Abstract
Perfusion of hippocampal slices with an inhibitor of nitric oxide (NO) synthase-blocked induction of long-term potentiation (LTP) produced by a one-train tetanus and significantly reduced LTP by a two-train tetanus, but only slightly reduced LTP by a four-train tetanus. Inhibitors of heme oxygenase, the synthetic enzyme for carbon monoxide (CO), significantly reduced LTP by either a two-train or four-train tetanus. These results suggest that NO and CO are both involved in LTP but may play somewhat different roles. One possibility is that NO serves a phasic, signaling role, whereas CO provides tonic, background stimulation. Another possibility is that NO and CO are phasically activated under somewhat different circumstances, perhaps involving different receptors and second messengers. Because NO is known to be activated by stimulation of NMDA receptors during tetanus, we investigated the possibility that CO might be activated by stimulation of metabotropic glutamate receptors (mGluRs). Consistent with this idea, long-lasting potentiation by the mGluR agonist tACPD was blocked by inhibitors of heme oxygenase but not NO synthase. Potentiation by tACPD was also blocked by inhibitors of soluble guanylyl cyclase (a target of both NO and CO) or cGMP-dependent protein kinase, and guanylyl cyclase was activated by tACPD in hippocampal slices. However, biochemical assays indicate that whereas heme oxygenase is constitutively active in hippocampus, it does not appear to be stimulated by either tetanus or tACPD. These results are most consistent with the possibility that constitutive (tonic) rather than stimulated (phasic) heme oxygenase activity is necessary for potentiation by tetanus or tACPD, and suggest that mGluR activation stimulates guanylyl cyclase phasically through some other pathway.
References
70
Referenced
17
10.1038/376074a0
10.1016/S0092-8674(00)81797-3
{'key': '2021111105534862000_5.6.467.3', 'first-page': '7425', 'article-title': 'Inhibition of nitric oxide synthase does not prevent induction of long-term potentiation in vivo.', 'volume': '14', 'author': 'Bannerman', 'year': '1994', 'journal-title': 'J. Neurosci.'}
/ J. Neurosci. / Inhibition of nitric oxide synthase does not prevent induction of long-term potentiation in vivo. by Bannerman (1994)10.1113/jphysiol.1991.sp018901
/ J. Physiol. / Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. by Baskys (1991)10.1038/361031a0
10.1016/0896-6273(95)90018-7
10.1016/0014-2999(91)90505-K
10.1126/science.7909958
10.1016/S0896-6273(00)80377-3
10.1038/368740a0
10.1016/0306-4522(95)00349-N
10.1146/annurev.neuro.20.1.157
10.1097/00001756-199307000-00020
10.1016/0896-6273(92)90078-R
10.1016/0304-3940(94)90883-4
10.1016/0163-1047(90)90595-W
10.1523/JNEUROSCI.16-01-00418.1996
/ J. Neurosci. / The selective neuronal NO synthase inhibitor 7-nitro-indazole blocks both long-term potentiation and depotentiation of field EPSPs in rat hippocampal CA1 in vivo. by Doyle (1996)10.1016/0304-3940(91)90147-L
10.1002/(SICI)1098-1063(1997)7:3<286::AID-HIPO4>3.0.CO;2-J
/ Hippocampus / Nitric-oxide-guanylyl-cyclase-dependent and independent components of multiple forms of long-term synaptic depression. by Gage (1997){'key': '2021111105534862000_5.6.467.20', 'first-page': '965', 'article-title': 'Zinc protoporphyrin-IX blocks the effects of metabotropic glutamate receptor activation in the rat nucleus tractus solitarii.', 'volume': '43', 'author': 'Glaum', 'year': '1993', 'journal-title': 'Mol. Pharmacol.'}
/ Mol. Pharmacol. / Zinc protoporphyrin-IX blocks the effects of metabotropic glutamate receptor activation in the rat nucleus tractus solitarii. by Glaum (1993)10.1152/jn.1992.68.2.639
/ J. Neurophysiol. / Evidence for nitric oxide synthase inhibitor-sensitive and insensitive hippocampal synaptic potentiation. by Gribkoff (1992)10.1016/0896-6273(92)90288-O
10.1016/0304-3940(93)90919-C
10.1101/lm.3.4.289
10.1146/annurev.ne.16.030193.003205
10.1016/0092-8674(93)90615-W
10.1101/lm.1.1.74
10.1016/S0021-9258(20)82126-7
/ J. Biol. Chem. / Regulation of soluble guanylate cyclase activity by porphyrins and metalloporphyrins. by Ignarro (1984)10.1254/jjp.64.225
/ Jpn. J. Pharmacol. / Involvement of carbon monoxide in long-term potentiation in the dentate gyrus of anesthetized rats. by Ikegaya (1994)10.1126/science.7886457
10.1126/science.274.5293.1744
10.1152/jn.1993.70.3.1260
/ J. Neurophysiol. / Nitric oxide inhibitors facilitate the induction of hippocampal long-term potentiation by modulating NMDA responses. by Kato (1993)10.1073/pnas.93.22.12547
10.1016/0006-8993(95)00761-E
10.1152/jn.1993.70.6.2673
/ J. Neurophysiol. / Protoprophyrins modulate voltage-gated Ca current in AtT-20 pituitary cells. by Linden (1993)10.1016/0922-4106(94)90149-X
10.1096/fasebj.2.10.3290025
/ FASEB J. / Heme oxygenase: Function, multiplicity, regulatory mechanisms, and clinical applications. by Maines (1988)10.1006/mcne.1993.1049
/ Mol. Cell. Neurosci. / Carbon monoxide: An emerging regulator of cGMP in the brain. (1993)10.1523/JNEUROSCI.17-07-02645.1997
/ J. Neurosci. / Nitric oxide facilitates long-term potentiaton, but not long-term depression. by Malen (1997){'key': '2021111105534862000_5.6.467.40', 'first-page': '708', 'article-title': 'Selective blockade of endothelium-dependent and glycerol trinitrate-induced relaxation by hemoglobin and by methylene blue in the rabbit aorta.', 'volume': '232', 'author': 'Martin', 'year': '1985', 'journal-title': 'J. Pharmacol. Exp. Ther.'}
/ J. Pharmacol. Exp. Ther. / Selective blockade of endothelium-dependent and glycerol trinitrate-induced relaxation by hemoglobin and by methylene blue in the rabbit aorta. by Martin (1985)10.1016/0896-6273(94)90060-4
10.1016/0006-8993(93)91756-I
10.1016/0896-6273(95)90222-8
10.1073/pnas.88.24.11285
10.1126/science.7518615
10.1046/j.1471-4159.1995.64031298.x
/ J. Neurochem. / Protein kinase C modulates calcium sensitivity of nitric oxide synthase in cerebellar slices. by Okada (1995)10.1016/0168-0102(96)01057-7
10.1016/0014-2999(91)90920-L
10.1016/0896-6273(95)90177-9
10.1016/0304-3940(92)90486-Q
10.1126/science.1720572
10.1073/pnas.91.25.11958
10.1101/lm.3.1.42
10.1073/pnas.81.12.3905
10.1016/S0306-4522(97)00592-7
10.1016/S0092-8674(00)81796-1
10.1101/lm.5.3.231
/ Learn. & Mem. / The specific role of cGMP in hippocampal LTP. by Son (1998)10.1038/364147a0
10.1126/science.270.5236.593
10.1126/science.7678352
10.1016/0896-6273(93)90342-O
10.1038/341739a0
10.1016/0896-6273(93)90117-A
10.1016/S0092-8674(00)80896-X
10.1016/S0306-4522(97)84911-1
10.1523/JNEUROSCI.18-10-03589.1998
/ J. Neurosci. / Evidence for involvement of the cGMP-protein kinase G signaling system in the induction of long-term depression, but not long-term potentiation, in the dentate gyrus in vitro. (1998)10.1073/pnas.93.2.795
10.1073/pnas.94.26.14848
10.1126/science.8100368
10.1038/368635a0
Dates
Type | When |
---|---|
Created | 3 years, 9 months ago (Nov. 11, 2021, 8:53 a.m.) |
Deposited | 3 years, 9 months ago (Nov. 11, 2021, 8:54 a.m.) |
Indexed | 11 months, 3 weeks ago (Sept. 11, 2024, 12:42 a.m.) |
Issued | 26 years, 10 months ago (Nov. 1, 1998) |
Published | 26 years, 10 months ago (Nov. 1, 1998) |
Published Online | 26 years, 10 months ago (Nov. 1, 1998) |
Published Print | 26 years, 10 months ago (Nov. 1, 1998) |
@article{Zhuo_1998, title={On the Respective Roles of Nitric Oxide and Carbon Monoxide in Long-Term Potentiation in the Hippocampus}, volume={5}, ISSN={1549-5485}, url={http://dx.doi.org/10.1101/lm.5.6.467}, DOI={10.1101/lm.5.6.467}, number={6}, journal={Learning & Memory}, publisher={Cold Spring Harbor Laboratory}, author={Zhuo, Min and Laitinen, Jarmo T. and Li, Xiao-Ching and Hawkins, Robert D.}, year={1998}, month=nov, pages={467–480} }