Ischemic stroke injury is mediated by aberrant Cdk5

Journal of Neuroscience

Volumn 34, Issue 24, 2014, Pages 8259-8267

  Meyer, Douglas A ^a   Torres Altoro, Melissa I ^a   Tan, Zhenjun ^c   Tozzi, Alessandro ^e,f   Filippo, Massimiliano Di ^e,f   DiNapoli, Vincent ^c   Plattner, Florian ^a   Kansy, Janice W ^a   Benkovic, Stanley A ^d   Huber, Jason D ^c   Miller, Diane B ^d   Greengard, Paul ^g   Calabresi, Paolo ^e,f   Rosen, Charles L ^c   Bibb, James A ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^e UNIVERSITY OF PERUGIA   (Italy)

^f IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^g ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Biomarker; Calpain; Cdk5; Ischemia; Neuroprotection; Stroke

Indexed keywords

CALPAIN; CALPEPTIN; CYCLIN DEPENDENT KINASE 5; DOPAMINE; GLUCOSE; OXYGEN; PHOSPHOPROTEIN DARPP 32; PROTEIN P25; PROTEIN P35; TRIPHENYLTETRAZOLIUM;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL DEATH; CONTROLLED STUDY; EMBOLISM; ENZYME INHIBITION; EXCITOTOXICITY; FEMALE; HISTOLOGY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; ISCHEMIC STROKE INJURY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL; NEUROPHYSIOLOGY; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; STAINING; STROKE INFARCT VOLUME;

BIOMARKER; CALPAIN; CDK5; ISCHEMIA; NEUROPROTECTION; STROKE;

ANIMALS; ANOXIA; CALPAIN; CELL DEATH; CORPUS STRIATUM; CYCLIN-DEPENDENT KINASE 5; DISEASE MODELS, ANIMAL; ESTROGENS; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NERVOUS SYSTEM DISEASES; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; TETRAZOLIUM SALTS; TIME FACTORS; TISSUE PLASMINOGEN ACTIVATOR;

EID: 84902152605     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4368-13.2014     Document Type: Article

References (44)

1. Alkayed NJ, Murphy SJ, Traystman RJ, Hurn PD, Miller VM (2000) Neuroprotective effects of female gonadal steroids in reproductively senescent female rats. Stroke 31:161-168. CrossRef Medline
2. Alvira D, Tajes M, Verdaguer E, Acuña-Castroviejo D, Folch J, Camins A, Pallas M (2006) Inhibition of the cdk5/p25 fragment formation may explain the antiapoptotic effects of melatonin in an experimental model of Parkinson's disease. J Pineal Res 40:251-258. CrossRef Medline
3. Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, Bartkowski HM (1986) Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17:1304-1308. CrossRef Medline
4. Bibb JA, Snyder GL, Nishi A, Yan Z, Meijer L, Fienberg AA, Tsai LH, Kwon YT, Girault JA, Czernik AJ, Huganir RL, Hemmings HC Jr, Nairn AC, Greengard P (1999) Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature 402:669-671. CrossRef Medline
5. Bibb JA, Yan Z, Svenningsson P, Snyder GL, Pieribone VA, Horiuchi A, Nairn AC, Messer A, Greengard P (2000) Severe deficiencies in dopamine signaling in presymptomatic Huntington's disease mice. Proc Natl Acad Sci U S A 97:6809-6814. CrossRef Medline
6. Butler TL, Kassed CA, Sanberg PR, Willing AE, Pennypacker KR (2002) Neurodegeneration in the rat hippocampus and striatum after middle cerebral artery occlusion. Brain Res 929:252-260. CrossRef Medline
7. Calabresi P, Centonze D, Pisani A, Sancesario G, Gubellini P, Marfia GA, Bernardi G (1998) Striatal spiny neurons and cholinergic interneurons express differential ionotropic glutamatergic responses and vulnerability: implications for ischemia and Huntington's disease. Ann Neurol 43:586-597. CrossRef Medline
8. Calabresi P, Saulle E, Centonze D, Pisani A, Marfia GA, Bernardi G (2002) Post-ischaemic long-term synaptic potentiation in the striatum: a putative mechanism for cell type-specific vulnerability. Brain 125:844-860. CrossRef Medline
9. Calabresi P, Centonze D, Pisani A, Cupini L, Bernardi G (2003) Synaptic plasticity in the ischaemic brain. Lancet Neurol 2:622-629. CrossRef Medline
10. Centonze D, Marfia GA, Pisani A, Picconi B, Giacomini P, Bernardi G, Calabresi P (2001) Ionic mechanisms underlying differential vulnerability to ischemia in striatal neurons. Prog Neurobiol 63:687-696. CrossRef Medline
11. Cheung U, Atwood HL, Zucker RS (2006) Presynaptic effectors contributing to c AMP-induced synaptic potentiation in Drosophila. J Neurobiol 66:273-280. CrossRef Medline
12. Cheung ZH, Fu AK, Ip NY (2006) Synaptic roles of Cdk5: implications in higher cognitive functions and neurodegenerative diseases. Neuron 50: 13-18. CrossRef Medline
13. Clark RK, Lee EV, White RF, Jonak ZL, Feuerstein GZ, Barone FC (1994) Reperfusion following focal stroke hastens inflammation and resolution of ischemic injured tissue. Brain Res Bull 35:387-392. CrossRef Medline
14. Costa C, Martella G, Picconi B, Prosperetti C, Pisani A, Di Filippo M, Pisani F, Bernardi G, Calabresi P (2006) Multiple mechanisms underlying the neuroprotective effects of antiepileptic drugs against in vitro ischemia. Stroke 37:1319-1326. CrossRef Medline
15. Dinapoli VA, Rosen CL, Nagamine T, Crocco T (2006) Selective MCA occlusion: a precise embolic stroke model. J Neurosci Methods 154:233-238. CrossRef Medline
16. Gillardon F, Schrattenholz A, Sommer B (2005) Investigating the neuroprotective mechanism of action of a CDK5 inhibitor by phosphoproteome analysis. J Cell Biochem 95:817-826. CrossRef Medline
17. Green AR, Cross AJ (1997) Techniques for examining neuroprotective drugs in vivo. Int Rev Neurobiol 40:47-68. Medline
18. Greengard P, Allen PB, Nairn AC (1999) Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23:435-447. CrossRef Medline
19. Hagemann G, Redecker C, Neumann-Haefelin T, Freund HJ, Witte OW (1998) Increased long-term potentiation in the surround of experimentally induced focal cortical infarction. Ann Neurol 44:255-258. CrossRef Medline
20. Hawasli AH, Benavides DR, Nguyen C, Kansy JW, Hayashi K, Chambon P, Greengard P, Powell CM, Cooper DC, Bibb JA (2007) Cyclindependent kinase 5 governs learning and synaptic plasticity via control of NMDAR degradation. Nat Neurosci 10:880-886. CrossRef Medline
21. Lagace DC, Benavides DR, Kansy JW, Mapelli M, Greengard P, Bibb JA, Eisch AJ (2008) Cdk5 is essential for adult hippocampal neurogenesis. Proc Natl Acad Sci U S A 105:18567-18571. CrossRef Medline
22. Larsen GA, Skjellegrind HK, Berg-Johnsen J, Moe MC, Vinje ML (2006) Depolarization of mitochondria in isolated CA1 neurons during hypoxia, glucose deprivation and glutamate excitotoxicity. Brain Res 1077:153-160. CrossRef Medline
23. Larsson E, Lindvall O, Kokaia Z (2001) Stereological assessment of vulnerability of immunocytochemically identified striatal and hippocampal neurons after global cerebral ischemia in rats. Brain Res 913:117-132. CrossRef Medline
24. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568. Medline
25. Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4:399-415. CrossRef Medline
26. Loubinoux I, Kronenberg G, Endres M, Schumann-Bard P, Freret T, Filipkowski RK, Kaczmarek L, Popa-Wagner A (2012) Post-stroke depression: mechanisms, translation and therapy. J Cell Mol Med 16:1961-1969. CrossRef Medline
27. Meyer DA, Richer E, Benkovic SA, Hayashi K, Kansy JW, Hale CF, Moy LY, Kim Y, O'Callaghan JP, Tsai LH, Greengard P, Nairn AC, Cowan CW, Miller DB, Antich P, Bibb JA (2008) Striatal dysregulation of Cdk5 alters locomotor responses to cocaine, motor learning, and dendritic morphology. Proc Natl Acad Sci U S A 105:18561-18566. CrossRef Medline
28. Monaco EA 3rd (2004) Recent evidence regarding a role for Cdk5 dysregulation in Alzheimer's disease. Curr Alzheimer Res 1:33-38. CrossRef Medline
29. Nath R, Davis M, Probert AW, Kupina NC, Ren X, Schielke GP, Wang KK (2000) Processing of cdk5 activator p35 to its truncated form (p25) by calpain in acutely injured neuronal cells. Biochem Biophys Res Commun 274:16-21. CrossRef Medline
30. Nishi A, Snyder GL, Greengard P (1997) Bidirectional regulation of DARPP-32 phosphorylation by dopamine. J Neurosci 17:8147-8155. Medline
31. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402:615-622. CrossRef Medline
32. Picconi B, Centonze D, Håkansson K, Bernardi G, Greengard P, Fisone G, Cenci MA, Calabresi P (2003) Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat Neurosci 6:501-506. Medline
33. Rashidian J, Iyirhiaro G, Aleyasin H, Rios M, Vincent I, Callaghan S, Bland RJ, Slack RS, During MJ, Park DS (2005) Multiple cyclin-dependent kinases signals are critical mediators of ischemia/hypoxic neuronal death in vitro and in vivo. Proc Natl Acad Sci U S A 102:14080-14085. CrossRef Medline
34. Sahin B, Kansy JW, Nairn AC, Spychala J, Ealick SE, Fienberg AA, Greene RW, Bibb JA (2004) Molecular characterization of recombinant mouse adenosine kinase and evaluation as a target for protein phosphorylation. Eur J Biochem 271:3547-3555. CrossRef Medline
35. Sahin B, Galdi S, Hendrick J, Greene RW, Snyder GL, Bibb JA (2007) Evaluation of neuronal phosphoproteins as effectors of caffeine and mediators of striatal adenosine A2A receptor signaling. Brain Res 1129:1-14. CrossRef Medline
36. Sahin B, Hawasli AH, Greene RW, Molkentin JD, Bibb JA (2008) Negative regulation of cyclin-dependent kinase 5 targets by protein kinase C. Eur J Pharmacol 581:270-275. CrossRef Medline
37. Smith PD, Mount MP, Shree R, Callaghan S, Slack RS, Anisman H, Vincent I, Wang X, Mao Z, Park DS (2006) Calpain-regulated p35/cdk5 plays a central role in dopaminergic neuron death through modulation of the transcription factor myocyte enhancer factor 2. J Neurosci 26:440-447. CrossRef Medline
38. Stoll G, Jander S, Schroeter M (1998) Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 56:149-171. CrossRef Medline
39. Tamada Y, Nakajima E, Nakajima T, Shearer TR, Azuma M (2005) Proteolysis of neuronal cytoskeletal proteins by calpain contributes to rat retinal cell death induced by hypoxia. Brain Res 1050:148-155. CrossRef Medline
40. Weber P, Metzger D, Chambon P (2001) Temporally controlled targeted somatic mutagenesis in the mouse brain. Eur J Neurosci 14:1777-1783. CrossRef Medline
41. Weishaupt JH, Kussmaul L, Grötsch P, Heckel A, Rohde G, Romig H, Bähr M, Gillardon F (2003) Inhibition of CDK5 is protective in necrotic and apoptotic paradigms of neuronal cell death and prevents mitochondrial dysfunction. Mol Cell Neurosci 24:489-502. CrossRef Medline
42. Wells GJ, Bihovsky R (1998) Calpain inhibitors as potential treatment for stroke and other neurodegenerative diseases: recent trends and developments. Expert Opin Ther Pat 8:1707-1727. CrossRef
43. Yang Y, Shuaib A, Li Q (1998) Quantification of infarct size on focal cerebral ischemia model of rats using a simple and economical method. J Neurosci Methods 84:9-16. CrossRef Medline
44. Zhang RL, Chopp M, Zhang ZG, Jiang Q, Ewing JR (1997) A rat model of focal embolic cerebral ischemia. Brain Res 766:83-92. CrossRef Medline