Neuroprotective effects of serotonin 5-HT1A receptor activation against ischemic cell damage in gerbil hippocampus: Involvement of NMDA receptor NR1 subunit and BDNF

Brain Research

Volumn 1199, Issue , 2008, Pages 159-166

  Salazar Colocho, Pablo ^a   Del Río, Joaquín ^a   Frechilla, Diana ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

Author keywords

5 HT1A receptor; Brain derived neurotrophic factor; Global ischemia; Hippocampus; Neuroprotection; NMDA receptor

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NEUROTROPHIN; PHOSPHOPROTEIN PHOSPHATASE 1; RECEPTOR SUBUNIT; SERINE; SEROTONIN 1A AGONIST; SEROTONIN 1A RECEPTOR; SEROTONIN AGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN REGION; CELL LOSS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GERBIL; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION;

GERBILLINAE;

EID: 40049097417     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.12.032     Document Type: Article

References (58)

1. Beck T. Lindholm D. Castren E. Wree A. Brain-derived neurotrophic factor protects against ischemic cell damage in rat hippocampus J. Cereb. Blood Flow Metab. 14 1994 689 692
2. Becquet D. Hery M. Deprez P. Faudon M. Fache M.P. Giraud P. Hery F. N -methyl- d -aspartic acid/glycine interactions on the control of 5-hydroxytryptamine release in raphe primary cultures J. Neurochem. 61 1993 1692 1697
3. Bielenberg G.W. Burkhardt M. 5-hydroxytryptamine1A agonists. A new therapeutic principle for stroke treatment Stroke 21 1990 IV161 IV163
4. Blomqvist P. Lindvall O. Stenevi U. Wieloch T. Cyclic AMP concentrations in rat neocortex and hippocampus during and following incomplete ischemia: effects of central noradrenergic neurons, prostaglandins, and adenosine J. Neurochem. 44 1985 1345 1353
5. Carr D.B. Cooper D.C. Ulrich S.L. Spruston N. Surmeier D.J. Serotonin receptor activation inhibits sodium current and dendritic excitability in prefrontal cortex via a protein kinase C-dependent mechanism J. Neurosci. 22 2002 6846 6855
6. Cohen G.M. Caspases: the executioners of apoptosis Biochem. J. 326 Pt 1 1997 1 16
7. Chen J. Nagayama T. Jin K. Stetler R.A. Zhu R.L. Graham S.H. Simon R.P. Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia J. Neurosci. 18 1998 4914 4928
8. Cheung H.H. Teves L. Wallace M.C. Gurd J.W. Increased phosphorylation of the NR1 subunit of the NMDA receptor following cerebral ischemia J. Neurochem. 78 2001 1179 1182
9. Choi D.W. Calcium: still center-stage in hypoxic-ischemic neuronal death Trends Neurosci. 18 1995 58 60
10. Choi D.W. Excitotoxic cell death J. Neurobiol. 23 1992 1261 1276
11. Dugich-Djordjevic M.M. Peterson C. Isono F. Ohsawa F. Widmer H.R. Denton T.L. Bennett G.L. Hefti F. Immunohistochemical visualization of brain-derived neurotrophic factor in the rat brain Eur. J. Neurosci. 7 1995 1831 1839
12. Dunah A.W. Wang Y. Yasuda R.P. Kameyama K. Huganir R.L. Wolfe B.B. Standaert D.G. Alterations in subunit expression, composition, and phosphorylation of striatal N -methyl- d -aspartate glutamate receptors in a rat 6-hydroxydopamine model of Parkinson's disease Mol. Pharmacol. 57 2000 342 352
13. Ferrer I. Lopez E. Pozas E. Ballabriga J. Marti E. Multiple neurotrophic signals converge in surviving CA1 neurons of the gerbil hippocampus following transient forebrain ischemia J. Comp. Neurol. 394 1998 416 430
14. Ferrer I. Ballabriga J. Marti E. Pozas E. Planas A.M. Blasi J. BDNF and TrkB co-localize in CA1 neurons resistant to transient forebrain ischemia in the adult gerbil J. Neuropathol. Exp. Neurol. 56 1997 790 797
15. Gaese B.H. Ostwald J. Temporal coding of amplitude and frequency modulation in the rat auditory cortex Eur. J. Neurosci. 7 1995 438 450
16. Gaese B.H. Ostwald J. Anesthesia changes frequency tuning of neurons in the rat primary auditory cortex J. Neurophysiol. 86 2001 1062 1066
17. Galter D. Unsicker K. Sequential activation of the 5-HT1(A) serotonin receptor and TrkB induces the serotonergic neuronal phenotype Mol. Cell Neurosci. 15 2000 446 455
18. Harkany T. Mulder J. Horvath K.M. Keijser J. van der Meeberg E.K. Nyakas C. Luiten P.G. Oral post-lesion administration of 5-HT(1A) receptor agonist repinotan hydrochloride (BAY × 3702) attenuates NMDA-induced delayed neuronal death in rat magnocellular nucleus basalis Neuroscience 108 2001 629 642
19. Hollmann M. Heinemann S. Cloned glutamate receptors Annu. Rev. Neurosci. 17 1994 31 108
20. Horiguchi T. Shima H. Suga S. Ogino M. Shimizu K. Toya S. Nagao M. Kawase T. Transient forebrain ischemia induces expression of serine/threonine protein phosphatase 1 mRNA in the vulnerable regions of gerbil brain Neurosci. Lett. 325 2002 115 118
21. Kaplan D.R. Miller F.D. Neurotrophin signal transduction in the nervous system Curr. Opin. Neurobiol. 10 2000 381 391
22. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia Brain Res. 239 1982 57 69
23. Larsson E. Nanobashvili A. Kokaia Z. Lindvall O. Evidence for neuroprotective effects of endogenous brain-derived neurotrophic factor after global forebrain ischemia in rats J. Cereb. Blood Flow Metab. 19 1999 1220 1228
24. Leker R.R. Shohami E. Cerebral ischemia and trauma-different etiologies yet similar mechanisms: neuroprotective opportunities Brain Res. Brain Res. Rev. 39 2002 55 73
25. Leonard A.S. Hell J.W. Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N -methyl- d -aspartate receptors at different sites J. Biol. Chem. 272 1997 12107 12115
26. Madhavan L. Freed W.J. Anantharam V. Kanthasamy A.G. 5-hydroxytryptamine 1A receptor activation protects against N -methyl- d -aspartate-induced apoptotic cell death in striatal and mesencephalic cultures J. Pharmacol. Exp. Ther. 304 2003 913 923
27. Matsuyama S. Nei K. Tanaka C. Regulation of GABA release via NMDA and 5-HT1A receptors in guinea pig dentate gyrus Brain Res. 761 1997 105 112
28. Mattson M.P. Maudsley S. Martin B. BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders Trends Neurosci. 27 2004 589 594
29. Moyano S. Del Rio J. Frechilla D. Role of hippocampal CaMKII in serotonin 5-HT(1A) receptor-mediated learning deficit in rats Neuropsychopharmacology 29 2004 2216 2224
30. Nakata N. Suda H. Izumi J. Tanaka Y. Ikeda Y. Kato H. Itoyama Y. Kogure K. Role of hippocampal serotonergic neurons in ischemic neuronal death Behav. Brain Res. 83 1997 217 220
31. Namura S. Zhu J. Fink K. Endres M. Srinivasan A. Tomaselli K.J. Yuan J. Moskowitz M.A. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia J. Neurosci. 18 1998 3659 3668
32. Nicholson D.W. Thornberry N.A. Caspases: killer proteases Trends Biochem. Sci. 22 1997 299 306
33. Nuydens R. de Jong M. Van Den Kieboom G. Heers C. Dispersyn G. Cornelissen F. Nuyens R. Borgers M. Geerts H. Okadaic acid-induced apoptosis in neuronal cells: evidence for an abortive mitotic attempt J. Neurochem. 70 1998 1124 1133
34. Oosterink B.J. Korte S.M. Nyakas C. Korf J. Luiten P.G. Neuroprotection against N -methyl- d -aspartate-induced excitotoxicity in rat magnocellular nucleus basalis by the 5-HT1A receptor agonist 8-OH-DPAT Eur. J. Pharmacol. 358 1998 147 152
35. Parsons C.G. Danysz W. Quack G. Glutamate in CNS disorders as a target for drug development: an update Drug News Perspect. 11 1998 523 569
36. Peruche B. Backhauss C. Prehn J.H. Krieglstein J. Protective effects of 5-HT1A receptor agonists against neuronal damage demonstrated in vivo and in vitro J. Neural. Transm. Park Dis. Dement. Sect. 8 1994 73 83
37. Piera M.J. Beaughard M. Michelin M.T. Massingham R. Effects of the 5-hydroxytryptamine1A receptor agonists, 8-OH-DPAT, buspirone and flesinoxan, upon brain damage induced by transient global cerebral ischaemia in gerbils Arch. Int. Pharmacodyn. Ther. 329 1995 347 359
38. Prehn J.H. Backhauss C. Karkoutly C. Nuglisch J. Peruche B. Rossberg C. Krieglstein J. Neuroprotective properties of 5-HT1A receptor agonists in rodent models of focal and global cerebral ischemia Eur. J. Pharmacol. 203 1991 213 222
39. Pulsinelli W.A. Brierley J.B. Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia Ann. Neurol. 11 1982 491 498
40. Raman I.M. Tong G. Jahr C.E. Beta-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase Neuron. 16 1996 415 421
41. Raymond J.R. Mukhin Y.V. Gelasco A. Turner J. Collinsworth G. Gettys T.W. Grewal J.S. Garnovskaya M.N. Multiplicity of mechanisms of serotonin receptor signal transduction Pharmacol. Ther. 92 2001 179 212
42. Ross S.B. Renyi L. Kelder D. N -methyl- d -aspartate receptor antagonists counteract the long lasting 5-HT1A receptor-induced attenuation of postsynaptic responses in the rat in vivo Naunyn Schmiedebergs Arch. Pharmacol. 346 1992 138 143
43. Rothman S.M. Olney J.W. Glutamate and the pathophysiology of hypoxic–ischemic brain damage Ann. Neurol. 19 1986 105 111
44. Schabitz W.R. Sommer C. Zoder W. Kiessling M. Schwaninger M. Schwab S. Intravenous brain-derived neurotrophic factor reduces infarct size and counterregulates Bax and Bcl-2 expression after temporary focal cerebral ischemia Stroke 31 2000 2212 2217
45. Schabitz W.R. Schwab S. Spranger M. Hacke W. Intraventricular brain-derived neurotrophic factor reduces infarct size after focal cerebral ischemia in rats J. Cereb. Blood Flow Metab. 17 1997 500 506
46. Schiapparelli L. Del Rio J. Frechilla D. Serotonin 5-HT receptor blockade enhances Ca(2+)/calmodulin-dependent protein kinase II function and membrane expression of AMPA receptor subunits in the rat hippocampus: implications for memory formation J. Neurochem. 94 2005 884 895
47. Siesjo B.K. Historical overview. Calcium, ischemia, and death of brain cells Ann. N. Y. Acad. Sci. 522 1988 638 661
48. Strosznajder J. Chalimoniuk M. Samochocki M. Activation of serotonergic 5-HT1A receptor reduces Ca(2+)- and glutamatergic receptor-evoked arachidonic acid and No/cGMP release in adult hippocampus Neurochem. Int. 28 1996 439 444
49. Swope S.L. Moss S.J. Raymond L.A. Huganir R.L. Regulation of ligand-gated ion channels by protein phosphorylation Adv. Second Messenger Phosphoprotein Res. 33 1999 49 78
50. Takagi N. Shinno K. Teves L. Bissoon N. Wallace M.C. Gurd J.W. Transient ischemia differentially increases tyrosine phosphorylation of NMDA receptor subunits 2A and 2B J. Neurochem. 69 1997 1060 1065
51. Tingley W.G. Ehlers M.D. Kameyama K. Doherty C. Ptak J.B. Riley C.T. Huganir R.L. Characterization of protein kinase A and protein kinase C phosphorylation of the N -methyl- d -aspartate receptor NR1 subunit using phosphorylation site-specific antibodies J. Biol. Chem. 272 1997 5157 5166
52. Torup L. Moller A. Sager T.N. Diemer N.H. Neuroprotective effect of 8-OH-DPAT in global cerebral ischemia assessed by stereological cell counting Eur. J. Pharmacol. 395 2000 137 141
53. Tsukahara T. Yonekawa Y. Tanaka K. Ohara O. Wantanabe S. Kimura T. Nishijima T. Taniguchi T. The role of brain-derived neurotrophic factor in transient forebrain ischemia in the rat brain Neurosurgery 34 1994 323 331 discussion 331
54. Uchino H. Minamikawa-Tachino R. Kristian T. Perkins G. Narazaki M. Siesjo B.K. Shibasaki F. Differential neuroprotection by cyclosporin A and FK506 following ischemia corresponds with differing abilities to inhibit calcineurin and the mitochondrial permeability transition Neurobiol. Dis. 10 2002 219 233
55. Wetmore C. Ernfors P. Persson H. Olson L. Localization of brain-derived neurotrophic factor mRNA to neurons in the brain by in situ hybridization Exp. Neurol. 109 1990 141 152
56. Wu D. Neuroprotection in experimental stroke with targeted neurotrophins NeuroRx 2 2005 120 128
57. Yamashita K. Wiessner C. Lindholm D. Thoenen H. Hossmann K.A. Post-occlusion treatment with BDNF reduces infarct size in a model of permanent occlusion of the middle cerebral artery in rat Metab. Brain Dis. 12 1997 271 280
58. Yuen E.Y. Jiang Q. Chen P. Gu Z. Feng J. Yan Z. Serotonin 5-HT1A receptors regulate NMDA receptor channels through a microtubule-dependent mechanism J. Neurosci. 25 2005 5488 5501