GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2+-binding protein parvalbumin

Nitsch, Cordula; Scotti, Alessandra L.; Sommacal, Arianna; Kalt, Gabriela

doi:10.1016/0304-3940(89)90631-9

Cited by 206 publications

(74 citation statements)

References 17 publications

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“…Possibly, the loss of postsynaptic targets is associated with a progres sive loss of feedback inhibition and hence increased activity of the presynaptic cell bodies. Our finding of a secondary elevation of glucose utilization in the oriens layer between 2 and 3 weeks would support this notion, since the hippocampal interneurons in the oriens layer of CAl were demonstrated to be relatively ischemia resistant (Johansen et al, 1983;Nitsch et al , 1989b). It is also intriguing that Crepel et al (1988) pointed out that 10 days post ischemia 40% of NMDA binding sites in the CAl sector are still present and suggested them to be located on interneurons.…”

Section: Figsupporting

confidence: 74%

Glucose Utilization in Rat Hippocampus after Long-Term Recovery from Ischemia

Beck

Wree

Schleicher

1990

J Cereb Blood Flow Metab

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Summary:The influence on hippocampal glucose utiliza tion of a transient lO-min forebrain ischemia was quanti fied in male Wi star rats after 2 and 3 weeks as well as after 3 months by application of the [14C]2-deoxyglucose tech nique. Ischemia was induced by occlusion of the carotid arteries and simultaneous lowering of the blood pressure to 40 mm Hg. For identification of the hippocampal ar chitecture, sections were stained for perikarya (cresyl vi olet) and for acetylcholinesterase. The hippocampal re gions clearly showed different responses to the ischemic insult. The necrotic pyramidal cells being almost com pletely removed, significant increases in glucose utiliza tion occurred in most layers of the CAl sector at 2 and 3For over 100 years it has been a well-documented fact that cell populations in the brain do not suc cumb to an ischemic insult uniformly (Sommer, 1880; Bratz, 1899). This concept of selective vulner ability has been addressed in numerous experimen tal studies. Recently, evidence has been presented that accumulation of Ca 2 + on cellular as well as on subcellular levels (Dienel, 1984; Simon et aI., 1984a; Hossmann et aI. , 1985; Sakamoto et aI. , 1986; van Reempts et aI. , 1986; Deshpande et aI., 1987; Dux et aI. , 1987) and excessive excitatory in put due to excitatory amino acids (Benveniste et aI. , 1984; Simon et aI., 1984b; Lodge et aI. , 1986) are interwoven and play a key role in ischemic cell damage. These studies as well as work on postisch emic capillary perfusion (lmdahl and Hossmann, 1986), impaired protein synthesis (Thiel mann et aI., Received November 2, 1989; revised December 12, 1989; ac cepted December 22, 1989. Address correspondence and reprint requests to Dr. T. Beck at Laboratory of Cellular and Molecular Neurobiology, Depart ment of Pathology, Columbia University College of Physicians and Surgeons, 630 W. 168 St., New York, NY 10032, U.S.A.Abbreviations used: NMDA, N-methyl-D-aspartate. 542weeks post ischemia, while widespread reductions pre vailed in all other sectors and the dentate gyrus. At 3 months after the ischemic insult, glucose utilization was reduced in all hippocampal structures including the CAl region. The increases in glucose utilization in the CAl sector are suggested to indicate long-lasting presynaptic hyperexcitation, while the widespread reductions in glu cose utilization demonstrate that neuronal activity is also altered in hippocampal areas that do not show major his tological damage. Key Words: Cerebral ischemia Hippocampus-Local cerebral glucose utilization Long-term recovery.1986), and impaired normalization of pH in the CAl sector (Munekata and Hossmann, 1987) cover a time range that extends up to 7 days post ischemia. The same holds true for the extensive histological work characterizing the temporal profile of isch emic damage in gerbil and rat models of cerebral ischemia (Kirino, 1982; Pulsinelli et aI. , 1982a; Kirino et aI., 1984; Smith et aI., 1984;Schmidt Kastner and Hossmann, 1988), the respective time points ranging from 3 ...

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Section: Figsupporting

confidence: 74%

Glucose Utilization in Rat Hippocampus after Long-Term Recovery from Ischemia

Beck

Wree

Schleicher

1990

J Cereb Blood Flow Metab

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“…The pyramidal neurons in the hippocampal CA1 sector begin to degenerate a few days after ischemia. In contrast, interneurons of the hippocampal CA1 sector and granule cells of dentate gyrus are resistant to such a brief period of ischemic insult (Nitsch et al, 1989;Tortosa and Ferrer, 1993). A similar pattern is seen in the human hippocampus after cerebral ischemia (Petito et al, 1987).…”

Section: Introductionmentioning

confidence: 74%

“…Therefore, the PV has been regarded as a superior marker for a subpopulation of GABAergic interneurons throughout the brain (Celio, 1986;Schwartz-Bloom and Sah, 2001). A previous study has shown that PV-immunoreactive neurons are particularly resistant to transient ischemic insult which produces hippocampal CA1 neuronal death (Nitsch et al, 1989). Furthermore, Tortosa and Ferrer (1993) also demonstrated that PV-immunoreactive neurons in the hippocampus are preserved after a brief period of cerebral ischemia in gerbils.…”

Section: Discussionmentioning

confidence: 99%

Alterations of Interneurons of the Gerbil Hippocampus after Transient Cerebral Ischemia: Effect of Pitavastatin

Himeda

Hayakawa

Tounai

et al. 2005

Neuropsychopharmacol

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We investigated the immunohistochemical alterations of parvalbumin (PV)-expressing interneurons in the hippocampus after transient cerebral ischemia in gerbils in comparison with neuronal nitric oxide synthase (nNOS)-expressing interneurons. We also examined the effect of 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitor pitavastatin against the damage of neurons and interneurons in the hippocampus after cerebral ischemia. Severe neuronal damage was observed in the hippocampal CA1 pyramidal neurons 5 and 14 days after ischemia. The PV immunoreactivity was unchanged up to 2 days after ischemia. At 5 and 14 days after ischemia, in contrast, a conspicuous reduction of PV immunoreactivity was observed in interneurons of the hippocampal CA1 sector. Furthermore, a significant decrease of PV immunoreactivity was found in interneurons of the hippocampal CA3 sector. No damage of nNOS-immunopositive interneurons was detected in the gerbil hippocampus up to 1 day after ischemia. Thereafter, a decrease of nNOS immunoreactive interneurons was found in the hippocampal CA1 sector up to 14 days after ischemia. Pitavastatin significantly prevented the neuronal cell loss in the hippocampal CA1 sector 5 days after ischemia. Our immunohistochemical study also showed that pitavastatin prevented significant decrease of PV-and nNOS-positive interneurons in the hippocampus after ischemia. Double-labeled immunostainings showed that PV immunoreactivity was not found in nNOS-immunopositive interneurons of the brain. The present study demonstrates that cerebral ischemia can cause a loss of both PV-and nNOS-immunoreactive interneurons in the hippocampal CA1 sector. Our findings also show that the damage to nNOS-immunopositive interneurons may precede the neuronal cell loss in the hippocampal CA1 sector after ischemia and nNOS-positive interneurons may play some role in the pathogenesis of cerebral ischemic diseases. Furthermore, our present study indicates that pitavastatin can prevent the damage of interneurons in the hippocampus after cerebral ischemia. Thus, our study provides valuable information for the pathogenesis after cerebral ischemia.

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“…On the one hand, a neuroprotective role for PV has been described in hippocampal interneurons surviving delayed ischemic cell death after a transient bilateral occlusion of the carotid arteries (Nitsch et al, 1989). PV-containing neurons also exhibit a higher survival rate in the human epileptic hippocampus (Sloviter et al, 1991), and recently, a protective effect of PV on excitotoxic motor neuron death has been observed (Van Den Bosch et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Ectopic parvalbumin expression in mouse forebrain neurons increases excitotoxic injury provoked by ibotenic acid injection into the striatum

Maetzler

Nitsch

Bendfeldt

et al. 2004

Experimental Neurology

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A neuroprotective role for Ca 2+ -binding proteins in neurodegenerative conditions ranging from ischemia to Alzheimer's disease has been suggested in several studies. A key phenomenon in neurodegeneration is the Ca 2+ -mediated excitotoxicity brought about by the neurotransmitter glutamate. To evaluate the relative ability to resist excitotoxicity of neurons containing the slow-onset Ca 2+ -binding protein parvalbumin (PV), we injected the glutamate agonist ibotenic acid (IBO) into the striatum of adult mice ectopically expressing PV in neurons. Striatal ibotenic acid injection results in local nerve cell loss and reactive astrogliosis. Light microscopic evaluation, carried out after a delay of 2 and 4 weeks, reveals an enlarged and accelerated neurodegenerative process in mice ectopically expressing neuronal PV. Thus, PV is not neuroprotective, it rather enhances nerve cell death. This result implicates that the increase in cytosolic Ca 2+ -buffering capacity in the transgenic mice impairs other systems involved in Ca 2+ sequestration. In addition, ultrastructural morphometric analysis shows that in neurons the mitochondrial volume is reduced in mice ectopically expressing neuronal PV. This is paralleled by a reduction in the amount of the mitochondrial marker enzyme cytochrome c oxidase subunit I (COXI). We conclude that alterations in the Ca 2+ homeostasis present in mice ectopically expressing neuronal PV are more deleterious under excitotoxic stress and largely outweigh the potential benefits of an increased Ca 2+ -buffering capacity resulting from PV.

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GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2+-binding protein parvalbumin

Cited by 206 publications

References 17 publications

Glucose Utilization in Rat Hippocampus after Long-Term Recovery from Ischemia

Glucose Utilization in Rat Hippocampus after Long-Term Recovery from Ischemia

Alterations of Interneurons of the Gerbil Hippocampus after Transient Cerebral Ischemia: Effect of Pitavastatin

Ectopic parvalbumin expression in mouse forebrain neurons increases excitotoxic injury provoked by ibotenic acid injection into the striatum

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