Traumatic brain injury increases levels of miR-21 in extracellular vesicles: Implications for neuroinflammation

FEBS Open Bio

Volumn 6, Issue 8, 2016, Pages 835-846

  Harrison, Emily B ^a   Hochfelder, Colleen G ^a,b   Lamberty, Benjamin G ^a   Meays, Brittney M ^a   Morsey, Brenda M ^a   Kelso, Matthew L ^a,c   Fox, Howard S ^a   Yelamanchili, Sowmya V ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c Medpace Reference Laboratories ^*  (United States)

Author keywords

Controlled cortical impact; Exosomes; Microglia; MicroRNA; Neuroinflammation; Secondary injury

Indexed keywords

MICRORNA; MICRORNA 146; MICRORNA 21; MICRORNA 212; MICRORNA 7A; MICRORNA 7B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN NERVE CELL; CELL ACTIVATION; CELL COMMUNICATION; CELL ISOLATION; CONTROLLED STUDY; EXOSOME; MALE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SEQUENCE; TRAUMATIC BRAIN INJURY;

EID: 85081459741     PISSN: None     EISSN: 22115463     Source Type: Journal    
DOI: 10.1002/2211-5463.12092     Document Type: Article

References (60)

1. Zaloshnja E, Miller T, Langlois JA and Selassie AW (2008) Prevalence of long-term disability from traumatic brain injury in the civilian population of the United States, 2005. J Head Trauma Rehabil 23, 394-400.
2. CDC Weekly (2013) CDC grand rounds: reducing severe traumatic brain injury in the United States. MMWR Morb Mortal Wkly Rep 62, 549-552
3. Kuo CY, Liou TH, Chang KH, Chi WC, Escorpizo R, Yen CF, Liao HF, Chiou HY, Chiu WT and Tsai JT (2015) Functioning and disability analysis of patients with traumatic brain injury and spinal cord injury by using the world health organization disability assessment schedule 2.0. Int J Environ Res Public Health 12, 4116-4127.
4. Finnie JW (2013) Neuroinflammation: beneficial and detrimental effects after traumatic brain injury. Inflammopharmacology 21, 309-320.
5. Gyoneva S and Ransohoff RM (2015) Inflammatory reaction after traumatic brain injury: therapeutic potential of targeting cell-cell communication by chemokines. Trends Pharmacol Sci 36, 471-480
6. Woodcock T and Morganti-Kossmann MC (2013) The role of markers of inflammation in traumatic brain injury. Front Neurol 4, 18.
7. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A and Sanchez-Madrid F (2011) Unidirectional transfer of microRNA-loaded exosomes from T cells to antigenpresenting cells. Nat Commun 2, 282.
8. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z et al. (2012) Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119, 756-766.
9. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo GJ et al. (2012) MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 109, E2110-E2116.
10. Thery C, Ostrowski M and Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9, 581-593.
11. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ and Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9, 654-659.
12. Mattson MP and Scheff SW (1994) Endogenous neuroprotection factors and traumatic brain injury: mechanisms of action and implications for therapy. J Neurotrauma 11, 3-33.
13. Smith DH, Soares HD, Pierce JS, Perlman KG, Saatman KE, Meaney DF, Dixon CE and McIntosh TK (1995) A model of parasagittal controlled cortical impact in the mouse: cognitive and histopathologic effects. J Neurotrauma 12, 169-178.
14. O’Connor C, Heath DL, Cernak I, Nimmo AJ and Vink R (2003) Effects of daily versus weekly testing and pre-training on the assessment of neurologic impairment following diffuse traumatic brain injury in rats. J Neurotrauma 20, 985-993.
15. Yelamanchili SV, Chaudhuri AD, Flynn CT and Fox HS (2011) Upregulation of cathepsin D in the caudate nucleus of primates with experimental parkinsonism. Mol Neurodegener 6, 52.
16. Chaudhuri AD, Yelamanchili SV and Fox HS (2013) Combined fluorescent in situ hybridization for detection of microRNAs and immunofluorescent labeling for celltype markers. Front Cell Neurosci 7, 160.
17. Yelamanchili SV, Lamberty BG, Rennard DA, Morsey BM, Hochfelder CG, Meays BM, Levy E and Fox HS (2015) MiR-21 in extracellular vesicles leads to neurotoxicity via TLR7 signaling in SIV neurological disease. PLoS Pathog 11, e1005032.
18. Perez-Gonzalez R, Gauthier SA, Kumar A and Levy E (2012) The exosome secretory pathway transports amyloid precursor protein carboxyl-terminal fragments from the cell into the brain extracellular space. J Biol Chem 287, 43108-43115.
19. Cole JT, Yarnell A, Kean WS, Gold E, Lewis B, Ren M, McMullen DC, Jacobowitz DM, Pollard HB, O’Neill JT et al. (2011) Craniotomy: true sham for traumatic brain injury, or a sham of a sham? J Neurotrauma 28, 359-369.
20. Lagraoui M, Latoche JR, Cartwright NG, Sukumar G, Dalgard CL and Schaefer BC (2012) Controlled cortical impact and craniotomy induce strikingly similar profiles of inflammatory gene expression, but with distinct kinetics. Front Neurol 3, 155.
21. Fujimoto ST, Longhi L, Saatman KE, Conte V, Stocchetti N and McIntosh TK (2004) Motor and cognitive function evaluation following experimental traumatic brain injury. Neurosci Biobehav Rev 28, 365-378.
22. Faden AI, Wu J, Stoica BA and Loane DJ (2016) Progressive inflammation-mediated neurodegeneration after traumatic brain or spinal cord injury. Br J Pharmacol 173, 681-691.
23. Whittemore ER, Korotzer AR, Etebari A and Cotman CW (1993) Carbachol increases intracellular free calcium in cultured rat microglia. Brain Res 621, 59-64
24. Lehmann SM, Kruger C, Park B, Derkow K, Rosenberger K, Baumgart J, Trimbuch T, Eom G, Hinz M, Kaul D et al. (2012) An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat Neurosci 15, 827-835.
25. Liu HY, Huang CM, Hung YF and Hsueh YP (2015) The microRNAs Let7c and miR21 are recognized by neuronal Toll-like receptor 7 to restrict dendritic growth of neurons. Exp Neurol 269, 202-212
26. Forsbach A, Nemorin JG, Montino C, Muller C, Samulowitz U, Vicari AP, Jurk M, Mutwiri GK, Krieg AM, Lipford GB et al. (2008) Identification of RNA sequence motifs stimulating sequence-specific TLR8-dependent immune responses. J Immunol 180, 3729-3738
27. Redell JB, Liu Y and Dash PK (2009) Traumatic brain injury alters expression of hippocampal microRNAs: potential regulators of multiple pathophysiological processes. J Neurosci Res 87, 1435-1448.
28. Ge XT, Lei P, Wang HC, Zhang AL, Han ZL, Chen X, Li SH, Jiang RC, Kang CS and Zhang JN (2014) miR-21 improves the neurological outcome after traumatic brain injury in rats. Sci Rep 4, 6718
29. Sandhir R, Gregory E and Berman NE (2014) Differential response of miRNA-21 and its targets after traumatic brain injury in aging mice. Neurochem Int 78, 117-121.
30. Lei P, Li Y, Chen X, Yang S and Zhang J (2009) Microarray based analysis of microRNA expression in rat cerebral cortex after traumatic brain injury. Brain Res 1284, 191-201.
31. Hu Z, Yu D, Almeida-Suhett C, Tu K, Marini AM, Eiden L, Braga MF, Zhu J and Li Z (2012) Expression of miRNAs and their cooperative regulation of the pathophysiology in traumatic brain injury. PLoS One 7, e39357.
32. Liu L, Sun T, Liu Z, Chen X, Zhao L, Qu G and Li Q (2014) Traumatic brain injury dysregulates microRNAs to modulate cell signaling in rat hippocampus. PLoS One 9, e103948.
33. Sun TY, Chen XR, Liu ZL, Zhao LL, Jiang YX, Qu GQ, Wang RS, Huang SZ and Liu L (2014) Expression profiling of microRNAs in hippocampus of rats following traumatic brain injury. J Huazhong Univ Sci Technolog Med Sci 34, 548-553.
34. Meissner L, Gallozzi M, Balbi M, Schwarzmaier S, Tiedt S, Terpolilli NA and Plesnila N (2016) Temporal profile of MicroRNA expression in contused cortex after traumatic brain injury in mice. J Neurotrauma 33, 713-720.
35. Bergman P, James T, Kular L, Ruhrmann S, Kramarova T, Kvist A, Supic G, Gillett A, Pivarcsi A and Jagodic M (2013) Next-generation sequencing identifies microRNAs that associate with pathogenic autoimmune neuroinflammation in rats. J Immunol 190, 4066-4075.
36. Tang Y, Ling ZM, Fu R, Li YQ, Cheng X, Song FH, Luo HX and Zhou LH (2014) Time-specific microRNA changes during spinal motoneuron degeneration in adult rats following unilateral brachial plexus root avulsion: ipsilateral vs. contralateral changes. BMC Neurosci 15, 92.
37. Sakai A and Suzuki H (2013) Nerve injury-induced upregulation of miR-21 in the primary sensory neurons contributes to neuropathic pain in rats. Biochem Biophys Res Commun 435, 176-181.
38. Strickland IT, Richards L, Holmes FE, Wynick D, Uney JB and Wong LF (2011) Axotomy-induced miR-21 promotes axon growth in adult dorsal root ganglion neurons. PLoS One 6, e23423.
39. Bhalala OG, Pan L, Sahni V, McGuire TL, Gruner K, Tourtellotte WG and Kessler JA (2012) microRNA-21 regulates astrocytic response following spinal cord injury. J Neurosci 32, 17935-17947.
40. Yelamanchili SV, Chaudhuri AD, Chen LN, Xiong H and Fox HS (2010) MicroRNA-21 dysregulates the expression of MEF2C in neurons in monkey and human SIV/HIV neurological disease. Cell Death Dis 1, e77.
41. Lescher J, Paap F, Schultz V, Redenbach L, Scheidt U, Rosewich H, Nessler S, Fuchs E, Gartner J, Bruck W et al. (2012) MicroRNA regulation in experimental autoimmune encephalomyelitis in mice and marmosets resembles regulation in human multiple sclerosis lesions. J Neuroimmunol 246, 27-33.
42. Han Z, Chen F, Ge X, Tan J, Lei P and Zhang J (2014) miR-21 alleviated apoptosis of cortical neurons through promoting PTEN-Akt signaling pathway in vitro after experimental traumatic brain injury. Brain Res 1582, 12-20.
43. Bhalala OG, Srikanth M and Kessler JA (2013) The emerging roles of microRNAs in CNS injuries. Nat Rev Neurol 9, 328-339.
44. Buller B, Liu X, Wang X, Zhang RL, Zhang L, Hozeska-Solgot A, Chopp M and Zhang ZG (2010) MicroRNA-21 protects neurons from ischemic death. FEBS J 277, 4299-4307.
45. Montalban E, Mattugini N, Ciarapica R, Provenzano C, Savino M, Scagnoli F, Prosperini G, Carissimi C, Fulci V, Matrone C et al. (2014) MiR-21 is an Ngfmodulated microRNA that supports Ngf signaling and regulates neuronal degeneration in PC12 cells. NeuroMol Med 16, 415-430.
46. Zhang L, Dong LY, Li YJ, Hong Z and Wei WS (2012) miR-21 represses FasL in microglia and protects against microglia-mediated neuronal cell death following hypoxia/ischemia. Glia 60, 1888-1895
47. Patz S, Trattnig C, Grunbacher G, Ebner B, Gully C, Novak A, Rinner B, Leitinger G, Absenger M, Tomescu OA et al. (2013) More than cell dust: microparticles isolated from cerebrospinal fluid of brain injured patients are messengers carrying mRNAs, miRNAs, and proteins. J Neurotrauma 30, 1232-1242
48. Bellingham SA, Coleman BM and Hill AF (2012) Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res 40, 10937-10949
49. Kraft-Terry SD, Buch SJ, Fox HS and Gendelman HE (2009) A coat of many colors: neuroimmune crosstalk in human immunodeficiency virus infection. Neuron 64, 133-145.
50. Hu G, Yao H, Chaudhuri AD, Duan M, Yelamanchili SV, Wen H, Cheney PD, Fox HS and Buch S (2012) Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction. Cell Death Dis 3, e381.
51. Crozat K and Beutler B (2004) TLR7: a new sensor of viral infection. Proc Natl Acad Sci USA 101, 6835-6836.
52. Taganov KD, Boldin MP, Chang KJ and 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 USA 103, 12481-12486.
53. Boldin MP, Taganov KD, Rao DS, Yang L, Zhao JL, Kalwani M, Garcia-Flores Y, Luong M, Devrekanli A, Xu J et al. (2011) miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med 208, 1189-1201.
54. Alexander M, Hu R, Runtsch MC, Kagele DA, Mosbruger TL, Tolmachova T, Seabra MC, Round JL, Ward DM and O’Connell RM (2015) Exosomedelivered microRNAs modulate the inflammatory response to endotoxin. Nat Commun 6, 7321.
55. Choi DC, Chae YJ, Kabaria S, Chaudhuri AD, Jain MR, Li H, Mouradian MM and Junn E (2014) MicroRNA-7 protects against 1-methyl-4-phenylpyridinium-induced cell death by targeting RelA. J Neurosci 34, 12725-12737.
56. Choudhury NR, de Lima Alves F, de Andres-Aguayo L, Graf T, Caceres JF, Rappsilber J and Michlewski G (2013) Tissue-specific control of brain-enriched miR-7 biogenesis Genes Dev 27, 24-38.
57. Wanet A, Tacheny A, Arnould T and Renard P (2012) miR-212/132 expression and functions: within and beyond the neuronal compartment. Nucleic Acids Res 40, 4742-4753.
58. Zhang Z, Chang H, Li Y, Zhang T, Zou J, Zheng X and Wu J (2010) MicroRNAs: potential regulators involved in human anencephaly. Int J Biochem Cell Biol 42, 367-374.
59. Kim AH, Reimers M, Maher B, Williamson V, McMichael O, McClay JL, van den Oord EJ, Riley BP, Kendler KS and Vladimirov VI (2010) MicroRNA expression profiling in the prefrontal cortex of individuals affected with schizophrenia and bipolar disorders. Schizophr Res 124, 183-191.
60. Wang WX, Huang Q, Hu Y, Stromberg AJ and Nelson PT (2011) Patterns of microRNA expression in normal and early Alzheimer’s disease human temporal cortex: white matter versus gray matter. Acta Neuropathol 121, 193-205.