MicroRNA 146a (miR-146a) is over-expressed during prion disease and modulates the innate immune response and the microglial activation state

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Saba, Reuben ^a,b   Gushue, Shantel ^a,b   Huzarewich, Rhiannon L C H ^a   Manguiat, Kathy ^a   Medina, Sarah ^a   Robertson, Catherine ^a   Booth, Stephanie A ^a,b  

^a PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JANUS KINASE; MICRORNA; MICRORNA 146A; MITOGEN ACTIVATED PROTEIN KINASE; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; AUTACOID; CYTOKINE; LIPOPOLYSACCHARIDE; MIRN146 MICRORNA, MOUSE; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL LINEAGE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; IMMUNOMODULATION; INNATE IMMUNITY; MICROARRAY ANALYSIS; MICROGLIA; MOUSE; NEUROPATHOLOGY; NONHUMAN; PRION DISEASE; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; CELL LINE; CELL MOTION; CLUSTER ANALYSIS; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; IMMUNOLOGY; KINETICS; METABOLISM; OXIDATIVE PHOSPHORYLATION; PATHOLOGY; PRION; PROTEIN SYNTHESIS; TIME; UPREGULATION;

ANIMALS; BRAIN; CELL LINE; CELL MOVEMENT; CLUSTER ANALYSIS; CYTOKINES; GENE EXPRESSION PROFILING; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; KINETICS; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; MICRORNAS; OXIDATIVE PHOSPHORYLATION; PRION DISEASES; PRIONS; PROTEIN BIOSYNTHESIS; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84857154347     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030832     Document Type: Article

References (55)

1. Prusiner SB, (1998) Prions. Proc Natl Acad Sci U S A 95 (23): 13363-13383.
2. Giese A, Brown DR, Groschup MH, Feldmann C, Haist I, et al. (1998) Role of microglia in neuronal cell death in prion disease. Brain Pathol 8 (3): 449-457.
3. Shepard LW, Yang M, Xie P, Browning DD, Voyno-Yasenetskaya T, et al. (2001) Constitutive activation of NF-kappa B and secretion of interleukin-8 induced by the G protein-coupled receptor of kaposi's sarcoma-associated herpesvirus involve G alpha(13) and RhoA. J Biol Chem 276 (49): 45979-45987.
4. Streit WJ, (2002) Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40 (2): 133-139.
5. Liu B, Hong JS, (2003) Role of microglia in inflammation-mediated neurodegenerative diseases: Mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther 304 (1): 1-7.
6. Ghoshal A, Das S, Ghosh S, Mishra MK, Sharma V, et al. (2007) Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 55 (5): 483-496.
7. Wyss-Coray T, Mucke L, (2002) Inflammation in neurodegenerative disease-a double-edged sword. Neuron 35 (3): 419-432.
8. Cunningham C, Campion S, Lunnon K, Murray CL, Woods JF, et al. (2009) Systemic inflammation induces acute behavioral and cognitive changes and accelerates neurodegenerative disease. Biol Psychiatry 65 (4): 304-312.
9. Sethi S, Lipford G, Wagner H, Kretzschmar H, (2002) Postexposure prophylaxis against prion disease with a stimulator of innate immunity. Lancet 360 (9328): 229-230.
10. Spinner DS, Kascsak RB, Lafauci G, Meeker HC, Ye X, et al. (2007) CpG oligodeoxynucleotide-enhanced humoral immune response and production of antibodies to prion protein PrPSc in mice immunized with 139A scrapie-associated fibrils. J Leukoc Biol 81 (6): 1374-1385.
11. Spinner DS, Cho IS, Park SY, Kim JI, Meeker HC, et al. (2008) Accelerated prion disease pathogenesis in toll-like receptor 4 signaling-mutant mice. J Virol 82 (21): 10701-10708.
12. Prinz M, Heikenwalder M, Schwarz P, Takeda K, Akira S, et al. (2003) Prion pathogenesis in the absence of toll-like receptor signalling. EMBO Rep 4 (2): 195-199.
13. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D, (2010) Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 10 (2): 111-122.
14. Bartel DP, (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116 (2): 281-297.
15. Bartel DP, (2009) MicroRNAs: Target recognition and regulatory functions. Cell 136 (2): 215-233.
16. Taganov KD, Boldin MP, Chang KJ, Baltimore D, (2006) NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 103 (33): 12481-12486.
17. Saba R, Goodman CD, Huzarewich RL, Robertson C, Booth SA, (2008) A miRNA signature of prion induced neurodegeneration. PLoS One 3 (11): e3652.
18. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 (9): 5116-5121.
19. Saba R, Booth SA, (2006) Target labelling for the detection and profiling of microRNAs expressed in CNS tissue using microarrays. BMC Biotechnol 6: 47.
20. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, et al. (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12 (9): 735-739.
21. Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, et al. (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 5 (3): R13.
22. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS, (2006) Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24 (4): 857-864.
23. Hu G, Gong AY, Liu J, Zhou R, Deng C, et al. (2010) miR-221 suppresses ICAM-1 translation and regulates interferon-gamma-induced ICAM-1 expression in human cholangiocytes. Am J Physiol Gastrointest Liver Physiol 298 (4): G542-50.
24. Liu G, Friggeri A, Yang Y, Park YJ, Tsuruta Y, et al. (2009) miR-147, a microRNA that is induced upon toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc Natl Acad Sci U S A 106 (37): 15819-15824.
25. Henn A, Lund S, Hedtjarn M, Schrattenholz A, Porzgen P, et al. (2009) The suitability of BV2 cells as alternative model system for primary microglia cultures or for animal experiments examining brain inflammation. ALTEX 26 (2): 83-94.
26. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, et al. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 282 (5396): 2085-2088.
27. Coutinho A, Meo T, (1978) Genetic basis for unresponsiveness to lipopolysaccharide in C57BL/10Cr mice. Immunogenetics 7 (1): 17-24.
28. Walker WS, Gatewood J, Olivas E, Askew D, Havenith CE, (1995) Mouse microglial cell lines differing in constitutive and interferon-gamma-inducible antigen-presenting activities for naive and memory CD4+ and CD8+ T cells. J Neuroimmunol 63 (2): 163-174.
29. Qin H, Wilson CA, Lee SJ, Zhao X, Benveniste EN, (2005) LPS induces CD40 gene expression through the activation of NF-kappaB and STAT-1alpha in macrophages and microglia. Blood 106 (9): 3114-3122.
30. Perry MM, Moschos SA, Williams AE, Shepherd NJ, Larner-Svensson HM, et al. (2008) Rapid changes in microRNA-146a expression negatively regulate the IL-1beta-induced inflammatory response in human lung alveolar epithelial cells. J Immunol 180 (8): 5689-5698.
31. Nahid MA, Pauley KM, Satoh M, Chan EK, (2009) miR-146a is critical for endotoxin-induced tolerance: IMPLICATION IN INNATE IMMUNITY. J Biol Chem 284 (50): 34590-34599.
32. Pogue AI, Li YY, Cui JG, Zhao Y, Kruck TP, et al. (2009) Characterization of an NF-kappaB-regulated, miRNA-146a-mediated down-regulation of complement factor H (CFH) in metal-sulfate-stressed human brain cells. J Inorg Biochem 103 (11): 1591-1595.
33. Li YY, Cui JG, Hill JM, Bhattacharjee S, Zhao Y, et al. (2011) Increased expression of miRNA-146a in alzheimer's disease transgenic mouse models. Neurosci Lett 487 (1): 94-98.
34. Guo H, Ingolia NT, Weissman JS, Bartel DP, (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466 (7308): 835-840.
35. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, et al. (2008) The impact of microRNAs on protein output. Nature 455 (7209): 64-71.
36. Lemmers B, Salmena L, Bidere N, Su H, Matysiak-Zablocki E, et al. (2007) Essential role for caspase-8 in toll-like receptors and NFkappaB signaling. J Biol Chem 282 (10): 7416-7423.
37. Hou J, Wang P, Lin L, Liu X, Ma F, et al. (2009) MicroRNA-146a feedback inhibits RIG-I-dependent type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J Immunol 183 (3): 2150-2158.
38. Junker A, Krumbholz M, Eisele S, Mohan H, Augstein F, et al. (2009) MicroRNA profiling of multiple sclerosis lesions identifies modulators of the regulatory protein CD47. Brain 132 (Pt 12): 3342-3352.
39. Hughes MM, Field RH, Perry VH, Murray CL, Cunningham C, (2010) Microglia in the degenerating brain are capable of phagocytosis of beads and of apoptotic cells, but do not efficiently remove PrPSc, even upon LPS stimulation. Glia 58 (16): 2017-2030.
40. Letiembre M, Liu Y, Walter S, Hao W, Pfander T, et al. (2009) Screening of innate immune receptors in neurodegenerative diseases: A similar pattern. Neurobiol Aging 30 (5): 759-768.
41. Richard KL, Filali M, Prefontaine P, Rivest S, (2008) Toll-like receptor 2 acts as a natural innate immune receptor to clear amyloid beta 1-42 and delay the cognitive decline in a mouse model of alzheimer's disease. J Neurosci 28 (22): 5784-5793.
42. Chen K, Iribarren P, Hu J, Chen J, Gong W, et al. (2006) Activation of toll-like receptor 2 on microglia promotes cell uptake of alzheimer disease-associated amyloid beta peptide. J Biol Chem 281 (6): 3651-3659.
43. Iribarren P, Chen K, Hu J, Gong W, Cho EH, et al. (2005) CpG-containing oligodeoxynucleotide promotes microglial cell uptake of amyloid beta 1-42 peptide by up-regulating the expression of the G-protein- coupled receptor mFPR2. FASEB J 19 (14): 2032-2034.
44. Kakimura J, Kitamura Y, Takata K, Umeki M, Suzuki S, et al. (2002) Microglial activation and amyloid-beta clearance induced by exogenous heat-shock proteins. FASEB J 16 (6): 601-603.
45. Landreth GE, Reed-Geaghan EG, (2009) Toll-like receptors in alzheimer's disease. Curr Top Microbiol Immunol 336: 137-153.
46. Pichler K, Schneider G, Grassmann R, (2008) MicroRNA miR-146a and further oncogenesis-related cellular microRNAs are dysregulated in HTLV-1-transformed T lymphocytes. Retrovirology 5: 100.
47. Lukiw WJ, Zhao Y, Cui JG, (2008) An NF-kappaB-sensitive micro RNA-146a-mediated inflammatory circuit in alzheimer disease and in stressed human brain cells. J Biol Chem 283 (46): 31315-31322.
48. Hill JM, Zhao Y, Clement C, Neumann DM, Lukiw WJ, (2009) HSV-1 infection of human brain cells induces miRNA-146a and alzheimer-type inflammatory signaling. Neuroreport 20 (16): 1500-1505.
49. Zipprich JT, Bhattacharyya S, Mathys H, Filipowicz W, (2009) Importance of the C-terminal domain of the human GW182 protein TNRC6C for translational repression. RNA 15 (5): 781-793.
50. Stoeck K, Bodemer M, Zerr I, (2006) Pro- and anti-inflammatory cytokines in the CSF of patients with creutzfeldt-jakob disease. J Neuroimmunol 172 (1-2): 175-181.
51. Wang Y, Moges H, Bharucha Y, Symes A, (2007) Smad3 null mice display more rapid wound closure and reduced scar formation after a stab wound to the cerebral cortex. Exp Neurol 203 (1): 168-184.
52. Akira S, Takeda K, (2004) Toll-like receptor signalling. Nat Rev Immunol 4 (7): 499-511.
53. Henneke P, Takeuchi O, Malley R, Lien E, Ingalls RR, et al. (2002) Cellular activation, phagocytosis, and bactericidal activity against group B streptococcus involve parallel myeloid differentiation factor 88-dependent and independent signaling pathways. J Immunol 169 (7): 3970-3977.
54. Michaud JP, Richard KL, Rivest S, (2011) MyD88-adaptor protein acts as a preventive mechanism for memory deficits in a mouse model of alzheimer's disease. Mol Neurodegener 6 (1): 5.
55. Tahara K, Kim HD, Jin JJ, Maxwell JA, Li L, et al. (2006) Role of toll-like receptor signalling in abeta uptake and clearance. Brain 129 (Pt 11): 3006-3019.