Epigenetic changes induced by adenosine augmentation therapy prevent epileptogenesis

Journal of Clinical Investigation

Volumn 123, Issue 8, 2013, Pages 3552-3563

  Williams Karnesky, Rebecca L ^a,b   Sandau, Ursula S ^a   Lusardi, Theresa A ^a   Lytle, Nikki K ^a   Farrell, Joseph M ^a   Pritchard, Eleanor M ^c   Kaplan, David L ^c   Boison, Detlev ^a,b  

^a LEGACY RESEARCH   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c Tufts University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; DNA; DNA METHYLTRANSFERASE; HOMOCYSTEINE; S ADENOSYLMETHIONINE; SILK;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICONVULSANT THERAPY; ARTICLE; BRAIN; CONTROLLED STUDY; DNA METHYLATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; ENZYME ACTIVITY; EPIGENETICS; EPILEPTOGENESIS; HIPPOCAMPAL MOSSY FIBER; HIPPOCAMPUS; IMPLANT; MALE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECURRENT DISEASE; SEIZURE; SIGNAL TRANSDUCTION; SILK IMPLANT; TEMPORAL LOBE EPILEPSY;

ADENOSINE; ADENOSINE KINASE; ANIMALS; ANTICONVULSANTS; AZACITIDINE; BASE SEQUENCE; BRAIN; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DRUG IMPLANTS; EPIGENESIS, GENETIC; EPILEPSY; MALE; MICE; MOSSY FIBERS, HIPPOCAMPAL; RATS; RATS, SPRAGUE-DAWLEY; SEQUENCE ANALYSIS, DNA;

EID: 84879710932     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI65636     Document Type: Article

References (48)

1. Löscher W, Brandt C. Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol Rev. 2010;62(4):668-700.
2. Kobow K, Blümcke I. The methylation hypothesis: do epigenetic chromatin modifications play a role in epileptogenesis? Epilepsia. 2011;52(suppl 4):15-19.
3. Qureshi IA, Mehler MF. Epigenetic mechanisms underlying human epileptic disorders and the process of epileptogenesis. Neurobiol Dis. 2010; 39(1):53-60.
4. Feng J, et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci. 2010; 13(4):423-430.
5. Ma DK, et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science. 2009;323(5917):1074-1077.
6. Nelson ED, Kavalali ET, Monteggia LM. Activitydependent suppression of miniature neurotransmission through the regulation of DNA methylation. J Neurosci. 2008;28(2):395-406.
7. Kobow K, et al. Increased reelin promoter methylation is associated with granule cell dispersion in human temporal lobe epilepsy. J Neuropathol Exp Neurol. 2009;68(4):356-364.
8. Lubin FD. Epileptogenesis: can the science of epigenetics give us answers? Epilepsy Curr. 2012; 12(3):105-110.
9. Kredich NM, Martin DV. Role of S-adenosylhomocysteine in adenosinemediated toxicity in cultured mouse T lymphoma cells. Cell. 1977;12(4):931-938.
10. Boison D, et al. Neonatal hepatic steatosis by disruption of the adenosine kinase gene. Proc Natl Acad Sci U S A. 2002;99(10):6985-6990.
11. Fredholm BB. Rethinking the purinergic neuronglia connection. Proc Natl Acad Sci U S A. 2012; 109(16):5913-5914.
12. Boison D. Adenosine kinase: exploitation for therapeutic gain. Pharmacol Rev. 2013;65(3):906-943.
13. Pignataro G, Maysami S, Studer FE, Wilz A, Simon RP, Boison D. Downregulation of hippocampal adenosine kinase after focal ischemia as potential endogenous neuroprotective mechanism. J Cereb Blood Flow Metab. 2008;28(1):17-23.
14. James SJ, Melnyk S, Pogribna M, Pogribny IP, Caudill MA. Elevation in S-adenosylhomocysteine and DNA hypomethylation: potential epigenetic mechanism for homocysteine-related pathology. J Nutr. 2002;132(8 suppl):2361S-2366S.
15. Boison D. Adenosine kinase, epilepsy and stroke: mechanisms and therapies. Trends Pharmacol Sci. 2006;27(12):652-658.
16. Johansson B, et al. Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc Natl Acad Sci U S A. 2001;98(16):9407-9412.
17. Boison D. Adenosine as a modulator of brain activity. Drug News Persp. 2007;20(10):607-611.
18. Lovatt D, et al. Neuronal adenosine release, and not astrocytic ATP release, mediates feedback inhibition of excitatory activity. Proc Natl Acad Sci U S A. 2012; 109(16):6265-6270.
19. Boison D, Chen JF, Fredholm BB. Adenosine signalling and function in glial cells. Cell Death Differ. 2010; 17(7):1071-1082.
20. Boison D. Adenosine augmentation therapies (AATs) for epilepsy: prospect of cell and gene therapies. Epilepsy Res. 2009;85(2-3):131-141.
21. Li T, et al. Adenosine kinase is a target for the prediction and prevention of epileptogenesis in mice. J Clin Invest. 2008;118(2):571-582.
22. Masino SA, et al. A ketogenic diet suppresses seizures in mice through adenosine A1 receptors. J Clin Invest. 2011;121(7):2679-2683.
23. Shen HY, Lusardi TA, Williams-Karnesky RL, Lan JQ, Poulsen DJ, Boison D. Adenosine kinase determines the degree of brain injury after ischemic stroke in mice. J Cereb Blood Flow Metab. 2011;31(7):1648-1659.
24. Gouder N, Fritschy JM, Boison D. Seizure suppression by adenosine A1 receptor activation in a mouse model of pharmacoresistant epilepsy. Epilepsia. 2003;44(7):877-885.
25. Cui XA, Singh B, Park J, Gupta RS. Subcellular localization of adenosine kinase in mammalian cells: The long isoform of AdK is localized in the nucleus. Biochem Biophys Res Commun. 2009; 388(1):46-50.
26. Huber A, Padrun V, Deglon N, Aebischer P, Mohler H, Boison D. Grafts of adenosine-releasing cells suppress seizures in kindling epilepsy. Proc Natl Acad Sci U S A. 2001;98(1):7611-7616.
27. Szybala C, Pritchard EM, Wilz A, Kaplan DL, Boison D. Antiepileptic effects of silk-polymer based adenosine release in kindled rats. Exp Neurol. 2009; 219(1):126-135.
28. Wilz A, Pritchard EM, Li T, Lan JQ, Kaplan DL, Boison D. Silk polymer-based adenosine release: Therapeutic potential for epilepsy. Biomaterials. 2008; 29(26):3609-3616.
29. Gouder N, Scheurer L, Fritschy J-M, Boison D. Overexpression of adenosine kinase in epileptic hippocampus contributes to epileptogenesis. J Neurosci. 2004;24(3):692-701.
30. Pitkanen A, Lukasiuk K. Mechanisms of epileptogenesis and potential treatment targets. Lancet Neurol. 2011;10(2):173-186.
31. Dudek FE, Staley KJ. The time course of acquired epilepsy: implications for therapeutic intervention to suppress epileptogenesis. Neurosci Lett. 2011; 497(3):240-246.
32. Dudek FE, Sutula TP. Epileptogenesis in the dentate gyrus: a critical perspective. Prog Brain Res. 2007; 163:755-773.
33. Csoka AB, Szyf M. Epigenetic side-effects of common pharmaceuticals: a potential new field in medicine and pharmacology. Med Hypotheses. 2009; 73(5):770-780.
34. Tsai HC, et al. Transient low doses of DNAdemethylating agents exert durable antitumor effects on hematological and epithelial tumor cells. Cancer Cell. 2012;21(3):430-446.
35. Zampieri M, et al. ADP-ribose polymers localized on Ctcf-Parp1-Dnmt1 complex prevent methylation of Ctcf target sites. Biochem J. 2012;441(2):645-652.
36. Henshall DC, Sinclair J, Simon RP. Relationship between seizure-induced transcription of the DNA damage-inducible gene GADD45, DNA fragmentation, and neuronal death in focally evoked limbic epilepsy. J Neurochem. 1999;73(4):1573-1583.
37. Aronica E, et al. Upregulation of adenosine kinase in astrocytes in experimental and human temporal lobe epilepsy. Epilepsia. 2011;52(9):1645-1655.
38. Rebola N, et al. Decrease of adenosine A1 receptor density and of adenosine neuromodulation in the hippocampus of kindled rats. Eur J Neurosci. 2003; 18(4):820-828.
39. Boison D. The adenosine kinase hypothesis of epileptogenesis. Prog Neurobiol. 2008;84(3):249-262.
40. Gray JH, Owen RP, Giacomini KM. The concentrative nucleoside transporter family, SLC28. Pflugers Arch. 2004;447(5):728-734.
41. Baldwin SA, Beal PR, Yao SY, King AE, Cass CE, Young JD. The equilibrative nucleoside transporter family, SLC29. Pflugers Arch. 2004;447(5):735-743.
42. de Tisi J, et al. The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet. 2011; 378(9800):1388-1395.
43. White HS, Wolf HH, Woodhead JH, Kupferberg HJ. The National Institutes of Health Anticonvulsant Drug Development Program: screening for efficacy. Adv Neurol. 1998;76:29-39.
44. Boison D, Huber A, Padrun V, Deglon N, Aebischer P, Mohler H. Seizure suppression by adenosinereleasing cells is independent of seizure frequency. Epilepsia. 2002;43(8):788-796.
45. Studer FE, et al. Shift of adenosine kinase expression from neurons to astrocytes during postnatal development suggests dual functionality of the enzyme. Neuroscience. 2006;142(1):125-137.
46. Cavazos JE, Golarai G, Sutula TP. Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J Neurosci. 1991;11(9):2795-2803.
47. Fedele DE, et al. Astrogliosis in epilepsy leads to overexpression of adenosine kinase resulting in seizure aggravation. Brain. 2005;128(Pt 10):2383-2395.
48. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics. 2002; 18(11):1427-1431.