A cellular mechanism for dendritic spine loss in the pilocarpine model of status epilepticus

Epilepsia

Volumn 49, Issue 10, 2008, Pages 1696-1710

  Kurz, Jonathan E ^a   Moore, Bryan J ^a   Henderson, Scott C ^b   Campbell, John N ^b   Churn, Severn B ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Calcineurin; Cofilin; Cognitive function; Epilepsy; Epileptogenesis

Indexed keywords

ACTIN; CALCINEURIN; CALCINEURIN INHIBITOR; COFILIN; PILOCARPINE; PHOSPHOPROTEIN DARPP 32; PPP1R1B PROTEIN, RAT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRIFUGATION; CONTROLLED STUDY; DENDRITIC SPINE; DEPOLYMERIZATION; ELECTROENCEPHALOGRAM; EPILEPTIC STATE; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN MODIFICATION; PROTEIN POLYMERIZATION; RAT; SEIZURE; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; CELL FRACTIONATION; CHEMICALLY INDUCED DISORDER; DENDRITE; DISEASE MODEL; DRUG EFFECT; METABOLISM; METHODOLOGY; PATHOLOGY; PHOSPHORYLATION; SILVER STAINING; SPRAGUE DAWLEY RAT; TIME; ULTRASTRUCTURE;

ACTINS; ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CALCINEURIN; DENDRITES; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; IMMUNOPRECIPITATION; PHOSPHORYLATION; PILOCARPINE; RATS; RATS, SPRAGUE-DAWLEY; SILVER STAINING; STATUS EPILEPTICUS; SUBCELLULAR FRACTIONS; TIME FACTORS;

EID: 58149234407     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2008.01616.x     Document Type: Article

References (40)

1. Agnew BJ, Minamide LS, Bamburg JR. (1995) Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J Biol Chem 270:17582-17587.
2. Bamburg JR. (1999) Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol 15:185-230.
3. Bleck TP. (1991) Convulsive disorders: status epilepticus. Clin Neuro- pharmacol 14:191-198.
4. Bradford MM. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein- dye binding. Anal Biochem 72:248-254.
5. Bragin A, Wilson CL, Engel J Jr. (2000) Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia 41(Suppl. 6):S144-S152.
6. Churn SB, Taft WC, Billingsley MS, Sankaran B, DeLorenzo RJ. (1992) Global forebrain ischemia induces a posttranslational modification of multifunctional calcium- and calmodulin-dependent kinase II. JNeuro- chem 59:1221-1232.
7. Edelman AM, Hunter DD, Hendrickson AE, Krebs EG. (1985) Subcellu- lar distribution of calcium- and calmodulin-dependent myosin light chain phosphorylating activity in rat cerebral cortex. J Neurosci 5:2609-2617.
8. Ferhat L, Esclapez M, Represa A, Fattoum A, Shirao T, Ben-Ari Y. (2003) Increased levels of acidic calponin during dendritic spine plasticity after pilocarpine-induced seizures. Hippocampus 13:845-858.
9. Fountain NB. (2000) Status epilepticus: risk factors and complications. Epilepsia 41(Suppl. 2):S23-S30.
10. Gray EG. (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183:1592-1593.
11. Halpain S, Hipolito A, Saffer L. (1998) Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J Neurosci 18:9835-9844.
12. Hayashi Y, Majewska AK. (2005) Dendritic spine geometry: functional implication and regulation. Neuron 46:529-532. Isokawa M. (1998) Remodeling dendritic spines in the rat pilocarpine model of temporal lobe epilepsy. Neurosci Lett 258:73-76.
13. Isokawa M. (2000) Remodeling dendritic spines of dentate granule cells in temporal lobe epilepsy patients and the rat pilocarpine model. Epilepsia 41(Suppl. 6):S14-S17.
14. Kurz JE, Sheets D, Parsons JT, Rana A, Delorenzo RJ, Churn SB. (2001) A significant increase in both basal and maximal calcineurin activity in the rat pilocarpine model of status epilepticus. J Neurochem 78:304-315.
15. Kurz JE, Rana A, Parsons JT, Churn SB. (2003) Status epilepticus- induced changes in the subcellular distribution and activity of calci- neurin in rat forebrain. Neurobiol Dis 14:483-493.
16. Kurz JE, Singleton MW, Churn SB. (2005a) Temporally disparate effects on CaN activity and subcellular distribution in the rat pilocarpine model. (Abstract 2.063). Epilepsia46(Suppl. 8):112.
17. Kurz JE, Hamm RJ, Singleton RH, Povlishock JT, Churn SB. (2005b) A persistent change in subcellular distribution of calcineurin following fluid percussion injury in the rat. Brain Res 1048:153-160.
18. Leuner B, Falduto J, Shors TJ. (2003) Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci 23:659-665.
19. Leuner B, Shors TJ. (2004) New spines, new memories. Mol Neurobiol 29:117-130.
20. Lowenstein DH, Alldredge BK. (1998) Status epilepticus. N Engl J Med 338:970-976.
21. McNamara JO, Huang YZ, Leonard AS. (2006) Molecular signaling mechanisms underlying epileptogenesis. Sci STKE 2006:re12.
22. Meberg PJ, Ono S, Minamide LS, Takahashi M, Bamburg JR. (1998)
23. Actin depolymerizing factor and cofilin phosphorylation dynamics: response to signals that regulate neurite extension. Cell Motil Cyto- skeleton 39:172-190.
24. Meng Y, Takahashi H, Meng J, Zhang Y, Lu G, Asrar S, Nakamura T, Jia Z. (2004) Regulation of ADF/cofilin phosphorylation and synap- tic function by LIM-kinase. Neuropharmacology 47:746-754.
25. Moia LJ, Matsui H, de Barros GA, Tomizawa K, Miyamoto K, Kuwata Y, Tokuda M, Itano T, Hatase O. (1994) Immunosuppres- sants and calcineurin inhibitors, cyclosporin A and FK506, reversibly inhibit epileptogenesis in amygdaloid kindled rat. Brain Res 648: 337-341.
26. Moriwaki A, Lu YF, Hayashi Y, Tomizawa K, Tokuda M, Itano T, Hatase O, Matsui H. (1996) Immunosuppressant FK506 prevents mossy fiber sprouting induced by kindling stimulation. Neurosci Res 25:191-194.
27. Moriwaki A, Lu YF, Tomizawa K, Matsui H. (1998) An immunosuppres- sant, FK506, protects against neuronal dysfunction and death but has no effect on electrographic and behavioral activities induced by systemic kainate. Neuroscience 86:855-865.
28. O'Malley A, O'Connell C, Murphy KJ, Regan CM. (2000) Transient spine density increases in the mid-molecular layer of hippocampal dentate gyrus accompany consolidation of a spatial learning task in the rodent. Neuroscience 99:229-232.
29. Racine RJ. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
30. Rice AC, Floyd CL, Lyeth BG, Hamm RJ, DeLorenzo RJ. (1998) Status epilepticus causes long-term NMDA receptor-dependent behavioral changes and cognitive deficits. Epilepsia 39:1148-1157.
31. Sanchez RM, Dai W, Levada RE, Lippman JJ, Jensen FE. (2005) AMPA/ kainate receptor-mediated downregulation of GABAergic synaptic transmission by calcineurin after seizures in the developing rat brain. J Neurosci 25:3442-3451.
32. Sarmiere PD, Bamburg JR. (2004) Regulation of the neuronal actin cyto- skeleton by ADF/cofilin. J Neurobiol 58:103-117.
33. Sierra-Paredes G, Oreiro-Garcia T, Nunez-Rodriguez A, Vazquez-Lopez A, Sierra-Marcuno G. (2006) Seizures induced by in vivo latrunculin a and jasplakinolide microperfusion in the rat hippocampus. J Mol Neurosci 28:151-160.
34. Singleton MW, Holbert WH 2nd, Ryan ML, Lee AT, Kurz JE, Churn SB. (2005a) Age dependence of pilocarpine-induced status epilepticus and inhibition of CaM kinase II activity in the rat. Brain Res Dev Brain Res 156:67-77.
35. Singleton MW, Holbert WH 2nd, Lee AT, Bracey JM, Churn SB. (2005b) Modulation of CaM kinase II activity is coincident with induction of status epilepticus in the rat pilocarpine model. Epilepsia 46:1389-1400.
36. Sloviter RS. (1999) Status epilepticus-induced neuronal injury and network reorganization. Epilepsia 40(Suppl. 1):S34-S39; discussion S40-31.
37. Turski L, Ikonomidou C, Turski WA, Bortolotto ZA, Cavalheiro EA. (1989) Review: cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel experimental model of intractable epilepsy. Synapse 3:154-171.
38. Wang Y, Shibasaki F, Mizuno K. (2005) Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J Biol Chem 280:12683-12689.
39. Wong M. (2005) Modulation of dendritic spines in epilepsy: cellular mechanisms and functional implications. Epilepsy Behav 7:569-577.
40. Zhou Q, Homma KJ, Poo MM. (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.