Drebrin A expression is altered after pilocarpine-induced seizures: Time course of changes is consistent for a role in the integrity and stability of dendritic spines of hippocampal granule cells

Hippocampus

Volumn 22, Issue 3, 2012, Pages 477-493

  Sbai, Oualid ^a,b   Khrestchatisky, Michel ^a,b   Esclapez, Monique ^b,c   Ferhat, Lotfi ^a,b  

^a CNRS   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c INSERM   (France)

Author keywords

Bassoon; Chronic; F actin; Latent; VGlut1

Indexed keywords

DREBRIN A; MESSENGER RNA; PILOCARPINE; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LABELING; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS; HIPPOCAMPUS; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; MORPHOGENESIS; NERVE CELL PLASTICITY; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SEIZURE; SYNAPTOGENESIS; TEMPORAL LOBE EPILEPSY;

ANIMALS; DENDRITIC SPINES; HIPPOCAMPUS; MALE; NEURONS; NEUROPEPTIDES; PILOCARPINE; RATS; RATS, WISTAR; SEIZURES; SYNAPSES;

EID: 84857222669     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20914     Document Type: Article

References (92)

1. Allison DW, Gelfand VI, Spector I, Craig AM. 1998. Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: Differential attachment of NMDA versus AMPA receptors. J Neurosci 18: 2423-2436.
2. Amaral DG. 1978. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182: 851-914.
3. Aoki C, Sekino Y, Hanamura K, Fujisawa S, Mahadomrongkul V, Ren Y, Shirao T. 2005. Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses. J Comp Neurol 483: 383-402.
4. Arber S, Barbayannis FA, Hanser H, Schneider C, Stanyon CA, Bernard O, Caroni P. 1998. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393: 805-809.
5. Boulland JL, Ferhat L, Tallak Solbu T, Ferrand N, Chaudhry FA, Storm-Mathisen J, Esclapez M. 2007. Changes in vesicular transporters for gamma-aminobutyric acid and glutamate reveal vulnerability and reorganization of hippocampal neurons following pilocarpine-induced seizures. J Comp Neurol 503: 466-485.
6. Buckmaster PS, Schwartzkroin PA. 1994. Hippocampal mossy cell function: A speculative view. Hippocampus 4: 393-402.
7. Buckmaster PS, Strowbridge BW, Kunkel DD, Schmiege DL, Schwartzkroin PA. 1992. Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus 2: 349-362.
8. Buckmaster PS, Strowbridge BW, Schwartzkroin PA. 1993. A comparison of rat hippocampal mossy cells and CA3c pyramidal cells. J Neurophysiol 70: 1281-1299.
9. Buckmaster PS, Wenzel HJ, Kunkel DD, Schwartzkroin PA. 1996. Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366: 271-292.
10. Buckmaster PS, Zhang GF, Yamawaki R. 2002. Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J Neurosci 22: 6650-6658.
11. Buss F, Temm-Grove C, Henning S, Jockusch BM. 1992. Distribution of profilin in fibroblasts correlates with the presence of highly dynamic actin filaments. Cell Motil Cytoskel 22: 51-61.
12. Calabrese B, Wilson MS, Halpain S. 2006. Development and regulation of dendritic spine synapses. Physiology 21: 38-47.
13. Capani F, Martone ME, Deerinck TJ, Ellisman MH. 2001. Selective localization of high concentrations of F-actin in subpopulations of dendritic spines in rat central nervous system: A three-dimensional electron microscopic study. J Comp Neurol 435: 156-170.
14. Carlsson L, Nyström LE, Sundkvist I, Markey F, Lindberg U. 1977. Actin polymerizability is influenced by profilin, a low molecular weight protein in non-muscle cells. J Mol Biol 115: 465-483.
15. Covolan L, Ribeiro LT, Longo BM, Mello LE. 2000. Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine or kainate-induced status epilepticus. Hippocampus 10: 169-180.
16. Dalby NO, Mody I. 2001. The process of epileptogenesis: A pathophysiological approach. Curr Opin Neurol 14: 187-192.
17. Dinocourt C, Petanjek Z, Freund TF, Ben-Ari Y, Esclapez M. 2003. Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J Comp Neurol 459: 407-425.
18. Dresbach T, Qualmann B, Kessels MM, Garner CC, Gun delfinger ED. 2001. The presynaptic cytomatrix of brain synapse. Cell Mol Life Sci 58: 94-116.
19. Engert F, Bonhoeffer T. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399: 66-70.
20. Esclapez M, Houser CR. 1999. Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. J Comp Neurol 412: 488-505.
21. Esclapez M, Tillakaratne NJK, Tobin AJ, Houser CR. 1993. Comparative localization of mRNAs encoding two forms of glutamic acid decarboxylase with nonradioactive in situ hybridization methods. J Comp Neurol 331: 339-362.
22. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR. 1994. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14: 1834-1855.
23. Ethell IM, Pasquale EB. 2005. Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 75: 161-205.
24. Ferhat L, Cook C, Chauviere M, Harper M, Kress M, Lyons GE, Baas PW. 1998a. Expression of the mitotic motor protein Eg5 in postmitotic neurons: Implications for neuronal development. JNeurosci 18: 7822-7835.
25. Ferhat L, Kuriyama R, Lyons GE, Micales B, Baas PW. 1998b. Expression of the mitotic motor protein CHO1/MKLP1 in postmitotic neurons. Eur J Neurosci 10: 1383-1393.
26. Ferhat L, Rami G, Medina I, Ben-Ari Y, Represa A. 2001. Process formation results from the imbalance between motor-mediated forces. J Cell Sci 114(Pt 21): 3899-3904.
27. Ferrer I, Lopez E, Blanco R, Rivera R, Krupinski J, Marti E. 2000. Differential c-Fos and caspase expression following kainic acid excitotoxicity. Acta Neuropathol 99: 245-256.
28. 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.
29. Fifkova E, Delay RJ. 1982. Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol 95: 345-350.
30. Fremeau RT, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH. 2001. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31: 247-260.
31. Freund TF, Buzsàki G. 1996. Interneurons of the hippocampus. Hippocampus 6: 347-470.
32. Freund TF, Ylinen A, Miettinen R, Pitkänen A, Lahtinen H, Baimbridge KG, Riekkinen PJ. 1991. Pattern of neuronal death in the rat hippocampus after status epilepticus. Relationship to calcium binding protein content and ischemic vulnerability. Brain Res Bull 28: 27-38.
33. Frotscher M, Seress L, Schwerdtfeger WK, Buhl E. 1991. The mossy cells of the fascia dentata: A comparative study of their fine structure and synaptic connections in rodents and primates. J Comp Neurol 312: 145-163.
34. Frotscher M, Jonas P, Sloviter RS. 2006. Synapses formed by normal and abnormal hippocampal mossy fibers. Cell Tissue Res 326: 361-367.
35. Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K. 2003. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38: 447-460.
36. Garner CC, Kindler S, Gundelfinger ED. 2000. Molecular determinants of presynaptic active zones. Curr Opin Neurobiol 10: 321-327.
37. Geinisman Y, de Toledo-Morrell L, Morrell F, Persina IS, Rossi M. 1992. Age-related loss of axospinous synapses formed by two afferent systems in the rat dentate gyrus as revealed by the unbiased stereological dissector technique. Hippocampus 2: 437-444.
38. Hayashi K, Shirao T. 1999. Change in the shape of dendritic spines caused by overexpression of drebrin in cultured cortical neurons. J Neurosci 19: 3918-3925.
39. Hayashi K, Ishikawa R, Ye LH, He XL, Takata K, Kohama K, Shirao T. 1996. Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex. J Neurosci 16: 7161-7170.
40. Harris KM, Kater SB. 1994. Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17: 341-371.
41. Henshall DC, Skradski SL, Meller R, Araki T, Minami M, Schindler CK, Lan JQ, Bonislawski DP, Simon RP. 2002. Expression and differential processing of caspases 6 and 7 in relation to specific epileptiform EEG patterns following limbic seizures. Neurobiol Dis 10: 71-87.
42. Ikeda K, Kaub PA, Asada H, Uyemura K, Toya S, Shirao T. 1996. Stabilization of adhesion plaques by the expression of drebrin A in fibroblasts. Brain Res Dev Brain Res 91: 227-236.
43. Ishikawa R, Hayashi K, Shirao T, Xue Y, Takagi T, Sasaki Y, Kohama K. 1994. Drebrin, a development-associated brain protein from rat embryo, causes the dissociation of tropomyosin from actin filaments. J Biol Chem 269: 29928-29933.
44. Ishikawa R, Katoh K, Takahashi A, Xie C, Oseki K, Watanabe M, Igarashi M, Nakamura A, Kohama K. 2007. Drebrin attenuates the interaction between actin and myosin-V. Biochem Biophys Res Commun 359: 398-401.
45. Ivanov A, Esclapez M, Ferhat L. 2009a. Role of drebrin A in dendritic spine plasticity and synaptic function: Implications in neurological disorders. Commun Integr Biol 2: 268-270.
46. Ivanov A, Esclapez M, Pellegrino C, Shirao T, Ferhat L. 2009b. Drebrin A regulates dendritic spine plasticity and synaptic function in mature cultured hippocampal neurons. J Cell Sci 122: 524-534.
47. Isokawa M. 1998. Remodeling dendritic spines in the rat pilocarpine model of temporal lobe epilepsy. Neurosci Lett 258: 73-76.
48. 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.
49. Isokawa M, Mello LE. 1991. NMDA receptor-mediated excitability in dendritically deformed dentate granule cells in pilocarpine-treated rats. Neurosci Lett 129: 69-73.
50. Julien C, Tremblay C, Bendjelloul F, Phivilay A, Coulombe MA, Emond V, Calon F. 2008. Decreased drebrin mRNA expression in Alzheimer disease: Correlation with tau pathology. J Neurosci Res 86: 2292-2302.
51. Klaiman G, Petzke TL, Hammond J, Leblanc AC. 2008. Targets of caspase-6 activity in human neurons and Alzheimer disease. Mol Cell Proteom 7: 1541-1555.
52. Kobayashi M, Buckmaster PS. 2003. Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J Neurosci 23: 2440-2452.
53. Kobayashi R, Sekino Y, Shirao T, Tanaka S, Ogura T, Inada K, Saji M. 2004. Antisense knockdown of drebrin A, a dendritic spine protein, causes stronger preference, impaired pre-pulse inhibition, and an increased sensitivity to psychostimulant. Neurosci Res 49: 205-217.
54. Kojima N, Shirao T. 2007. Synaptic dysfunction and disruption of postsynaptic drebrin-actin complex: A study of neurological disorders accompanied by cognitive deficits. Neurosci Res 58: 1-5.
55. Kurz JE, Moore BJ, Henderson SC, Campbell JN, Churn SB. 2008. A cellular mechanism for dendritic spine loss in the pilocarpine model of status epilepticus. Epilepsia 49: 1696-1710.
56. Liu Y, Fujise N, Kosaka T. 1996. Distribution of calretinin immunoreactivity in the mouse dentate gyrus. I. General description. Exp Brain Res 108: 389-403.
57. McCloskey DP, Hintz TM, Pierce JP, Scharfman HE. 2006. Stereological methods reveal the robust size and stability of ectopic hilar granule cells after pilocarpine-induced status epilepticus in the adult rat. Eur J Neurosci 24: 2203-2210.
58. Maletic-Savatic M, Malinow R, Svoboda K. 1999. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283: 1923-1927.
59. Matus A. 2000. Actin-based plasticity in dendritic spines. Science 290: 754-758.
60. Matus A, Ackermann M, Pehling G, Byers HR, Fujiwara K. 1982. High actin concentrations in brain dendritic spines and postsynaptic densities. Proc Natl Acad Sci USA 79: 7590-7594.
61. Mello LE, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM. 1993. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: Cell loss and mossy fiber sprouting. Epilepsia 34: 985-995.
62. Moser MB, Trommald M, Andersen P. 1994. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc Natl Acad Sci USA 91: 12673-12675.
63. Narkilahti S, Pitkänen A. 2005. Caspase 6 expression in the rat hippocampus during epileptogenesis and epilepsy. Neuroscience 131: 887-897.
64. Okazaki MM, Nadler JV. 2001. Glutamate receptor involvement in dentate granule cell epileptiform activity evoked by mossy fiber stimulation. Brain Res 915: 58-69.
65. Okazaki MM, Evenson DA, Nadler JV. 1995. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: Visualization after retrograde transport of biocytin. J Comp Neurol 352: 515-534.
66. Parent JM, Lowenstein DH. 2002. Seizure-induced neurogenesis: Are more new neurons good for an adult brain? Prog Brain Res 135: 121-131.
67. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. 1997. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17: 3727-3738.
68. Parent JM, Elliott RC, Pleasure SJ, Barbaro NM, Lowenstein DH. 2006. Aberrant seizure-induced neurogenesis in experimental temporal lobe epilepsy. Ann Neurol 59: 81-91.
69. Rami G, Caillard O, Medina I, Pellegrino C, Fattoum A, Ben-Ari Y, Ferhat L. 2006. Change in the shape and density of dendritic spines caused by overexpression of acidic calponin in cultured hippocampal neurons. Hippocampus 16: 183-197.
70. Ribak CE, Seress L, Amaral DG. 1985. The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J Neurocytol 14: 835-857.
71. Richter K, Langnaese K, Kreutz MR, Olias G, Zhai R, Scheich H, Garner CC, Gundelfinger ED. 1999. Presynaptic cytomatrix protein Bassoon is localized at both excitatory and inhibitory synapses of rat brain. J Comp Neurol 408: 437-448.
72. Roth SU, Sommer C, Mundel P, Kiessling M. 2001. Expression of synaptopodin, an actin-associated protein, in the rat hippocampus after limbic epilepsy. Brain Pathol 11: 169-181.
73. Rothkegel M, Mayboroda O, Rohde M, Wucherpfennig C, Valenta R, Jockusch BM. 1996. Plant and animal profilins are functionally equivalent and stabilize microfilaments in living animal cells. J Cell Sci 109 (Pt 1): 83-90.
74. Sasaki Y, Hayashi K, Shirao T, Ishikawa R, Kohama K. 1996. Inhibition by drebrin of the actin-bundling activity of brain fascin, a protein localized in filopodia of growth cones. J Neurochem 66: 980-988.
75. Scharfman HE. 1995. Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J Neurophysiol 74: 179-194.
76. Scharfman HE, Goodman JH, Sollas AL. 2000. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: Functional implications of seizure-induced neurogenesis. J Neurosci 20: 6144-6158.
77. Schoch S, Gundelfinger ED. 2006. Molecular organization of the presynaptic active zone. Cell Tissue Res 326: 379-391.
78. Scorza FA, Arida RM, Naffah-Mazzacoratti Mda G, Scerni DA, Calderazzo L, Cavalheiro EA. 2009. The pilocarpine model of epilepsy: What have we learned? Ann Acad Bras Cienc 81: 345-365.
79. Sekino Y, Kojima N, Shirao T. 2007. Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem Int 51: 92-104.
80. Shirao T, Kojima N, Obata K. 1992. Cloning of drebrin A, induction of neurite-like processes in drebrin-transfected cells. Neuroreport 3: 109-112.
81. Soriano E, Frotscher M. 1994. Mossy cells of the rat fascia dentata are glutamate-immunoreactive. Hippocampus 4: 65-69.
82. Takahashi H, Sekino Y, Tanaka S, Mizui T, Kishi S, Shirao T. 2003. Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis. J Neurosci 23: 6586-6595.
83. Takahashi H, Mizui T, Shirao T. 2006. Downregulation of drebrin A expression suppresses synaptic targeting of NMDA receptors in developing hippocampal neurones. J Neurochem 97: 110-115.
84. Tang FR, Lee WL, Yang J, Sim MK, Ling EA. 2001. Metabotropic glutamate receptor 8 in the rat hippocampus after pilocarpine induced status epilepticus. Neurosci Lett 300: 137-140.
85. Tauck DL, Nadler JV. 1985. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5: 1016-1022.
86. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D. 1999. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402: 421-425.
87. Troy CM, Friedman JE, Friedman WJ. 2002. Mechanisms of p75-mediated death of hippocampal neurons. Role of caspases. J Biol Chem 277: 34295-34302.
88. Wenzel HJ, Buckmaster PS, Anderson NL, Wenzel ME, Schwartzkroin PA. 1997. Ultrastructural localization of neurotransmitter immunoreactivity in mossy cell axons and their synaptic targets in the rat dentate gyrus. Hippocampus 7: 559-570.
89. Winder SJ, Walsh MP. 1996. Calponin. Curr Top Cell Regul 34: 33-61.
90. Winder SJ, Allen BG, Clément-Chomienne O, Walsh MP. 1998. Regulation of smooth muscle actin-myosin interaction and force by calponin. Acta Physiol Scand 164: 415-426.
91. Yang N, Higuchi O, Ohashi K, Nagata K, Wada A, Kangawa K, Nishida E, Mizuno K. 1998. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393: 809-812.
92. Zhao L, Ma QL, Calon F, Harris-White ME, Yang F, Lim GP, Morihara T, Ubeda OJ, Ambegaokar S, Hansen JE, Weisbart RH, Teter B, Frautschy SA, Cole GM. 2006. Role of p21-activated kinase pathway defects in the cognitive deficits of Alzheimer disease. Nat Neurosci 9: 234-242.