Overexpression of DSCR1 blocks zinc-induced neuronal cell death through the formation of nuclear aggregates

Molecular and Cellular Neuroscience

Volumn 35, Issue 4, 2007, Pages 585-595

  Lee, Eun Jung ^a   Lee, Jae Youn ^a   Seo, Su Ryeon ^b   Chung, Kwang Chul ^a  

^a Yonsei University   (South Korea)

^b Kangwon National University   (South Korea)

Author keywords

Aggregate; Alzheimer's disease; Down syndrome; DSCR1; H19 7; Neuronal cell death; Ubiquitin proteasome; Zinc

Indexed keywords

ZINC;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DEGRADATION KINETICS; DOWN SYNDROME; DOWN SYNDROME CANDIDATE REGION GENE 1; EMBRYO; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; GENE; GENE OVEREXPRESSION; MOLECULAR BIOLOGY; NERVE CELL NECROSIS; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; STATISTICAL SIGNIFICANCE; UPREGULATION;

ANIMALS; CALCINEURIN; CELL DEATH; CELL LINE; CELL NUCLEUS; CYTOPROTECTION; EMBRYO; HIPPOCAMPUS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUSCLE PROTEINS; NEURONS; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRIDINES; RATS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; STEM CELLS; THIONES; ZINC;

EID: 34547425301     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2007.05.003     Document Type: Article

References (50)

1. Beyersmann D., and Haase H. Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biometals 14 (2001) 331-341
2. Blagosklonny M.V., Wu G.S., Omura S., and el-Deiry W.S. Proteasome-dependent regulation of p21WAF1/CIP1 expression. Biochem. Biophys. Res. Commun. 227 (1996) 564-569
3. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., Taddei N., Ramponi G., Dobson C.M., and Stefani M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
4. Chang Y.C., Lee Y.S., Tejima T., Tanaka K., Omura S., Heintz N.H., Mitsui Y., and Magae J. Mdm2 and bax, downstream mediators of the p53 response, are degraded by the ubiquitin-proteasome pathway. Cell Growth Differ. 9 (1998) 79-84
5. Choi D.W., and Koh J.Y. Zinc and brain injury. Annu. Rev. Neurosci. 21 (1998) 347-375
6. Cook C.N., Hejna M.J., Magnuson D.J., and Lee J.M. Expression of calcipressin1, an inhibitor of the phosphatase calcineurin, is altered with aging and Alzheimer's disease. J. Alzheimer's Dis. 8 (2005) 63-73
7. Cuajungco M.P., and Lees G.J. Zinc metabolism in the brain: relevance to human neurodegenerative disorders. Neurobiol. Dis. 4 (1997) 137-169
8. Coyle J.T., Oster-Granite M.L., and Gearhart J.D. The neurobiologic consequences of Down syndrome. Brain Res. Bull. 16 (1986) 773-787
9. Desdouits F., Buxbaum J.D., Desdouits-Magnen J., Nairn A.C., and Greengard P. Amyloid β peptide formation in cell-free preparations. Regulation by protein kinase C, calmodulin, and calcineurin. J. Biol. Chem. 271 (1996) 24670-24674
10. Epstein C.J. Epilogue: toward the twenty-first century with Down syndrome-a personal view of how far we have come and of how far we can reasonably expect to go. Prog. Clin. Biol. Res. 393 (1995) 241-246
11. Ermak G., Margan T.E., and Davies K.J. Chronic overexpression of the calcineurin inhibitory gene DSCR1 (Adapt78) is associated with Alzheimer's disease. J. Biol. Chem. 276 (2001) 38787-38794
12. Ermak G., Harris C.D., and Davies K.J. The DSCR1 (Adapt78) isoform 1 protein calcipressin 1 inhibits calcineurin and protects against acute calcium-mediated stress damage, including transient oxidative stress. FASEB J. 16 (2002) 814-824
13. Ermak G., Harris C.D., Battocchio D., and Davies K.J. RCAN (DSCR1 or Adapt78) stimulates expression of GSK-3β. FEBS J. 273 (2006) 2100-2109
14. Fuentes J.J., Pritchard M.A., Planas A.M., Bosch A., Ferrer I., and Estivill X. A new human gene from the Down syndrome critical region encodes a proline-rich protein highly expressed in fetal brain and heart. Hum. Mol. Genet. 4 (1995) 1935-1944
15. Fuentes J.J., Pritchard M.A., and Estivill X. Genomic organization, alternative splicing, and expression patterns of the DSCR1 (Down Syndrome Critical Region 1). Gene Genomics 44 (1997) 358-361
16. Fuentes J.J., Genesca L., Kingsbury T.J., Cunningham K.W., Perez-Riba M., Estivill X., and de la Luna S. DSCR1, overexpressed in Down syndrome, is an inhibitor of calcineurin-mediated signaling pathways. Hum. Mol. Genet. 9 (2000) 1681-1690
17. Harris C.D., Ermak G., and Davies K.J. Multiple roles of the DSCR1 (Adapt78 or RCAN1) gene and its protein product calcipressin 1 (or RCAN1) in disease. Cell. Mol. Life Sci. 62 (2005) 2477-2486
18. Hasegawa T., Matsuzaki M., Takeda A., Kikuchi A., Akita H., Perry G., Smith M.A., and Itoyama Y. Accelerated α-synuclein aggregation after differentiation of SH-SY5Y neuroblastoma cells. Brain Res. 1013 (2004) 51-59
19. Hesser B.A., Liang X.H., Camenisch G., Yang S., Lewin D.A., Scheller R., Ferrara N., and Gerber H.P. Down syndrome critical region protein 1 (DSCR1), a novel VEGF target gene that regulates expression of inflammatory markers on activated endothelial cells. Blood 104 (2004) 149-158
20. Kayyali U.S., Zhang W., Yee A.G., Seidman J.G., and Potter H. Cytoskeletal changes in the brains of mice lacking calcineurin Aα. J. Neurochem. 68 (1997) 1668-1678
21. Kim I., Kim C.H., Kim J.H., Lee J., Choi J.J., Chen Z.A., Lee M.G., Chung K.C., Hsu C.Y., and Ahn Y.S. Pyrrolidine dithiocarbamate and zinc inhibit proteasome-dependent proteolysis. Exp. Cell Res. 298 (2004) 229-238
22. Koh J.Y. Zinc and disease of the brain. Mol. Neurobiol. 24 (2001) 99-106
23. Kozin S.A., Zirah S., Rebuffat S., Hoa G.H., and Debey P. Zinc binding to Alzheimer's Aβ(1-16) peptide results in stable soluble complex. Biochem. Biophys. Res. Commun. 285 (2001) 959-964
24. Kubbutat M.H., and Vousden K.H. Proteolytic cleavage of human p53 by calpain: a potential regulator of protein stability. Mol. Cell. Biol. 17 (1997) 460-468
25. Kuemmerle S., Gutekunst C.A., Klein A.M., Li X.J., Li S.H., Beal M.F., Hersch S.M., and Ferrante R.J. Huntington aggregates may not predict neuronal death in Huntington's disease. Ann. Neurol. 46 (1999) 842-849
26. Leahy K.P., and Crawford D.R. Adapt78 protects cells against stress damage and suppresses cell growth. Arch. Biochem. Biophys. 379 (2000) 221-228
27. Lee J.Y., Mook-Jung I., and Koh J.Y. Histochemically reactive zinc in plaques of the Swedish mutant β-amyloid precursor protein transgenic mice. J. Neurosci. 19 (1999) RC10
28. Li Q.X., Evin G., Small D.H., Multhaup G., Beyreuther K., and Masters C.L. Proteolytic processing of Alzheimer's disease βA4 amyloid precursor protein in human platelets. J. Biol. Chem. 270 (1995) 14140-14147
29. Lukiw W.J., and Bazan N.G. Neuroinflammatory signaling upregulation in Alzheimer's disease. Neurochem. Res. 25 (2000) 1173-1184
30. Ma H., Xiong H., Liu T., Zhang L., Godzik A., and Zhang Z. Aggregate formation and synaptic abnormality induced by DSCR1. J. Neurochem. 88 (2004) 1485-1496
31. Maki C.G., Huibregtse J.M., and Howley P.M. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res. 56 (1996) 2649-2654
32. Maynard C.J., Bush A.I., Masters C.L., Cappai R., and Li Q.X. Metals and amyloid-β in Alzheimer's disease. Int. J. Exp. Pathol. 86 (2005) 147-159
33. Min Y.K., Park J.H., Chong S.A., Kim Y.S., Ahn Y.S., Seo J.T., Bae Y.S., and Chung K.C. Pyrrolidine dithiocarbamate-induced neuronal cell death is mediated by Akt, casein kinase 2, c-Jun N-terminal kinase, and IêB kinase in embryonic hippocampal progenitor cells. J. Neurosci. Res. 71 (2003) 689-700
34. Min Y.K., Lee J.E., and Chung K.C. Zinc induces cell death in immortalized embryonic hippocampal cells via activation of Akt-GSK-3β signaling. Exp. Cell Res. 313 (2007) 312-321
35. Muchowski P.J., Ning K., D'Souza-Schorey C., and Fields S. Requirement of an intact microtubule cytoskeleton for aggregation and inclusion body formation by a mutant huntingtin fragment. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 727-732
36. Pfister S.C., Machado-Santelli G.M., Han S.W., and Henrique-Silva F. Mutational analyses of the signals involved in the subcellular location of DSCR1. BMC Cell Biol. 3 (2002) 24
37. Religa D., Strozyk D., Cherny R.A., Volitakis I., Haroutunian V., Winblad B., Naslund J., and Bush A.I. Elevated cortical zinc in Alzheimer disease. Neurology 67 (2006) 69-75
38. Roizen N.J., and Patterson D. Down's syndrome. Lancet 361 (2003) 1281-128
39. Ross C.A., and Poirier M.A. Opinion: what is the role of protein aggregation in neurodegeneration?. Nat. Rev., Mol. Cell Biol. 26 (2005) 891-898
40. Rothermel B.A., Vega R.B., Yang J., Wu H., Bassel-Duby R., and Williams R.S. A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling. J. Biol. Chem. 275 (2000) 8719-8725
41. Rothermel B.A., McKinsey T.A., Vega R.B., Nicol R.L., Mammen P., Yang J., Antos C.L., Shelton J.M., Bassel-Duby R., Olson E.N., and Williams R.S. Myocyte-enriched calcineurin-interacting protein, MCIP1, inhibits cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 3328-3333
42. Ryeom S., Greenwald R.J., Sharpe A.H., and Mckeon F. The threshold pattern of calcineurin-dependent gene expression is altered by loss of the endogenous inhibitor calcipressin. Nat. Immunol. 4 (2003) 874-881
43. Sanna B., Brandt E.B., Kaiser R.A., Pfluger P., Witt S., Kimball A., van Rooij R., De Windt E., Rothenberg L.J., Tschop E., Benoit M.H., and Molkentin S.C. Modulatory calcineurin-interacting proteins 1 and 2 function as calcineurin facilitators in vivo. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 7327-7332
44. Smedman M., Potempska A., Rubenstein R., Ju W., Ramakrishna N., and Denman R.B. Effects of cadmium, copper, and zinc and βAPP processing and turnover in COS-7 and PC12 cells. Mol. Chem. Neuropathol. 31 (1997) 13-28
45. Suzuki K., Miura T., and Takeuchi H. Inhibitory effect of copper(II) on zinc(II)-induced aggregation of amyloid β-peptide. Biochem. Biophys. Res. Commun. 285 (2001) 991-996
46. Tanaka M., Kim Y.M., Lee G., Junn E., Iwatsubo T., and Mouradian M.M. Aggresomes formed by α-synuclein and synphilin-1 are cytoprotective. J. Biol. Chem. 279 (2004) 4625-4631
47. Toyoda A., Noguchi H., Taylor T.D., Ito T., Pletcher M.T., Sakaki Y., Reeves R.H., and Hattori M. Comparative genomic sequence analysis of the human chromosome 21 Down syndrome critical region. Genome Res. 12 (2002) 1323-1332
48. Vega R.B., Rothermel B.A., Weinheimer C.J., Kovacs A., Naseem R.H., Bassel-Duby R., Williams R.S., and Olson E.N. Dual roles of modulatory calcineurin-interacting protein 1 in cardiac hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 669-674
49. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., and Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416 (2002) 535-539
50. Yao Y.G., and Duh E.J. VEGF selectively induces Down syndrome critical region 1 gene expression in endothelial cells: a mechanism for feedback regulation of angiogenesis?. Biochem. Biophys. Res. Commun. 321 (2004) 648-656