DOI: 10.1152/jn.1999.82.3.1569. Induction of Hippocampal LTD Requires Nitric-Oxide-Stimulated PKG Activity and Ca<sup>2+</sup>Release From Cyclic ADP-Ribose-Sensitive Stores

Induction of Hippocampal LTD Requires Nitric-Oxide-Stimulated PKG Activity and Ca2+Release From Cyclic ADP-Ribose-Sensitive Stores

10.1152/jn.1999.82.3.1569

Crossref journal-article

American Physiological Society

Journal of Neurophysiology (24)

Abstract

Long-term depression (LTD) of synaptic transmission can be induced by several mechanisms, one thought to involve Ca2+-dependent activation of postsynaptic nitric oxide (NO) synthase and subsequent diffusion of NO to the presynaptic terminal. We used the stable NO donor S-nitroso- N-acetylpenicillamine (SNAP) to study the NO-dependent form of LTD at Schaffer collateral-CA1 synapses in vitro. SNAP (100 μM) enhanced the induction of LTD via a cascade that was blocked by the N-methyl-d-aspartate receptor antagonist d-2-amino-5-phosphonopentanoic acid (50 μM), NO guanylyl cyclase inhibitor 1H-[1,2,4] oxadiazolo [4,3-a] quinoxalin-1-one (10 μM), and the PKG inhibitor KT5823 (1 μM). We further show that LTD induced by low-frequency stimulation in the absence of SNAP also is blocked by KT5823 or Rp-8-(4-chlorophenylthio)-guanosine 3′,5′-cyclic monophosphorothioate (10 μM), cyclic guanosine 3′,5′ monophosphate-dependent protein kinase (PKG) inhibitors with different mechanisms of action. Furthermore SNAP-facilitated LTD was blocked when release from intracellular calcium stores was inhibited by ryanodine (10 μM). Finally, two cell-permeant antagonists of the cyclic ADP-ribose binding site on ryanodine receptors also were able to block the induction of LTD. These results support a cascade for induction of homosynaptic, NO-dependent LTD involving activation of guanylyl cyclase, production of guanosine 3′,5′ cyclic monophosphate and subsequent PKG activation. This process has an additional requirement for release of Ca2+from ryanodine-sensitive stores, perhaps dependent on the second-messenger cyclic ADP ribose.

Bibliography

Reyes-Harde, M., Potter, B. V. L., Galione, A., & Stanton, P. K. (1999). Induction of Hippocampal LTD Requires Nitric-Oxide-Stimulated PKG Activity and Ca2+Release From Cyclic ADP-Ribose-Sensitive Stores. Journal of Neurophysiology, 82(3), 1569â1576.

Authors 4

Magali Reyes-Harde (first)
Barry V. L. Potter (additional)
Antony Galione (additional)
Patric K. Stanton (additional)

References 45 Referenced 88

10.1146/annurev.ne.19.030196.002253
10.1126/science.7909958
10.1016/0028-3908(95)00127-R
10.1111/j.1460-9568.1994.tb00543.x
10.1073/pnas.86.22.9030
10.1016/0896-6273(92)90104-L
10.1016/0922-4106(94)90095-7
10.1091/mbc.3.12.1415
10.1152/ajpcell.1996.271.4.C1007
10.1073/pnas.89.10.4363
10.1002/(SICI)1098-1063(1997)7:3<286::AID-HIPO4>3.0.CO;2-J
10.1126/science.1909457
10.1038/365456a0
10.1016/S0021-9258(18)47339-5 / J. Biol. Chem. by Garbers D. L. (1994)
10.1111/j.1471-4159.1987.tb13123.x
10.1016/0922-4106(89)90023-0
10.1016/S0026-895X(25)10233-2 / Mol. Pharmcol. by Garthwaite J. (1995)
10.1074/jbc.270.5.2074
{'key': 'B19', 'first-page': '1131', 'volume': '4', 'author': 'Izumi Y.', 'year': '1993', 'journal-title': 'Neuroreport'} / Neuroreport by Izumi Y. (1993)
10.1002/(SICI)1096-9861(19960506)368:3<335::AID-CNE2>3.0.CO;2-6
10.1016/0006-291X(87)90293-2
{'key': 'B22', 'first-page': '23', 'volume': '3', 'author': 'Katsuki S.', 'year': '1977', 'journal-title': 'J. Cyclic Nucleic Res.'} / J. Cyclic Nucleic Res. by Katsuki S. (1977)
10.1016/S0021-9258(19)47328-6 / J. Biol. Chem. by Koshiyama H. (1991)
10.1038/370307a0
10.1016/S0021-9258(18)94230-4 / J. Biol. Chem. by Lee H. C. (1989)
10.1016/0922-4106(95)00084-4
10.2108/zsj.12.151
10.1016/0896-6273(92)90248-C
10.1126/science.271.5253.1294
10.1523/JNEUROSCI.16-19-05951.1996
10.1016/S0304-3940(98)00496-0
10.1523/JNEUROSCI.13-07-03051.1993
10.1074/jbc.272.26.16358
10.1016/S0014-2999(96)00937-5
10.1016/0028-3908(93)90021-T
10.1016/0014-2999(95)00022-D
10.1152/jn.1996.76.3.2097
10.1126/science.8420005
10.1038/25547
10.1016/0167-4889(93)90199-Y
10.1046/j.1471-4159.1995.65020595.x
10.1097/00001756-199305000-00034
10.1074/jbc.271.7.3699
10.1146/annurev.pa.35.040195.001241
10.1097/00001756-199405000-00004

Dates

Type	When
Created	7 years, 8 months ago (Dec. 25, 2017, 12:29 a.m.)
Deposited	2 months ago (June 29, 2025, 1:41 a.m.)
Indexed	2 months ago (June 29, 2025, 2:10 a.m.)
Issued	25 years, 11 months ago (Sept. 1, 1999)
Published	25 years, 11 months ago (Sept. 1, 1999)
Published Print	25 years, 11 months ago (Sept. 1, 1999)

Funders 0

None

BibTeX

@article{Reyes_Harde_1999, title={Induction of Hippocampal LTD Requires Nitric-Oxide-Stimulated PKG Activity and Ca2+Release From Cyclic ADP-Ribose-Sensitive Stores}, volume={82}, ISSN={1522-1598}, url={http://dx.doi.org/10.1152/jn.1999.82.3.1569}, DOI={10.1152/jn.1999.82.3.1569}, number={3}, journal={Journal of Neurophysiology}, publisher={American Physiological Society}, author={Reyes-Harde, Magali and Potter, Barry V. L. and Galione, Antony and Stanton, Patric K.}, year={1999}, month=sep, pages={1569–1576} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        29
      ]
    ],
    "date-time": "2025-06-29T06:10:09Z",
    "timestamp": 1751177409431,
    "version": "3.41.0"
  },
  "reference-count": 45,
  "publisher": "American Physiological Society",
  "issue": "3",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1999,
        9,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Long-term depression (LTD) of synaptic transmission can be induced by several mechanisms, one thought to involve Ca<jats:sup>2+</jats:sup>-dependent activation of postsynaptic nitric oxide (NO) synthase and subsequent diffusion of NO to the presynaptic terminal. We used the stable NO donor S-nitroso- N-acetylpenicillamine (SNAP) to study the NO-dependent form of LTD at Schaffer collateral-CA1 synapses in vitro. SNAP (100 \u03bcM) enhanced the induction of LTD via a cascade that was blocked by the N-methyl-d-aspartate receptor antagonist d-2-amino-5-phosphonopentanoic acid (50 \u03bcM), NO guanylyl cyclase inhibitor 1H-[1,2,4] oxadiazolo [4,3-a] quinoxalin-1-one (10 \u03bcM), and the PKG inhibitor KT5823 (1 \u03bcM). We further show that LTD induced by low-frequency stimulation in the absence of SNAP also is blocked by KT5823 or Rp-8-(4-chlorophenylthio)-guanosine 3\u2032,5\u2032-cyclic monophosphorothioate (10 \u03bcM), cyclic guanosine 3\u2032,5\u2032 monophosphate-dependent protein kinase (PKG) inhibitors with different mechanisms of action. Furthermore SNAP-facilitated LTD was blocked when release from intracellular calcium stores was inhibited by ryanodine (10 \u03bcM). Finally, two cell-permeant antagonists of the cyclic ADP-ribose binding site on ryanodine receptors also were able to block the induction of LTD. These results support a cascade for induction of homosynaptic, NO-dependent LTD involving activation of guanylyl cyclase, production of guanosine 3\u2032,5\u2032 cyclic monophosphate and subsequent PKG activation. This process has an additional requirement for release of Ca<jats:sup>2+</jats:sup>from ryanodine-sensitive stores, perhaps dependent on the second-messenger cyclic ADP ribose.</jats:p>",
  "DOI": "10.1152/jn.1999.82.3.1569",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2017,
        12,
        25
      ]
    ],
    "date-time": "2017-12-25T05:29:51Z",
    "timestamp": 1514179791000
  },
  "page": "1569-1576",
  "source": "Crossref",
  "is-referenced-by-count": 88,
  "title": "Induction of Hippocampal LTD Requires Nitric-Oxide-Stimulated PKG Activity and Ca<sup>2+</sup>Release From Cyclic ADP-Ribose-Sensitive Stores",
  "prefix": "10.1152",
  "volume": "82",
  "author": [
    {
      "given": "Magali",
      "family": "Reyes-Harde",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Departments of Neuroscience and Neurology, Albert Einstein College of Medicine, Bronx, New York 10461;"
        }
      ]
    },
    {
      "given": "Barry V. L.",
      "family": "Potter",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Medicinal Chemistry, School of Pharmacy and Pharmacology, University of Bath, Bath BA2 7AY; and"
        }
      ]
    },
    {
      "given": "Antony",
      "family": "Galione",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "University Department of Pharmacology, Oxford University, Oxford OX1 3QT, United Kingdom"
        }
      ]
    },
    {
      "given": "Patric K.",
      "family": "Stanton",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Departments of Neuroscience and Neurology, Albert Einstein College of Medicine, Bronx, New York 10461;"
        }
      ]
    }
  ],
  "member": "24",
  "reference": [
    {
      "key": "B1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.ne.19.030196.002253"
    },
    {
      "key": "B2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7909958"
    },
    {
      "key": "B3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3908(95)00127-R"
    },
    {
      "key": "B4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1460-9568.1994.tb00543.x"
    },
    {
      "key": "B5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.22.9030"
    },
    {
      "key": "B6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(92)90104-L"
    },
    {
      "key": "B7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0922-4106(94)90095-7"
    },
    {
      "key": "B8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.3.12.1415"
    },
    {
      "key": "B9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.1996.271.4.C1007"
    },
    {
      "key": "B10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.10.4363"
    },
    {
      "key": "B11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1098-1063(1997)7:3<286::AID-HIPO4>3.0.CO;2-J"
    },
    {
      "key": "B12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1909457"
    },
    {
      "key": "B13",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/365456a0"
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "30741",
      "DOI": "10.1016/S0021-9258(18)47339-5",
      "volume": "269",
      "author": "Garbers D. L.",
      "year": "1994",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1987.tb13123.x"
    },
    {
      "key": "B16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0922-4106(89)90023-0"
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "184",
      "DOI": "10.1016/S0026-895X(25)10233-2",
      "volume": "48",
      "author": "Garthwaite J.",
      "year": "1995",
      "journal-title": "Mol. Pharmcol."
    },
    {
      "key": "B18",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.5.2074"
    },
    {
      "key": "B19",
      "first-page": "1131",
      "volume": "4",
      "author": "Izumi Y.",
      "year": "1993",
      "journal-title": "Neuroreport"
    },
    {
      "key": "B20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1096-9861(19960506)368:3<335::AID-CNE2>3.0.CO;2-6"
    },
    {
      "key": "B21",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(87)90293-2"
    },
    {
      "key": "B22",
      "first-page": "23",
      "volume": "3",
      "author": "Katsuki S.",
      "year": "1977",
      "journal-title": "J. Cyclic Nucleic Res."
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "16985",
      "DOI": "10.1016/S0021-9258(19)47328-6",
      "volume": "266",
      "author": "Koshiyama H.",
      "year": "1991",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/370307a0"
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "1608",
      "DOI": "10.1016/S0021-9258(18)94230-4",
      "volume": "264",
      "author": "Lee H. C.",
      "year": "1989",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0922-4106(95)00084-4"
    },
    {
      "key": "B27",
      "doi-asserted-by": "publisher",
      "DOI": "10.2108/zsj.12.151"
    },
    {
      "key": "B28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(92)90248-C"
    },
    {
      "key": "B29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.271.5253.1294"
    },
    {
      "key": "B30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.16-19-05951.1996"
    },
    {
      "key": "B31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0304-3940(98)00496-0"
    },
    {
      "key": "B32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.13-07-03051.1993"
    },
    {
      "key": "B33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.26.16358"
    },
    {
      "key": "B34",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0014-2999(96)00937-5"
    },
    {
      "key": "B35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3908(93)90021-T"
    },
    {
      "key": "B36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-2999(95)00022-D"
    },
    {
      "key": "B37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1996.76.3.2097"
    },
    {
      "key": "B38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8420005"
    },
    {
      "key": "B39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/25547"
    },
    {
      "key": "B40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0167-4889(93)90199-Y"
    },
    {
      "key": "B41",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1471-4159.1995.65020595.x"
    },
    {
      "key": "B42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00001756-199305000-00034"
    },
    {
      "key": "B43",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.7.3699"
    },
    {
      "key": "B44",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.pa.35.040195.001241"
    },
    {
      "key": "B45",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00001756-199405000-00004"
    }
  ],
  "container-title": "Journal of Neurophysiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.physiology.org/doi/pdf/10.1152/jn.1999.82.3.1569",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        6,
        29
      ]
    ],
    "date-time": "2025-06-29T05:41:42Z",
    "timestamp": 1751175702000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.physiology.org/doi/10.1152/jn.1999.82.3.1569"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        9,
        1
      ]
    ]
  },
  "references-count": 45,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          1999,
          9,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1152/jn.1999.82.3.1569"
  ],
  "URL": "http://dx.doi.org/10.1152/jn.1999.82.3.1569",
  "relation": {},
  "ISSN": [
    "0022-3077",
    "1522-1598"
  ],
  "subject": [],
  "container-title-short": "Journal of Neurophysiology",
  "published": {
    "date-parts": [
      [
        1999,
        9,
        1
      ]
    ]
  }
}