MicroRNA targeting of the P2X7 purinoceptor opposes a contralateral epileptogenic focus in the hippocampus

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Jimenez Mateos, Eva M ^a   Arribas Blazquez, Marina ^b   Sanz Rodriguez, Amaya ^a   Concannon, Caoimhin ^a   Olivos Ore, Luis A ^b   Reschke, Cristina R ^a   Mooney, Claire M ^a   Mooney, Catherine ^a   Lugara, Eleonora ^a   Morgan, James ^a   Langa, Elena ^a   Jimenez Pacheco, Alba ^a   Silva, Luiz Fernando Almeida ^a   Mesuret, Guillaume ^a   Boison, Detlev ^c   Miras Portugal, M Teresa ^b   Letavic, Michael ^d   Artalejo, Antonio R ^b   Bhattacharya, Anindya ^d   Diaz Hernandez, Miguel ^b   Henshall, David C ^a   Engel, Tobias ^a   more..

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c LEGACY RESEARCH   (United States)

^d JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MIRN22 MICRORNA, MOUSE; PURINERGIC P2X7 RECEPTOR; RNA INDUCED SILENCING COMPLEX;

ANIMAL; ASTROCYTE; C57BL MOUSE; ELECTROENCEPHALOGRAPHY; EPILEPTIC STATE; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; INFLAMMATION; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RNA INTERFERENCE;

ANIMALS; ASTROCYTES; ELECTROENCEPHALOGRAPHY; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INFLAMMATION; MALE; MICE, INBRED C57BL; MICRORNAS; RECEPTORS, PURINERGIC P2X7; RNA INTERFERENCE; RNA-INDUCED SILENCING COMPLEX; STATUS EPILEPTICUS;

EID: 84948808507     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17486     Document Type: Article

References (75)

1. Chang, B. S., Lowenstein, D. H. Epilepsy. New Engl J Med 349, 1257-1266 (2003).
2. Vezzani, A., French, J., Bartfai, T., Baram, T. Z. The role of inflammation in epilepsy. Nat Rev Neurol 7, 31-40 (2011).
3. Marchi, N., Granata, T., Janigro, D. Inflammatory pathways of seizure disorders. Trend Neurosci 37, 55-65 (2014).
4. Pernot, F. et al. Inflammatory changes during epileptogenesis and spontaneous seizures in a mouse model of mesiotemporal lobe epilepsy. Epilepsia 52, 2315-2325 (2011).
5. Gershen, L. D. et al. Neuroinflammation in temporal lobe epilepsy measured using positron emission tomographic imaging of translocator protein. JAMA neurology 72, 882-888 (2015).
6. Khalilov, I., Holmes, G. L., Ben-Ari, Y. In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat Neurosci 6, 1079-1085 (2003).
7. Burnstock, G. Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Disc 7, 575-590 (2008).
8. Sperlagh, B., Illes, P. P2X7 receptor: an emerging target in central nervous system diseases. Trend Pharmacol Sci 35, 537-547 (2014).
9. North, R. A. Molecular physiology of P2X receptors. Physiol Rev 82, 1013-1067 (2002).
10. Henshall, D. C., Diaz-Hernandez, M., Miras-Portugal, M. T., Engel, T. P2X receptors as targets for the treatment of status epilepticus. Front Cell Neurosci 7, 237 (2013).
11. Rappold, P. M., Lynd-Balta, E., Joseph, S. A. P2X7 receptor immunoreactive profile confined to resting and activated microglia in the epileptic brain. Brain Res 1089, 171-178 (2006).
12. Mingam, R. et al. In vitro and in vivo evidence for a role of the P2X7 receptor in the release of IL-1 beta in the murine brain. Brain Behav Immun 22, 234-244 (2008).
13. Monif, M., Reid, C. A., Powell, K. L., Smart, M. L., Williams, D. A. The P2X7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore. J Neurosci 29, 3781-3791 (2009).
14. Armstrong, J. N., Brust, T. B., Lewis, R. G., MacVicar, B. A. Activation of presynaptic P2X7-like receptors depresses mossy fiber-CA3 synaptic transmission through p38 mitogen-activated protein kinase. J Neurosci 22, 5938-5945 (2002).
15. Sperlagh, B. et al. Involvement of P2X7 receptors in the regulation of neurotransmitter release in the rat hippocampus. J Neurochem 81, 1196-1211 (2002).
16. Dona, F. et al. Alteration of purinergic P2X4 and P2X7 receptor expression in rats with temporal-lobe epilepsy induced by pilocarpine. Epilepsy Res 83, 157-167 (2009).
17. Jimenez-Pacheco, A. et al. Increased neocortical expression of the P2X7 receptor after status epilepticus and anticonvulsant effect of P2X7 receptor antagonist A-438079. Epilepsia 54, 1551-1561 (2013).
18. Engel, T. et al. Seizure suppression and neuroprotection by targeting the purinergic P2X7 receptor during status epilepticus in mice. FASEB J 26, 1616-1628 (2012).
19. Mesuret, G. et al. P2X7 receptor inhibition interrupts the progression of seizures in immature rats and reduces hippocampal damage. CNS Neurosci Thera 20, 556-564 (2014).
20. Soni, N., Koushal, P., Reddy, B. V., Deshmukh, R., Kumar, P. Effect of GLT-1 modulator and P2X7 antagonists alone and in combination in the kindling model of epilepsy in rats. Epilepsy Behav 48, 4-14 (2015).
21. Zhou, L., Qi, X., Potashkin, J. A., Abdul-Karim, F. W., Gorodeski, G. I. MicroRNAs miR-186 and miR-150 down-regulate expression of the pro-apoptotic purinergic P2X7 receptor by activation of instability sites at the 3-untranslated region of the gene that decrease steady-state levels of the transcript. J Biol Chem 283, 28274-28286 (2008).
22. Huang, S. et al. miR-150 promotes human breast cancer growth and malignant behavior by targeting the pro-apoptotic purinergic P2X7 receptor. PLoS One 8, e80707 (2013).
23. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
24. Fabian, M. R., Sonenberg, N., Filipowicz, W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79, 351-379 (2010).
25. Czech, B., Hannon, G. J. Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 12, 19-31 (2011).
26. Henshall, D. C. MicroRNA and epilepsy: profiling, functions and potential clinical applications. Curr Opin Neurol 27, 199-205 (2014).
27. Jimenez-Mateos, E. M. et al. Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat Med 18, 1087-1094 (2012).
28. Tan, C. L. et al. MicroRNA-128 governs neuronal excitability and motor behavior in mice. Science 342, 1254-1258 (2013).
29. Iyer, A. et al. MicroRNA-146a: A Key Regulator of Astrocyte-Mediated Inflammatory Response. PLoS one 7, e44789 (2012).
30. Letellier, M. et al. miR-92a regulates expression of synaptic GluA1-containing AMPA receptors during homeostatic scaling. Nat Neurosci 17, 1040-1042 (2014).
31. Araki, T., Simon, R. P., Taki, W., Lan, J. Q., Henshall, D. C. Characterization of neuronal death induced by focally evoked limbic seizures in the C57BL/6 mouse. J Neurosci Res 69, 614-621 (2002).
32. Mouri, G. et al. Unilateral hippocampal CA3-predominant damage and short latency epileptogenesis after intra-amygdala microinjection of kainic acid in mice. Brain Res. 1213, 140-151 (2008).
33. Paxinos, G., Franklin, K. B. J. The mouse brain in stereotaxic coordinates, second edition, (Elsevier, San Diego, CA, 2001).
34. Jimenez-Mateos, E. M. et al. Antagomirs targeting microRNA-134 increase hippocampal pyramidal neuron spine volume in vivo and protect against pilocarpine-induced status epilepticus. Brain Struc Func 220, 2387-2399 (2015).
35. Jimenez-Mateos, E. M. et al. Hippocampal transcriptome after status epilepticus in mice rendered seizure damage-tolerant by epileptic preconditioning features suppressed calcium and neuronal excitability pathways. Neurobiol Dis 32, 442-453 (2008).
36. Junker, A. et al. MicroRNA profiling of multiple sclerosis lesions identifies modulators of the regulatory protein CD47. Brain 132, 3342-3352 (2009).
37. Pradervand, S. et al. Impact of normalization on miRNA microarray expression profiling. RNA 15, 493-501 (2009).
38. Huber, W. et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods 12, 115-121 (2015).
39. Kozomara, A., Griffiths-Jones, S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acid Res 42, D68-73 (2014).
40. Engel, T. et al. CHOP regulates the p53-MDM2 axis and is required for neuronal survival after seizures. Brain 136, 577-592 (2013).
41. Allan, S. M., Tyrrell, P. J., Rothwell, N. J. Interleukin-1 and neuronal injury. Nat Rev Immunol 5, 629-640 (2005).
42. Flores, O., Kennedy, E. M., Skalsky, R. L., Cullen, B. R. Differential RISC association of endogenous human microRNAs predicts their inhibitory potential. Nucleic Acid Res 42, 4629-4639 (2014).
43. Bhattacharya, A. et al. Pharmacological characterization of a novel centrally permeable P2X7 receptor antagonist: JNJ-47965567. Br J Pharmacol 170, 624-640 (2013).
44. Bouchie, A. First microRNA mimic enters clinic. Nat Biotech 31, 577 (2013).
45. Bialer, M. et al. Progress report on new antiepileptic drugs: a summary of the Eleventh Eilat Conference (EILAT XI). Epilepsy Res 103, 2-30 (2013).
46. Roth, T. L. et al. Transcranial amelioration of inflammation and cell death after brain injury. Nature 505, 223-228 (2014).
47. Henshall, D. C. MicroRNAs in the pathophysiology and treatment of status epilepticus. Front Mol Neurosci 6, 1-11 (2013).
48. Kan, A. A. et al. Genome-wide microRNA profiling of human temporal lobe epilepsy identifies modulators of the immune response. Cell Mol Life Sci 69, 3127-3145 (2012).
49. McKiernan, R. C. et al. Reduced mature microRNA levels in association with dicer loss in human temporal lobe epilepsy with hippocampal sclerosis. PLoS One 7, e35921 (2012).
50. Zucchini, S. et al. Identification of miRNAs differentially expressed in human epilepsy with or without granule cell pathology. PLoS One 9, e105521 (2014).
51. Miller-Delaney, S. F. et al. Differential DNA methylation profiles of coding and non-coding genes define hippocampal sclerosis in human temporal lobe epilepsy. Brain 138, 616-631 (2015).
52. Hu, K. et al. Expression profile of microRNAs in rat hippocampus following lithium-pilocarpine-induced status epilepticus. Neurosci Lett 488, 252-257 (2011).
53. Risbud, R. M., Porter, B. E. Changes in microRNA expression in the whole hippocampus and hippocampal synaptoneurosome fraction following pilocarpine induced status epilepticus. PLoS One 8, e53464 (2013).
54. Xiong, J., Du, Q., Liang, Z. Tumor-suppressive microRNA-22 inhibits the transcription of E-box-containing c-Myc target genes by silencing c-Myc binding protein. Oncogene 29, 4980-4988 (2010).
55. Jovicic, A., Zaldivar Jolissaint, J. F., Moser, R., Silva Santos Mde, F., Luthi-Carter, R. MicroRNA-22 (miR-22) overexpression is neuroprotective via general anti-apoptotic effects and may also target specific Huntington's disease-related mechanisms. PLoS One 8, e54222 (2013).
56. Yu, H. et al. Neuroprotective effects of viral overexpression of microRNA-22 in rat and cell models of cerebral ischemiareperfusion injury. J Cell Biochem 116, 233-241 (2015).
57. Vale, F. L., Pollock, G., Benbadis, S. R. Failed epilepsy surgery for mesial temporal lobe sclerosis: a review of the pathophysiology. Neurosurg Focus 32, E9 (2012).
58. Hegde, M., Lowenstein, D. H. The search for circulating epilepsy biomarkers. Biomarkers Med 8, 413-427 (2014).
59. Wilczynska, A., Bushell, M. The complexity of miRNA-mediated repression. Cell Death Differ 22, 22-33 (2015).
60. Lee, K. et al. An activity-regulated microRNA, miR-188, controls dendritic plasticity and synaptic transmission by downregulating neuropilin-2. J Neurosci 32, 5678-5687 (2012).
61. Berenguer, J. et al. MicroRNA 22 regulates cell cycle length in cerebellar granular neuron precursors. Mol Cell Biol 33, 2706-2717 (2013).
62. Gavala, M. L., Hill, L. M., Lenertz, L. Y., Karta, M. R., Bertics, P. J. Activation of the transcription factor FosB/activating protein-1 (AP-1) is a prominent downstream signal of the extracellular nucleotide receptor P2RX7 in monocytic and osteoblastic cells. J Biol Chem 285, 34288-34298 (2010).
63. Watanabe, Y. et al. Null mutation of c-fos impairs structural and functional plasticities in the kindling model of epilepsy. J Neurosci 16, 3827-3836 (1996).
64. Ferrari, D., Wesselborg, S., Bauer, M. K., Schulze-Osthoff, K. Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65. J Cell Biol 139, 1635-1643 (1997).
65. Kim, J. E., Kang, T. C. The P2X7 receptor-pannexin-1 complex decreases muscarinic acetylcholine receptor-mediated seizure susceptibility in mice. J Clin Invest 121, 2037-2047 (2011).
66. Boison, D. The adenosine kinase hypothesis of epileptogenesis. Prog Neurobiol 84, 249-262 (2008).
67. Ortinski, P. I. et al. Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci 13, 584-591 (2010).
68. Clasadonte, J., Haydon, P. G. Astrocytes and Epilepsy. in Jasper's Basic Mechanisms of the Epilepsies (eds. Noebels, J. L., Avoli, M., Rogawski, M. A., Olsen, R. W., Delgado-Escueta, A. V.) (Bethesda (MD), 2012).
69. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A., Bessis, A. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci USA 109, E197-205 (2012).
70. Brough, D., Le Feuvre, R. A., Iwakura, Y., Rothwell, N. J. Purinergic (P2X7) receptor activation of microglia induces cell death via an interleukin-1-independent mechanism. Mol Cell Neurosci 19, 272-280 (2002).
71. Salter, M. W., Beggs, S. Sublime microglia: expanding roles for the guardians of the CNS. Cell 158, 15-24 (2014).
72. Chandradoss, S. D., Schirle, N. T., Szczepaniak, M., MacRae, I. J., Joo, C. A dynamic search process underlies microRNA targeting. Cell 162, 96-107 (2015).
73. Garcia-Huerta, P. et al. The specificity protein factor Sp1 mediates transcriptional regulation of P2X7 receptors in the nervous system. J Biol Chem 287, 44628-44644 (2012).
74. Ebert, M. S., Sharp, P. A. Roles for microRNAs in conferring robustness to biological processes. Cell 149, 515-524 (2012).
75. Broderick, J. A., Zamore, P. D. MicroRNA therapeutics. Gene Thera 18, 1104-1110 (2011).