Decrease of mRNA Editing after Spinal Cord Injury is Caused by Down-regulation of ADAR2 that is Triggered by Inflammatory Response

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Narzo, Antonio Fabio Di ^a   Kozlenkov, Alexey ^a,b   Ge, Yongchao ^a   Zhang, Bin ^a   Sanelli, Leo ^c   May, Zacnicte ^c   Li, Yanqing ^c   Fouad, Karim ^c   Cardozo, Christopher ^b   Koonin, Eugene V ^d   Bennett, David J ^c   Dracheva, Stella ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAR2 PROTEIN, RAT; ADENOSINE DEAMINASE; KCNA1 PROTEIN, RAT; MESSENGER RNA; POTASSIUM CHANNEL KV1.1; SEROTONIN 2A RECEPTOR; SEROTONIN 2C RECEPTOR;

ANIMAL; BAYES THEOREM; CHEMISTRY; DOWN REGULATION; FEMALE; GENETICS; METABOLISM; MICROGLIA; PATHOLOGY; PHYSIOLOGY; RAT; RNA EDITING; SEQUENCE ANALYSIS; SPINAL CORD INJURY; SPRAGUE DAWLEY RAT;

ADENOSINE DEAMINASE; ANIMALS; BAYES THEOREM; DOWN-REGULATION; FEMALE; KV1.1 POTASSIUM CHANNEL; MICROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT2A; RECEPTOR, SEROTONIN, 5-HT2C; RNA EDITING; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; SPINAL CORD INJURIES;

EID: 84938318439     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12615     Document Type: Article

References (57)

1. Rekling, J. C., Funk, G. D., Bayliss, D. A., Dong, X. W. & Feldman, J. L. Synaptic control of motoneuronal excitability. Physiol Rev 80, 767-852 (2000).
2. Hultborn, H., Denton, M. E., Wienecke, J. & Nielsen, J. B. Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current. J Physiol 552, 945-52 (2003).
3. ElBasiouny, S. M., Schuster, J. E. & Heckman, C. J. Persistent inward currents in spinal motoneurons: important for normal function but potentially harmful after spinal cord injury and in amyotrophic lateral sclerosis. Clin Neurophysiol 121, 1669-79 (2010).
4. Li, Y., Gorassini, M. A. & Bennett, D. J. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol. 91, 767-783 (2004).
5. Bennett, D. J. et al. Spasticity in rats with sacral spinal cord injury. J Neurotrauma 16, 69-84 (1999).
6. Bennett, D. J., Sanelli, L., Cooke, C. L., Harvey, P. J. & Gorassini, M. A. Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J Neurophysiol. 91, 2247-2258 (2004).
7. Button, D. C. et al. Does elimination of afferent input modify the changes in rat motoneurone properties that occur following chronic spinal cord transection? J Physiol 586, 529-544 (2008).
8. Norton, J. A., Bennett, D. J., Knash, M. E., Murray, K. C. & Gorassini, M. A. Changes in sensory-evoked synaptic activation of motoneurons after spinal cord injury in man. Brain 131, 1478-1491 (2008).
9. Gorassini, M. A., Knash, M. E., Harvey, P. J., Bennett, D. J. & Yang, J. F. Role of motoneurons in the generation of muscle spasms after spinal cord injury. Brain 127, 2247-2258 (2004).
10. Dietz, V. & Sinkjaer, T. Spastic movement disorder: impaired reflex function and altered muscle mechanics. Lancet Neurol. 6, 725-733 (2007).
11. Murray, K. C. et al. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. Nat Med 16, 694-700 (2010).
12. Kong, X. Y., Wienecke, J., Hultborn, H. & Zhang, M. Robust upregulation of serotonin 2A receptors after chronic spinal transection of rats: an immunohistochemical study. Brain Res. 1320, 60-68 (2010).
13. Hannon, J. & Hoyer, D. Molecular biology of 5-HT receptors. Behav.Brain Res. 195, 198-213 (2008).
14. Gott, J. M. & Emeson, R. B. Functions and mechanisms of RNA editing. Annu.Rev.Genet. 34, 499-531 (2000).
15. Valente, L. & Nishikura, K. ADAR gene family and A-to-I RNA editing: diverse roles in posttranscriptional gene regulation. Prog. Nucleic Acid Res.Mol.Biol. 79, 299-338 (2005).
16. Werry, T. D., Loiacono, R., Sexton, P. M. & Christopoulos, A. RNA editing of the serotonin 5HT2C receptor and its effects on cell signalling, pharmacology and brain function. Pharmacol.Ther. 119, 7-23 (2008).
17. Rosenthal, J. J. & Seeburg, P. H. A-to-I RNA editing: effects on proteins key to neural excitability. Neuron 74, 432-439 (2012).
18. Penn, A. C., Balik, A. & Greger, I. H. Reciprocal regulation of A-to-I RNA editing and the vertebrate nervous system. Front Neurosci 7, 61 (2013).
19. Burns, C. M. et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387, 303-308 (1997).
20. Wang, Q. et al. Altered G protein-coupling functions of RNA editing isoform and splicing variant serotonin2C receptors. J Neurochem. 74, 1290-1300 (2000).
21. Moro, O., Lameh, J., Hogger, P. & Sadee, W. Hydrophobic amino acid in the i2 loop plays a key role in receptor-G protein coupling. J.Biol.Chem. 268, 22273-22276 (1993).
22. Niswender, C. M., Copeland, S. C., Herrick-Davis, K., Emeson, R. B. & Sanders-Bush, E. RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. J.Biol.Chem. 274, 9472-9478 (1999).
23. Navarrett, S., Collier, L., Cardozo, C. & Dracheva, S. Alterations of serotonin 2C and 2A receptors in response to T10 spinal cord transection in rats. Neurosci Lett. 506, 74-78 (2012).
24. Lyddon, R., Dwork, A. J., Keddache, M., Siever, L. J. & Dracheva, S. Serotonin 2c receptor RNA editing in major depression and suicide. World J Biol.Psychiatry 14, 590-601 (2013).
25. Morabito, M. V. et al. High-throughput multiplexed transcript analysis yields enhanced resolution of 5-hydroxytryptamine 2C receptor mRNA editing profiles. Mol.Pharmacol. 77, 895-902 (2010).
26. Bhalla, T., Rosenthal, J. J., Holmgren, M. & Reenan, R. Control of human potassium channel inactivation by editing of a small mRNA hairpin. Nat.Struct.Mol.Biol. 11, 950-956 (2004).
27. Zhang, B. & Horvath, S. A general framework for weighted gene co-expression network analysis. Stat.Appl.Genet.Mol.Biol. 4, Article17 (2005).
28. Oldham, M. C. et al. Functional organization of the transcriptome in human brain. Nat.Neurosci 11, 1271-1282 (2008).
29. Winden, K. D. et al. The organization of the transcriptional network in specific neuronal classes. Mol.Syst.Biol. 5, 291 (2009).
30. Hawrylycz, M. J. et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489, 391-399 (2012).
31. Voineagu, I. et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474, 380-384 (2011).
32. Zhang, B. et al. Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer's disease. Cell 153, 707-20 (2013).
33. Yang, X. et al. Validation of candidate causal genes for obesity that affect shared metabolic pathways and networks. Nat Genet 41, 415-23 (2009).
34. Tran, L. M. et al. Inferring causal genomic alterations in breast cancer using gene expression data. BMC Syst Biol 5, 121 (2011).
35. Di Narzo, A. F. et al. A unique gene expression signature associated with serotonin 2C receptor RNA editing in the prefrontal cortex and altered in suicide. Hum.Mol.Genet. 23, 4801-13 (2014).
36. Pe'er, D. Bayesian network analysis of signaling networks: a primer. Sci STKE 281, pl4 (2005).
37. Saher, G. et al. High cholesterol level is essential for myelin membrane growth. Nat Neurosci 8, 468-75 (2005).
38. Plemel, J. R. et al. Remyelination after spinal cord injury: is it a target for repair? Prog Neurobiol 117, 54-72 (2014).
39. Matsuda, K., Kamiya, Y., Matsuda, S. & Yuzaki, M. Cloning and characterization of a novel NMDA receptor subunit NR3B: a dominant subunit that reduces calcium permeability. Brain Res Mol Brain Res 100, 43-52 (2002).
40. Vitalis, T. et al. Developmental expression of monoamine oxidases A and B in the central and peripheral nervous systems of the mouse. J Comp Neurol 442, 331-47 (2002).
41. Taricco, M., Pagliacci, M. C., Telaro, E. & Adone, R. Pharmacological interventions for spasticity following spinal cord injury: results of a Cochrane systematic review. Eura.Medicophys. 42, 5-15 (2006).
42. Roy, R. R. & Edgerton, V. R. Neurobiological perspective of spasticity as occurs after a spinal cord injury. Exp Neurol 235, 116-22 (2012).
43. Chi, X. X. & Nicol, G. D. Manipulation of the potassium channel Kv1.1 and its effect on neuronal excitability in rat sensory neurons. J Neurophysiol. 98, 2683-2692 (2007).
44. Robbins, C. A. & Tempel, B. L. Kv1.1 and Kv1.2: similar channels, different seizure models. Epilepsia 53 Suppl 1, 134-141 (2012).
45. Harvey, P. J., Li, Y., Li, X. & Bennett, D. J. Persistent sodium currents and repetitive firing in motoneurons of the sacrocaudal spinal cord of adult rats. J Neurophysiol. 96, 1141-1157 (2006).
46. Schwab, J. M., Zhang, Y., Kopp, M. A., Brommer, B. & Popovich, P. G. The paradox of chronic neuroinflammation, systemic immune suppression, autoimmunity after traumatic chronic spinal cord injury. Exp Neurol 258, 121-9 (2014).
47. Perrier, J. F. & Hounsgaard, J. 5-HT2 receptors promote plateau potentials in turtle spinal motoneurons by facilitating an L-type calcium current. J Neurophysiol. 89, 954-959 (2003).
48. Hideyama, T. et al. Profound downregulation of the RNA editing enzyme ADAR2 in ALS spinal motor neurons. Neurobiol Dis 45, 1121-8 (2012).
49. Brites, D. & Vaz, A. R. Microglia centered pathogenesis in ALS: insights in cell interconnectivity. Front Cell Neurosci 8, 117 (2014).
50. Kang, S. H. et al. Degeneration and impaired regeneration of gray matter oligodendrocytes in amyotrophic lateral sclerosis. Nat Neurosci 16, 571-9 (2013).
51. Mattick, J. S. & Mehler, M. F. RNA editing, DNA recoding and the evolution of human cognition. Trends Neurosci. 31, 227-233 (2008).
52. Eran, A. et al. Comparative RNA editing in autistic and neurotypical cerebella. Mol.Psychiatry 18, 1041-1048 (2013).
53. Dracheva, S. et al. Editing of serotonin 2C receptor mRNA in the prefrontal cortex characterizes high-novelty locomotor response behavioral trait. Neuropsychopharmacology 34, 2237-2251 (2009).
54. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-11 (2009).
55. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
56. Friedman, N., Linial, M., Nachman, I. & Pe'er, D. Using Bayesian networks to analyze expression data. J Comput Biol 7, 601-20 (2000).
57. Thorvaldsdottir, H., Robinson, J. T. & Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14, 178-92 (2013).