Diverging mRNA and Protein Networks in Activated Microglia Reveal SRSF3 Suppresses Translation of Highly Upregulated Innate Immune Transcripts

Cell Reports

Volumn 21, Issue 11, 2017, Pages 3220-3233

  Boutej, Hejer ^a   Rahimian, Reza ^a   Thammisetty, Sai Sampath ^a   Béland, Louis Charles ^a   Lalancette Hébert, Mélanie ^a   Kriz, Jasna ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

innate immune response; microglia; microglia proteomics; translatome profiling

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MESSENGER RNA; RNA BINDING PROTEIN; SERINE ARGININE RICH SPLICING FACTOR 3 PROTEIN; UNCLASSIFIED DRUG; PROTEIN BINDING; SERINE ARGININE RICH SPLICING FACTOR; SRSF3 PROTEIN, MOUSE;

3' UNTRANSLATED REGION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CELL ACTIVATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; IN VIVO STUDY; INNATE IMMUNITY; MALE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RIBOSOME; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; BRAIN CORTEX; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; IMMUNOLOGY; PATHOLOGY;

ANIMALS; BINDING SITES; CEREBRAL CORTEX; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; SERINE-ARGININE SPLICING FACTORS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 85037865324     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.11.058     Document Type: Article

References (48)

1. Anderson, P., Post-transcriptional regulons coordinate the initiation and resolution of inflammation. Nat. Rev. Immunol. 10 (2010), 24–35.
2. Beutner, C., Linnartz-Gerlach, B., Schmidt, S.V., Beyer, M., Mallmann, M.R., Staratschek-Jox, A., Schultze, J.L., Neumann, H., Unique transcriptome signature of mouse microglia. Glia 61 (2013), 1429–1442.
3. Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W.H., Pagès, F., Trajanoski, Z., Galon, J., ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25 (2009), 1091–1093.
4. Bindea, G., Galon, J., Mlecnik, B., CluePedia Cytoscape plugin: pathway insights using integrated experimental and in silico data. Bioinformatics 29 (2013), 661–663.
5. Butovsky, O., Jedrychowski, M.P., Moore, C.S., Cialic, R., Lanser, A.J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P.M., Doykan, C.E., et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 17 (2014), 131–143.
6. Cao, J., Geballe, A.P., Inhibition of nascent-peptide release at translation termination. Mol. Cell. Biol. 16 (1996), 7109–7114.
7. Carpenter, S., Fitzgerald, K.A., Transcription of inflammatory genes: long noncoding RNA and beyond. J. Interferon Cytokine Res. 35 (2015), 79–88.
8. Carpenter, S., Ricci, E.P., Mercier, B.C., Moore, M.J., Fitzgerald, K.A., Post-transcriptional regulation of gene expression in innate immunity. Nat. Rev. Immunol. 14 (2014), 361–376.
9. Chen, Z., Trapp, B.D., Microglia and neuroprotection. J. Neurochem. 136:Suppl 1 (2016), 10–17.
10. Chen, Z., Jalabi, W., Shpargel, K.B., Farabaugh, K.T., Dutta, R., Yin, X., Kidd, G.J., Bergmann, C.C., Stohlman, S.A., Trapp, B.D., Lipopolysaccharide-induced microglial activation and neuroprotection against experimental brain injury is independent of hematogenous TLR4. J. Neurosci. 32 (2012), 11706–11715.
11. Ciafrè S.A., Galardi, S., microRNAs and RNA-binding proteins: a complex network of interactions and reciprocal regulations in cancer. RNA Biol. 10 (2013), 935–942.
12. Danoff, T.M., Lalley, P.A., Chang, Y.S., Heeger, P.S., Neilson, E.G., Cloning, genomic organization, and chromosomal localization of the Scya5 gene encoding the murine chemokine RANTES. J. Immunol. 152 (1994), 1182–1189.
13. David, S., Kroner, A., Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 12 (2011), 388–399.
14. Doyle, J.P., Dougherty, J.D., Heiman, M., Schmidt, E.F., Stevens, T.R., Ma, G., Bupp, S., Shrestha, P., Shah, R.D., Doughty, M.L., et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135 (2008), 749–762.
15. Flo, T.H., Smith, K.D., Sato, S., Rodriguez, D.J., Holmes, M.A., Strong, R.K., Akira, S., Aderem, A., Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432 (2004), 917–921.
16. Gao, B., Roux, P.P., Translational control by oncogenic signaling pathways. Biochim. Biophys. Acta 1849 (2015), 753–765.
17. Glisovic, T., Bachorik, J.L., Yong, J., Dreyfuss, G., RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 582 (2008), 1977–1986.
18. Gowing, G., Vallières, L., Julien, J.P., Mouse model for ablation of proliferating microglia in acute CNS injuries. Glia 53 (2006), 331–337.
19. Gravel, M., Béland, L.C., Soucy, G., Abdelhamid, E., Rahimian, R., Gravel, C., Kriz, J., IL-10 Controls Early Microglial Phenotypes and Disease Onset in ALS Caused by Misfolded Superoxide Dismutase 1. J. Neurosci. 36 (2016), 1031–1048.
20. Hanisch, U.K., Kettenmann, H., Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10 (2007), 1387–1394.
21. Heiman, M., Schaefer, A., Gong, S., Peterson, J.D., Day, M., Ramsey, K.E., Suárez-Fariñas, M., Schwarz, C., Stephan, D.A., Surmeier, D.J., et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 135 (2008), 738–748.
22. Hickman, S.E., Kingery, N.D., Ohsumi, T.K., Borowsky, M.L., Wang, L.C., Means, T.K., El Khoury, J., The microglial sensome revealed by direct RNA sequencing. Nat. Neurosci. 16 (2013), 1896–1905.
23. Jiang, P., Coller, H., Functional interactions between microRNAs and RNA binding proteins. MicroRNA 1 (2012), 70–79.
24. Jin, M., Jang, E., Suk, K., Lipocalin-2 Acts as a Neuroinflammatogen in Lipopolysaccharide-injected Mice. Exp. Neurobiol. 23 (2014), 155–162.
25. Kierdorf, K., Prinz, M., Factors regulating microglia activation. Front. Cell. Neurosci., 7, 2013, 44.
26. Kim, J.H., Park, K.W., Lee, E.W., Jang, W.S., Seo, J., Shin, S., Hwang, K.A., Song, J., Suppression of PPARγ through MKRN1-mediated ubiquitination and degradation prevents adipocyte differentiation. Cell Death Differ. 21 (2014), 594–603.
27. Laflamme, N., Soucy, G., Rivest, S., Circulating cell wall components derived from gram-negative, not gram-positive, bacteria cause a profound induction of the gene-encoding Toll-like receptor 2 in the CNS. J. Neurochem. 79 (2001), 648–657.
28. Lalancette-Hébert, M., Gowing, G., Simard, A., Weng, Y.C., Kriz, J., Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 27 (2007), 2596–2605.
29. Lalancette-Hébert, M., Phaneuf, D., Soucy, G., Weng, Y.C., Kriz, J., Live imaging of Toll-like receptor 2 response in cerebral ischaemia reveals a role of olfactory bulb microglia as modulators of inflammation. Brain 132 (2009), 940–954.
30. Lalancette-Hébert, M., Julien, C., Cordeau, P., Bohacek, I., Weng, Y.C., Calon, F., Kriz, J., Accumulation of dietary docosahexaenoic acid in the brain attenuates acute immune response and development of postischemic neuronal damage. Stroke 42 (2011), 2903–2909.
31. Lalancette-Hébert, M., Swarup, V., Beaulieu, J.M., Bohacek, I., Abdelhamid, E., Weng, Y.C., Sato, S., Kriz, J., Galectin-3 is required for resident microglia activation and proliferation in response to ischemic injury. J. Neurosci. 32 (2012), 10383–10395.
32. Lee, S., Jha, M.K., Suk, K., Lipocalin-2 in the Inflammatory Activation of Brain Astrocytes. Crit. Rev. Immunol. 35 (2015), 77–84.
33. Madeddu, S., Woods, T.A., Mukherjee, P., Sturdevant, D., Butchi, N.B., Peterson, K.E., Identification of Glial Activation Markers by Comparison of Transcriptome Changes between Astrocytes and Microglia following Innate Immune Stimulation. PLoS ONE, 10, 2015, e0127336.
34. Manley, J.L., Krainer, A.R., A rational nomenclature for serine/arginine-rich protein splicing factors (SR proteins). Genes Dev. 24 (2010), 1073–1074.
35. Medzhitov, R., Horng, T., Transcriptional control of the inflammatory response. Nat. Rev. Immunol. 9 (2009), 692–703.
36. Mino, T., Murakawa, Y., Fukao, A., Vandenbon, A., Wessels, H.H., Ori, D., Uehata, T., Tartey, S., Akira, S., Suzuki, Y., et al. Regnase-1 and Roquin Regulate a Common Element in Inflammatory mRNAs by Spatiotemporally Distinct Mechanisms. Cell 161 (2015), 1058–1073.
37. Misteli, T., Spector, D.L., Protein phosphorylation and the nuclear organization of pre-mRNA splicing. Trends Cell Biol. 7 (1997), 135–138.
38. Nilson, S.E., Assmann, S.M., The control of transpiration. Insights from Arabidopsis. Plant Physiol. 143 (2007), 19–27.
39. O'Brien, K.D., Chait, A., Serum amyloid A: the “other” inflammatory protein. Curr. Atheroscler. Rep. 8 (2006), 62–68.
40. Paz, I., Kosti, I., Ares, M. Jr., Cline, M., Mandel-Gutfreund, Y., RBPmap: a web server for mapping binding sites of RNA-binding proteins. Nucleic Acids Res. 42 (2014), W361–367.
41. Prinz, M., Priller, J., Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat. Rev. Neurosci. 15 (2014), 300–312.
42. Ransohoff, R.M., Brown, M.A., Innate immunity in the central nervous system. J. Clin. Invest. 122 (2012), 1164–1171.
43. Schwartz, M., Shechter, R., Systemic inflammatory cells fight off neurodegenerative disease. Nat. Rev. Neurol. 6 (2010), 405–410.
44. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., Ideker, T., Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13 (2003), 2498–2504.
45. Sharma, K., Schmitt, S., Bergner, C.G., Tyanova, S., Kannaiyan, N., Manrique-Hoyos, N., Kongi, K., Cantuti, L., Hanisch, U.K., Philips, M.A., et al. Cell type- and brain region-resolved mouse brain proteome. Nat. Neurosci. 18 (2015), 1819–1831.
46. Sonenberg, N., Hinnebusch, A.G., Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136 (2009), 731–745.
47. Tremblay, M.E., Stevens, B., Sierra, A., Wake, H., Bessis, A., Nimmerjahn, A., The role of microglia in the healthy brain. J. Neurosci. 31 (2011), 16064–16069.
48. Zhang, Y., Chen, K., Sloan, S.A., Bennett, M.L., Scholze, A.R., O'Keeffe, S., Phatnani, H.P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34 (2014), 11929–11947.