167 10.1007/s13238-012-2118-2 2-s2.0-84874919170 23483477 PMC4533838 · DOI
  14. [18]Park J. S. Svetkauskaite D. He Q. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein Journal of Biological Chemistry 2004 279 9 7370 7377 10.1074/jbc.m306793200 2-s2.0-1542380035 14660645 · DOI
  15. [20]Righi M. Mori L. De Libero G. Monokine production by microglial cell clones European Journal of Immunology 1989 19 8 1443 1448 10.1002/eji.1830190815 2-s2.0-0024464856 2789141 2789141 · DOI
  16. [21]Nikodemova M. Watters J. J. Outbred ICR/CD1 mice display more severe neuroinflammation mediated by microglial TLR4/CD14 activation than inbred C57Bl/6 mice Neuroscience 2011 190 67 74 10.1016/j.neuroscience.2011.06.006 2-s2.0-80051587671 21683771 21683771 PMC3156380 · DOI
  17. [22]Freilich R. W. Woodbury M. E. Ikezu T. Integrated expression profiles of mRNA and miRNA in polarized primary murine microglia PLoS ONE 2013 8 11 e79416 10.1371/journal.pone.0079416 2-s2.0-84893202052 24244499 24244499 PMC3823621 · DOI · Paper page
  18. [24]Ponomarev E. D. Veremeyko T. Weiner H. L. MicroRNAs are universal regulators of differentiation, activation, and polarization of microglia and macrophages in normal and diseased CNS GLIA 2013 61 1 91 103 10.1002/glia.22363 2-s2.0-84869171691 22653784 22653784 PMC3434289 · DOI
  19. [25]Jiang M. Xiang Y. Wang D. Dysregulated expression of miR-146a contributes to age-related dysfunction of macrophages Aging Cell 2012 11 1 29 40 10.1111/j.1474-9726.2011.00757.x 2-s2.0-84855859453 21981419 · DOI
  20. [26]Veremeyko T. Siddiqui S. Sotnikov I. Yung A. Ponomarev E. D. IL-4/IL-13-dependent and independent expression of miR-124 and its contribution to M2 phenotype of monocytic cells in normal conditions and during allergic inflammation PLOS ONE 2013 8 12 e81774 10.1371/journal.pone.0081774 2-s2.0-84892959681 PMC3864800 24358127 · DOI · Paper page
  21. [28]Aryani A. Denecke B. Exosomes as a nanodelivery system: a key to the future of neuromedicine? Molecular Neurobiology 2016 53 2 818 834 10.1007/s12035-014-9054-5 2-s2.0-84958111818 25502465 PMC4752585 · DOI
  22. [30]Burm S. M. Zuiderwijk-Sick E. A. T Jong A. E. J. Inflammasome-induced IL-1β secretion in microglia is characterized by delayed kinetics and is only partially dependent on inflammatory caspases Journal of Neuroscience 2015 35 2 678 687 10.1523/JNEUROSCI.2510-14.2015 2-s2.0-84920982518 25589762 25589762 PMC6605364 · DOI · Paper page
  23. [31]Ksiazek-Winiarek D. J. Kacperska M. J. Glabinski A. MicroRNAs as novel regulators of neuroinflammation Mediators of inflammation 2013 2013 11 172351 10.1155/2013/172351 2-s2.0-84894520394 PMC3745967 23983402 · DOI
  24. [32]Alexander M. Hu R. Runtsch M. C. Exosome-delivered microRNAs modulate the inflammatory response to endotoxin Nature Communications 2015 6, article 7321 10.1038/ncomms8321 2-s2.0-84934903985 PMC4557301 26084661 · DOI · Paper page
  25. [33]Cui Y.-H. Le Y. Gong W. Bacterial lipopolysaccharide selectively up-regulates the function of the chemotactic peptide receptor formyl peptide receptor 2 in murine microglial cells The Journal of Immunology 2002 168 1 434 442 10.4049/jimmunol.168.1.434 2-s2.0-0036135610 11751990 · DOI
  26. [34]Barateiro A. Vaz A. R. Silva S. L. Fernandes A. Brites D. ER stress, mitochondrial dysfunction and calpain/JNK activation are involved in oligodendrocyte precursor cell death by unconjugated bilirubin NeuroMolecular Medicine 2012 14 4 285 302 10.1007/s12017-012-8187-9 2-s2.0-84870563054 22707385 · DOI
  27. [35]Barateiro A. Miron V. E. Santos S. D. Unconjugated bilirubin restricts oligodendrocyte differentiation and axonal myelination Molecular neurobiology 2013 47 2 632 644 10.1007/s12035-012-8364-8 2-s2.0-84894303554 23086523 · DOI
  28. [37]Fernandes A. Falcão A. S. Silva R. F. M. Inflammatory signalling pathways involved in astroglial activation by unconjugated bilirubin Journal of Neurochemistry 2006 96 6 1667 1679 10.1111/j.1471-4159.2006.03680.x 2-s2.0-33644812051 16476078 · DOI
  29. [38]Kurpius D. Wilson N. Fuller L. Hoffman A. Dailey M. E. Early activation, motility, and homing of neonatal microglia to injured neurons does not require protein synthesis GLIA 2006 54 1 58 70 10.1002/glia.20355 2-s2.0-33745548105 16715500 16715500 · DOI
  30. [39]Caldeira C. Oliveira A. F. Cunha C. Microglia change from a reactive to an age-like phenotype with the time in culture Frontiers in Cellular Neuroscience 2014 8, article no. 152 10.3389/fncel.2014.00152 2-s2.0-84901848126 PMC4040822 24917789 · DOI · Paper page
  31. [40]Silva S. L. Osório C. Vaz A. R. Dynamics of neuron-glia interplay upon exposure to unconjugated bilirubin Journal of Neurochemistry 2011 117 3 412 424 10.1111/j.1471-4159.2011.07200.x 2-s2.0-79954420884 21275990 · DOI
  32. [41]Silva S. L. Vaz A. R. Barateiro A. Features of bilirubin-induced reactive microglia: from phagocytosis to inflammation Neurobiology of Disease 2010 40 3 663 675 10.1016/j.nbd.2010.08.010 2-s2.0-77957807564 20727973 · DOI
  33. [42]Fernandes A. Falcão A. S. Silva R. F. M. Brito M. A. Brites D. MAPKs are key players in mediating cytokine release and cell death induced by unconjugated bilirubin in cultured rat cortical astrocytes European Journal of Neuroscience 2007 25 4 1058 1068 10.1111/j.1460-9568.2007.05340.x 2-s2.0-33847203682 17331202 17331202 · DOI
  34. [43]Wang K. Zhang S. Weber J. Baxter D. Galas D. J. Export of microRNAs and microRNA-protective protein by mammalian cells Nucleic Acids Research 2010 38 20 7248 7259 10.1093/nar/gkq601 2-s2.0-78149409316 20615901 PMC2978372 · DOI · Paper page
  35. [44]Streit W. J. Walter S. A. Pennell N. A. Reactive microgliosis Progress in Neurobiology 1999 57 6 563 581 10.1016/S0301-0082(98)00069-0 2-s2.0-0033044951 10221782 10221782 · DOI · Paper page
  36. [45]Mashimo H. Ohguro N. Nomura S. Hashida N. Nakai K. Tano Y. Neutrophil chemotaxis and local expression of interleukin-10 in the tolerance of endotoxin-induced uveitis Investigative Ophthalmology and Visual Science 2008 49 12 5450 5457 10.1167/iovs.08-1878 2-s2.0-58149229870 18757518 18757518 · DOI
  37. [46]Napoli I. Neumann H. Microglial clearance function in health and disease Neuroscience 2009 158 3 1030 1038 10.1016/j.neuroscience.2008.06.046 2-s2.0-59349112140 18644426 · DOI
  38. [47]Bauernfeind F. G. Horvath G. Stutz A. Cutting edge: NF-κB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression The Journal of Immunology 2009 183 2 787 791 10.4049/jimmunol.0901363 2-s2.0-70249138036 19570822 PMC2824855 · DOI
  39. [48]Liu R. T. Wang A. To E. Vinpocetine inhibits amyloid-beta induced activation of NF-κB, NLRP3 inflammasome and cytokine production in retinal pigment epithelial cells Experimental Eye Research 2014 127 49 58 10.1016/j.exer.2014.07.003 2-s2.0-84904917944 25041941 25041941 PMC4461375 · DOI
  40. [49]Lee H.-M. Kang J. Lee S. J. Jo E.-K. Microglial activation of the NLRP3 inflammasome by the priming signals derived from macrophages infected with mycobacteria Glia 2013 61 3 441 452 10.1002/glia.22448 2-s2.0-84872617996 23280493 · DOI
  41. [50]Falcão A. Carvalho L. A. R. Lidónio G. Dipeptidyl vinyl sulfone as a novel chemical tool to inhibit HMGB1/NLRP3-inflammasome and inflamma-miRs in Aβ-mediated microglial inflammation ACS Chemical Neuroscience 2016 10.1021/acschemneuro.6b00250 27797173 · DOI
  42. [52]Fanjul-Fernández M. Folgueras A. R. Cabrera S. López-Otín C. Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models Biochimica et Biophysica Acta—Molecular Cell Research 2010 1803 1 3 19 10.1016/j.bbamcr.2009.07.004 2-s2.0-77149137406 19631700 · DOI
  43. [53]Gao H.-M. Zhou H. Zhang F. Wilson B. C. Kam W. Hong J.-S. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration Journal of Neuroscience 2011 31 3 1081 1092 10.1523/JNEUROSCI.3732-10.2011 2-s2.0-78751502344 21248133 21248133 PMC3046932 · DOI · Paper page
  44. [54]Kim J.-B. Joon S. C. Yu Y.-M. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain Journal of Neuroscience 2006 26 24 6413 6421 10.1523/JNEUROSCI.3815-05.2006 2-s2.0-33745788420 16775128 16775128 PMC6674036 · DOI
  45. [55]Kim J.-B. Lim C.-M. Yu Y.-M. Lee J.-K. Induction and subcellular localization of high-mobility group box-1 (HMGB1) in the postischemic rat brain Journal of Neuroscience Research 2008 86 5 1125 1131 10.1002/jnr.21555 2-s2.0-41149105399 17975839 · DOI
  46. [56]Wu D. Cerutti C. Lopez-Ramirez M. A. Brain endothelial miR-146a negatively modulates T-cell adhesion through repressing multiple targets to inhibit NF-κB activation Journal of Cerebral Blood Flow and Metabolism 2015 35 3 412 423 10.1038/jcbfm.2014.207 2-s2.0-84938496871 25515214 PMC4348377 · DOI
  47. [57]Zhao S. Zhang L. Lian G. Sildenafil attenuates LPS-induced pro-inflammatory responses through down-regulation of intracellular ROS-related MAPK/NF-κB signaling pathways in N9 microglia International Immunopharmacology 2011 11 4 468 474 10.1016/j.intimp.2010.12.017 2-s2.0-79952736802 21220057 21220057 · DOI
  48. [58]Zhang G. He J.-L. Xie X.-Y. Yu C. LPS-induced iNOS expression in N9 microglial cells is suppressed by geniposide via ERK, p38 and nuclear factor-κB signaling pathways International Journal of Molecular Medicine 2012 30 3 561 568 10.3892/ijmm.2012.1030 2-s2.0-84865161234 22710392 · DOI
  49. [59]Lu X. Ma L. Ruan L. Resveratrol differentially modulates inflammatory responses of microglia and astrocytes Journal of Neuroinflammation 2010 7, article 46 10.1186/1742-2094-7-46 2-s2.0-77955540457 PMC2936301 20712904 · DOI
  50. [60]Bruce-Keller A. J. Keeling J. L. Keller J. N. Huang F. F. Camondola S. Mattson M. P. Antiinflammatory effects of estrogen on microglial activation Endocrinology 2000 141 10 3646 3656 2-s2.0-0033752744 11014219 11014219
  51. [61]Shechter R. Miller O. Yovel G. Recruitment of Beneficial M2 Macrophages to Injured Spinal Cord Is Orchestrated by Remote Brain Choroid Plexus Immunity 2013 38 3 555 569 10.1016/j.immuni.2013.02.012 2-s2.0-84875553508 23477737 23477737 PMC4115271 · DOI · Paper page
  52. [62]Boddeke E. W. G. M. Meigel I. Frentzel S. Biber K. Renn L. Q. Gebicke-Härter P. Functional expression of the fractalkine (CX3C) receptor and its regulation by lipopolysaccharide in rat microglia European Journal of Pharmacology 1999 374 2 309 313 10.1016/S0014-2999(99)00307-6 2-s2.0-0033030288 10422773 10422773 · DOI
  53. [63]Pachot A. Cazalis M.-A. Venet F. Decreased expression of the fractalkine receptor CX3CR1 on circulating monocytes as new feature of sepsis-induced immunosuppression Journal of Immunology 2008 180 9 6421 6429 10.4049/jimmunol.180.9.6421 2-s2.0-44449152668 18424766 18424766 · DOI
  54. [64]Jose S. Tan S. W. Ooi Y. Y. Ramasamy R. Vidyadaran S. Mesenchymal stem cells exert anti-proliferative effect on lipopolysaccharide-stimulated BV2 microglia by reducing tumour necrosis factor-α levels Journal of Neuroinflammation 2014 11 1, article 149 10.1186/s12974-014-0149-8 2-s2.0-84906835858 PMC4156657 25182840 · DOI
  55. [65]Chen Z. Jalabi W. Shpargel K. B. Lipopolysaccharide-induced microglial activation and neuroprotection against experimental brain injury is independent of hematogenous TLR4 Journal of Neuroscience 2012 32 34 11706 11715 10.1523/JNEUROSCI.0730-12.2012 2-s2.0-84865238053 22915113 22915113 PMC4461442 · DOI · Paper page
  56. [66]Li T. Pang S. Yu Y. Wu X. Guo J. Zhang S. Proliferation of parenchymal microglia is the main source of microgliosis after ischaemic stroke Brain: A Journal Of Neurology 2013 136 3578 3588 10.1093/brain/awt287 2-s2.0-84893515578 24154617 · DOI · Paper page
  57. [67]Orr A. G. Orr A. L. Li X.-J. Gross R. E. Traynelis S. F. Adenosine A2A receptor mediates microglial process retraction Nature Neuroscience 2009 12 7 872 878 10.1038/nn.2341 2-s2.0-67649797862 19525944 PMC2712729 · DOI
  58. [69]Honda S. Sasaki Y. Ohsawa K. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors The Journal of Neuroscience 2001 21 6 1975 1982 2-s2.0-0035869474 11245682 PMC6762617
  59. [70]Lively S. Schlichter L. C. The microglial activation state regulates migration and roles of matrix-dissolving enzymes for invasion Journal of Neuroinflammation 2013 10, article 75 10.1186/1742-2094-10-75 2-s2.0-84879092634 PMC3693964 23786632 · DOI
  60. [71]Scheiblich H. Roloff F. Singh V. Stangel M. Stern M. Bicker G. Nitric oxide/cyclic GMP signaling regulates motility of a microglial cell line and primary microglia in vitro Brain Research 2014 1564 9 21 10.1016/j.brainres.2014.03.048 2-s2.0-84899910680 24713349 · DOI
  61. [72]Babcock A. A. Kuziel W. A. Rivest S. Owens T. Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS Journal of Neuroscience 2003 23 21 7922 7930 2-s2.0-0041319041 12944523 12944523 PMC6740601
  62. [74]Fricker M. Neher J. J. Zhao J.-W. Théry C. Tolkovsky A. M. Brown G. C. MFG-E8 mediates primary phagocytosis of viable neurons during neuroinflammation The Journal of Neuroscience 2012 32 8 2657 2666 10.1523/jneurosci.4837-11.2012 2-s2.0-84863141913 22357850 PMC3312099 · DOI · Paper page
  63. [75]Spittau B. Rilka J. Steinfath E. Zöller T. Krieglstein K. TGFβ1 increases microglia-mediated engulfment of apoptotic cells via upregulation of the milk fat globule-EGF factor 8 GLIA 2015 63 1 142 153 10.1002/glia.22740 2-s2.0-84911986915 25130376 25130376 · DOI
  64. [76]Komura H. Miksa M. Wu R. Goyert S. M. Wang P. Milk fat globule epidermal growth factor-factor VIII is down-regulated in sepsis via the lipopolysaccharide-CD14 pathway The Journal of Immunology 2009 182 1 581 587 10.4049/jimmunol.182.1.581 2-s2.0-59849099434 19109191 PMC2788770 · DOI
  65. [77]Liu Y. Yang X. Guo C. Nie P. Liu Y. Ma J. Essential role of MFG-E8 for phagocytic properties of microglial cells PLoS ONE 2013 8 2 e55754 10.1371/journal.pone.0055754 2-s2.0-84873530432 PMC3565973 23405209 · DOI
  66. [78]Hanamsagar R. Torres V. Kielian T. Inflammasome activation and IL-1β/IL-18 processing are influenced by distinct pathways in microglia Journal of Neurochemistry 2011 119 4 736 748 10.1111/j.1471-4159.2011.07481.x 2-s2.0-80054795572 21913925 PMC3202981 · DOI
  67. [79]Lee E.-J. Kim H.-S. Inhibitory mechanism of MMP-9 gene expression by ethyl pyruvate in lipopolysaccharide-stimulated BV2 microglial cells Neuroscience Letters 2011 493 1-2 38 43 10.1016/j.neulet.2011.02.016 2-s2.0-79952620639 21316417 · DOI
  68. [80]Bai Y. Zhu Z. Gao Z. Kong Y. TLR2 signaling directs NO-dependent MMP-9 induction in mouse microglia Neuroscience Letters 2014 571 5 10 10.1016/j.neulet.2014.04.025 2-s2.0-84899849537 24780563 24780563 · DOI
  69. [81]Cho K.-O. La H. O. Cho Y.-J. Sung K.-W. Kim S. Y. Minocycline attenuates white matter damage in a rat model of chronic cerebral hypoperfusion Journal of Neuroscience Research 2006 83 2 285 291 10.1002/jnr.20727 2-s2.0-31844454079 16385583 · DOI
  70. [82]Wu C.-X. Sun H. Liu Q. Guo H. Gong J.-P. LPS induces HMGB1 relocation and release by activating the NF-κB-CBP signal transduction pathway in the murine macrophage-like cell line RAW264.7 Journal of Surgical Research 2012 175 1 88 100 10.1016/j.jss.2011.02.026 2-s2.0-84860336916 21571302 21571302 · DOI
  71. [83]Guedes J. Cardoso A. L. C. Pedroso de Lima M. C. Involvement of microRNA in microglia-mediated immune response Clinical and Developmental Immunology 2013 2013 11 186872 10.1155/2013/186872 2-s2.0-84878648745 PMC3676986 23762086 · DOI
  72. [84]Cãtaña C. S. Calin G. A. Berindan-Neagoe I. Inflamma-miRs in aging and breast cancer: are they reliable players? Frontiers in Medicine 2015 2, article article 85 10.3389/fmed.2015.00085 PMC4678211 26697428 · DOI
  73. [85]Quinn S. R. O'Neill L. A. A trio of microRNAs that control Toll-like receptor signalling International Immunology 2011 23 7 421 425 10.1093/intimm/dxr034 2-s2.0-79960073532 21652514 21652514 · DOI · Paper page
  74. [88]Nahid M. A. Pauley K. M. Satoh M. Chan E. K. L. miR-146a is critical for endotoxin-induced tolerance: implication in innate immunity Journal of Biological Chemistry 2009 284 50 34590 34599 10.1074/jbc.m109.056317 2-s2.0-71749096218 19840932 PMC2787321 · DOI · Paper page
  75. [90]Willemen H. L. D. M. Huo X.-J. Mao-Ying Q.-L. Zijlstra J. Heijnen C. J. Kavelaars A. MicroRNA-124 as a novel treatment for persistent hyperalgesia Journal of Neuroinflammation 2012 9, article 143 10.1186/1742-2094-9-143 2-s2.0-84862635378 PMC3418202 22731384 · DOI

Cited by

Sorted by citations

Authors
Cunha, C., Gomes, C., Vaz, A. R., & Brites, D.
Affiliations
University of Lisbon (PT)
Corresponding author
Brites, Dora
Venue
Mediators of Inflammation
Publisher
Wiley
Published
2016
Volume
2016
Pages
1-17
ISSN
  • 0962-9351 (ISSN-L)
  • 1466-1861
OpenAlex
W2567699986
Cited by
153
References
15
Citations by year
2026: 8 · 2025: 10 · 2024: 11 · 2023: 9 · 2022: 25 · 2021: 23 · 2020: 21 · 2019: 22 · 2018: 12 · 2017: 11 · 2016: 1
FWCI
8.40
Type
journal article
Language
en
Open access
Locations
  • Mediators of Inflammation (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Fundação para a Ciência e a Tecnologia (PTDC/SAU-FAR/118787/2010, UID/DTP/04138/2013, SFRH/BPD/76590/2011, SFRH/BD/91316/2012, SFRH/BD/102718/2014)
Topics
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords
microglial activation, M1 macrophage polarization, lipopolysaccharide, exosomal microRNAs, neuroinflammation, NLRP3 inflammasome, HMGB1, MMP-9, MFG-E8, miR-155, miR-146a, miR-124, inducible nitric oxide synthase, MHC class II, arginase-1, Fizz1, CX3CR1, neurodegeneration
MeSH terms
Animals, Arginase, Inflammation, Lipopolysaccharides, Macrophages, Phagocytosis, Phenotype, Biomarkers, Cytokines, Cell Death, Microglia, Matrix Metalloproteinase 9, Receptors, Interleukin-8A, HMGB1 Protein, MicroRNAs, Intercellular Signaling Peptides and Proteins, Cell Proliferation, Mice, Exosomes, Inflammasomes

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