Glycogen synthase kinase 3β inhibitors protect hippocampal neurons from radiation-induced apoptosis by regulating MDM2-p53 pathway

Cell Death and Differentiation

Volumn 19, Issue 3, 2012, Pages 387-396

  Thotala, D K ^a   Hallahan, D E ^a,b,c   Yazlovitskaya, E M ^d,e  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b USA   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

GSK 3 ; hippocampal neurons; ionizing radiation; MDM2; p53

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; 2 (3 CHLORO 4 HYDROXYANILINO) 3 (2 NITROPHENYL)MALEIMIDE; ACTIN; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN MDM2; PROTEIN P53; SHORT HAIRPIN RNA;

APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL PROTECTION; CELLULAR DISTRIBUTION; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME INHIBITION; HIPPOCAMPUS; HUMAN; HUMAN CELL; IONIZING RADIATION; NEUROPROTECTION; PRIORITY JOURNAL; RADIATION EXPOSURE; RADIATION PROTECTION;

ANIMALS; APOPTOSIS; CELL LINE, TRANSFORMED; ENZYME INHIBITORS; GAMMA RAYS; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; MICE; NEURONS; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-MDM2; RADIATION TOLERANCE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84857038779     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2011.94     Document Type: Article

References (46)

1. Deweer B, Pillon B, Pochon JB, Dubois B. Is the HM story only a 'remote memory'? Some facts about hippocampus and memory in humans. Behav Brain Res 2001; 127: 209-224. (Pubitemid 33062411)
2. Monje ML, Mizumatsu S, Fike JR, Palmer TD. Irradiation induces neural precursor-cell dysfunction. Nat Med 2002; 8: 955-962. (Pubitemid 35033699)
3. Nagai R, Tsunoda S, Hori Y, Asada H. Selective vulnerability to radiation in the hippocampal dentate granule cells. Surg Neurol 2000; 53: 503-506; discussion 506-507.
4. Peissner W, Kocher M, Treuer H, Gillardon F. Ionizing radiation-induced apoptosis of proliferating stem cells in the dentate gyrus of the adult rat hippocampus. Brain Res Mol Brain Res 1999; 71: 61-68. (Pubitemid 29320056)
5. Yazlovitskaya EM, Edwards E, Thotala D, Fu A, Osusky KL, Whetsell Jr. WO et al. Lithium treatment prevents neurocognitive deficit resulting from cranial irradiation. Cancer Res 2006; 66: 11179-11186. (Pubitemid 46009945)
6. Ferrer I, Serrano T, Alcantara S, Tortosa A, Graus F. X-ray-induced cell death in the developing hippocampal complex involves neurons and requires protein synthesis. J Neuropathol Exp Neurol 1993; 52: 370-378. (Pubitemid 23199197)
7. Mizumatsu S, Monje ML, Morhardt DR, Rola R, Palmer TD, Fike JR. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res 2003; 63: 4021-4027. (Pubitemid 36917922)
8. Madsen TM, Kristjansen PE, Bolwig TG, Wortwein G. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 2003; 119: 635-642. (Pubitemid 36694791)
9. Rola R, Raber J, Rizk A, Otsuka S, VandenBerg SR, Morhardt DR et al. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp Neurol 2004; 188: 316-330. (Pubitemid 38891593)
10. Raber J, Rola R, LeFevour A, Morhardt D, Curley J, Mizumatsu S et al. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 2004; 162: 39-47. (Pubitemid 39044717)
11. Thotala DK, Hallahan DE, Yazlovitskaya EM. Inhibition of glycogen synthase kinase 3 beta attenuates neurocognitive dysfunction resulting from cranial irradiation. Cancer Res 2008; 68: 5859-5868.
12. Embi N, Rylatt DB, Cohen P. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur J Biochem 1980; 107: 519-527.
13. Doble BW, Woodgett JR. GSK-3: Tricks of the trade for a multi-tasking kinase. J Cell Sci 2003; 116: 1175-1186. (Pubitemid 36410657)
14. Pap M, Cooper GM. Role of translation initiation factor 2B in control of cell survival by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta signaling pathway. Mol Cell Biol 2002; 22: 578-586. (Pubitemid 34027502)
15. Sanchez JF, Sniderhan LF, Williamson AL, Fan S, Chakraborty-Sett S, Maggirwar SB. Glycogen synthase kinase 3beta-mediated apoptosis of primary cortical astrocytes involves inhibition of nuclear factor kappaB signaling. Mol Cell Biol 2003; 23: 4649-4662. (Pubitemid 36734753)
16. Jope RS, Johnson GV. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 2004; 29: 95-102. (Pubitemid 38186580)
17. Beurel E, Jope RS. The paradoxical pro-And anti-Apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol 2006; 79: 173-189. (Pubitemid 44331500)
18. Bijur GN, De Sarno P, Jope RS. Glycogen synthase kinase-3beta facilitates staurosporineand heat shock-induced apoptosis. Protection by lithium. J Biol Chem 2000; 275: 7583-7590. (Pubitemid 30159657)
19. Grimes CA, Jope RS. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 2001; 65: 391-426. (Pubitemid 32781670)
20. Forde JE, Dale TC. Glycogen synthase kinase 3: A key regulator of cellular fate. Cell Mol Life Sci 2007; 64: 1930-1944. (Pubitemid 47094432)
21. Bijur GN, Jope RS. Glycogen synthase kinase-3 beta is highly activated in nuclei and mitochondria. Neuroreport 2003; 14: 2415-2419.
22. Ciani L, Salinas PC. WNTs in the vertebrate nervous system: From patterning to neuronal connectivity. Nat Rev Neurosci 2005; 6: 351-362. (Pubitemid 40593481)
23. Watcharasit P, Bijur GN, Zmijewski JW, Song L, Zmijewska A, Chen X et al. Direct, activating interaction between glycogen synthase kinase-3beta and p53 after DNA damage. Proc Natl Acad Sci USA 2002; 99: 7951-7955. (Pubitemid 34650986)
24. Eom TY, Roth KA, Jope RS. Neural precursor cells are protected from apoptosis induced by trophic factor withdrawal or genotoxic stress by inhibitors of glycogen synthase kinase 3. J Biol Chem 2007; 282: 22856-22864. (Pubitemid 47267357)
25. Oren M. Decision making by p53: Life, death and cancer. Cell Death Differ 2003; 10: 431-442. (Pubitemid 36626355)
26. Kruse JP, Gu W. Modes of p53 regulation. Cell 2009; 137: 609-622.
27. Watcharasit P, Bijur GN, Song L, Zhu J, Chen X, Jope RS. Glycogen synthase kinase-3beta (GSK3beta) binds to and promotes the actions of p53. J Biol Chem 2003; 278: 48872-48879.
28. Beurel E, Kornprobst M, Blivet-Van Eggelpoel MJ, Ruiz-Ruiz C, Cadoret A, Capeau J et al. GSK-3beta inhibition by lithium confers resistance to chemotherapy-induced apoptosis through the repression of CD95 (Fas/APO-1) expression. Exp Cell Res 2004; 300: 354-364. (Pubitemid 39314425)
29. Turenne GA, Price BD. Glycogen synthase kinase3 beta phosphorylates serine 33 of p53 and activates p53's transcriptional activity. BMC Cell Biol 2001; 2: 12.
30. Pluquet O, Qu LK, Baltzis D, Koromilas AE. Endoplasmic reticulum stress accelerates p53 degradation by the cooperative actions of Hdm2 and glycogen synthase kinase 3beta. Mol Cell Biol 2005; 25: 9392-9405. (Pubitemid 41507840)
31. Qu L, Huang S, Baltzis D, Rivas-Estilla AM, Pluquet O, Hatzoglou M et al. Endoplasmic reticulum stress induces p53 cytoplasmic localization and prevents p53-dependent apoptosis by a pathway involving glycogen synthase kinase-3beta. Genes Dev 2004; 18: 261-277. (Pubitemid 38199252)
32. Kulikov R, Boehme KA, Blattner C. Glycogen synthase kinase 3-dependent phosphorylation of Mdm2 regulates p53 abundance. Mol Cell Biol 2005; 25: 7170-7180. (Pubitemid 41105913)
33. Lu C, El-Deiry WS. Targeting p53 for enhanced radio-And chemo-sensitivity. Apoptosis 2009; 14: 597-606.
34. Johnson MD, Xiang H, London S, Kinoshita Y, Knudson M, Mayberg M et al. Evidence for involvement of Bax and p53, but not caspases, in radiation-induced cell death of cultured postnatal hippocampal neurons. J Neurosci Res 1998; 54: 721-733. (Pubitemid 28544374)
35. Limoli CL, Giedzinski E, Rola R, Otsuka S, Palmer TD, Fike JR. Radiation response of neural precursor cells: Linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress. Radiat Res 2004; 161: 17-27. (Pubitemid 38018720)
36. Silva R, Mesquita AR, Bessa J, Sousa JC, Sotiropoulos I, Leao P et al. Lithium blocks stress-induced changes in depressive-like behavior and hippocampal cell fate: The role of glycogen-synthase-kinase-3beta. Neuroscience 2008; 152: 656-669.
37. Min YK, Lee JE, Chung KC. Zinc induces cell death in immortalized embryonic hippocampal cells via activation of Akt-GSK-3beta signaling. Exp Cell Res 2007; 313: 312-321.
38. Ghosh JC, Altieri DC. Activation of p53-dependent apoptosis by acute ablation of glycogen synthase kinase-3beta in colorectal cancer cells. Clin Cancer Res 2005; 11: 4580-4588. (Pubitemid 40825649)
39. Lu R, Song L, Jope RS. Lithium attenuates p53 levels in human neuroblastoma SH-SY5Y cells. Neuroreport 1999; 10: 1123-1125. (Pubitemid 29318000)
40. Zmijewski JW, Jope RS. Nuclear accumulation of glycogen synthase kinase-3 during replicative senescence of human fibroblasts. Aging Cell 2004; 3: 309-317. (Pubitemid 40246699)
41. Shangary S, Wang S. Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: A novel approach for cancer therapy. Annu Rev Pharmacol Toxicol 2009; 49: 223-241.
42. van Leeuwen IM, Higgins M, Campbell J, Brown CJ, McCarthy AR, Pirrie L et al. Mechanism-specific signatures for small-molecule p53 activators. Cell Cycle 2011; 10: 1590-1598.
43. Villalonga-Planells R, Coll-Mulet L, Martinez-Soler F, Castano E, Acebes JJ, Gimenez-Bonafe P et al. Activation of p53 by nutlin-3a induces apoptosis and cellular senescence in human glioblastoma multiforme. PLoS One 2011; 6: E18588.
44. Meek DW, Knippschild U. Posttranslational modification of MDM2. Mol Cancer Res 2003; 1: 1017-1026. (Pubitemid 38044977)
45. Morimoto BH, Koshland Jr. DE. Induction and expression of long-And short-term neurosecretory potentiation in a neural cell line. Neuron 1990; 5: 875-880.
46. Persons DL, Yazlovitskaya EM, Pelling JC. Effect of extracellular signal-regulated kinase on p53 accumulation in response to cisplatin. J Biol Chem 2000; 275: 35778-35785.