Regulation of amygdalar PKA by β-arrestin-2/phosphodiesterase-4 complex is critical for fear conditioning

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 51, 2009, Pages 21918-21923

  Li, Yuting ^a,b   Li, Haohong ^a   Liu, Xing ^a   Bao, Guobin ^a   Tao, Yezheng ^a   Wu, Ziyan ^a   Xia, Peng ^a   Wu, Chunfu ^b   Li, Baoming ^a   Ma, Lan ^a  

^a FUDAN UNIVERSITY   (China)

^b SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; PHOSPHODIESTERASE IV;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATIVE MEMORY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEAR; FEEDBACK SYSTEM; GENE OVEREXPRESSION; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SYNAPSE;

AMYGDALA; ANIMALS; ARRESTINS; BIOFEEDBACK, PSYCHOLOGY; BLOTTING, WESTERN; CONDITIONING, OPERANT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; FEAR; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT;

MUS;

EID: 76049091992     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906941106     Document Type: Article

References (48)

1. DeWire SM, Ahn S, Lefkowitz RJ, Shenoy SK (2007) Beta-arrestins and cell signaling. Annu Rev Physiol 69:483-510.
2. Attramadal H, et al. (1992) Beta-arrestin-2, a novel member of the arrestin/beta-arrestin gene family. J Biol Chem 267:17882-17890.
3. Fan XL, Zhang JS, Zhang XQ, Yue W, MaL (2003) Differential regulation of beta-arrestin-1 and beta-arrestin-2 gene expression in rat brain by morphine. Neuroscience 117:383-389.
4. Su Y, et al. (2005) Altered CXCR2 signaling in beta-arrestin-2-deficient mouse models. J Immunol 175:5396-5402.
5. Walker JK, et al. (2003) Beta-arrestin-2 regulates thedevelopmentof allergic asthma. J Clin Invest 112:566-574.
6. WangY, et al. (2006) Association of beta-arrestin and TRAF6 negatively regulates Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 7:139-147.
7. Shi Y, et al. (2007) Critical regulation of CD4(+) T cell survival and autoimmunity by beta-arrestin-1. Nat Immunol 8:817-824.
8. Yu MC, et al. (2008) An essential function for beta-arrestin-2 in the inhibitory signaling of natural killer cells. Nat Immunol 9:898-907.
9. Bohn LM, et al. (1999) Enhanced morphine analgesia in mice lacking beta-arrestin-2. Science 286:2495-2498.
10. Kang J, et al. (2005) A nuclear function of beta-arrestin1 in GPCR signaling: Regulation of histone acetylation and gene transcription. Cell 123:833-847.
11. Bychkov ER, Gurevich VV, Joyce JN, Benovic JL, Gurevich EV (2008) Arrestins and two receptor kinases are upregulated in Parkinson's disease with dementia. Neurobiol Aging 29:379-396.
12. Beaulieu JM, et al. (2005) An Akt/beta-arrestin-2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122:261-273.
13. Beaulieu JM, et al. (2008) A beta-arrestin-2 signaling complex mediates lithium action on behavior. Cell 132:125-136.
14. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897-931.
15. McKernan MG, Shinnick-Gallagher P (1997) Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390:607-611.
16. Rogan MT, Staubli UV, LeDoux JE (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390:604-607.
17. Romanski LM, LeDoux JE (1992) Equipotentiality of thalamo-amygdala and thalamocortico-amygdala circuits in auditory fear conditioning. J Neurosci 12:4501-4509.
18. Schafe GE, LeDoux JE (2000) Memory consolidation of auditory Pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J Neurosci 20:RC96.
19. Schafe GE, et al. (2000) Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J Neurosci 20:8177-8187.
20. Impey S, et al. (1998) Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1:595-601.
21. Rodrigues SM, Schafe GE, LeDoux JE (2004) Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44:75-91.
22. O'Donnell JM, Zhang HT (2004) Antidepressant effects of inhibitors of cAMP phosphodiesterase (PDE-4). Trends Pharmacol Sci 25:158-163.
23. Millar JK, et al. (2007) Disrupted in schizophrenia 1andphosphodiesterase-4B: Towardsan understanding of psychiatric illness. J Physiol 584:401-405.
24. Conti M, Beavo J (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: Essential components in cyclic nucleotide signaling. Annu Rev Biochem 76:481-511.
25. Houslay MD, Baillie GS, Maurice DH (2007) cAMP-Specific phosphodiesterase-4 enzymes in the cardiovascular system: A molecular toolbox for generating compartmentalized cAMP signaling. Circ Res 100:950-966.
26. Houslay MD, Schafer P, Zhang KY (2005) Keynote review: Phosphodiesterase-4 as a therapeutic target. Drug Discov Today 10:1503-1519.
27. Bolger GB, et al. (2003) The unique amino-terminal region of the PDE-4D5 cAMP phosphodiesterase isoform confers preferential interaction with beta-arrestins. J Biol Chem 278:49230-49238.
28. Baillie GS, Houslay MD (2005) Arrestin times for compartmentalised cAMP signalling and phosphodiesterase-4 enzymes. Curr Opin Cell Biol 17:129-134.
29. Lynch MJ, et al. (2005) RNA silencing identifies PDE4D5 as the functionally relevant cAMP phosphodiesterase interacting with beta-arrestin to control the protein kinase A/AKAP79-mediated switching of the beta2-adrenergic receptor to activation of ERK in HEK293B2 cells. J Biol Chem 280:33178-33189.
30. Maren S (1999) Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditional fear in rats. J Neurosci 19:8696-8703.
31. Perry SJ, et al. (2002) Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins. Science 298:834-836.
32. Rutten K, et al. (2008) Enhanced long-term potentiation and impaired learning in phosphodiesterase,4D-knockout (PDE,4D) mice. Eur J Neurosci 28:625-632.
33. Davis JA, Gould TJ (2005) Rolipram attenuates MK-801-induced deficits in latent inhibition. Behav Neurosci 119:595-602.
34. Sette C, Conti M (1996) Phosphorylation and activation of a cAMP-specific phosphodiesterase by the cAMP-dependent protein kinase. Involvement of serine 54 in the enzyme activation. J Biol Chem 271:16526-16534.
35. Baillie GS, et al. (2007) Mapping binding sites for the PDE4D5 cAMP-specific phosphodiesterase to the N- and C-domains of beta-arrestin using spot-immobilized peptide arrays. Biochem J 404:71-80.
36. HuangYY, Kandel ER (1998) Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21:169-178.
37. Huang YY, Martin KC, Kandel ER (2000) Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J Neurosci 20:6317-6325.
38. Kelly MP, et al. (2008) Constitutive activation of the G-protein subunit Galphas within forebrain neurons causes PKA-dependent alterations in fear conditioning and cortical Arc mRNA expression. Learn Mem 15:75-83.
39. Park H, et al. (2005) An Aplysia type 4 phosphodiesterase homolog localizes at the presynaptic terminals of Aplysia neuron and regulates synaptic facilitation. J Neurosci 25:9037-9045.
40. Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E (1998) Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci USA 95:15020-15025.
41. Domenech T, et al. (1994) Identification and characterization of serotonin 5-HT4 receptor binding sites in human brain: Comparison with other mammalian species. Brain Res Mol Brain Res 21:176-180.
42. Roberts JC, et al. (2002) The distribution of 5-HT(6) receptors in rat brain: An autoradiographic binding study using the radiolabelled 5-HT(6) receptor antagonist [(125)I]SB-258585. Brain Res 934:49-57.
43. Baillie GS, et al. (2003) beta-Arrestin-mediated PDE-4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci USA 100:940-945.
44. MacKenzie SJ, Baillie GS, McPhee I, Bolger GB, Houslay MD (2000) ERK2 mitogen-activated protein kinase binding, phosphorylation, 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.
45. Zhang HT, et al. (2004) Inhibition of the phosphodiesterase-4 (PDE-4) enzyme reverses memory deficits produced by infusion of theMEKinhibitor U0126 into the CA1 subregion of the rat hippocampus. Neuropsychopharmacology 29:1432-1439.
46. Lin CH, et al. (2001) A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 31:841-851.
47. Shumyatsky GP, et al. (2005) stathmin, a gene enriched in the amygdala, controls both learned and innate fear. Cell 123:697-709.
48. Luan B, et al. (2009) Deficiency of a beta-arrestin-2 signal complex contributes to insulin resistance. Nature 457:1146-1149.