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

Mediators of Inflammation

Volumn 2016, Issue , 2016, Pages

  Cunha, Carolina ^a   Gomes, Cátia ^a   Vaz, Ana Rita ^a   Brites, Dora ^a  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; BIOLOGICAL MARKER; CHEMOKINE RECEPTOR CX3CR1; CRYOPYRIN; FOUND IN INFLAMMATORY ZONE 1 PROTEIN; GELATINASE B; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INFLAMMASOME; LACTADHERIN; LIPOPOLYSACCHARIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MICRORNA 124; MICRORNA 146A; MICRORNA 155; PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; ARG1 PROTEIN, MOUSE; ARGINASE; CHEMOKINE RECEPTOR CXCR1; CYTOKINE; HMGB1 PROTEIN, MOUSE; MICRORNA; MMP9 PROTEIN, MOUSE; RETNLA PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EXOSOME; EXTRACELLULAR SPACE; MACROPHAGE; MICROGLIA; MOLECULAR PATHOLOGY; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHAGOCYTOSIS; PROTEIN CONTENT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL DEATH; CYTOLOGY; INFLAMMATION; METABOLISM; PHENOTYPE;

ANIMALS; ARGINASE; BIOMARKERS; CELL DEATH; CELL PROLIFERATION; CYTOKINES; EXOSOMES; HMGB1 PROTEIN; INFLAMMASOMES; INFLAMMATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPOLYSACCHARIDES; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MICE; MICROGLIA; MICRORNAS; PHAGOCYTOSIS; PHENOTYPE; RECEPTORS, INTERLEUKIN-8A;

EID: 85008894491     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2016/6986175     Document Type: Article

References (90)

1. F. Vilhardt, "Microglia: phagocyte and glia cell," International Journal of Biochemistry and Cell Biology, vol. 37, no. 1, pp. 17-21, 2005.
2. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, "Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo," Science, vol. 308, no. 5726, pp. 1314-1318, 2005.
3. D. Davalos, J. Grutzendler, G. Yang et al., "ATP mediates rapid microglial response to local brain injury in vivo," Nature Neuroscience, vol. 8, no. 6, pp. 752-758, 2005.
4. C. S. McKimmie, D. Roy, T. Forster, and J. K. Fazakerley, "Innate immune response gene expression profiles of N9 microglia are pathogen-type specific," Journal of Neuroimmunology, vol. 175, no. 1-2, pp. 128-141, 2006.
5. V. H. Perry and V. O'Connor, "The role of microglia in synaptic stripping and synaptic degeneration: a revised perspective," ASN Neuro, vol. 2, no. 5, Article ID e00047, 2010.
6. M. B. Graeber and W. J. Streit, "Microglia: biology and pathology," Acta Neuropathologica, vol. 119, no. 1, pp. 89-105, 2010.
7. D. Brites and A. R. Vaz, "Microglia centered pathogenesis in ALS: insights in cell interconnectivity," Frontiers in Cellular Neuroscience, vol. 8, no. MAY, article 117, 2014.
8. A. Fernandes, L. Miller-Fleming, and T. F. Pais, "Microglia and inflammation: conspiracy, controversy or control?" Cellular and Molecular Life Sciences, vol. 71, no. 20, pp. 3969-3985, 2014.
9. K. Ohsawa and S. Kohsaka, "Dynamic motility of microglia: purinergic modulation of microglial movement in the normal and pathological brain," GLIA, vol. 59, no. 12, pp. 1793-1799, 2011.
10. 3CR1 take centre stage," Open Biology, vol. 3, no. 12, Article ID130181, 2013.
11. A. E. Cardona, E. P. Pioro, M. E. Sasse et al., "Control of microglial neurotoxicity by the fractalkine receptor," Nature Neuroscience, vol. 9, no. 7, pp. 917-924, 2006.
12. B. A. Durafourt, C. S. Moore, D. A. Zammit et al., "Comparison of polarization properties of human adult microglia and bloodderived macrophages," Glia, vol. 60, no. 5, pp. 717-727, 2012.
13. V. Chhor, T. Le Charpentier, S. Lebon et al., "Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia In vitro," Brain, Behavior, and Immunity, vol. 32, pp. 70-85, 2013.
14. H.-C. Liu, M.-H. Zheng, Y.-L. Du et al., "N9 microglial cells polarized by LPS and IL4 show differential responses to secondary environmental stimuli," Cellular Immunology, vol. 278, no. 1-2, pp. 84-90, 2012.
15. H.-T. Zhu, C. Bian, J.-C. Yuan et al., "Curcumin attenuates acute inflammatory injury by inhibiting the TLR4/MyD88/NF-κB signaling pathway in experimental traumatic brain injury," Journal of Neuroinflammation, vol. 11, article 59, 2014.
16. J. G. Walsh, D. A. Muruve, and C. Power, "Inflammasomes in the CNS," Nature Reviews Neuroscience, vol. 15, no. 2, pp. 84-97, 2014.
17. B. Lu, H. Wang, U. Andersson, and K. J. Tracey, "Regulation of HMGB1 release by inflammasomes," Protein and Cell, vol. 4, no. 3, pp. 163-167, 2013.
18. J. S. Park, D. Svetkauskaite, Q. He et al., "Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein," Journal of Biological Chemistry, vol. 279, no. 9, pp. 7370-7377, 2004.
19. R. Hanayama, M. Tanaka, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata, "Identification of a factor that links apoptotic cells to phagocytes," Nature, vol. 417, no. 6885, pp. 182-187, 2002.
20. M. Righi, L. Mori, G. De Libero et al., "Monokine production by microglial cell clones," European Journal of Immunology, vol. 19, no. 8, pp. 1443-1448, 1989.
21. M. Nikodemova and J. J. Watters, "Outbred ICR/CD1 mice displaymore severe neuroinflammation mediated by microglial TLR4/CD14 activation than inbred C57Bl/6 mice," Neuroscience, vol. 190, pp. 67-74, 2011.
22. R. W. Freilich, M. E. Woodbury, and T. Ikezu, "Integrated expression profiles of mRNA and miRNA in polarized primary murine microglia," PLoS ONE, vol. 8, no. 11, Article ID e79416, 2013.
23. X. He, Z. Jing, and G. Cheng, "MicroRNAs: new regulators of Toll-like receptor signalling pathways," BioMed Research International, vol. 2014, Article ID 945169, 14 pages, 2014.
24. E.D. Ponomarev, T. Veremeyko, and H. L. Weiner, "MicroRNAs are universal regulators of differentiation, activation, and polarization of microglia and macrophages in normal and diseased CNS," GLIA, vol. 61, no. 1, pp. 91-103, 2013.
25. M. Jiang, Y. Xiang, D. Wang et al., "Dysregulated expression of miR-146a contributes to age-related dysfunction of macrophages," Aging Cell, vol. 11, no. 1, pp. 29-40, 2012.
26. T. Veremeyko, S. Siddiqui, I. Sotnikov, A. Yung, and E. D. Ponomarev, "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, vol. 8, no. 12, Article IDe81774, 2013.
27. D. Brites and A. Fernandes, "Neuroinflammation and depression: microglia activation, extracellular microvesicles and microRNA dysregulation," Frontiers in Cellular Neuroscience, vol. 9, article no. 476, pp. 1-20, 2015.
28. A. Aryani and B. Denecke, "Exosomes as a nanodelivery system: a key to the future of neuromedicine?"Molecular Neurobiology, vol. 53, no. 2, pp. 818-834, 2016.
29. A. Gustin, M. Kirchmeyer, E. Koncina et al., "NLRP3 inflammasome is expressed and functional in mouse brain microglia but not in astrocytes," PLoS ONE, vol. 10, no. 6, Article IDe0130624, 2015.
30. S. M. Burm, E. A. Zuiderwijk-Sick, A. E. J. T Jong et al., "Inflammasome-induced IL-1β secretion in microglia is characterized by delayed kinetics and is only partially dependent on inflammatory caspases," Journal of Neuroscience, vol. 35, no. 2, pp. 678-687, 2015.
31. D. J. Ksiazek-Winiarek, M. J. Kacperska, and A. Glabinski, "MicroRNAs as novel regulators of neuroinflammation," Mediators of inflammation, vol. 2013, Article ID172351, 11 pages, 2013.
32. M. Alexander, R. Hu, M. C. Runtsch et al., "Exosome-delivered microRNAs modulate the inflammatory response to endotoxin," Nature Communications, vol. 6, article 7321, 2015.
33. Y.-H. Cui, Y. Le, W. Gong et al., "Bacterial lipopolysaccharide selectively up-regulates the function of the chemotactic peptide receptor formyl peptide receptor 2 in murine microglial cells," The Journal of Immunology, vol. 168, no. 1, pp. 434-442, 2002.
34. A. Barateiro, A. R. Vaz, S. L. Silva, A. Fernandes, and D. Brites, "ER stress, mitochondrial dysfunction and calpain/JNK activation are involved in oligodendrocyte precursor cell death by unconjugated bilirubin," Neuro Molecular Medicine, vol. 14, no. 4, pp. 285-302, 2012.
35. A. Barateiro, V. E. Miron, S. D. Santos et al., "Unconjugated bilirubin restricts oligodendrocyte differentiation and axonal myelination," Molecular neurobiology, vol. 47, no. 2, pp. 632-644, 2013.
36. A. L. Cardoso, J. R. Guedes, L. Pereira de Almeida, and M. C. Pedroso de Lima, "miR-155 modulates microglia-mediated immune response by down-regulating SOCS-1 and promoting cytokine and nitric oxide production," Immunology, vol. 135, no. 1, pp. 73-88, 2012.
37. A. Fernandes, A. S. Falcão, R. F. M. Silva et al., "Inflammatory signalling pathways involved in astroglial activation by unconjugated bilirubin," Journal of Neurochemistry, vol. 96, no. 6, pp. 1667-1679, 2006.
38. D. Kurpius, N. Wilson, L. Fuller, A. Hoffman, and M. E. Dailey, "Early activation, motility, and homing of neonatal microglia to injured neurons does not require protein synthesis," GLIA, vol. 54, no. 1, pp. 58-70, 2006.
39. C. Caldeira, A. F. Oliveira, C. Cunha et al., "Microglia change from a reactive to an age-like phenotype with the time in culture," Frontiers in Cellular Neuroscience, vol. 8, article no. 152, 2014.
40. S. L. Silva, C. Osório, A. R. Vaz et al., "Dynamics of neuron-glia interplay upon exposure to unconjugated bilirubin," Journal of Neurochemistry, vol. 117, no. 3, pp. 412-424, 2011.
41. S. L. Silva, A. R. Vaz, A. Barateiro et al., "Features of bilirubininduced reactive microglia: from phagocytosis to inflammation," Neurobiology of Disease, vol. 40, no. 3, pp. 663-675, 2010.
42. A. Fernandes, A. S. Falcão, R. F. M. Silva, M. A. Brito, and D. Brites, "MAPKs are key players in mediating cytokine release and cell death induced by unconjugated bilirubin in cultured rat cortical astrocytes," European Journal of Neuroscience, vol. 25, no. 4, pp. 1058-1068, 2007.
43. K. Wang, S. Zhang, J. Weber, D. Baxter, and D. J. Galas, "Export of microRNAs and microRNA-protective protein by mammalian cells," Nucleic Acids Research, vol. 38, no. 20, pp. 7248-7259, 2010.
44. W. J. Streit, S. A. Walter, and N. A. Pennell, "Reactivemicrogliosis," Progress in Neurobiology, vol. 57, no. 6, pp. 563-581, 1999.
45. H. Mashimo, N. Ohguro, S. Nomura, N. Hashida, K. Nakai, and Y. Tano, "Neutrophil chemotaxis and local expression of interleukin-10 in the tolerance of endotoxin-induced uveitis," Investigative Ophthalmology and Visual Science, vol. 49, no. 12, pp. 5450-5457, 2008.
46. I. Napoli and H. Neumann, "Microglial clearance function in health and disease," Neuroscience, vol. 158, no. 3, pp. 1030-1038, 2009.
47. F. G. Bauernfeind, G. Horvath, A. Stutz et al., "Cutting edge: NF-κB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression," The Journal of Immunology, vol. 183, no. 2, pp. 787-791, 2009.
48. R. T. Liu, A. Wang, E. To et al., "Vinpocetine inhibits amyloidbeta induced activation of NF-κB, NLRP3 inflammasome and cytokine production in retinal pigment epithelial cells," Experimental Eye Research, vol. 127, pp. 49-58, 2014.
49. H.-M. Lee, J. Kang, S. J. Lee, and E.-K. Jo, "Microglial activation of the NLRP3 inflammasome by the priming signals derived frommacrophages infected with mycobacteria," Glia, vol. 61, no. 3, pp. 441-452, 2013.
50. A. Falcão, L. A. R. Carvalho, G. Lidónio et al., "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.
51. A. Halle, V. Hornung, G. C. Petzold et al., "The NALP3 inflammasome is involved in the innate immune response to amyloid-β,"Nature Immunology, vol. 9, no. 8, pp. 857-865, 2008.
52. M. Fanjul-Fernández, A. R. Folgueras, S. Cabrera, and C. López-Otín, "Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models," Biochimica et Biophysica Acta-Molecular Cell Research, vol. 1803, no. 1, pp. 3-19, 2010.
53. H.-M. Gao, H. Zhou, F. Zhang, B. C. Wilson, W. Kam, and J.- S. Hong, "HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration," Journal of Neuroscience, vol. 31, no. 3, pp. 1081-1092, 2011.
54. J.-B. Kim, S. C. Joon, Y.-M. Yu et al., "HMGB1, a novel cytokinelike mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain," Journal of Neuroscience, vol. 26, no. 24, pp. 6413-6421, 2006.
55. J.-B. Kim, C.-M. Lim, Y.-M. Yu, and J.-K. Lee, "Induction and subcellular localization of high-mobility group box-1 (HMGB1) in the postischemic rat brain," Journal of Neuroscience Research, vol. 86, no. 5, pp. 1125-1131, 2008.
56. D. Wu, C. Cerutti, M. A. Lopez-Ramirez et al., "Brain endothelial miR-146a negatively modulates T-cell adhesion through repressingmultiple targets to inhibit NF-κB activation," Journal of Cerebral Blood Flow and Metabolism, vol. 35, no. 3, pp. 412-423, 2015.
57. S. Zhao, L. Zhang, G. Lian et al., "Sildenafil attenuates LPSinduced pro-inflammatory responses through down-regulation of intracellular ROS-related MAPK/NF-κB signaling pathways in N9 microglia," International Immunopharmacology, vol. 11, no. 4, pp. 468-474, 2011.
58. G. Zhang, J.-L. He, X.-Y. Xie, and C. Yu, "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, vol. 30, no. 3, pp. 561-568, 2012.
59. X. Lu, L. Ma, L. Ruan et al., "Resveratrol differentially modulates inflammatory responses of microglia and astrocytes," Journal of Neuroinflammation, vol. 7, article 46, 2010.
60. A. J. Bruce-Keller, J. L. Keeling, J. N. Keller, F. F. Huang, S. Camondola, and M. P. Mattson, "Antiinflammatory effects of estrogen on microglial activation," Endocrinology, vol. 141, no. 10, pp. 3646-3656, 2000.
61. R. Shechter, O. Miller, G. Yovel et al., "Recruitment of Beneficial M2 Macrophages to Injured Spinal Cord Is Orchestrated by Remote Brain Choroid Plexus," Immunity, vol. 38, no. 3, pp. 555-569, 2013.
62. E.W.G.M. Boddeke, I. Meigel, S. Frentzel, K. Biber, L. Q. Renn, and P. Gebicke-Härter, "Functional expression of the fractalkine (CX3C) receptor and its regulation by lipopolysaccharide in rat microglia," European Journal of Pharmacology, vol. 374, no. 2, pp. 309-313, 1999.
63. A. Pachot, M.-A. Cazalis, F. Venet et al., "Decreased expression of the fractalkine receptor CX3CR1 on circulating monocytes as new feature of sepsis-induced immunosuppression," Journal of Immunology, vol. 180, no. 9, pp. 6421-6429, 2008.
64. S. Jose, S. W. Tan, Y. Y. Ooi, R. Ramasamy, and S. Vidyadaran, "Mesenchymal stem cells exert anti-proliferative effect on lipopolysaccharide-stimulated BV2 microglia by reducing tumour necrosis factor-α levels," Journal of Neuroinflammation, vol. 11, no. 1, article 149, 2014.
65. Z. Chen, W. Jalabi, K. B. Shpargel et al., "Lipopolysaccharide-induced microglial activation and neuroprotection against experimental brain injury is independent of hematogenous TLR4," Journal of Neuroscience, vol. 32, no. 34, pp. 11706-11715, 2012.
66. T. Li, S. Pang, Y. Yu, X. Wu, J. Guo, and S. Zhang, "Proliferation of parenchymal microglia is the main source of microgliosis after ischaemic stroke," Brain: A Journal Of Neurology, vol. 136, pp. 3578-3588, 2013.
67. 2A receptor mediates microglial process retraction," Nature Neuroscience, vol. 12, no. 7, pp. 872-878, 2009.
68. S. E. Haynes, G. Hollopeter, G. Yang et al., "The P2Y12 receptor regulates microglial activation by extracellular nucleotides," Nature Neuroscience, vol. 9, no. 12, pp. 1512-1519, 2006.
69. i/o-coupled P2Y receptors," The Journal of Neuroscience, vol. 21, no. 6, pp. 1975-1982, 2001.
70. S. Lively and L. C. Schlichter, "The microglial activation state regulates migration and roles of matrix-dissolving enzymes for invasion," Journal of Neuroinflammation, vol. 10, article 75, 2013.
71. H. Scheiblich, F. Roloff, V. Singh, M. Stangel, M. Stern, and G. Bicker, "Nitric oxide/cyclic GMP signaling regulates motility of a microglial cell line and primary microglia in vitro," Brain Research, vol. 1564, pp. 9-21, 2014.
72. A. A. Babcock, W. A. Kuziel, S. Rivest, and T. Owens, "Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS," Journal of Neuroscience, vol. 23, no. 21, pp. 7922-7930, 2003.
73. P. Majerova, M. Zilkova, Z. Kazmerova et al., "Microglia display modest phagocytic capacity for extracellular tau oligomers," Journal of Neuroinflammation, vol. 11, no. 1, article 161, 2014.
74. M. Fricker, J. J. Neher, J.-W. Zhao, C. Théry, A. M. Tolkovsky, and G. C. Brown, "MFG-E8 mediates primary phagocytosis of viable neurons during neuroinflammation," The Journal of Neuroscience, vol. 32, no. 8, pp. 2657-2666, 2012.
75. B. Spittau, J. Rilka, E. Steinfath, T. Zöller, and K. Krieglstein, "TGFβ1 increases microglia-mediated engulfment of apoptotic cells via upregulation of the milk fat globule-EGF factor 8," GLIA, vol. 63, no. 1, pp. 142-153, 2015.
76. H. Komura, M. Miksa, R. Wu, S. M. Goyert, and P. Wang, "Milk fat globule epidermal growth factor-factor VIII is downregulated in sepsis via the lipopolysaccharide-CD14 pathway," The Journal of Immunology, vol. 182, no. 1, pp. 581-587, 2009.
77. Y. Liu, X. Yang, C. Guo, P. Nie, Y. Liu, and J. Ma, "Essential role of MFG-E8 for phagocytic properties of microglial cells," PLoS ONE, vol. 8, no. 2, Article ID e55754, 2013.
78. R. Hanamsagar, V. Torres, and T. Kielian, "Inflammasome activation and IL-1β/IL-18 processing are influenced by distinct pathways in microglia," Journal of Neurochemistry, vol. 119, no. 4, pp. 736-748, 2011.
79. E.-J. Lee and H.-S. Kim, "Inhibitorymechanism of MMP-9 gene expression by ethyl pyruvate in lipopolysaccharide-stimulated BV2 microglial cells," Neuroscience Letters, vol. 493, no. 1-2, pp. 38-43, 2011.
80. Y. Bai, Z. Zhu, Z. Gao, and Y. Kong, "TLR2 signaling directs NO-dependent MMP-9 induction in mouse microglia," Neuroscience Letters, vol. 571, pp. 5-10, 2014.
81. K.-O. Cho, H. O. La, Y.-J. Cho, K.-W. Sung, and S. Y. Kim, "Minocycline attenuates white matter damage in a rat model of chronic cerebral hypoperfusion," Journal of Neuroscience Research, vol. 83, no. 2, pp. 285-291, 2006.
82. C.-X. Wu, H. Sun, Q. Liu, H. Guo, and J.-P. Gong, "LPS induces HMGB1 relocation and release by activating the NF-κB-CBP signal transduction pathway in themurinemacrophage-like cell line RAW264.7," Journal of Surgical Research, vol. 175, no. 1, pp. 88-100, 2012.
83. J. Guedes, A. L. C. Cardoso, and M. C. Pedroso de Lima, "Involvement of microRNA in microglia-mediated immune response," Clinical and Developmental Immunology, vol. 2013, Article ID 186872, 11 pages, 2013.
84. C. S. Cãtaña, G. A. Calin, and I. Berindan-Neagoe, "InflammamiRs in aging and breast cancer: are they reliable players?" Frontiers in Medicine, vol. 2, article article 85, 2015.
85. S. R. Quinn and L. A. O'Neill, "A trio of microRNAs that control Toll-like receptor signalling," International Immunology, vol. 23, no. 7, pp. 421-425, 2011.
86. R. Saba, S. Gushue, R. L. C. H. Huzarewich et al., "MicroRNA 146a (miR-146a) is over-expressed during prion disease and modulates the innate immune response and the microglial activation state," PLoSONE, vol. 7, no. 2, Article IDe30832, 2012.
87. K.D. Taganov, M. P. Boldin, K.-J. Chang, and D. Baltimore, "NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses," Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 33, pp. 12481-12486, 2006.
88. M. A. Nahid, K. M. Pauley, M. Satoh, and E. K. L. Chan, "miR-146a is critical for endotoxin-induced tolerance: implication in innate immunity," Journal of Biological Chemistry, vol. 284, no. 50, pp. 34590-34599, 2009.
89. E. D. Ponomarev, T. Veremeyko, N. Barteneva, A. M. Krichevsky, and H. L. Weiner, "MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α-PU.1 pathway," Nature Medicine, vol. 17, no. 1, pp. 64-70, 2011.
90. H. L.D. M. Willemen, X.-J. Huo, Q.-L. Mao-Ying, J. Zijlstra, C. J. Heijnen, and A. Kavelaars, "MicroRNA-124 as a novel treatment for persistent hyperalgesia," Journal of Neuroinflammation, vol. 9, article 143, 2012.