Acute stress impairs hippocampal mossy fiber-CA3 long-term potentiation by enhancing cAMP-specific phosphodiesterase 4 activity

Neuropsychopharmacology

Volumn 35, Issue 7, 2010, Pages 1605-1617

  Chen, Chien Chung ^a   Yang, Chih Hao ^a   Huang, Chiung Chun ^a   Hsu, Kuei Sen ^a,b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Adenosine; CAMP; Long term potentiation; Mossy fiber; Phosphodiesterase; Stress

Indexed keywords

3 ISOBUTYLXANTHINE; 4 (3 BUTOXY 4 METHOXYPHENYL)METHYL 2 IMIDAZOLIDONE; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE; ADENOSINE A1 RECEPTOR; CYCLIC AMP; FORSKOLIN; MIFEPRISTONE; PHOSPHODIESTERASE IV; PHOSPHODIESTERASE IV INHIBITOR; UNCLASSIFIED DRUG;

ADRENALECTOMY; ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL STRESS; ENZYME ACTIVITY; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SYNAPTIC TRANSMISSION;

4-(3-BUTOXY-4-METHOXYBENZYL)-2-IMIDAZOLIDINONE; ADRENALECTOMY; ALDOSTERONE ANTAGONISTS; ANIMALS; ANTI-INFLAMMATORY AGENTS; BIOPHYSICAL PHENOMENA; CORTICOSTERONE; CYCLIC AMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FORSKOLIN; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; MOSSY FIBERS, HIPPOCAMPAL; PHOSPHODIESTERASE INHIBITORS; SPIRONOLACTONE; STRESS, PSYCHOLOGICAL; SYNAPTOSOMES; XANTHINES;

EID: 77952415052     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.33     Document Type: Article

References (72)

1. Ahmed T, Frey JU, Korz V (2006). Long-term effects of brief acute stress on cellular signaling and hippocampal LTP. J Neurosci 26: 3951-3958.
2. Alzheimer C, Röhrenbeck J, ten Bruggencate G (1991). Adenosine depresses induction of LTP at the mossy fiber-CA3 synapse in vitro. Brain Res 543: 163-165.
3. Baillie GS, MacKenzie SJ, McPhee I, Houslay MD (2000). Subfamily selective actions in the ability of Erk2 MAP kinase to phosphorylate and regulate the activity of PDE4 cyclic AMP-specific phosphodiesterases. Br J Pharmacol 131: 811-819.
4. Bains JS, Longacher JM, Staley KJ (1999). Reciprocal interactions between CA3 network activity and strength of recurrent collateral synapses. Nat Neurosci 2: 720-726.
5. 3H]NECA in rat striatal membranes. Mol Pharmacol 29: 331-346.
6. Castillo PE, Janz R, Südhof TC, Tzounopoulos T, Malenka RC, Nicoll RA (1997). Rab3A is essential for mossy fibre long-term potentiation in the hippocampus. Nature 388: 590-593.
7. Chen YL, Huang CC, Hsu KS (2001). Time-dependent reversal of long-term potentiation by low-frequency stimulation at the hippocampal mossy fiber-CA3 synapses. J Neurosci 21: 3705-3714.
8. Cherry JA, Davis RL (1999). Cyclic AMP phosphodiesterases are localized in regions of the mouse brain associated with reinforcement, movement, and affect. J Comp Neurol 407: 287-301.
9. Coffin VL, Spealman RD (1989). Psychomotor-stimulant effects of 3-isobutyl-1-methylxanthine: comparison with caffeine and 7-(2-chloroethyl) theophylline. Eur J Pharmacol 170: 35-40.
10. Diamond DM, Bennett MC, Fleshner M, Rose GM (1992). Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2: 421-430.
11. Diamond DM, Park CR, Campbell AM, Woodson JC (2004). Competitive interactions between endogenous LTD and LTP in the hippocampus underlie the storage of emotional memories and stress-induced amnesia. Hippocampus 15: 1006-1025.
12. Feder A, Nestler EJ, Charney DS (2009). Psychobiology and molecular genetics of resilience. Nat Rev Neurosci 10: 446-457.
13. Fredholm BB, Dunwiddie TV (1988). How does adenosine inhibit transmitter release? Trends Pharmacol Sci 9: 130-134.
14. Garcia R (2001). Stress, hippocampal plasticity, and spatial learning. Synapse 40: 180-183.
15. Griffith WH (1990). Voltage-clamp analysis of posttetanic potentiation of the mossy fiber to CA3 synapse in hippocampus. J Neurophysiol 63: 491-501.
16. Gruart A, Muñoz MD, Delgado-Garća JM (2006). Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 26: 1077-1087. (Pubitemid 43237039)
17. Gundlfinger A, Bischofberger J, Johenning FW, Torvinen M, Schmitz D, Breustedt J (2007). Adenosine modulates transmission at the hippocampal mossy fibre synapse via direct inhibition of presynaptic calcium channels. J Physiol 582: 263-277.
18. Harris EW, Cotman CW (1986). Long-term potentiation of guinea pig mossy fiber responses is not blocked by N-methyl D-aspartate antagonists. Neurosci Lett 70: 132-137.
19. Huang CC, Chen YL, Liang YC, Hsu KS (2002). Role for cAMP and protein phosphatase in the presynaptic expression of mouse hippocampal mossy fibre depotentiation. J Physiol 543: 767-778.
20. Huang CC, Yang CH, Hsu KS (2005). Do stress and long-term potentiation share the same molecular mechanisms? Mol Neurobiol 32: 223-235.
21. Huang YY, Li XC, Kandel ER (1994). cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79: 69-79.
22. Jackson EK, Ren J, Zacharia LC, Mi Z (2007). Characterization of renal ecto-phosphodiesterase. J Pharmacol Exp Ther 321: 810-815.
23. Jacobson L, Sapolsky R (1991). The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocorti-cal axis. Endocr Rev 12: 118-134.
24. Kavushansky A, Vouimba RM, Cohen H, Richter-Levin G (2006). Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs uncontrollable water stress. Hippocampus 16: 35-42.
25. Kawamura Y, Manita S, Nakamura T, Inoue M, Kudo Y, Miyakawa H (2004). Glutamate release increases during mossy-CA3 LTP but not during Schaffer-CA1 LTP. Eur J Neurosci 19: 1591-1600.
26. Kerr DS, Huggett AM, Abraham WC (1994). Modulation of hippocampal long-term potentiation and long-term depression by corticosteroid receptor activation. Psychobiology 22: 123-133.
27. Kim JJ, Diamond DM (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3: 453-462.
28. Kim JJ, Foy MR, Thompson RF (1996). Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc Natl Acad Sci USA 93: 4750-4753.
29. Kim JJ, Yoon KS (1998). Stress: metaplastic effects in the hippocampus. Trends Neurosci 21: 505-509.
30. Kim PJ, Cole MA, Kalman BA, Spencer RL (1998). Evaluation of RU28318 and RU40555 as selective mineralocorticoid receptor and glucocorticoid receptor antagonists, respectively: receptor measures and functional studies. J Steroid Biochem Mol Biol 67: 213-222.
31. Korz V, Frey JU (2003). Stress-related modulation of hippocampal long-term potentiation in rats: involvement of adrenal steroid receptors. J Neurosci 23: 7281-7287.
32. Korz V, Frey JU (2005). Bidirectional modulation of hippocampal long-term potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. J Neurosci 25: 7393-7400.
33. Kukley M, Schwan M, Fredholm BB, Dietrich D (2005). The role of extracellular adenosine in regulating mossy fiber synaptic plasticity. J Neurosci 25: 2832-2837.
34. Latini S, Pedata F (2001). Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J Neuro-chem 79: 463-484.
35. 1 adenosine receptors. Naunyn Schmiedebergs Arch Pharmacol 336: 204-210.
36. Lu KT, Gean PW (1999). Masking of forskolin-induced long-term potentiation by adenosine accumulation in area CA1 of the rat hippocampus. Neuroscience 88: 69-78.
37. MacKenzie SJ, Baillie GS, McPhee I, Bolger GB, Houslay MD (2000). ERK2 mitogen-activated protein kinase binding, phos-phorylation, and regulation of the PDE4D cAMP-specific phosphodiesterases. The involvement of COOH-terminal docking sites and NH2-terminal UCR regions. J Biol Chem 275: 16609-16617.
38. McEwen BS (1999). Stress and hippocampal plasticity. Annu Rev Neurosci 22: 105-122.
39. McEwen BS, Sapolsky RM (1995). Stress and cognitive function. Curr Opin Neurobiol 5: 205-216.
40. McPhee I, Cochran S, Houslay MD (2001). The novel long PDE4A10 cyclic AMP phosphodiesterase shows a pattern of expression within brain that is distinct from the long PDE4A5 and short PDE4A1 isoforms. Cell Signal 13: 911-918.
41. Moore KA, Nicoll RA, Schmitz D (2003). Adenosine gates synaptic plasticity at hippocampal mossy fiber synapses. Proc Natl Acad Sci USA 100: 14397-14402.
42. Mitsuno K, Sasa M, Ishihara K, Ishikawa M, Kikuchi H (1994). LTP of mossy fiber-stimulated potentials in CA3 during learning in rats. Physiol Behav 55: 633-638.
43. Nicoll RA, Malenka RC (1995). Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377: 115-118.
44. Nicoll RA, Schmitz D (2005). Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6: 863-876.
45. Ortiz J, Harris HW, Guitart X, Terwilliger RZ, Haycock JW, Nestler EJ (1995). Extracellular signal-regulated protein kinases (ERKs) and ERK kinase (MEK) in brain: regional distribution and regulation by chronic morphine. J Neurosci 15: 1285-1297.
46. Otto C, Kovalchuk Y, Wolfer DP, Gass P, Martin M, Zuschratter W et al (2001). Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J Neurosci 21: 5520-5527.
47. Pavlides C, Nivón LG, McEwen BS (2002). Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12: 245-257.
48. Pavlides C, Watanabe Y, McEwen BS (1993). Effects of glucocorti-coids on hippocampal long-term potentiation. Hippocampus 3: 183-192.
49. Reid CA, Dixon DB, Takahashi M, Bliss TV, Fine A (2004). Optical quantal analysis indicates that long-term potentiation at single hippocampal mossy fiber synapses is expressed through increased release probability, recruitment of new release sites, and activation of silent synapses. J Neurosci 24: 3618-3626.
50. Roozendaal B, McEwen BS, Chattarji S (2009). Stress, memory and the amygdala. Nat Rev Neurosci 10: 423-433.
51. Saal D, Dong Y, Bonci A, Malenka RC (2003). Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37: 577-582.
52. Salin PA, Scanziani M, Malenka RC, Nicoll RA (1996). Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci USA 93: 13304-13309.
53. Seligman ME, Maier SF (1967). Failure to escape traumatic shock. J Exp Psychol 74: 1-9.
54. Shen CP, Tsimberg Y, Salvadore C, Meller E (2004). Activation of ERK and JNK MAPK pathways by acute swim stress in rat brain regions. BMC Neurosci 5: 36.
55. Shors TJ, Dryver E (1994). Effect of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus. Brain Res 666: 232-238.
56. Shors TJ, Foy MR, Levine S, Thompson RF (1989). Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus. Brain Res Bull 24: 663-667.
57. Südhof TC (2004). The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547.
58. Takeda A, Ando M, Kanno S, Oku N (2009). Unique response of zinc in the hippocampus to behavioral stress and attenuation of subsequent mossy fiber long-term potentiation. Neurotoxicology 30: 712-717.
59. Tzounopoulos T, Janz R, Südhof TC, Nicoll RA, Malenka RC (1998). A role for cAMP in long-term depression at hippocampal mossy fiber synapses. Neuron 21: 837-845.
60. Vecsey CG, Baillie GS, Jaganath D, Havekes R, Daniels A, Wimmer M et al (2009). Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461: 1122-1125.
61. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA (1994). Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265: 1878-1882.
62. Weisskopf MG, Nicoll RA (1995). Presynaptic changes during mossy fibre LTP revealed by NMDA receptor-mediated synaptic responses. Nature 376: 256-259.
63. Wu ZL, Thomas SA, Villacres EC, Xia Z, Simmons ML, Chavkin C et al (1995). Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proc Natl Acad Sci USA 92: 220-224.
64. Xu L, Anwyl R, Rowan MJ (1997). Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387: 497-500.
65. Yang CH, Huang CC, Hsu KS (2004). Behavioral stress modifies hippocampal synaptic plasticity through corticosterone-induced sustained extracellular signal-regulated kinase/mitogen-acti-vated protein kinase activation. J Neurosci 24: 11029-11034.
66. Yang CH, Huang CC, Hsu KS (2005). Behavioral stress enhances hippocampal CA1 long-term depression through the blockade of the glutamate uptake. J Neurosci 25: 4288-4293.
67. Yang CH, Huang CC, Hsu KS (2006). Novelty exploration elicits a reversal of acute stress-induced modulation of hippocampal synaptic plasticity in the rat. J Physiol 577: 601-615.
68. Yang PC, Yang CH, Huang CC, Hsu KS (2008). Phosphatidylinositol 3-kinase activation is required for stress protocol-induced modification of hippocampal synaptic plasticity. J Biol Chem 283: 2631-2643.
69. Yuen EY, Liu W, Karatsoreos IN, Feng J, McEwen BS, Yan Z (2009). Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proc Natl Acad Sci USA 106: 14075-14079.
70. Zalutsky RA, Nicoll RA (1990). Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248: 1619-1624.
71. Zucker RS (1989). Short-term synaptic plasticity. Annu Rev Neurosci 12: 13-31.
72. Zucker RS, Regehr WG (2002). Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.