Long-term potentiation in the hippocampal CA1 region of mice lacking cGMP-dependent kinases is normal and susceptible to inhibition of nitric oxide synthase

Journal of Neuroscience

Volumn 19, Issue 1, 1999, Pages 48-55

  Kleppisch, Thomas ^a,d   Pfeifer, Alexander ^a   Klatt, Peter ^a   Ruth, Peter ^a   Montkowski, Alexandra ^b   Fässler, Reinhard ^c   Hofmann, Franz ^a  

^a Inst fur Pharmakologie Toxikologie   (Germany)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^c LUND UNIVERSITY HOSPITAL   (Sweden)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

cGMP dependent kinase; Gene targeting; Hippocampus; Mouse; Nitric oxide; Synaptic plasticity

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 8 (4 CHLOROPHENYLTHIO) CYCLIC AMP; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; GUANYLATE CYCLASE; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; GENE TARGETING; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION;

EID: 0032906585     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-01-00048.1999     Document Type: Article

References (37)

1. Arancio O, Kandel ER, Hawkins RD (1995) Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic GMP in cultured hippocampal neurons. Nature 376:74-80.
2. Arancio O, Kiebler M, Lee CJ, Lev-Ram V, Tsien RY, Kandel ER, Hawkins RD (1996) Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87:1025-1035.
3. Bliss TVP, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
4. Böhme GA, Bon C, Stutzmann JM, Doble A, Blanchard JC (1991) Possible involvement of nitric oxide in long-term potentiation. Eur J Pharmacol 199:379-381.
5. Bolshakov VY, Siegelbaum SA (1995) Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269:1730-1734.
6. Boulton CL, Southam E, Garthwaite J (1995) Nitric oxide-dependent long-term potentiation is blocked by a specific inhibitor of soluble guanylyl cyclase. Neuroscience 69:699-703.
7. 2+ channel. Neuron 18:951-958.
8. Chetkovich DM, Klann E, Sweatt JD (1993) Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus. NeuroReport 4:919-922.
9. Duman RS, Terwillinger RZ, Nestler EJ (1993) Alteration in nitric oxide-stimulated endogenous ADP-ribosylation associated with long-term potentiation in rat hippocampus. J Neurochem 61:1542-1545.
10. Ecker T, Gobel C, Hullin R, Rettig R, Seitz G, Hofmann F (1989) Decreased cardiac concentration of cGM P kinase in hypertensive animals. An index for cardiac vascularization? Circ Res 65:1361-1369.
11. El-Din El-Husseini A, Bladen C, Vincent SR (1995) Molecular characterization of type II cyclic GMP-dependent protein kinase expressed in the rat brain. J Neurochem 64:2314-2817.
12. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B (1995) Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol 48:184-188.
13. Haley JE, Wilcox GL, Chapman PF (1992) The role of nitric oxide in hippocampal long-term potentiation. Neuron 8:211-216.
14. Jarchau T, Häusler C, Markert T, Pöhler D, Vandekekerckhove J, De Jonge HR, Lohmann SM, Walter U (1994) Cloning, expression, and in situ localization of rat intestinal cGM P-dependent protein kinase II. Proc Natl Acad Sci USA 91:9426-9430.
15. Kantor DB, Lanzrein M, Stary SJ, Sandoval GM, Smith WB, Sullivan BM, Davidson N, Schuman EM (1996) A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science 274:1744-1748.
16. Lum-Ragan JT, Gribkoff VK (1993) The sensitivity of hippocampal long-term potentiation to nitric oxide synthase inhibitors is dependent upon the pattern of conditioning stimulation. Neuroscience 57:973-983.
17. Malinow R (1991) Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. Science 252:722-724.
18. O'Dell TJ, Hawkins RD, Kandel ER, Arancio O (1991) Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc Natl Acad Sci USA 88:11285-11289.
19. 2+ entry via spatially activated NMDA receptors in the induction of long-term potentiation. Neuron 11:817-823.
20. Pfeifer A, Aszodi A, Seidler U, Ruth P, Hofmann F, Fässler R (1996) Intestinal secretory defects and dwarfism in mice lacking cGMP-dependent protein kinase II. Science 274:2082-2086.
21. Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, Hirneiß C, Wang G-X, Korth M, Aszódi A, Andersson K-E, Krombach F, Mayerhofer A, Ruth P, Hofmann F, Fässler R (1998) Defective smooth muscle regulation in cGMP Kinase I-deficient mice. EMBO J 17:3045-3052.
22. Rankin PW, Jacobson EL, Benjamin RC, Moss J, Jacobson MK (1989) Quantitative studies of inhibitors of ADP-ribosylation in vitro and in vivo. J Biol Chem 264:4312-4317.
23. Ruth P, Landgraf W, Keilbach A, May B, Egléme C, Hofmann F (1991) The activation of cGM P-dependent protein kinase isoenzymes Iα and Iβ is determined by the different amino termini. Eur J Biochem 202:1339-1344.
24. Schuman EM, Madison DV (1991) A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254:1503-1506.
25. Schuman EM, Meffert MK, Schulman H, Madison DV (1994) An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation. Proc Natl Acad Sci USA 91:11958-11962.
26. Selig DK, Segal MR, Liao D, Malenka RC, Malinow R, Nicoll RA, Lisman JE (1996) Examination of the role of cGMP in long-term potentiation in the CA1 region of the hippocampus. Learn Mem 3:42-48.
27. Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER (1996) Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87:1015-1023.
28. Sullivan BM, Wong S, Schuman EM (1997) Modification of hippocampal synaptic proteins by nitric oxide-stimulated ADP ribosylation. Learn Mem 3:414-424.
29. Tsien JZ, Huerta PT, Tonegawa S (1996) The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial learning. Cell 87:1327-1338.
30. Uhler MD (1993) Cloning and expression of a novel cyclic GMP-dependent protein kinase from mouse brain. J Biol Chem 268:13586-13591.
31. Wernet W, Flockerzi V, Hofmann F (1989) The cDNA of the two isoforms of bovine cGM P-dependent protein kinase. FEBS Lett 251:191-196.
32. Williams JH, Li X, Gu X, Jope RS (1992) Modulation of endogenous ADP-ribosylation in rat brain. Brain Res 592:49-56.
33. Williams JH, Li YG, Nayak A, Errington ML, Murphy KPSJ, Bliss TVP (1993) The suppression of long-term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent. Neuron 11:877-884.
34. Wilson RI, Yanovsky J, Gödecke A, Stevens DR, Schrader J, Haas HL (1997) Endothelial nitric oxide synthase and LTP. Nature 386:338.
35. Xu L, Eu JP, Meissner G, Stamler JS (1998) Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Nature 279:234-237.
36. Zhuo M, Small SA, Kandel ER, Hawkins RD (1993) Nitric oxide and carbon monoxide produce activity dependent long-term synaptic enhancement in hippocampus. Science 260:1946-1950.
37. Zhuo M, Hu Y, Schultz C, Kandel ER, Hawkins RD (1994) Role of guanylyl cyclase and cGM P-dependent protein kinase in long-term potentiation. Nature 368:635-639.