CDK5-mediated phosphorylation of p19INK4d avoids DNA damage-induced neurodegeneration in mouse hippocampus and prevents loss of cognitive functions

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 7, 2014, Pages 1309-1324

  Ogara, María Florencia ^a   Belluscio, Laura M ^a   de la Fuente, Verónica ^a   Berardino, Bruno G ^a   Sonzogni, Silvina V ^a   Byk, Laura ^a   Marazita, Mariela ^a   Cánepa, Eduardo T ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Apoptosis; Beta amyloid peptide; DNA damage; Learning and memory; Neocarzinostatin; Neurodegeneration

Indexed keywords

CALCIUM; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE INHIBITOR 2D; DNA; RNA; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (25-35); CDK5 PROTEIN, MOUSE; CDKN2D PROTEIN, MOUSE; CYTOTOXIN; PEPTIDE FRAGMENT; ZINOSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL SURVIVAL; COGNITIVE DEFECT; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; EMBRYO; FEMALE; GENOTOXICITY; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOUSE; NERVE DEGENERATION; NEUROFEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; RAT; ANIMAL; COGNITION; CYTOLOGY; DRUG EFFECTS; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NERVE CELL; PHOSPHORYLATION; PHYSIOLOGY; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AMYLOID BETA-PEPTIDES; ANIMALS; APOPTOSIS; CALCIUM; CELL LINE, TUMOR; CELL SURVIVAL; COGNITION; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASE INHIBITOR P19; CYTOTOXINS; DNA DAMAGE; DNA REPAIR; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMANS; MICE; NEURONS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; ZINOSTATIN;

EID: 84928581524     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.03.026     Document Type: Article

References (58)

1. Becker E.B., Bonni A. Cell cycle regulation of neuronal apoptosis in development and disease. Prog. Neurobiol. 2004, 72:1-25.
2. Barzilai A. DNA damage, neuronal and glial cell death and neurodegeneration. Apoptosis 2010, 15:1371-1381.
3. Dekkers M.P., Barde Y.A. Developmental biology. Programmed cell death in neuronal development. Science 2013, 340:39-41.
4. Buss R.R., Sun W., Oppenheim R.W. Adaptive roles of programmed cell death during nervous system development. Annu. Rev. Neurosci. 2006, 29:1-35.
5. Southwell D.G., Paredes M.F., Galvao R.P., Jones D.L., Froemke R.C., Sebe J.Y., Alfaro-Cervello C., Tang Y., Garcia-Verdugo J.M., Rubenstein J.L., Baraban S.C., Alvarez-Buylla A. Intrinsically determined cell death of developing cortical interneurons. Nature 2012, 491:109-113.
6. Suzanne M., Steller H. Shaping organisms with apoptosis. Cell Death Differ. 2013, 20:669-675.
7. Shen Y., He P., Zhong Z., McAllister C., Lindholm K. Distinct destructive signal pathways of neuronal death in Alzheimer's disease. Trends Mol. Med. 2006, 12:574-579.
8. Vila M., Przedborski S. Targeting programmed cell death in neurodegenerative diseases. Nat. Rev. Neurosci. 2003, 4:365-375.
9. Barzilai A., Biton S., Shiloh Y. The role of the DNA damage response in neuronal development, organization and maintenance. DNA Repair (Amst) 2008, 7:1010-1027.
10. Klein J.A., Ackerman S.L. Oxidative stress, cell cycle, and neurodegeneration. J. Clin. Invest. 2003, 111:785-793.
11. McKinnon P.J. DNA repair deficiency and neurological disease. Nat. Rev. Neurosci. 2009, 10:100-112.
12. Bender A., Krishnan K.J., Morris C.M., Taylor G.A., Reeve A.K., Perry R.H., Jaros E., Hersheson J.S., Betts J., Klopstock T., Taylor R.W., Turnbull D.M. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet. 2006, 38:515-517.
13. Mao P., Reddy P.H. Aging and amyloid beta-induced oxidative DNA damage and mitochondrial dysfunction in Alzheimer's disease: implications for early intervention and therapeutics. Biochim. Biophys. Acta 2011, 1812:1359-1370.
14. Rodier F., Coppe J.P., Patil C.K., Hoeijmakers W.A., Munoz D.P., Raza S.R., Freund A., Campeau E., Davalos A.R., Campisi J. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat. Cell Biol. 2009, 11:973-979.
15. Sulli G., Di Micco R., d'Adda di Fagagna F. Crosstalk between chromatin state and DNA damage response in cellular senescence and cancer. Nat. Rev. Cancer 2012, 12:709-720.
16. Dhavan R., Tsai L.H. A decade of CDK5. Nat. Rev. Mol. Cell Biol. 2001, 2:749-759.
17. Jessberger S., Gage F.H., Eisch A.J., Lagace D.C. Making a neuron: Cdk5 in embryonic and adult neurogenesis. Trends Neurosci. 2009, 32:575-582.
18. Sananbenesi F., Fischer A., Wang X., Schrick C., Neve R., Radulovic J., Tsai L.H. A hippocampal Cdk5 pathway regulates extinction of contextual fear. Nat. Neurosci. 2007, 10:1012-1019.
19. Cruz J.C., Tsai L.H. A Jekyll and Hyde kinase: roles for Cdk5 in brain development and disease. Curr. Opin. Neurobiol. 2004, 14:390-394.
20. Raynaud F., Marcilhac A. Implication of calpain in neuronal apoptosis. A possible regulation of Alzheimer's disease. FEBS J. 2006, 273:3437-3443.
21. O'Hare M.J., Kushwaha N., Zhang Y., Aleyasin H., Callaghan S.M., Slack R.S., Albert P.R., Vincent I., Park D.S. Differential roles of nuclear and cytoplasmic cyclin-dependent kinase 5 in apoptotic and excitotoxic neuronal death. J. Neurosci. 2005, 25:8954-8966.
22. Lee J.H., Kim K.T. Regulation of cyclin-dependent kinase 5 and p53 by ERK1/2 pathway in the DNA damage-induced neuronal death. J. Cell. Physiol. 2007, 210:784-797.
23. Al-Mohanna M.A., Al-Khalaf H.H., Al-Yousef N., Aboussekhra A. The p16INK4a tumor suppressor controls p21WAF1 induction in response to ultraviolet light. Nucleic Acids Res. 2007, 35:223-233.
24. Ceruti J.M., Scassa M.E., Flo J.M., Varone C.L., Canepa E.T. Induction of p19INK4d in response to ultraviolet light improves DNA repair and confers resistance to apoptosis in neuroblastoma cells. Oncogene 2005, 24:4065-4080.
25. Ceruti J.M., Scassa M.E., Marazita M.C., Carcagno A.C., Sirkin P.F., Canepa E.T. Transcriptional upregulation of p19INK4d upon diverse genotoxic stress is critical for optimal DNA damage response. Int. J. Biochem. Cell Biol. 2009, 41:1344-1353.
26. Scassa M.E., Marazita M.C., Ceruti J.M., Carcagno A.L., Sirkin P.F., Gonzalez-Cid M., Pignataro O.P., Canepa E.T. Cell cycle inhibitor, p19INK4d, promotes cell survival and decreases chromosomal aberrations after genotoxic insult due to enhanced DNA repair. DNA Repair (Amst) 2007, 6:626-638.
27. Tavera-Mendoza L., Wang T.T., Lallemant B., Zhang R., Nagai Y., Bourdeau V., Ramirez-Calderon M., Desbarats J., Mader S., White J.H. Convergence of vitamin D and retinoic acid signalling at a common hormone response element. EMBO Rep. 2006, 7:180-185.
28. Canepa E.T., Scassa M.E., Ceruti J.M., Marazita M.C., Carcagno A.L., Sirkin P.F., Ogara M.F. INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life 2007, 59:419-426.
29. Cunningham J.J., Roussel M.F. Cyclin-dependent kinase inhibitors in the development of the central nervous system. Cell Growth Differ. 2001, 12:387-396.
30. Zindy F., Soares H., Herzog K.H., Morgan J., Sherr C.J., Roussel M.F. Expression of INK4 inhibitors of cyclin d-dependent kinases during mouse brain development. Cell Growth Differ. 1997, 8:1139-1150.
31. Rosso S.B., Sussman D., Wynshaw-Boris A., Salinas P.C. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat. Neurosci. 2005, 8:34-42.
32. Ogara M.F., Sirkin P.F., Carcagno A.L., Marazita M.C., Sonzogni S.V., Ceruti J.M., Canepa E.T. Chromatin relaxation-mediated induction of p19INK4d increases the ability of cells to repair damaged DNA. PLoS ONE 2013, 8(2013):e61143.
33. Ceruti J.M., Ogara M.F., Menendez C., Palmero I., Canepa E.T. Inhibitor of growth 1 (ING1) acts at early steps of multiple DNA repair pathways. Mol. Cell. Biochem. 2013, 378:117-126.
34. Marazita M.C., Ogara M.F., Sonzogni S.V., Marti M., Dusetti N.J., Pignataro O.P., Canepa E.T. CDK2 and PKA mediated-sequential phosphorylation is critical for p19INK4d function in the DNA damage response. PLoS ONE 2012, 7(2012):e35638.
35. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 2007, Academic Press, London.
36. Chen D.Y., Stern S.A., Garcia-Osta A., Saunier-Rebori B., Pollonini G., Bambah-Mukku D., Blitzer R.D., Alberini C.M. A critical role for IGF-II in memory consolidation and enhancement. Nature 2011, 469:491-497.
37. Sarnyai Z., Sibille E.L., Pavlides C., Fenster R.J., McEwen B.S., Toth M. Impaired hippocampal-dependent learning and functional abnormalities in the hippocampus in mice lacking serotonin(1A) receptors. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:14731-14736.
38. de la Fuente V., Freudenthal R., Romano A. Reconsolidation or extinction: transcription factor switch in the determination of memory course after retrieval. J. Neurosci. 2011, 31:5562-5573.
39. Alvarez A., Munoz J.P., Maccioni R.B. A Cdk5-p35 stable complex is involved in the beta-amyloid-induced deregulation of Cdk5 activity in hippocampal neurons. Exp. Cell Res. 2001, 264:266-274.
40. Kim D., Frank C.L., Dobbin M.M., Tsunemoto R.K., Tu W., Peng P.L., Guan J.S., Lee B.H., Moy L.Y., Giusti P., Broodie N., Mazitschek R., Delalle I., Haggarty S.J., Neve R.L., Lu Y., Tsai L.H. Deregulation of HDAC1 by p25/Cdk5 in neurotoxicity. Neuron 2008, 60:803-817.
41. Qu J., Nakamura T., Cao G., Holland E.A., McKercher S.R., Lipton S.A. S-nitrosylation activates Cdk5 and contributes to synaptic spine loss induced by beta-amyloid peptide. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14330-14335.
42. Joy J., Nalabothula N., Ghosh M., Popp O., Jochum M., Machleidt W., Gil-Parrado S., Holak T.A. Identification of calpain cleavage sites in the G1 cyclin-dependent kinase inhibitor p19(INK4d). Biol. Chem. 2006, 387:329-335.
43. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106:274-285.
44. Lu T., Pan Y., Kao S.Y., Li C., Kohane I., Chan J., Yankner B.A. Gene regulation and DNA damage in the ageing human brain. Nature 2004, 429:883-891.
45. Rass U., Ahel I., West S.C. Defective DNA repair and neurodegenerative disease. Cell 2007, 130:991-1004.
46. Nouspikel T., Hanawalt P.C. When parsimony backfires: neglecting DNA repair may doom neurons in Alzheimer's disease. Bioessays 2003, 25:168-173.
47. Krantic S., Mechawar N., Reix S., Quirion R. Apoptosis-inducing factor: a matter of neuron life and death. Prog. Neurobiol. 2007, 81:179-196.
48. Sedarous M., Keramaris E., O'Hare M., Melloni E., Slack R.S., Elce J.S., Greer P.A., Park D.S. Calpains mediate p53 activation and neuronal death evoked by DNA damage. J. Biol. Chem. 2003, 278:26031-26038.
49. Xu W., Wong T.P., Chery N., Gaertner T., Wang Y.T., Baudry M. Calpain-mediated mGluR1alpha truncation: a key step in excitotoxicity. Neuron 2007, 53:399-412.
50. Zhu J., Li W., Mao Z. Cdk5: mediator of neuronal development, death and the response to DNA damage. Mech. Ageing Dev. 2011, 132:389-394.
51. Qu D., Rashidian J., Mount M.P., Aleyasin H., Parsanejad M., Lira A., Haque E., Zhang Y., Callaghan S., Daigle M., Rousseaux M.W., Slack R.S., Albert P.R., Vincent I., Woulfe J.M., Park D.S. Role of Cdk5-mediated phosphorylation of Prx2 in MPTP toxicity and Parkinson's disease. Neuron 2007, 55:37-52.
52. Huang E., Qu D., Zhang Y., Venderova K., Haque M.E., Rousseaux M.W., Slack R.S., Woulfe J.M., Park D.S. The role of Cdk5-mediated apurinic/apyrimidinic endonuclease 1 phosphorylation in neuronal death. Nat. Cell Biol. 2010, 12:563-571.
53. Park D.S., Levine B., Ferrari G., Greene L.A. Cyclin dependent kinase inhibitors and dominant negative cyclin dependent kinase 4 and 6 promote survival of NGF-deprived sympathetic neurons. J. Neurosci. 1997, 17:8975-8983.
54. Copani A., Uberti D., Sortino M.A., Bruno V., Nicoletti F., Memo M. Activation of cell-cycle-associated proteins in neuronal death: a mandatory or dispensable path?. Trends Neurosci. 2001, 24:25-31.
55. Zindy F., Cunningham J.J., Sherr C.J., Jogal S., Smeyne R.J., Roussel M.F. Postnatal neuronal proliferation in mice lacking Ink4d and Kip1 inhibitors of cyclin-dependent kinases. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13462-13467.
56. Thiel G., Cibelli G. Regulation of life and death by the zinc finger transcription factor Egr-1. J. Cell. Physiol. 2002, 193:287-292.
57. Yankner B.A., Lu T., Loerch P. The aging brain. Annu. Rev. Pathol. 2008, 3:41-66.
58. Ljungman M., Lane D.P. Transcription - guarding the genome by sensing DNA damage. Nat. Rev. Cancer 2004, 4:727-737.