Nitric oxide signaling contributes to late-phase LTP and CREB phosphorylation in the hippocampus

Journal of Neuroscience

Volumn 19, Issue 23, 1999, Pages 10250-10261

  Lu, Yun Fei ^a   Kandel, Eric R ^a,b,c   Hawkins, Robert D ^a,b  

^a Columbia University ^*  (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

cGMP dependent protein kinase; CREB; Guanylyl cyclase; Hippocampus; Long term potentiation; Nitric oxide

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GUANYLATE CYCLASE; NITRIC OXIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ENZYME ACTIVATION; HIPPOCAMPUS; IMMUNOFLUORESCENCE; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RNA SYNTHESIS; SIGNAL TRANSDUCTION;

EID: 0033493229     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-23-10250.1999     Document Type: Article

References (74)

1. Abel T, Nguyen PV, Barad M, Deuel TAS, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626.
2. 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.
3. 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.
4. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is regulated for mammalian associative learning. Nat Neurosci 1:602-609.
5. 2+ and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
6. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
7. Blitzer RD, Wong T, Nouranifar R, Iyengar R Landau EM (1995) Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15:1403-1414.
8. Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S, Iyengar R, Landau EM (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280:1940-1943.
9. Bohme 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.
10. Bonhoeffer T, Staiger V, Aertsen A (1989) Synaptic plasticity in rat hippocampal slice cultures: local "Hebbian" conjunction of pre- and postsynaptic stimulation leads to distributed synaptic enhancement. Proc Natl Acad Sci USA 86:8113-8117.
11. Boulton CL, Southam E, Garthwaite J (1995) Nitric-oxide dependent long-term potentiation is blocked by inhibitors of soluble guanylyl cyclase. Neuroscience 69:699-703.
12. Bourtchouladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59-68.
13. Bradley T, Zhang Y, Bakin R, Lester HA, Ronnett GV, Zin K (1997) Functional expression of the heteromeric "olfactory" cyclic nucleotidegated channel in the hippocampus: a potential effector of synaptic plasticity in brain neurons. J Neurosci 17:1993-2005.
14. Bredt DS, Snyder SH (1992) Nitric oxide, a novel neuronal messenger. Neuron 8:3-11.
15. Butt E, Nolte C, Schulz S, Beltman J, Beavo JA, Jastorff B, Walter U (1992) Analysis of the functional role of cGM P-dependent protein kinase in intact human platelets using a specific activator 8-parachlorophenylthio-cGMP. Biochem Pharmacol 43:2591-2600.
16. Chetkovich DM, Klann E, Sweatt JD (1993) Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus. NeuroReport 4:919-922.
17. Colbran JL, Roach PJ, Fiol CJ, Dixon JE, Andrisani OM, Corbin JD (1992) cAMP-dependent protein kinase, but not the cGMP-dependent enzyme, rapidly phosphorylates Δ-CREB, and a synthetic Δ-CREB peptide. Biochem Cell Biol 70:1277-1282.
18. Davis HP, Squire LR (1984) Protein synthesis and memory: a review. Psychol Bull 96:518-559.
19. Deisseroth K, Bito H, Tsien RW (1996) Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16:89-101.
20. Deisseroth K, Heist EK, Tsien RW (1998) Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392:198-202.
21. Ding JM, Faiman LE, Hurst WJ, Kuriashkina LR, Gillette MU (1997) Resetting the biological clock: mediation of nocturnal CREB phosphorylation via light, glutamate, and nitric oxide. J Neurosci 17:667-675.
22. East SJ, Garthwaite J (1991) NMDA receptor activation in rat hippocampus induces cyclic GMP formation through the L-arginine-nitric oxide pathway. Neurosci Lett 123:17-19.
23. English JD, Sweatt JD (1997) A requiremert for the mitogen-activated protein kinase cascade in hippocampal long-term potentiation. J Biol Chem 272:19103-19106.
24. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536.
25. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phase of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65.
26. Frey U, Krug M, Brodeman R, Reymann K, Matthies H (1989) Long-term potentiation induced in dendrites separated from rats CA1 pyramidal somata does not establish a late phase. Neurosci Lett 97:135-139.
27. Frey U, Huang Y-Y, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
28. 2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365:456-459.
29. Garthwaite J, Southam E, Boulton CL, Nielson EB, Schmidt K, Mayer B (1995) Potent and selective inhibition of nitric oxide sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3α]quinoxalin-1-one. Mol Pharmacol 48:184-188.
30. Gass P, Wolter DP, Balschun D, Rudolph D, Frey U, Lipp H-P, Schutz G (1998) Deficits in memory tasks of mice with CREB mutations depend on gene dosage. Learn Mem 5:274-288.
31. Geahlen RL, Krebs EG (1980) Regulatory subunit of the type 1 cAMP-dependent protein kinase as an inhibitor and substrate of the cGMP-dependent protein kinase. J Biol Chem 255:1164-1169.
32. Geahlen RL, Allen SM, Krebs EG (1981) Effect of phosphorylation on the regulatory subunit of the type 1 cAMP-dependent protein kinase. J Biol Chem 256:4536-4540.
33. Geiger J, Nolte C, Butt E, Sage SO, Walter U (1992) Role of cGMP and cGMP-dependent protein kinase in nitrovasodilator inhibition of agonist-evoked calcium elevation in human platelets. Proc Natl Acad Sci USA 89:1031-1035.
34. Ginty DD, Kornhauser JM, Thompson MA, Bading H, Mayo KE, Takahashi JS, Greenberg ME (1993) Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260:238-241.
35. Gribkoff VK, Lum-Ragan JT (1992) Evidence for nitric oxide synthase inhibitor-sensitive and insensitive hippocampal synaptic potentiation. J Neurophysiol 68:639-642.
36. Gudi T, Huvar I, Meinecke M, Lohmann SM, Boss GR, Pilz RB (1996) Regulation of gene expression by cGMP-dependent protein kinase. J Biol Chem 271:4597-4600.
37. Gudi T, Lohmann SM, Pilz RB (1997) Regulation of gene expression by cyclic GMP-dependent protein kinase requires nuclear translocation of the kinase: identification of a nuclear localization signal. Mol Cell Biol 17:5244-5254.
38. Haby C, Lisovoski F, Aunis D, Zwiller J (1994) Stimulation of the cyclic GMP pathway by NO induces expression of the immediate early genes c-fos and junB in PC12 cells. J Neurochem 62:496-501.
39. Haley JE, Malen PL, Chapman PF (1993) Nitric oxide synthase inhibitors block long-term potentiation induced by weak but not strong tetanic stimulation at physiological brain temperatures in rat hippocampal slices. Neurosci Lett 160:85-88.
40. Harvey J, Collingridge GL (1992) Thapsigargin blocks the induction of long-term potentiation in rat hippocampal slices. Neurosci Lett 139:197-200.
41. Hawkins RD (1996) NO honey, I don't remember. Neuron 16:465-467.
42. Hawkins RD, Kandel ER, Siegelbaum SA (1993) Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu Rev Neurosci 16:625-665.
43. Hawkins RD, Son H, Arancio O (1998) Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118:155-172.
44. Huang Y-Y, Kandel ER (1994) Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1:74-82.
45. Huang Y-Y, Nguyen PV, Abel T, Kandel ER (1996) Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learn Mem 3:74-85.
46. Impey S, Mark M, Villacres EC, Poser S, Chavkin C, Storm DR (1996) Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973-982.
47. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
48. Kandel ER (1989) Genes, nerve cells, and the remembrance of things past. J Neuropsychiatry Clin Neurosci 1:103-125.
49. Kang H, Schuman ER (1996) A requirement of local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1042-1046.
50. Kantor DB, Lanzrein J, 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.
51. Kingston PA, Zufall F, Barnstable CT (1996) Rat hippocampal neurons express genes for both rod retinal and olfactory cyclic nucleotide-gated channels: novel targets for cAMP/cGMP function. Proc Natl Acad Sci USA 93:10440-10445.
52. Kleppisch T, Pfeifer A, Klatt P, Ruth P, Montkowski A, Fassler R, Hofmann F (1999) Long-term potentiation in the hippocampal CA1 region of mice lacking cGMP-dependent kinases is normal and susceptible to inhibition of nitric oxide synthase. J Neurosci 19:48-55.
53. Lee HC (1993) Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J Biol Chem 268:293-299.
54. Malen P, Chapman PF (1997) Nitric oxide facilitates long-term potentiation, but not long-term depression. J Neurosci 17:2645-2651.
55. Martin KC, Casadio A, Zhu H, E Y, Rose J, Chen M, Bailey CH, Kandel ER (1997a) Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927-938.
56. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997b) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912.
57. Matthies H, Schulz S, Thiemann W, Siemer H, Schmidt H, Krug M, Holt V (1997) Design of a multiple slice interface chamber and application for resolving the temporal pattern of CREB phosphorylation in hippocampal long-term potentiation. J Neurosci Methods 78:173-179.
58. Michael D, Martin KC, Seger R, Ning MM, Baston R, Kandel ER (1998) Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia. Proc Natl Acad Sci USA 95:1864-1869.
59. Nguyen PV, Kandel ER (1997) Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 4:230-243.
60. Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104-1107.
61. O'Dell TJ, Huang PL, Dawson TM, Dinerman JL, Snyder SH, Kandel ER, Fishman MC (1994) Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science 265:542-546.
62. Ohki K, Yoshida K, Hagiwara M, Harada T, Takamura M, Ohashi T, Matsuda H, Imaki J (1995) Nitric oxide induces c-fos gene expression via cyclic AMP response element binding protein (CREB) phosphorylation in rat retinal pigment epithelium. Brain Res 696:140-144.
63. Peunova N, Enlkolopov G (1993) Amplification of calcium-induced gene transcription by nitric oxide in neuronal cells. Nature 364:450-453.
64. Repaske DR, Corbin JG, Conti M, Goy MF (1993) A cyclic GMP-stimulated cyclic nucleotide phosphodiesterase gene is highly expressed in the limbic system of the rat brain. Neuroscience 56:673-686.
65. Schuman EM, Madison DV (1994) Locally distributed synaptic potentiation in the hippocampus. Science 263:532-536.
66. Sekhar KR, Hatchett RJ, Shabb JB, Wolfe L, Francis SH, Wells JN, Jastorff B, Butt E, Chakinala MM, Corbin JD (1992) Relaxation of pig coronary arteries by new and potent cGMP analogs that selectively activate type I alpha, compared with type I beta, cGMP-dependent protein kinase. Mol Pharmacol 42:103-108.
67. Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER (1996) Long-term potentialion is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87:1015-1023.
68. Son H, Lu Y-F, Zhuo M, Arancio O, Kandel ER, Hawkins RD (1998) The specific role of cGMP in hippocampal LTP. Learn Mem 5:231-245.
69. Wang Y, Wu J, Rowan MJ, Anwyl R (1996) Ryanodine produces a low frequency stimulation-induced NMDA receptor-independent long-term potentiation in the rat dentate gyrus in vitro. J Physiol (Lond) 495:755-767.
70. Wexler EM, Stanton PK, Nawy S (1998) Nitric oxide depresses GABAA receptor function via coactivation of cGMP-dependent kinase and phosphodiesterase. J Neurosci 18:2342-2349.
71. Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER (1998) Genetic and pharmacological evidence of a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell 92:25-37.
72. 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.
73. Zhuo M, Hu Y, Schultz C, Kandel ER, Hawkins RD (1994) Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 368:635-639.
74. Zhuo M, Laitinen JT, Li X-C, Hawkins RD (1998) On the respective roles of nitric oxide and carbon monoxide in long-term potentiation in the hippocampus. Learn Mem 5:467-480.