Mitogen-Activated Protein Kinase Signaling in the Hippocampus and Its Modulation by Corticotropin-Releasing Factor Receptor 2: A Possible Link between Stress and Fear Memory

Journal of Neuroscience

Volumn 23, Issue 36, 2003, Pages 11436-11443

  Sananbenesi, Farahnaz ^a   Fischer, André ^a   Schrick, Christina ^a   Spiess, Joachim ^a   Radulovic, Jelena ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

CRF receptor 2; Erk; Fear conditioning; Hippocampus; MAPK; PKA; Stress

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ANTISAUVAGINE 30; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR RECEPTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; P90 RIBOSOMAL S KINASE 1; PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEAR; GENE EXPRESSION REGULATION; IMMOBILIZATION STRESS; LEARNING; MALE; MEMORY; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; STRESS;

EID: 0347479232     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-36-11436.2003     Document Type: Article

References (54)

1. Abel T, Nguyen PV, Barad M, Deuel TA, 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. Athos J, Impey S, Pineda VV, Chen X, Storm DR (2002) Hippocampal CRE-mediated gene expression is required for contextual memory formation. Nat Neurosci 5:1119-1120.
3. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609.
4. Bapat S, Verkleij A, Post JA (2001) Peroxynitrite activates mitogen-activated protein kinase (MAPK) via a MEK-independent pathway: a role for protein kinase C. FEBS Lett 499:21-26.
5. Behan DP, Heinrichs SC, Troncoso JC, Liu XJ, Kawas CH, Ling N, De Souza EB (1995) Displacement of corticotropin releasing factor from its binding protein as a possible treatment for Alzheimer's disease. Nature 378:284-287.
6. Blank T, Nijholt I, Grammatopoulos DK, Randeva HS, Hillhouse EW, Spiess J (2003) Corticotropin-releasing factor receptors couple to multiple G-proteins to activate diverse intracellular signaling pathways in mouse hippocampus: role in neuronal excitability and associative learning. J Neurosci 23:700-707.
7. Cano E, Mahadevan L (1995) Parallel signal processing among mammalian MAPKs. Trends Biochem Sci 20:117-122.
8. Chen RH, Sarnecki C, Blenis J (1992) Nuclear localization and regulation of Erk- and Rsk-encoded protein kinases. Mol Cell Biol 12:915-927.
9. Choe ES, McGinty JF (2000) N-methyl-D-aspartate receptors and p38 mitogen-activated protein kinase are required for cAMP-dependent cyclase response element binding protein and EIk-1 phosphorylation in the striatum. Neuroscience 101:607-617.
10. Coste SC, Kesterson RA, Heldwein KA, Stevens SL, Heard AD, Hollis JH, Murray SE, Hill JK, Pantely GA, Hohimer AR, Hatton DC, Phillips TJ, Finn DA, Low MJ, Rittenberg MB, Stenzel P, Stenzel-Poore MP (2000) Abnormal adaptations to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nat Genet 24:403-409.
11. De Souza EB (1995) Corticotropin-releasing factor receptors: physiology, pharmacology, biochemistry and role in central nervous system and immune disorders. Psychoneuroendocrinology 20:789-819.
12. Eckart K, Jahn O, Radulovic J, Radulovic M, Blank T, Stiedl O, Brauns O, Tezval H, Zeyda T, Spiess J (2002) Pharmacology and biology of corticotropin-releasing factor (CRF) receptors. Receptors Channels 8:163-177.
13. Elliott-Hunt CR, Kazlauskaite J, Wilde GJ, Grammatopoulos DK, Hillhouse EW (2002) Potential signaling pathways underlying corticotrophin-releasing hormone-mediated neuroprotection from excitotoxicity in rat hippocampus. J Neurochem 80:416-425.
14. Fischer A, Sananbenesi F, Schrick C, Spiess J, Radulovic J (2002) Cyclin-dependent kinase 5 is required for associative learning. J Neurosci 22:3700-3707.
15. Fischer A, Sananbenesi F, Schrick C, Spiess J, Radulovic J (2003) Regulation of contextual fear conditioning by baseline and inducible septohippocampal cyclin-dependent kinase 5. Neuropharmacology 44:1089-1099.
16. Grammer TC, Blenis J (1997) Evidence for MEK-independent pathways regulating the prolonged activation of the ERK-MAP kinases. Oncogene 14:1635-1642.
17. Hammack SE, Schmid MJ, LoPresti ML, Der-Avakian A, Pellymounter MA, Foster AC, Watkins LR, Maier SF (2003) Corticotropin releasing hormone type 2 receptors in the dorsal raphe nucleus mediate the behavioral consequences of uncontrollable stress. J Neurosci 23:1019-1025.
18. Hsu SY, Hsueh AJW (2001) Human stresscopin and stresscopin-related peptide are selective ligands for the type 2 corticotropin-releasing hormone receptor. Nat Med 7:605-611.
19. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
20. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-1038.
21. Key M, Wirick B, Cool D, Morris M (2001) Quantitative in situ hybridization for peptide mRNAs in mouse brain. Brain Res Protoc 8:8-15.
22. Kinkl N, Sahel J, Hicks D (2001) Alternate FGF2-ERK1/2 signaling pathways in retinal photoreceptor and glial cells in vitro. J Biol Chem 276:43871-43878.
23. Kishimoto T, Radulovic J, Radulovic M, Lin CR, Schrick C, Hooshmand F, Hermanson O, Rosenfeld MG, Spiess J (2000) Deletion of crhr2 reveals an anxiolytic role for corticotropin-releasing hormone receptor-2. Nat Genet 24:415-419.
24. Lewis K, Li C, Perrin MH, Blount A, Kunitake K, Donaldson C, Vaughan J, Reyes TM, Gulyas J, Fischer W, Bilezikjian L, Rivier J, Sawchenko PE, Vale WW (2001) Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc Natl Acad Sci USA 98:7570-7575.
25. Lu L, Liu Z, Huang M, Zhang (2003) Dopamine-dependent responses to cocaine depend on corticotropin-releasing factor receptor subtypes. J Neurochem 84:1378-1386.
26. Martinez V, Wang L, Rivier JE, Vale W, Tache Y (2002) Differential actions of peripheral corticotropin-releasing factor (CRF), urocortin II, and urocortin III on gastric emptying and colonic transit in mice: role of CRF receptor subtypes 1 and 2. J Pharmacol Exp Ther 301:611-617.
27. Matynia A, Anagnostaras SG, Silva AJ (2001) Weaving the molecular and cognitive strands of memory. Neuron 32:557-559.
28. Milanovic S, Radulovic J, Laban O, Stiedl O, Henn F, Spiess J (1998) Production of the Fos protein after contextual fear conditioning of C57BL/6N mice. Brain Res 784:37-47.
29. Pawlak R, Magarinos AM, Melchor J, McEwen B, Strickland S (2003) Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior. Nat Neurosci 6:168-174.
30. Pedersen WA, Wan R, Zhang P, Mattson MP (2002) Urocortin, but not urocortin II, protects cultured hippocampal neurons from oxidative and excitotoxic cell death via corticotropin-releasing hormone receptor type I. J Neurosci 22:404-412.
31. Pelleymounter MA, Joppa M, Ling N, Foster AC (2002) Evidence supporting a role for central corticotropin-releasing factor(2) receptors in behavioral, but not endocrine, response to environmental stress. J Pharmacol Exp Ther 302:145-152.
32. Radulovic J, Kammermeier J, Spiess J (1998) Relationship between fos production and classical fear conditioning: effects of novelty, latent inhibition, and unconditioned stimulus preexposure. J Neurosci 18:7452-7461.
33. Radulovic J, Ruhmann A, Liepold T, Spiess J (1999) Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J Neurosci 19:5016-5025.
34. Radulovic J, Fischer A, Katerkamp U, Spiess J (2000) Role of regional neurotransmitter receptors in corticotropin-releasing factor (CRF)-mediated modulation of fear conditioning. Neuropharmacology 39:707-710.
35. Radulovic M, Hippel C, Spiess J (2003) Corticotropin-releasing factor (CRF) rapidly suppresses apoptosis by acting upstream of the activation of caspases. J Neurochem 84:1074-1085.
36. Reyes TM, Lewis K, Perrin MH, Kunitake KS, Vaughan J, Arias CA, Hogenesch JB, Gulyas J, Rivier J, Vale WW, Sawchenko PE (2001) Urocortin II: a member of the corticotropin-releasing factor (CRF) neuropeptide family that is selectively bound by type 2 CRF. Proc Natl Acad Sci USA 98:2843-2848.
37. Roberson ED, English JD, Adams JP, Selcher JC, Kondratick C, Sweatt JD (1999) The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19:4337-4348.
38. Roozendaal B, Brunson KL, Holloway BL, McGaugh JL, Baram TZ (2002) Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc Natl Acad Sci USA 99:13908-13913.
39. Rossant CJ, Pinnock RD, Hughes J, Hall MD, McNulty S (1999) Corticotropin-releasing factor type 1 and type 2alpha receptors regulate phosphorylation of calcium/cyclic adenosine 3′,5′-monophosphate response element-binding protein and activation of p42/p44 mitogen-activated protein kinase. Endocrinology 140:1525-1536.
40. Ruhmann A, Bonk I, Lin CR, Rosenfeld MG, Spiess J (1998) Structural requirements for peptidic antagonists of the corticotropin-releasing factor receptor (CRFR): development of CRFR2beta-selective antisauvagine-30. Proc Natl Acad Sci USA 95:15264-15269.
41. Sananbenesi F, Fischer A, Schrick C, Spiess J, Radulovic J (2002) Phosphorylation of hippocampal Erk-1/2, Elk-1, and p90-Rsk-1 during contextual fear conditioning: interactions between Erk-1/2 and Elk-1. Mol Cell Neurosci 21:463-476.
42. Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE (2000) Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J Neurosci 20:8177-8187.
43. Selcher JC, Weeber EJ, Christian J, Nekrasova T, Landreth GE, Sweatt JD (2003) A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn Mem 10:26-39.
44. Shors TJ, Weiss C, Thompson RF (1992) Stress-induced facilitation of classical conditioning. Science 24:537-539.
45. Smith MA, Makino S, Kvetnansky R, Post RM (1995) Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15:1961-1970.
46. Spiess J, Rivier J, Rivier C, Vale W (1981) Primary structure of corticotropin-releasing factor from ovine hypothalamus. Proc Natl Acad Sci USA 78:6517-6521.
47. Stanciu M, Radulovic J, Spiess J (2000) Phosphorylated cAMP response element binding protein in the mouse brain after fear conditioning: relationship to Fos production. Mol Brain Res 94:15-24.
48. Sweatt JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10.
49. Valdez GR, Inoue K, Koob GF, Rivier J, Vale W, Zorrilla EP (2002) Human urocortin II: mild locomotor suppressive and delayed anxiolytic-like effects of a novel corticotropin-releasing factor related peptide. Brain Res 943:142-150.
50. Vale W, Spiess J, Rivier C, Rivier J (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and β-endorphin. Science 213:1394-1397.
51. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, Sawchenko PE (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428:191-212.
52. Vaughan J, Donaldson C, Bittencourt J, Perrin MH, Lewis K, Sutton S, Chan R, Turnbull AV, Lovejoy D, Rivier C, Rivier J, Sawchenko PE, Vale W (1995) Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor. Nature 378:287-292.
53. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24:715-726.
54. Zorrilla EP, Schulteis G, Ormsby A, Klaassen A, Ling N, McCarthy JR, Koob GF, De Souza EB (2002) Urocortin shares the memory modulating effects of corticotropin-releasing factor (CRF): mediation by CRF1 receptors. Brain Res 952:200-210.