Changes in hippocampal synapses and learning-memory abilities in a streptozotocin-treated rat model and intervention by using fasudil hydrochloride

Neuroscience

Volumn 200, Issue , 2012, Pages 120-129

  Hou, Y ^a   Zhou, L ^a   Yang, Q D ^a   Du, X P ^a   Li, M ^a   Yuan, M ^a   Zhou, Z W ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Cofilin; Fasudil hydrochloride; LIMK2; Streptozotocin; Synapses

Indexed keywords

ADENINE; CITRATE SODIUM; CITRIC ACID; COFILIN; CYTOSINE; FASUDIL; GUANOSINE; SYNAPTOPHYSIN; THYMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; MEMORY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; STREPTOZOCIN DIABETES; SYNAPSE; WESTERN BLOTTING;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LEARNING DISORDERS; LIM KINASES; MALE; MAZE LEARNING; MICROSCOPY, ELECTRON, TRANSMISSION; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RNA, MESSENGER; SYNAPSES; SYNAPTOPHYSIN; TIME FACTORS;

EID: 84855189897     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.10.030     Document Type: Article

References (78)

1. Agnew B.J., Minamide L.S., Bamburg J.R. Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J Biol Chem 1995, 270:17582-17587.
2. Anderton B.H., Callahan L., Coleman P., Davies P., Flood D., Jicha G.A., Ohm T., Weaver C. Dendritic changes in Alzheimer's disease and factors that may underlie these changes. Prog Neurobiol 1998, 55:595-609.
3. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 1998, 393:805-812.
4. Bamburg J.R. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol 1999, 15:185-230.
5. Blokland A., Jolles J. Spatial learning deficit and reduced hippocampal ChAT activity in rats after an ICV injection of streptozotocin. Pharmacol Biochem Behav 1993, 44:491-494.
6. Blokland A., Jolles J. Behavioral and biochemical effects of an ICV injection of streptozotocin in old Lewis rats. Pharmacol Biochem Behav 1994, 47:833-837.
7. Brian A.C., George J.D., Shannon L.G., Anthony J.K. Increased dendrite branching in AβPP/PS1 mice and elongation of dendrite arbors by fasudil administration. J Alzheimers Dis 2010, 20:1003-1008.
8. Calverly R.K., Jones D.G. Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain Res Rev 1990, 15:215-249.
9. Cohen R.S. The structure of postsynaptic densities isolated from dog cerebral cortex. I. Overall morphology and protein composition. J Cell Biol 1977, 74:181-203.
10. Coleman P., Federoff H., Kurlan R. A focus on the synapse for neuroprotection in Alzheimer disease and other dementias. Neurology 2004, 63:1155-1162.
11. Coleman P.D., Yao P.J. Synaptic slaughter in Alzheimer's disease. Neurobiol Aging 2003, 24:1023-1027.
12. DeKosky S.T., Scheff S.W. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990, 27:457-464.
13. Dickson D.W., Crystal H.A., Bevona C., Honer W., Vincent I., Davies P. Correlations of synaptic and pathological markers with cognition of the elderly. Neurobiol Aging 1995, 16:285-304.
14. Ding Y., Li J., Lai Q., Azam S., Rafols J.A., Diaz F.G. Functional improvement after motor training is correlated with synaptic plasticity in rat thalamus. Neurol Res 2002, 24:829-836.
15. Duelli R., Schröck H., Kuschinsky W., Hoyer S. Intracerebroventricular injection of streptozotocin induces discrete local changes in cerebral glucose utilization in rats. Int J Dev Neurosci 1994, 12:737-743.
16. Endo M., Ohashi K., Sasaki Y., Goshima Y., Niwa R., Uemura T., Mizuno K. Control of growth cone motility and morphology by LIM kinase and slingshot via phosphorylation and dephosphorylation of cofilin. J Neurosci 2003, 23:2527-2537.
17. Fukata Y., Amano M., Kaibuchi K. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol Sci 2001, 22:32-39.
18. Garcia P., Youssef I., Utvik J.K., Florent-Béchard S., Barthélémy V., Malaplate-Armand C., Kriem B., Stenger C., Koziel V., Olivier J.L., Escanye M.C., Hanse M., Allouche A., Desbène C., Yen F.T., Bjerkvig R., Oster T., Niclou S.P., Pillot T. Ciliary neurotrophic factor cell-based delivery prevents synaptic impairment and improves memory in mouse models of Alzheimer's disease. J Neurosci 2010, 30:7516-7527.
19. Güldner F.H., Bahar E., Young C.A., Ingham C.A. Structural plasticity of optic synapses in the rat suprachiasmatic nucleus: adaptation to long-term influence of light and darkness. Cell Tissue Res 1997, 287:43-60.
20. Güldner F.H., Ingham C.A. Increase in postsynaptic density material in optic target neurons of the rat suprachiasmatic nucleus after bilateral enucleation. Neurosci Lett 1980, 17:27-31.
21. Güldner F.H., Phillips S.C. Structural plasticity of developing optic synapses under different lighting conditions. Neurosci Lett 1986, 55:225-228.
22. Hamos J.E., DeGennaro L.J., Drachman D.A. Synaptic loss in Alzheimer's disease and other dementias. Neurology 1989, 39:355-361.
23. Heinonen O., Soininen H., Sorvari H., Kosunen O., Paljärvi L., Koivisto E., Riekkinen P.J. Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease. Neuroscience 1995, 64:375-384.
24. Honer W.G., Dickson D.W., Gleeson J., Davies P. Regional synaptic pathology in Alzheimer's disease. Neurobiol Aging 1992, 13:375-382.
25. Hoyer S., Lee S.K., Löffler T., Schliebs R. Inhibition of the neuronal insulin receptor. An in vivo model for sporadic Alzheimer disease?. Ann N Y Acad Sci 2000, 920:256-528.
26. Hu R., Cai W.Q., Wu X.G., Yang Z. Astrocyte-derived estrogen enhances synapse formation and synaptic transmission between cultured neonatal rat cortical neurons. Neuroscience 2007, 144:1229-1240.
27. Huang L., He Z., Guo L., Wang H. Improvement of cognitive deficit and neuronal damage in rats with chronic cerebral ischemia via relative long-term inhibition of rho-kinase. Cell Mol Neurobiol 2008, 28:757-768.
28. Huentelman M.J., Stephan D.A., Talboom J., Corneveaux J.J., Reiman D.M., Gerber J.D., Barnes C.A., Alexander G.E., Reiman E.M., Bimonte-Nelson H.A. Peripheral delivery of a ROCK inhibitor improves learning and working memory. Behav Neurosci 2009, 123:218-223.
29. Johannsen S., Duning K., Pavenstädt H., Kremerskothen J., Boeckers T.M. Temporal-spatial expression and novel biochemical properties of the memory-related protein KIBRA. Neuroscience 2008, 155:1165-1173.
30. Jones D.G., Calvery R.K.S. Perforated and non-perforated synapses in rat neocortex: three-dimensional reconstructions. Brain Res 1991, 556:247-258.
31. Jones D.G., Devon R.M. An ultrastructural study into the effects of pentobarbitone on synaptic organization. Brain Res 1978, 147:47-63.
32. Jones D.G., Harris R.J. An analysis of contemporary morphological concepts of synaptic remodeling in the CNS: the perforated synapses revisited. Rev Neurosci 1995, 6:177-219.
33. Kim C.H., Lisman J.E. A role of actin filaments in synaptic transmission and long-term potentiation. Neuroscience 1999, 19:4314-4324.
34. Krucker T., Siggins G.R., Halpain S. Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of hippocampus. Proc Natl Acad Sci U S A 2000, 97:6856-6861.
35. Luo L. Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu Rev Cell Dev Biol 2002, 18:601-635.
36. Maekawa M., Ishizaki T., Boku S., Watanabe N., Fujita A., Iwamatsu A., Obinata T., Ohashi K., Mizuno K., Narumiya S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 1999, 285:895-898.
37. Markus E.J., Petit T.L. Synaptic structural plasticity: role of synaptic shape. Synapse 1989, 3:1-11.
38. Masliah E., Mallory M., Alford M., DeTeresa R., Hansen L.A., McKeel D.W., Morris J.C. Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 2001, 56:127-129.
39. Masliah E., Mallory M., Hansen L., DeTeresa R., Alford M., Terry R.D. Synaptic and neuritic alterations during the progression of Alzheimer's disease. Neurosci Lett 1994, 174:67-72.
40. Matus A. The postsynaptic density. Trends Neurosci 1981, 4:51-53.
41. Meng Y., Takahashi H., Meng J., Zhang Y., Lu G., Asrar S., Nakamura T., Jia Z. Regulation of ADF/cofilin phosphorylation and synaptic function by LIM-kinase. Neuropharmacology 2004, 47:746-754.
42. Meng Y.H., Zhang Y., Tregoubov V., Janus C., Cruz L., Jackson M., Lu W.Y., MacDonald J.F., Wang J.Y., Falls D.L., Jia Z.P. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 2002, 35:121-133.
43. Morales M., Colicos M.A., Goda Y. Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 2000, 27:539-550.
44. Mori T., Okano I., Mizuno K., Tohyama M., Wanaka A. Comparison of tissue distribution of two novel serine/threonine kinase genes containing the LIM motif (LIMK-1 and LIMK-2) in the developing rat. Mol Brain Res 1997, 45:247-254.
45. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984, 11:47-60.
46. Mueller B.K., Mack H., Teusch N. Rho kinase, a promising drug target for neurological disorders. Nat Rev Drug Discov 2005, 4:387-398.
47. Mullany P.M., Lynch M.A. Evidence for a role for synaptophysin expression of long-term potentiation in rat dentate gyrus. Neuroreport 1998, 9:2489-2494.
48. Nakayama A.Y., Harms M.B., Luo L. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J Neurosci 2000, 20:5329-5338.
49. Petratos S., Li Q.X., George A.J., Hou X., Kerr M.L., Unabia S.E., Hatzinisiriou I., Maksel D., Aguilar M.I., Small D.H. The beta-amyloid protein of Alzheimer's disease increases neuronal CRMP-2 phosphorylation by a Rho-GTP mechanism. Brain 2008, 131:90-108.
50. Prickaerts J., Fahrig T., Blokland A. Cognitive performance and biochemical markers in septum, hippocampus and striatum of rats after an i.c.v. injection of streptozotocin: a correlation analysis. Behav Brain Res 1999, 102:73-88.
51. Qiu H., Jin G.Q., Jin R.F., Zhao W.K. Analysis of variance of repeated data measured by water maze with SPSS. J Chin Integr Med 2007, 5:101-105.
52. Rehm H., Wiedenmann B., Betz H. Molecular characterization of synaptophysin, a major calcium-binding protein of the synaptic vesicle membrane. EMBO J 1986, 5:535-541.
53. Rosenmund C., Rettig J., Brose N. Molecular mechanisms of active zone function. Curr Opin Neurobiol 2003, 13:509-519.
54. Rune G.M., Frotscher M. Neurosteroid synthesis in the hippocampus: role in synaptic plasticity. Neuroscience 2005, 136:833-842.
55. Salminen A., Suuronen T., Kaarniranta K. ROCK, PAK, and Toll of synapses in Alzheimer's disease. Biochem Biophys Res Commun 2008, 371:587-590.
56. Scheff S.W., Price D.A., Schmitt F.A., DeKosky S.T., Mufson E.J. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 2007, 68:1501-1508.
57. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
58. Sfakianos M.K., Eisman A., Gourley S.L., Bradley W.D., Scheetz A.J., Settleman J., Taylor J.R., Greer C.A., Williamson A., Koleske A.J. Inhibition of Rho via Arg and p190RhoGAP in the postnatal mouse hippocampus regulates dendritic spine maturation, synapse and dendrite stability, and behavior. J Neurosci 2007, 27:10982-10992.
59. Siekevits P. The postsynaptic density: a possible role in long-lasting effects in the rat central nervous system. Proc Natl Acad Sci U S A 1985, 82:3494-3498.
60. Streit P., Akert K., Sandri C., Livingston R.B., Moore H. Dynamic ultrastructure of presynaptic membranes at nerve terminals in the spinal cord of rats. Brain Res 1972, 48:11-26.
61. Sumi T., Matsumoto K., Nakamura T. Specific activation of LIM kinase 2 via phosphorylation of threonine 505 by ROCK, a Rho-dependent protein kinase. J Biol Chem 2001, 276:670-676.
62. Sze C.I., Troncoso J.C., Kawas C., Mouton P., Price D.L., Martin L.J. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer's disease. J Neuropathol Exp Neurol 1997, 56:933-944.
63. Takahashi H., Koshimizu U., Miyazaki M., Nakamura T. Impaired spermatogenic ability of testicular germ cells in mice deficient in the LIM-kinase 2 gene. Dev Biol 2002, 241:259-272.
64. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991, 30:572-580.
65. Thirone A.C., Speight P., Zulys M., Rotstein O.D., Szászi K., Pedersen S.F., Kapus A. Hyperosmotic stress induces Rho/Rho kinase/LIM kinase-mediated cofilin phosphorylation in tubular cells: key role in the osmotically triggered F-actin response. Am J Physiol Cell Physiol 2009, 296:C463-C475.
66. Toshima Y., Satoh S., Ikegaki I., Asano T. A new model of cerebral microthrombosis in rats and the neuroprotective effect of a Rho-kinase inhibitor. Stroke 2000, 31:2245-2250.
67. Van Kolen K., Slegers H. Atypical PKCzeta is involved in RhoA-dependent mitogenic signaling by the P2Y (12) receptor in C6 cells. FEBS J 2006, 273:1843-1854.
68. Wang R., Tang Y., Feng B., Ye C., Fang L., Zhang L., Li L. Changes in hippocampal synapses and learning-memory abilities in age-increasing rats and effects of tetrahydroxystilbene glucoside in aged rats. Neuroscience 2007, 149:739-746.
69. Wesa J.M., Chang F.L., Greenough W.T., West R.W. Synaptic contact curvature: effects of differential rearing on rat occipital cortex. Brain Res 1982, 4:253-257.
70. Wong T.P., Marchese G., Casu M.A., Ribeiro-da-Silva A., Cuello A.C., Koninck Y.D. Loss of presynaptic and postsynaptic structures is accompanied by compensatory increase in action potential-dependent synaptic input to layer V neocortical pyramidal neurons in aged rats. J Neurosci 2000, 20:8596-8606.
71. Wyszynski M., Lin J., Rao A., Nigh E., Beggs A.H., Craig A.M., Sheng M. Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 1997, 385:439-442.
72. Yang N., Higuchi O., Ohashi K., Nagata K., Wada A., Kangawa K., Nishida E., Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 1998, 393:809-812.
73. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001, 24:1071-1089.
74. Zebda N., Bernard O., Bailly M., Welti S., Lawrence D.S., Condeelis J.S. Phosphorylation of ADF/cofilin abolishes EGF-induced actin nucleation at the leading edge and subsequent lamellipod extension. J Cell Biol 2000, 151:1119-1128.
75. Zhang W., Benson D.L. Development and molecular organization of dendritic spines and their synapses. Hippocampus 2000, 10:512-526.
76. Zhang Z.G., Hu Y.Z. Correlation between aged learning-memory dysfunction and frequency of perforated synapses in brain. J Zhejiang Norm Univ 1999, 22:81-85.
77. Zhao Y.M., Pei J.J., Ji Z.J., Zhao Z.W., Qian Y.Y., Sheng S.L. Effect of amyloid precursor protein 17mer peptide on microtubule structure and tau protein in experimental diabetic mice. Neuroreport 2003, 14:61-66.
78. Zhou Q., Xiao M.Y., Nicoll R.A. Contribution of cytoskeleton to the internalization of AMPA receptors. Proc Natl Acad Sci U S A 2001, 98:1261-1266.