A decrease in phosphorylation of cAMP-response element-binding protein (CREBP) promotes retinal degeneration

Experimental Eye Research

Volumn 92, Issue 6, 2011, Pages 528-536

  Mali, Raghuveer S ^a   Zhang, Xiao M ^a   Chintala, Shravan K ^a  

^a OAKLAND UNIVERSITY   (United States)

Author keywords

Amacrine cells; Apoptosis; CREBP; Excitotoxicity; Ganglion cells; Retina; Retinal degeneration

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; KAINIC ACID; SERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; EXCITOTOXICITY; GEL MOBILITY SHIFT ASSAY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETINA AMACRINE CELL; RETINA DEGENERATION; RETINA GANGLION CELL; WESTERN BLOTTING;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; AMACRINE CELLS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CREB-BINDING PROTEIN; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INTRAVITREAL INJECTIONS; KAINIC ACID; MICE; PHOSPHORYLATION; RETINA; RETINAL DEGENERATION; RETINAL GANGLION CELLS; SERINE;

EID: 79956366230     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2011.03.017     Document Type: Article

References (44)

1. Alberts A.S., Arias J., Hagiwara M., Montminy M.R., Feramisco J.R. Recombinant cyclic AMP response element binding protein (CREB) phosphorylated on Ser-133 is transcriptionally active upon its introduction into fibroblast nuclei. J. Biol. Chem. 1994, 269:7623-7630.
2. Bito H., Deisseroth K., Tsien R.W. CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 1996, 87:1203-1214.
3. Chidlow G., Osborne N.N. Rat retinal ganglion cell loss caused by kainate, NMDA and ischemia correlates with a reduction in mRNA and protein of Thy-1 and neurofilament light. Brain Res. 2003, 963:298-306.
4. Chintala S.K., Sawaya R., Aggarwal B.B., Majumder S., Giri D.K., Kyritsis A.P., Gokaslan Z.L., Rao J.S. Induction of matrix metalloproteinase-9 requires a polymerized actin cytoskeleton in human malignant glioma cells. J. Biol. Chem. 1998, 273:13545-13551.
5. Choi J.S., Kim J.A., Joo C.K. Activation of MAPK and CREB by GM1 induces survival of RGCs in the retina with axotomized nerve. Invest. Ophthalmol. Vis. Sci. 2003, 44:1747-1752.
6. Dragunow M., Beilharz E., Sirimanne E., Lawlor P., Williams C., Bravo R., Gluckman P. Immediate-early gene protein expression in neurons undergoing delayed death, but not necrosis, following hypoxic-ischaemic injury to the young rat brain. Brain Res. Mol. Brain Res. 1994, 25:19-33.
7. Hansen H.H., Briem T., Dzietko M., Sifringer M., Voss A., Rzeski W., Zdzisinska B., Thor F., Heumann R., Stepulak A., Bittigau P., Ikonomidou C. Mechanisms leading to disseminated apoptosis following NMDA receptor blockade in the developing rat brain. Neurobiol. Dis. 2004, 16:440-453.
8. Harada T., Imaki J., Hagiwara M., Ohki K., Takamura M., Ohashi T., Matsuda H., Yoshida K. Phosphorylation of CREB in rat retinal cells after focal retinal injury. Exp. Eye Res. 1995, 61:769-772.
9. Impey S., Smith D.M., Obrietan K., Donahue R., Wade C., Storm D.R. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat. Neurosci. 1998, 1:595-601.
10. Isenoumi K., Kumai T., Kitaoka Y., Motoki M., Kuribayashi K., Munemasa Y., Kogo J., Kobayashi S., Ueno S. N-methyl-D-aspartate induces phosphorylation of cAMP response element (CRE)-binding protein and increases DNA-binding activity of CRE in rat retina. J. Pharmacol. Sci. 2004, 95:108-114.
11. Johannessen M., Delghandi M.P., Moens U. What turns CREB on?. Cell. Signal. 2004, 16:1211-1227.
12. Kasahara J., Fukunaga K., Miyamoto E. Activation of Ca (2+)/calmodulin-dependent protein kinase IV in cultured rat hippocampal neurons. J. Neurosci. Res. 2000, 59:594-600.
13. Kim H.S., Park C.K. Retinal ganglion cell death is delayed by activation of retinal intrinsic cell survival program. Brain Res. 2005, 1057:17-28.
14. Lee B., Butcher G.Q., Hoyt K.R., Impey S., Obrietan K. Activity-dependent neuroprotection and cAMP response element-binding protein (CREB): kinase coupling, stimulus intensity, and temporal regulation of CREB phosphorylation at serine 133. J. Neurosci. 2005, 25:1137-1148.
15. Lee J.K., Choi S.S., Lee H.K., Han K.J., Han E.J., Suh H.W. Effects of MK-801 and CNQX on various neurotoxic responses induced by kainic acid in mice. Mol. Cells 2002, 14:339-347.
16. Lonze B.E., Riccio A., Cohen S., Ginty D.D. Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 2002, 34:371-385.
17. Mabuchi T., Kitagawa K., Kuwabara K., Takasawa K., Ohtsuki T., Xia Z., Storm D., Yanagihara T., Hori M., Matsumoto M. Phosphorylation of cAMP response element-binding protein in hippocampal neurons as a protective response after exposure to glutamate in vitro and ischemia in vivo. J. Neurosci. 2001, 21:9204-9213.
18. Mali R.S., Cheng M., Chintala S.K. Plasminogen activators promote excitotoxicity-induced retinal damage. FASEB J. 2005, 19:1280-1289.
19. Manabe S., Lipton S.A. Divergent NMDA signals leading to proapoptotic and antiapoptotic pathways in the rat retina. Invest. Ophthalmol. Vis. Sci. 2003, 44:385-392.
20. Montminy M.R., Gonzalez G.A., Yamamoto K.K. Regulation of cAMP-inducible genes by CREB. Trends Neurosci. 1990, 13:184-188.
21. Montminy M.R., Sevarino K.A., Wagner J.A., Mandel G., Goodman R.H. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc. Natl. Acad. Sci. U S A 1986, 83:6682-6686.
22. Morgan I.G., Ingham C.A. Kainic acid affects both plexiform layers of chicken retina. Neurosci. Lett. 1981, 21:275-280.
23. Nadal-Nicolas F.M., Jimenez-Lopez M., Sobrado-Calvo P., Nieto-Lopez L., Canovas-Martinez I., Salinas-Navarro M., Vidal-Sanz M., Agudo M. Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest. Ophthalmol. Vis. Sci. 2009, 50:3860-3868.
24. Nateri A.S., Raivich G., Gebhardt C., Da Costa C., Naumann H., Vreugdenhil M., Makwana M., Brandner S., Adams R.H., Jefferys J.G., Kann O., Behrens A. ERK activation causes epilepsy by stimulating NMDA receptor activity. EMBO J. 2007, 26:4891-4901.
25. Ramirez M., Lamas M. NMDA receptor mediates proliferation and CREB phosphorylation in postnatal Muller glia-derived retinal progenitors. Mol. Vis. 2009, 15:713-721.
26. Schwarcz R., Coyle J.T. Kainic acid: neurotoxic effects after intraocular injection. Invest. Ophthalmol. Vis. Sci. 1977, 16:141-148.
27. Shaywitz A.J., Greenberg M.E. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 1999, 68:821-861.
28. Siliprandi R., Canella R., Carmignoto G., Schiavo N., Zanellato A., Zanoni R., Vantini G. N-methyl-d-aspartate-induced neurotoxicity in the adult rat retina. Vis. Neurosci. 1992, 8:567-573.
29. Soderling T.R. CaM-kinases: modulators of synaptic plasticity. Curr. Opin. Neurobiol. 2000, 10:375-380.
30. Sucher N.J., Aizenman E., Lipton S.A. N-methyl-d-aspartate antagonists prevent kainate neurotoxicity in rat retinal ganglion cells in vitro. J. Neurosci. 1991, 11:966-971.
31. Suh H.W., Lee H.K., Seo Y.J., Kwon M.S., Shim E.J., Lee J.Y., Choi S.S., Lee J.H. Kainic acid (KA)-induced Ca2+/calmodulin-dependent protein kinase II (CaMK II) expression in the neurons, astrocytes and microglia of the mouse hippocampal CA3 region, and the phosphorylated CaMK II only in the hippocampal neurons. Neurosci. Lett. 2005, 381:223-227.
32. Sun P., Enslen H., Myung P.S., Maurer R.A. Differential activation of CREB by Ca2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes. Dev. 1994, 8:2527-2539.
33. Wadzinski B.E., Wheat W.H., Jaspers S., Peruski L.F., Lickteig R.L., Johnson G.L., Klemm D.J. Nuclear protein phosphatase 2A dephosphorylates protein kinase A-phosphorylated CREB and regulates CREB transcriptional stimulation. Mol. Cell. Biol. 1993, 13:2822-2834.
34. Walton M., Woodgate A.M., Muravlev A., Xu R., During M.J., Dragunow M. CREB phosphorylation promotes nerve cell survival. J. Neurochem. 1999, 73:1836-1842.
35. Walton M.R., Dragunow I. Is CREB a key to neuronal survival?. Trends Neurosci. 2000, 23:48-53.
36. Wang J.Q., Fibuch E.E., Mao L. Regulation of mitogen-activated protein kinases by glutamate receptors. J. Neurochem. 2007, 100:1-11.
37. Wang N., Chintala S.K., Fini M.E., Schuman J.S. Ultrasound activates the TM ELAM-1/IL-1/NF-kappaB response: a potential mechanism for intraocular pressure reduction after phacoemulsification. Invest. Ophthalmol. Vis. Sci. 2003, 44:1977-1981.
38. Wilson B.E., Mochon E., Boxer L.M. Induction of bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Mol. Cell. Biol. 1996, 16:5546-5556.
39. Wu G.Y., Deisseroth K., Tsien R.W. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. U S A 2001, 98:2808-2813.
40. Xing J., Ginty D.D., Greenberg M.E. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 1996, 273:959-963.
41. Yoshida K., Imaki J., Matsuda H., Hagiwara M. Light-induced CREB phosphorylation and gene expression in rat retinal cells. J. Neurochem. 1995, 65:1499-1504.
42. Zhang X., Cheng M., Chintala S.K. Kainic acid-mediated upregulation of matrix metalloproteinase-9 p.omotes retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2004, 45:2374-2383.
43. Zhang X., Cheng M., Chintala S.K. Optic nerve ligation leads to astrocyte-associated matrix metalloproteinase-9 induction in the mouse retina. Neurosci. Lett. 2004, 356:140-144.
44. Zhang X., Odom D.T., Koo S.H., Conkright M.D., Canettieri G., Best J., Chen H., Jenner R., Herbolsheimer E., Jacobsen E., Kadam S., Ecker J.R., Emerson B., Hogenesch J.B., Unterman T., Young R.A., Montminy M. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc. Natl. Acad. Sci. U S A 2005, 102:4459-4464.