Long non-coding RNA C2dat1 regulates CaMKIIδ expression to promote neuronal survival through the NF-κB signaling pathway following cerebral ischemia

Cell Death and Disease

Volumn 7, Issue 3, 2016, Pages

  Xu, Q ^a,b   Deng, F ^c   Xing, Z ^c   Wu, Z ^b   Cen, B ^b   Xu, S ^a   Zhao, Z ^a   Nepomuceno, R ^a   Bhuiyan, M I H ^a   Sun, D ^a   Wang, Q J ^a   Ji, A ^b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IID ASSOCIATED TRANSCRIPT 1; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IIDELTA; GLUCOSE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LONG UNTRANSLATED RNA; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; OXYGEN; UNCLASSIFIED DRUG; CAMK2D PROTEIN, MOUSE; I KAPPA B KINASE;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL SURVIVAL; CELLULAR DISTRIBUTION; CEREBRAL ISCHEMIA REPERFUSION INJURY; CHROMOSOME 3; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXCITOTOXICITY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN; GENE SILENCING; MALE; MOUSE; NERVE CELL; NEURO-2A CELL LINE; NONHUMAN; PRIORITY JOURNAL; REOXYGENATION; RNA EXTRACTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CEREBRAL ARTERY DISEASE; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE;

ANIMALS; APOPTOSIS; BRAIN ISCHEMIA; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GLUCOSE; I-KAPPA B KINASE; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE; MICE, INBRED C57BL; NEURONS; NF-KAPPA B; OXYGEN; PHOSPHORYLATION; RNA INTERFERENCE; RNA, LONG NONCODING; SIGNAL TRANSDUCTION;

EID: 85014897704     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2016.57     Document Type: Article

References (44)

1. Saugstad JA. Non-coding RNAs in stroke and neuroprotection. Front Neurol 2015; 6: 50.
2. Vemuganti R. All's well that transcribes well: non-coding RNAs and post-stroke brain damage. Neurochem Int 2013; 63: 438–449.
3. Dharap A, Nakka VP, Vemuganti R. Effect of focal ischemia on long noncoding RNAs. Stroke 2012; 43: 2800–2802.
4. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci USA 2008; 105: 716–721.
5. Aprea J, Prenninger S, Dori M, Ghosh T, Monasor LS, Wessendorf E et al. Transcriptome sequencing during mouse brain development identifies long non-coding RNAs functionally involved in neurogenic commitment. EMBO J 2013; 32: 3145–3160.
6. Clark BS, Blackshaw S. Long non-coding RNA-dependent transcriptional regulation in neuronal development and disease. Front Genet 2014; 5: 164.
7. Mehler MF, Mattick JS. Noncoding RNAs and RNA editing in brain development, functional diversification, and neurological disease. Physiol Rev 2007; 87: 799–823.
8. Wu P, Zuo X, Deng H, Liu X, Liu L, Ji A. Roles of long noncoding RNAs in brain development, functional diversification and neurodegenerative diseases. Brain Res Bull 2013; 97: 69–80.
9. Qureshi IA, Mattick JS, Mehler MF. Long non-coding RNAs in nervous system function and disease. Brain Res 2010; 1338: 20–35.
10. Tobimatsu T, Fujisawa H. Tissue-specific expression of four types of rat calmodulin-dependent protein kinase II mRNAs. J Biol Chem 1989; 264: 17907–17912.
11. Erondu NE, Kennedy MB. Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain. J Neurosci 1985; 5: 3270–3277.
12. Coultrap SJ, Vest RS, Ashpole NM, Hudmon A, Bayer KU. CaMKII in cerebral ischemia. Acta Pharmacologica Sinica 2011; 32: 861–872.
13. Doyle KP, Simon RP, Stenzel-Poore MP. Mechanisms of ischemic brain damage. Neuropharmacology 2008; 55: 310–318.
14. Hanson SK, Grotta JC, Waxham MN, Aronowski J, Ostrow P. Calcium/calmodulin-dependent protein kinase II activity in focal ischemia with reperfusion in rats. Stroke 1994; 25: 466–473.
15. Zalewska T, Domanska-Janik K. Brain ischaemia transiently activates Ca2+/calmodulin-independent protein kinase II. Neuroreport 1996; 7: 637–641.
16. Westgate SA, Brown J, Aronowski J, Waxham MN. Activity of Ca2+/calmodulin-dependent protein kinase II following ischemia: a comparison between CA1 and dentate gyrus in a hippocampal slice model. J Neurochem 1994; 63: 2217–2224.
17. Waxham MN, Grotta JC, Silva AJ, Strong R, Aronowski J. Ischemia-induced neuronal damage: a role for calcium/calmodulin-dependent protein kinase II. J Cereb Blood Flow Metab 1996; 16: 1–6.
18. Ashpole NM, Song W, Brustovetsky T, Engleman EA, Brustovetsky N, Cummins TR et al. Calcium/calmodulin-dependent protein kinase II (CaMKII) inhibition induces neurotoxicity via dysregulation of glutamate/calcium signaling and hyperexcitability. J Biol Chem 2012; 287: 8495–8506.
19. Ashpole NM, Hudmon A. Excitotoxic neuroprotection and vulnerability with CaMKII inhibition. Mol Cell Neurosci 2011; 46: 720–730.
20. Vest RS, O'Leary H, Coultrap SJ, Kindy MS, Bayer KU. Effective post-insult neuroprotection by a novel Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) inhibitor. J Biol Chem 2010; 285: 20675–20682.
21. Laabich A, Cooper NG. Neuroprotective effect of AIP on N-methyl-D-aspartate-induced cell death in retinal neurons. Brain Res Mol Brain Res 2000; 85: 32–40.
22. Hajimohammadreza I, Probert AW, Coughenour LL, Borosky SA, Marcoux FW, Boxer PA et al. A specific inhibitor of calcium/calmodulin-dependent protein kinase-II provides neuroprotection against NMDA-and hypoxia/hypoglycemia-induced cell death. J Neurosci 1995; 15: 4093–4101.
23. Goebel DJ. Selective blockade of CaMKII-alpha inhibits NMDA-induced caspase-3-dependent cell death but does not arrest PARP-1 activation or loss of plasma membrane selectivity in rat retinal neurons. Brain Res 2009; 1256: 190–204.
24. Fan W, Agarwal N, Cooper NG. The role of CaMKII in BDNF-mediated neuroprotection of retinal ganglion cells (RGC-5). Brain Res 2006; 1067: 48–57.
25. Bayer KU, Lohler J, Schulman H, Harbers K. Developmental expression of the CaM kinase II isoforms: ubiquitous gamma-and delta-CaM kinase II are the early isoforms and most abundant in the developing nervous system. Brain Res Mol Brain Res 1999; 70: 147–154.
26. Dharap A, Bowen K, Place R, Li LC, Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 2009; 29: 675–687.
27. Begum G, Yuan H, Kahle KT, Li L, Wang S, Shi Y et al. Inhibition of WNK3 kinase signaling reduces brain damage and accelerates neurological recovery after stroke. Stroke 2015; 46: 1956–1965.
28. Van der Valk JB, Vijverberg HP. Glutamate-induced inward current in a clonal neuroblastoma cell line. Eur J Pharmacol 1990; 185: 99–102.
29. Moon JM, Xu L, Giffard RG. Inhibition of microRNA-181 reduces forebrain ischemia-induced neuronal loss. J Cereb Blood Flow Metab 2013; 33: 1976–1982.
30. Van Moorhem M, Decrock E, Coussee E, Faes L, De Vuyst E, Vranckx K et al. L-beta-ODAP alters mitochondrial Ca2+ handling as an early event in excitotoxicity. Cell Calcium 2010; 47: 287–296.
31. Mayer P, Mohlig M, Idlibe D, Pfeiffer A. Novel and uncommon isoforms of the calcium sensing enzyme calcium/calmodulin dependent protein kinase II in heart tissue. Basic Res Cardiol 1995; 90: 372–379.
32. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB et al. Executive summary: heart disease and stroke statistics–2013 update: a report from the American Heart Association. Circulation 2013; 127: 143–152.
33. Kung JT, Colognori D, Lee JT. Long noncoding RNAs: past, present, and future. Genetics 2013; 193: 651–669.
34. Zhang M, Shan H, Gu Z, Wang D, Wang T, Wang Z et al. Increased expression of calcium/calmodulin-dependent protein kinase type II subunit delta after rat traumatic brain injury. J Mol Neurosci 2012; 46: 631–643.
35. Ghosh A, Greenberg ME. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 1995; 268: 239–247.
36. Duckworth EA, Butler T, Collier L, Collier S, Pennypacker KR. NF-kappaB protects neurons from ischemic injury after middle cerebral artery occlusion in mice. Brain Res 2006; 1088: 167–175.
37. Kaltschmidt B, Kaltschmidt C. NF-kappaB in the nervous system. Cold Spring Harb Perspect Biol 2009; 1: a001271.
38. Schneider A, Martin-Villalba A, Weih F, Vogel J, Wirth T, Schwaninger M. NF-kappaB is activated and promotes cell death in focal cerebral ischemia. Nat Med 1999; 5: 554–559.
39. Ling H, Gray CB, Zambon AC, Grimm M, Gu Y, Dalton N et al. Ca2+/Calmodulin-dependent protein kinase II delta mediates myocardial ischemia/reperfusion injury through nuclear factor-kappaB. Circ Res 2013; 112: 935–944.
40. Chi W, Meng F, Li Y, Wang Q, Wang G, Han S et al. Downregulation of miRNA-134 protects neural cells against ischemic injury in N2A cells and mouse brain with ischemic stroke by targeting HSPA12B. Neuroscience 2014; 277: 111–122.
41. Gagnon KT, Li L, Chu Y, Janowski BA, Corey DR. RNAi factors are present and active in human cell nuclei. Cell Rep 2014; 6: 211–221.
42. Coassin SR, Orjalo AV Jr., Semaan SJ, Johansson HE. Simultaneous detection of nuclear and cytoplasmic RNA variants utilizing Stellaris(R) RNA fluorescence in situ hybridization in adherent cells. Methods Mol Biol 2014; 1211: 189–199.
43. Ashwal S, Tone B, Tian HR, Cole DJ, Liwnicz BH, Pearce WJ. Core and penumbral nitric oxide synthase activity during cerebral ischemia and reperfusion in the rat pup. Pediatr Res 1999; 46: 390–400.
44. Chen J, Deng F, Singh SV, Wang QJ. Protein kinase D3 (PKD3) contributes to prostate cancer cell growth and survival through a PKCepsilon/PKD3 pathway downstream of Akt and ERK 1/2. Cancer Res 2008; 68: 3844–3853.