Traumatic brain injury alters expression of hippocampal microRNAs: Potential regulators of multiple pathophysiological processes

Journal of Neuroscience Research

Volumn 87, Issue 6, 2009, Pages 1435-1448

  Redell, John B ^a   Liu, Yin ^a   Dash, Pramod K ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Hippocampus; Microarray; MiRNA; TBI

Indexed keywords

MICRORNA; MICRORNA 107; MICRORNA 130A; MICRORNA 223; MICRORNA 292 5P; MICRORNA 433 3P; MICRORNA 451; MICRORNA 541; MICRORNA 711; UNCLASSIFIED DRUG; PROTEIN; STAT1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; GENE EXPRESSION; HIPPOCAMPUS; MALE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN TARGETING; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRAUMATIC BRAIN INJURY; UPREGULATION; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGY; BRAIN INJURY; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MICROARRAY ANALYSIS; PROTEIN ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN INJURIES; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPUTATIONAL BIOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MICROARRAY ANALYSIS; MICRORNAS; PROTEIN INTERACTION MAPPING; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAT1 TRANSCRIPTION FACTOR;

EID: 65549158252     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21945     Document Type: Article

References (66)

1. An JJ, Gharami K, Liao GY, Woo NH, Lau AG, Vanevski F, Torre ER, Jones KR, Feng Y, Lu B, Xu B. 2008. Distinct role of long 30 UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134:175-187.
2. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. 2008. The impact of microRNAs on protein output. Nature 455(7209):64-71.
3. Bekinschtein P, Cammarota M, Izquierdo I, Medina JH. 2008. BDNF and memory formation and storage. Neuroscientist 14:147-156.
4. Berezikov E, Thuemmler F, van Laake LW, Kondova I, Bontrop R, Cuppen E, Plasterk RH. 2006. Diversity of microRNAs in human and chimpanzee brain. Nat Genet 38:1375-1377.
5. Betel D, Wilson M, Gabow A, Marks DS, Sander C. 2008. The micro-RNA.org resource: targets and expression. Nucleic Acids Res 36:D149-D153.
6. Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193.
7. Borchert GM, Lanier W, Davidson BL. 2006. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 13:1097-1101.
8. Brennecke J, Stark A, Russell RB, Cohen SM. 2005. Principles of microRNA-target recognition. PLoS Biol 3:e85.
9. Cai X, Hagedorn CH, Cullen BR. 2004. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10:1957-1966.
10. Carson JP, Thaller C, Eichele G. 2002. A transcriptome atlas of the mouse brain at cellular resolution. Curr Opin Neurobiol 12:562-565.
11. Carson JP, Eichele G, Chiu W. 2005. A method for automated detection of gene expression required for the establishment of a digital transcriptome-wide gene expression atlas. J Microsc 217:275-281.
12. Chen Y, Gorski DH. 2008. Regulation of angiogenesis through a micro-RNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood 111:1217-1226.
13. Dash PK, Kobori N, Moore AN. 2004. A molecular description of brain trauma pathophysiology using microarray technology: an overview. Neurochem Res 29:1275-1286.
14. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A. 2006. Augmentation of tumor angiogenesis by a Myc-activated micro-RNA cluster. Nat Genet 38:1060-1065.
15. Dieci G, Fiorino G, Castelnuovo M, Teichmann M, Pagano A. 2007. The expanding RNA polymerase III transcriptome. Trends Genet 23:614-622.
16. Dixon CE, Clifton GL, Lighthall JW, Yaghmai AA, Hayes RL. 1991. A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods 39:253-262.
17. Fazi F, Rosa A, Fatica A, Gelmetti V, De Marchis ML, Nervi C, Bozzoni I. 2005. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 123:819-831.
18. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811.
19. Gao X, Gulari E, Zhou X. 2004. In situ synthesis of oligonucleotide microarrays. Biopolymers 73:579-596.
20. Gygi SP, Rochon Y, Franza BR, Aebersold R. 1999. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720-1730.
21. Jeyaseelan K, Lim KY, Armugam A. 2008. MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 39:959-966.
22. Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H, Dean DB, Zhang C. 2007. MicroRNA expression signature and antisense-mediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation. Circ Res 100:1579-1588.
23. Joglekar MV, Parekh VS, Hardikar AA. 2007. New pancreas from old: microregulators of pancreas regeneration. Trends Endocrinol Metab 18:393-400.
24. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. 2004. Human MicroRNA targets. PLoS Biol 2:e363.
25. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, Kirak O, Brummelkamp TR, Fleming MD, Camargo FD. 2008. Regulation of progenitor cell proliferation and granulocyte function by micro-RNA-223. Nature 451:1125-1129.
26. Karginov FV, Conaco C, Xuan Z, Schmidt BH, Parker JS, Mandel G, Hannon GJ. 2007. A biochemical approach to identifying microRNA targets. Proc Natl Acad Sci U S A 104:19291-19296.
27. Kloosterman WP, Plasterk RH. 2006. The diverse functions of micro-RNAs in animal development and disease. Dev Cell 11:441-450.
28. Kloosterman WP, Wienholds E, de BE, Kauppinen S, Plasterk RH. 2006. In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat Methods 3:27-29.
29. Kobori N, Clifton GL, Dash P. 2002. Altered expression of novel genes in the cerebral cortex following experimental brain injury. Brain Res Mol Brain Res 104:148-158.
30. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N. 2005. Combinatorial microRNA target predictions. Nat Genet 37:495-500.
31. Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S. 2007. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res 101:59-68.
32. Kuzin A, Kundu M, Brody T, Odenwald WF. 2007. The Drosophila nerfin-1 mRNA requires multiple microRNAs to regulate its spatial and temporal translation dynamics in the developing nervous system. Dev Biol 310:35-43.
33. Kye MJ, Liu T, Levy SF, Xu NL, Groves BB, Bonneau R, Lao K, Kosik KS. 2007. Somatodendritic microRNAs identified by laser capture and multiplex RT-PCR. RNA 13:1224-1234.
34. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. 2004. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051-4060.
35. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. 2003. Prediction of mammalian microRNA targets. Cell 115:787-798.
36. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20.
37. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769-773.
38. Lu Y, Christian K, Lu B. 2008. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89:312-323.
39. Ma L, Carter RJ, Morton AJ, Nicholson LF. 2003. RAGE is expressed in pyramidal cells of the hippocampus following moderate hypoxic-ischemic brain injury in rats. Brain Res 966:167-174.
40. Masaki S, Ohtsuka R, Abe Y, Muta K, Umemura T. 2007. Expression patterns of microRNAs 155 and 451 during normal human erythropoiesis. Biochem Biophys Res Commun 364:509-514.
41. Mellios N, Huang HS, Grigorenko A, Rogaev E, Akbarian S. 2008. A set of differentially expressed miRNAs, including miR-30a-5p, act as post-transcriptional inhibitors of BDNF in prefrontal cortex. Hum Mol Genet 17:3030-3042.
42. Mishra GR, Suresh M, Kumaran K, Kannabiran N, Suresh S, Bala P, Shivakumar K, Anuradha N, Reddy R, Raghavan TM, Menon S, Hanumanthu G, Gupta M, Upendran S, Gupta S, Mahesh M, Jacob B, Mathew P, Chatterjee P, Arun KS, Sharma S, Chandrika KN, Deshpande N, Palvankar K, Raghavnath R, Krishnakanth R, Karathia H, Rekha B, Nayak R, Vishnupriya G, Kumar HG, Nagini M, Kumar GS, Jose R, Deepthi P, Mohan SS, Gandhi TK, Harsha HC, Deshpande KS, Sarker M, Prasad TS, Pandey A. 2006. Human protein reference database - 2006 update. Nucleic Acids Res 34:D411-D414.
43. Nelson PT, Wang WX, Rajeev BW. 2008. MicroRNAs (miRNAs) in neurodegenerative diseases. Brain Pathol 18:130-138.
44. O'Brien KP, Remm M, Sonnhammer EL. 2005. Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res 33:D476-D480.
45. Peri S, Navarro JD, Amanchy R, Kristiansen TZ, Jonnalagadda CK, Surendranath V, Niranjan V, Muthusamy B, Gandhi TK, Gronborg M, Ibarrola N, Deshpande N, Shanker K, Shivashankar HN, Rashmi BP, Ramya MA, Zhao Z, Chandrika KN, Padma N, Harsha HC, Yatish AJ, Kavitha MP, Menezes M, Choudhury DR, Suresh S, Ghosh N, Saravana R, Chandran S, Krishna S, Joy M, Anand SK, Madavan V, Joseph A, Wong GW, Schiemann WP, Constantinescu SN, Huang L, Khosravi-Far R, Steen H, Tewari M, Ghaffari S, Blobe GC, Dang CV, Garcia JG, Pevsner J, Jensen ON, Roepstorff P, Deshpande KS, Chinnaiyan AM, Hamosh A, Chakravarti A, Pandey A. 2003. Development of human protein reference database as an initial platform for approaching systems biology in humans. Genome Res 13:2363-2371.
46. Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G. 2006. MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108:3068-3071.
47. Quintana A, Molinero A, Borup R, Nielsen FC, Campbell IL, Penkowa M, Hidalgo J. 2008. Effect of astrocyte-targeted production of IL-6 on traumatic brain injury and its impact on the cortical transcriptome. Dev Neurobiol 68:195-208.
48. Raghupathi R. 2004. Cell death mechanisms following traumatic brain injury. Brain Pathol 14:215-222.
49. Rajewsky N. 2006. microRNA target predictions in animals. Nat Genet 38)Suppl):S8-S13.
50. Rana TM. 2007. Illuminating the silence: understanding the structure and function of small RNAs. Nat. Rev. Mol Cell Biol 8:23-36.
51. Richardson RM, Sun D, Bullock MR. 2007. Neurogenesis after traumatic brain injury. Neurosurg Clin N Am 18:169-181.
52. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. 2005. Animal MicroRNAs confer robustness to gene expression and have a significant impact on 30UTR evolution. Cell 123:1133-1146.
53. Suarez Y, Fernandez-Hernando C, Pober JS, Sessa WC. 2007. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 100:1164-1173.
54. Tang F, Hajkova P, Barton SC, Lao K, Surani MA. 2006. MicroRNA expression profiling of single whole embryonic stem cells. Nucleic Acids Res 34:e9.
55. Urbich C, Kuehbacher A, Dimmeler S. 2008. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 79:581-588.
56. Van Den HC, Thornton E, Vink R. 2007. Traumatic brain injury and Alzheimer's disease: a review. Prog Brain Res 161:303-316.
57. Victor NA, Wanderi EW, Gamboa J, Zhao X, Aronowski J, Deininger K, Lust WD, Landreth GE, Sundararajan S. 2006. Altered PPAR-gamma expression and activation after transient focal ischemia in rats. Eur J Neurosci 24:1653-1663.
58. Visel A, Thaller C, Eichele G. 2004. GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 32:D552-D556.
59. Wang WX, Rajeev BW, Stromberg AJ, Ren N, Tang G, Huang Q, Rigoutsos I, Nelson PT. 2008. The expression of microRNA miR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. J Neurosci 28:1213-1223.
60. Xie X, Lu J, Kulbokas EJ, Golub TR, Mootha V, Lindblad-Toh K, Lander ES, Kellis M. 2005. Systematic discovery of regulatory motifs in human promoters and 30 UTRs by comparison of several mammals. Nature 434:338-345.
61. Yamada K, Mizuno M, Nabeshima T. 2002. Role for brain-derived neurotrophic factor in learning and memory. Life Sci 70:735-744.
62. Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, Zhao G. 2005. Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem 280:9330-9335.
63. Yaylaoglu MB, Titmus A, Visel A, varez-Bolado G, Thaller C, Eichele G. 2005. Comprehensive expression atlas of fibroblast growth factors and their receptors generated by a novel robotic in situ hybridization platform. Dev Dyn 234:371-386.
64. Zhan M, Miller CP, Papayannopoulou T, Stamatoyannopoulos G, Song CZ. 2007. MicroRNA expression dynamics during murine and human erythroid differentiation. Exp Hematol 35:1015-1025.
65. Zhang B, West EJ, Van KC, Gurkoff GG, Zhou J, Zhang XM, Kozikowski AP, Lyeth BG. 2008. HDAC inhibitor increases histone H3 acetylation and reduces microglia inflammatory response following traumatic brain injury in rats. Brain Res 1226:181-191.
66. Zhu Q, Hong A, Sheng N, Zhang X, Matejko A, Jun KY, Srivannavit O, Gulari E, Gao X, Zhou X. 2007. MicroParaflo biochip for nucleic acid and protein analysis. Methods Mol Biol 382:287-312.