MicroRNAs mediating CNS inflammation: Small regulators with powerful potential

Brain, Behavior, and Immunity

Volumn 52, Issue , 2016, Pages 1-8

  Su, Wei ^a   Aloi, Macarena S ^a   Garden, Gwenn A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

C Maf; MicroRNA; MiR 146a; MiR 155; Neuroinflammation; P53; Presenilin 2

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MICRORNA; MICRORNA 124; MICRORNA 125B 5P; MICRORNA 145; MICRORNA 146A; MICRORNA 146B; MICRORNA 155; MICRORNA 19; MICRORNA 212; MICRORNA 223; MICRORNA 32; MICRORNA 342 3P; MICRORNA 34A; MICRORNA 376A; MICRORNA 434; MICRORNA 689; MICRORNA 711; MICRORNA 99A; PROTEIN P53; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

3' UNTRANSLATED REGION; CELL ACTIVATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ASSOCIATION; HUMAN; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MICROGLIA; NEGATIVE FEEDBACK; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CENTRAL NERVOUS SYSTEM DISEASE; CEREBROSPINAL FLUID; GENETICS; INFLAMMATION; METABOLISM;

ANIMALS; BIOMARKERS; CENTRAL NERVOUS SYSTEM DISEASES; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; MICROGLIA; MICRORNAS;

EID: 84953348402     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.07.003     Document Type: Review

References (68)

1. Alexandrov P.N., Dua P., Lukiw W.J. Up-regulation of miRNA-146a in progressive, age-related inflammatory neurodegenerative disorders of the human CNS. Front. Neurol. 2014, 5.
2. Arora S., Rana R., Chhabra A., Jaiswal A., Rani V. miRNA-transcription factor interactions: a combinatorial regulation of gene expression. Mol. Genet. Genomics 2013, 288:77-87.
3. Bala S., Marcos M., Kodys K., Csak T., Catalano D., Mandrekar P., Szabo G. Up-regulation of microRNA-155 in macrophages contributes to increased tumor necrosis factor α (TNFα) production via increased mRNA half-life in alcoholic liver disease. J. Biol. Chem. 2011, 286:1436-1444.
4. Baltimore D., Boldin M.P., O'Connell R.M., Rao D.S., Taganov K.D. MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 2008, 9:839-845.
5. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
6. Baumjohann D., Ansel K.M. MicroRNA-mediated regulation of T helper cell differentiation and plasticity. Nat. Rev. Immunol. 2013, 13:666-678.
7. Bird L. Immune regulation: microRNAs keep microglia quiet. Nat. Rev. Immunol. 2011, 11:76-77.
8. Boldin M.P., Taganov K.D., Rao D.S., Yang L., Zhao J.L., Kalwani M., Garcia-Flores Y., Luong M., Devrekanli A., Xu J., Sun G., Tay J., Linsley P.S., Baltimore D. miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J. Exp. Med. 2011, 208:1189-1201.
9. 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., Fanek Z., Liu L., Chen Z., Rothstein J.D., Ransohoff R.M., Gygi S.P., Antel J.P., Weiner H.L. Identification of a unique TGF-[beta]-dependent molecular and functional signature in microglia. Nat. Neurosci. 2014, 17:131-143.
10. Butovsky O., Jedrychowski M.P., Cialic R., Krasemann S., Murugaiyan G., Fanek Z., Greco D.J., Wu P.M., Doykan C.E., Kiner O., et al. Targeting miR-155 restores abnormal microglia and attenuates disease in SOD1 mice. Ann. Neurol. 2015, 77:75-79.
11. Caldeira C., Oliveira A.F., Cunha C., Vaz A.R., Falcão A.S., Fernandes A., Brites D. Microglia change from a reactive to an age-like phenotype with the time in culture. Front. Cell. Neurosci. 2014, 8.
12. Cardoso A., Guedes J., Pereira de Almeida L., Pedroso de Lima M. miR-155 modulates microglia-mediated immune response by down-regulating SOCS-1 and promoting cytokine and nitric oxide production. Immunology 2012, 135:73-88.
13. Cardoso A.L., Guedes J.R., Pereira de Almeida L., Pedroso de Lima M.C. miR-155 modulates microglia-mediated immune response by down-regulating SOCS-1 and promoting cytokine and nitric oxide production. Immunology 2012, 135:73-88.
14. Carson M.J., Reilly C.R., Sutcliffe J.G., Lo D. Mature microglia resemble immature antigen-presenting cells. Glia 1998, 22:72-85.
15. Chen X., Gong J., Zeng H., Chen N., Huang R., Huang Y., Nie L., Xu M., Xia J., Zhao F., Meng W., Zhou Q. MicroRNA145 targets BNIP3 and suppresses prostate cancer progression. Cancer Res. 2010, 70:2728-2738.
16. Cui J.G., Li Y.Y., Zhao Y., Bhattacharjee S., Lukiw W.J. Differential regulation of interleukin-1 receptor-associated kinase-1 (IRAK-1) and IRAK-2 by microRNA-146a and NF-κB in stressed human astroglial cells and in Alzheimer disease. J. Biol. Chem. 2010, 285:38951-38960.
17. De Strooper B., Iwatsubo T., Wolfe M.S. Presenilins and γ-secretase: structure, function, and role in Alzheimer disease. Cold Spring Harb. Perspect. Med. 2012, 2:a006304.
18. Dharap A., Bowen K., Place R., Li L.-C., Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral MicroRNAome. J. Cereb. Blood Flow Metab. 2009, 29:675-687.
19. Eis P.S., Tam W., Sun L., Chadburn A., Li Z., Gomez M.F., Lund E., Dahlberg J.E. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:3627-3632.
20. Elton T.S., Selemon H., Elton S.M., Parinandi N.L. Regulation of the miR155 host gene in physiological and pathological processes. Gene 2013, 532:1-12.
21. Freilich R.W., Woodbury M.E., Ikezu T. Integrated expression profiles of mRNA and miRNA in polarized primary murine microglia. PLoS ONE 2013, 8:e79416.
22. Ha M., Kim V.N. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 2014, 15:509-524.
23. 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. 2013, 16:1896-1905.
24. Hu Y.-L., Fong S., Largman C., Shen W.-F. HOXA9 regulates miR-155 in hematopoietic cells. Nucleic Acids Res. 2010, 38:5472-5478.
25. Iyer A., Zurolo E., Prabowo A., Fluiter K., Spliet W.G.M., van Rijen P.C., Gorter J.A., Aronica E. MicroRNA-146a: a key regulator of astrocyte-mediated inflammatory response. PLoS ONE 2012, 7:e44789.
26. Jayadev S., Leverenz J.B., Steinbart E., Stahl J., Klunk W., Yu C.-E., Bird T.D. Alzheimer's disease phenotypes and genotypes associated with mutations in presenilin 2. Brain 2010.
27. Jayadev S., Nesser N.K., Hopkins S., Myers S.J., Case A., Lee R.J., Seaburg L.A., Uo T., Murphy S.P., Morrison R.S., Garden G.A. Transcription factor p53 influences microglial activation phenotype. Glia 2011, 59:1402-1413.
28. Jayadev S., Case A., Alajajian B., Eastman A.J., Möller T., Garden G.A. Presenilin 2 influences miR146 level and activity in microglia. J. Neurochem. 2013, 127:592-599.
29. Jovičić A., Roshan R., Moisoi N., Pradervand S., Moser R., Pillai B., Luthi-Carter R. Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J. Neurosci. 2013, 33:5127-5137.
30. Kent O.A., McCall M.N., Cornish T.C., Halushka M.K. Lessons from miR-143/145: the importance of cell-type localization of miRNAs. Nucleic Acids Res. 2014, 42:7528-7538.
31. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 2009, 29:13435-13444.
32. Kim J., Krichevsky A., Grad Y., Hayes G.D., Kosik K.S., Church G.M., Ruvkun G. Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc. Natl. Acad. Sci. 2004, 101:360-365.
33. Kusuda R., Cadetti F., Ravanelli M., Sousa T., Zanon S., De Lucca F., Lucas G. Differential expression of microRNAs in mouse pain models. Mol. Pain 2011, 7:17.
34. Kynast K.L., Russe O.Q., Möser C.V., Geisslinger G., Niederberger E. Modulation of central nervous system-specific microRNA-124a alters the inflammatory response in the formalin test in mice. Pain® 2013, 154:368-376.
35. Lagos-Quintana M., Rauhut R., Yalcin A., Meyer J., Lendeckel W., Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 2002, 12:735-739.
36. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
37. Li Y.Y., Cui J.G., Dua P., Pogue A.I., Bhattacharjee S., Lukiw W.J. Differential expression of miRNA-146a-regulated inflammatory genes in human primary neural, astroglial and microglial cells. Neurosci. Lett. 2011, 499:109-113.
38. Lorente-Cebrián S., Mejhert N., Kulyté A., Laurencikiene J., Åström G., Hedén P., Rydén M., Arner P. MicroRNAs regulate human adipocyte lipolysis: effects of miR-145 are linked to TNF-α. PLoS ONE 2014, 9:e86800.
39. Lukiw W.J., Zhao Y., Cui J.G. An NF-κB-sensitive micro RNA-146a-mediated inflammatory circuit in Alzheimer disease and in stressed human brain cells. J. Biol. Chem. 2008, 283:31315-31322.
40. Lynch M. The multifaceted profile of activated microglia. Mol. Neurobiol. 2009, 40:139-156.
41. Marín-Teva J.L., Dusart I., Colin C., Gervais A., van Rooijen N., Mallat M. Microglia promote the death of developing purkinje cells. Neuron 2004, 41:535-547.
42. Mashima R. Physiological roles of miR-155. Immunology 2015, n/a-n/a.
43. Megiorni F., Cialfi S., Cimino G., De Biase R.V., Dominici C., Quattrucci S., Pizzuti A. Elevated levels of miR-145 correlate with SMAD3 down-regulation in Cystic Fibrosis patients. J. Cyst. Fibros. 2013, 12:797-802.
44. Motohashi H., Shavit J.A., Igarashi K., Yamamoto M., Engel J.D. The world according to Maf. Nucleic Acids Res. 1997, 25:2953-2959.
45. Murugaiyan G., Beynon V., Mittal A., Joller N., Weiner H.L. Silencing microRNA-155 ameliorates experimental autoimmune encephalomyelitis. J. Immunol. 2011, 187:2213-2221.
46. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
47. Norden D.M., Godbout J.P. Review: microglia of the aged brain: primed to be activated and resistant to regulation. Neuropathol. Appl. Neurobiol. 2013, 39:19-34.
48. O'Connell R.M., Rao D.S., Chaudhuri A.A., Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 2010, 10:111-122.
49. Paolicelli R.C., Bolasco G., Pagani F., Maggi L., Scianni M., Panzanelli P., Giustetto M., Ferreira T.A., Guiducci E., Dumas L., Ragozzino D., Gross C.T. Synaptic pruning by microglia is necessary for normal brain development. Science 2011, 333:1456-1458.
50. Pareek S., Roy S., Kumari B., Jain P., Banerjee A., Vrati S. miR-155 induction in microglial cells suppresses Japanese encephalitis virus replication and negatively modulates innate immune responses. J. Neuroinflammation 2014, 11:97.
51. Ponomarev E.D., Veremeyko T., Barteneva N., Krichevsky A.M., Weiner H.L. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-[alpha]-PU.1 pathway. Nat. Med. 2011, 17:64-70.
52. 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, 61:91-103.
53. Rathod S.S., Rani S.B., Khan M., Muzumdar D., Shiras A. Tumor suppressive miRNA-34a suppresses cell proliferation and tumor growth of glioma stem cells by targeting Akt and Wnt signaling pathways. FEBS Open Bio 2014, 4:485-495.
54. Rodriguez A., Vigorito E., Clare S., Warren M.V., Couttet P., Soond D.R., van Dongen S., Grocock R.J., Das P.P., Miska E.A., Vetrie D., Okkenhaug K., Enright A.J., Dougan G., Turner M., Bradley A. Requirement of bic/microRNA-155 for normal immune function. Science 2007, 316:608-611.
55. Scheffel J., Regen T., Van Rossum D., Seifert S., Ribes S., Nau R., Parsa R., Harris R.A., Boddeke H.W.G.M., Chuang H.-N., Pukrop T., Wessels J.T., Jürgens T., Merkler D., Brück W., Schnaars M., Simons M., Kettenmann H., Hanisch U.-K. Toll-like receptor activation reveals developmental reorganization and unmasks responder subsets of microglia. Glia 2012, 60:1930-1943.
56. Sharabi A.B., Aldrich M., Sosic D., Olson E.N., Friedman A.D., Lee S.-H., Chen S.-Y. Twist-2 controls myeloid lineage development and function. PLoS Biol. 2008, 6:e316.
57. Sierra A., Encinas J.M., Deudero J.J.P., Chancey J.H., Enikolopov G., Overstreet-Wadiche L.S., Tsirka S.E., Maletic-Savatic M. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010, 7:483-495.
58. Su W., Hopkins S., Nesser N.K., Sopher B., Silvestroni A., Ammanuel S., Jayadev S., Möller T., Weinstein J., Garden G.A. The p53 transcription factor modulates microglia behavior through microRNA-dependent regulation of c-Maf. J. Immunol. 2014, 192:358-366.
59. Tremblay M.-È., Lowery R.L., Majewska A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 2010, 8:e1000527.
60. Wake H., Moorhouse A.J., Jinno S., Kohsaka S., Nabekura J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 2009, 29:3974-3980.
61. Wang P., Hou J., Lin L., Wang C., Liu X., Li D., Ma F., Wang Z., Cao X. Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J. Immunol. 2010, 185:6226-6233.
62. Wang C.-Y., Yang S.-H., Tzeng S.-F. MicroRNA-145 as one negative regulator of astrogliosis. Glia 2015, 63:194-205.
63. Weigelt K., Bergink V., Burgerhout K.M., Pescatori M., Wijkhuijs A., Drexhage H.A. Down-regulation of inflammation-protective microRNAs 146a and 212 in monocytes of patients with postpartum psychosis. Brain Behav. Immun. 2013, 29:147-155.
64. Weinstein J.R., Koerner I.P., Möller T. Microglia in ischemic brain injury. Future Neurol. 2010, 5:227-246.
65. Witwer K.W., Sisk J.M., Gama L., Clements J.E. MicroRNA regulation of IFN-β protein expression: rapid and sensitive modulation of the innate immune response. J. Immunol. 2010, 184:2369-2376.
66. Yang C.-S., Lee H.-M., Lee J.-Y., Kim J.-A., Lee S.J., Shin D.-M., Lee Y.-H., Lee D.-S., El-Benna J., Jo E.-K. Reactive oxygen species and p47phox activation are essential for the Mycobacterium tuberculosis-induced pro-inflammatory response in murine microglia. J. Neuroinflammation 2007, 4:27.
67. Zeng L., Liu J., Wang Y., Wang L., Weng S., Tang Y., Zheng C., Cheng Q., Chen S., Yang G.-Y. MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Front. Biosci. (Elite Ed.) 2011, 3:1265-1272.
68. Zhao J.L., Rao D.S., O'Connell R.M., Garcia-Flores Y., Baltimore D. MicroRNA-146a acts as a guardian of the quality and longevity of hematopoietic stem cells in mice. Elife 2013.