Calcineurin phosphatase as a negative regulator of fear memory in hippocampus: Control on nuclear factor-κB signaling in consolidation and reconsolidation

Hippocampus

Volumn 24, Issue 12, 2014, Pages 1549-1561

  de la Fuente, Verónica ^a,b   Federman, Noel ^a,b   Fustiñana, María Sol ^a,b,c   Zalcman, Gisela ^a,b   Romano, Arturo ^a,b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Calcineurin; Consolidation; Fear conditioning; Hippocampus; NF B; Reconsolidation

Indexed keywords

CALCINEURIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SALAZOSULFAPYRIDINE; TACROLIMUS; CALCINEURIN INHIBITOR; CALCINEURIN PHOSPHATASE; CENTRAL NERVOUS SYSTEM AGENTS; PHOSPHATASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; FACILITATION; FEAR CONDITIONING TEST; HIPPOCAMPUS; MALE; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; RECALL; REINFORCEMENT; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CONDITIONED REFLEX; DRUG EFFECTS; ELECTRIC SHOCK; FEAR; MEMORY; METABOLISM; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY;

ANIMALS; CALCINEURIN INHIBITORS; CENTRAL NERVOUS SYSTEM AGENTS; CONDITIONING, CLASSICAL; ELECTROSHOCK; FEAR; HIPPOCAMPUS; MALE; MEMORY; MICE, INBRED C57BL; NEUROPSYCHOLOGICAL TESTS; NF-KAPPA B; PHOSPHORIC MONOESTER HYDROLASES; SIGNAL TRANSDUCTION; SULFASALAZINE; TACROLIMUS;

EID: 84911002692     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22334     Document Type: Article

References (85)

1. Ahn HJ, Hernandez CM, Levenson JM, Lubin FD, Liou HC, Sweatt JD. 2008. c-Rel, an NF-kappaB family transcription factor, is required for hippocampal long-term synaptic plasticity and memory formation. Learn Mem 15:539-549.
2. Alberini CM. 2005. Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? Trends Neurosci 28:51-56.
3. Alberini CM. 2009. Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89:121-145.
4. Alexanian AR, Bamburg JR. 1999. Neuronal survival activity of s100betabeta is enhanced by calcineurin inhibitors and requires activation of NF-kappaB. FASEB J Off Publ Fed Am Soc Exp Biol 13:1611-1620.
5. Anokhin KV, Tiunova AA, Rose SPR. 2002. Reminder effects - reconsolidation or retrieval deficit? Pharmacological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks. Eur J Neurosci 15:1759-1765.
6. Baumgartel K, Genoux D, Welzl H, Tweedie-Cullen RY, Koshibu K, Livingstone-Zatchej M, Mamie C, Mansuy IM. 2008. Control of the establishment of aversive memory by calcineurin and Zif268. Nat Neurosci 11:572-578.
7. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda H, von Zastrow M, Malenka RC. 2000. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3:1291-1300.
8. Biswas G, Anandatheerthavarada HK, Zaidi M, Avadhani NG. 2003. Mitochondria to nucleus stress signaling: a distinctive mechanism of NFkappaB/Rel activation through calcineurin-mediated inactivation of IkappaBbeta. J Cell Biol 161:507-519.
9. Bito H, Deisseroth K, Tsien RW. 1996. CREB phosphorylation and dephosphorylation: A Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
10. Blanchard RJ, Blanchard DC. 1969. Crouching as an index of fear. J Comp Physiol Psychol 67:370-375.
11. Blumenthal DK, Takio K, Hansen RS, Krebs EG. 1986. Dephosphorylation of cAMP-dependent protein kinase regulatory subunit (type II) by calmodulin-dependent protein phosphatase. Determinants of substrate specificity. J Biol Chem 261:8140-8145.
12. Boccia M, Freudenthal R, Blake M, de la Fuente V, Acosta G, Baratti C, Romano A. 2007. Activation of hippocampal nuclear factor-kappa B by retrieval is required for memory reconsolidation. J Neurosci 27:13436-13445.
13. Carayol N, Chen J, Yang F, Jin T, Jin L, States D, Wang CY. 2006. A dominant function of IKK/NF-kappaB signaling in global lipopolysaccharide-induced gene expression. J Biol Chem 281:31142-31151.
14. de la Fuente V, Freudenthal R, Romano A. 2011. Reconsolidation or extinction: transcription factor switch in the determination of memory course after retrieval. J Neurosci 31: 5562-5573.
15. Donella-Deana A, Krinks MH, Ruzzene M, Klee C, Pinna LA. 1994. Dephosphorylation of phosphopeptides by calcineurin (protein phosphatase 2B). Eur J Biochem FEBS 219:109-117.
16. Dong J, Jimi E, Zhong H, Hayden MS, Ghosh S. 2008. Repression of gene expression by unphosphorylated NF-kappaB p65 through epigenetic mechanisms. Genes Dev 22:1159-1173.
17. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Lüthi A. 2009. Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757-771.
18. El-Armouche A, Bednorz A, Pamminger T, Ditz D, Didié M, Dobrev D, Eschenhagen T. 2006. Role of calcineurin and protein phosphatase-2A in the regulation of phosphatase inhibitor-1 in cardiac myocytes. Biochem Biophys Res Commun 346:700-706.
19. Federman N, de la Fuente V, Zalcman G, Corbi N, Onori A, Passananti C, Romano A. 2013. Nuclear factor κB-dependent histone acetylation is specifically involved in persistent forms of memory. J Neurosci Off J Soc Neurosci 33:7603-7614.
20. Fernandez AM, Fernandez S, Carrero P, Garcia-Garcia M, Torres-Aleman I. 2007. Calcineurin in reactive astrocytes plays a key role in the interplay between proinflammatory and anti-inflammatory signals. J Neurosci 27:8745-8756.
21. Fiorenza NG, Sartor D, Myskiw JC, Izquierdo I. 2011. Treatment of fear memories: Interactions between extinction and reconsolidation. An Acad Bras Ciênc 83:1363-1372.
22. Forcato C, Rodriguez ML, Pedreira ME. 2011. Repeated labilization-reconsolidation processes strengthen declarative memory in humans. PLoS One 6:e23305.
23. Forcato C, Fernandez RS, Pedreira ME. 2013. The role and dynamic of strengthening in the reconsolidation process in a human declarative memory: What decides the fate of recent and older memories? PloS One 8:e61688.
24. Franklin KBJ, Paxinos G. 2001. The mouse brain in stereotaxic coordinates. London: Academic.
25. Frantz B, Nordby EC, Bren G, Steffan N, Paya CV, Kincaid RL, Tocci MJ, O'Keefe SJ, O'Neill EA. 1994. Calcineurin acts in synergy with PMA to inactivate I kappa B/MAD3, an inhibitor of NF-kappa B. EMBO J 13:861-870.
26. Frenkel L, Maldonado H, Delorenzi A. 2005. Memory strengthening by a real-life episode during reconsolidation: An outcome of water deprivation via brain angiotensin II. Eur J Neurosci 22:1757-1766.
27. Freudenthal R, Romano A. 2000. Participation of Rel/NF-kappaB transcription factors in long-term memory in the crab Chasmagnathus. Brain Res 855: 274-281.
28. Freudenthal R, Boccia MM, Acosta GB, Blake MG, Merlo E, Baratti CM, Romano A. 2005. NF-kappaB transcription factor is required for inhibitory avoidance long-term memory in mice. Eur J Neurosci 21:2845-2852.
29. Genoux D, Haditsch U, Knobloch M, Michalon A, Storm D, Mansuy IM. 2002. Protein phosphatase 1 is a molecular constraint on learning and memory. Nature 418:970-975.
30. Gerdjikov TV, Beninger RJ. 2005. Differential effects of calcineurin inhibition and protein kinase A activation on nucleus accumbens amphetamine-produced conditioned place preference in rats. Eur J Neurosci 22:697-705.
31. Glowinski J, Iversen L. 1966. Regional studies of catecholamines in the rat brain. 3. Subcellullar distribution of endogenous and exogenous catecholamines in various brain regions. Biochem Pharmacol 15:977-987.
32. Havekes R, Nijholt IM, Luiten PGM, Van der Zee EA. 2006. Differential involvement of hippocampal calcineurin during learning and reversal learning in a Y-maze task. Learn Mem Cold Spring Harb N 13:753-759.
33. Havekes R, Nijholt IM, Visser AK, Eisel UL, Van der Zee EA. 2008. Transgenic inhibition of neuronal calcineurin activity in the forebrain facilitates fear conditioning, but inhibits the extinction of contextual fear memories. Neurobiol Learn Mem 89:595-598.
34. Ikegami S, Inokuchi K. 2000. Antisense DNA against calcineurin facilitates memory in contextual fear conditioning by lowering the threshold for hippocampal long-term potentiation induction. Neuroscience 98:637-646.
35. Inda MC, Muravieva EV, Alberini CM. 2011. Memory retrieval and the passage of time: From reconsolidation and strengthening to extinction. J Neurosci 31:1635-1643.
36. Kaltschmidt B, Widera D, Kaltschmidt C. 2005. Signaling via NF-kappaB in the nervous system. Biochim Biophys Acta 1745:287-299.
37. Kandel ER. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-1038.
38. Kim Y, Moon JS, Lee KS, Park SY, Cheong J, Kang HS, Lee HY, Kim HD. 2004. Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates the expression of iNOS through IKK and NF-kappaB activity in LPS-stimulated mouse peritoneal macrophages and RAW 264.7 cells. Biochem Biophys Res Commun 314:695-703.
39. Klee CB, Ren H, Wang X. 1998. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 273:13367-13370.
40. Kuno T, Mukai H, Ito A, Chang CD, Kishima K, Saito N, Tanaka C. 1992. Distinct cellular expression of calcineurin A alpha and A beta in rat brain. J Neurochem 58:1643-1651.
41. Lee JL. 2009. Reconsolidation: maintaining memory relevance. Trends Neurosci 32:413-420.
42. Lee JL, Everitt BJ, Thomas KL. 2004. Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304:839-843.
43. Lee JL, Milton AL, Everitt BJ. 2006. Reconsolidation and extinction of conditioned fear: Inhibition and potentiation. J Neurosci 26:10051-10056.
44. Lee JLC, Hynds RE. 2013. Divergent cellular pathways of hippocampal memory consolidation and reconsolidation. Hippocampus 23:233-244.
45. Letzkus JJ, Wolff SBE, Meyer EMM, Tovote P, Courtin J, Herry C, Lüthi A. 2011. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480:331-335.
46. Levenson JM, Choi S, Lee SY, Cao YA, Ahn HJ, Worley KC, Pizzi M, Liou HC, Sweatt JD. 2004. A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel. J Neurosci 24:3933-3943.
47. Lin CH, Lee CC, Gean PW. 2003a. Involvement of a calcineurin cascade in amygdala depotentiation and quenching of fear memory. Mol Pharmacol 63:44-52.
48. Lin CH, Yeh SH, Leu TH, Chang WC, Wang ST, Gean PW. 2003b. Identification of calcineurin as a key signal in the extinction of fear memory. J Neurosci 23:1574-1579.
49. Lin CH, Yeh SH, Lu HY, Gean PW. 2003c. The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. J Neurosci 23:8310-8317.
50. Liu JO, Nacev BA, Xu J, Bhat S. 2009. It takes two binding sites for calcineurin and NFAT to tango. Mol Cell 33:676-678.
51. Lopez-Salon M, Alonso M, Vianna MR, Viola H, Mello e Souza T, Izquierdo I, Pasquini JM, Medina JH. 2001. The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur J Neurosci 14:1820-1826.
52. Lubin FD, Sweatt JD. 2007. The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 55:942-957.
53. Malleret G, Haditsch U, Genoux D, Jones MW, Bliss TV, Vanhoose AM, Weitlauf C, Kandel ER, Winder DG, Mansuy IM. 2001. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell 104:675-686.
54. Martin SJ, Grimwood PD, Morris RG. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
55. Meffert MK, Baltimore D. 2005. Physiological functions for brain NF-kappaB. Trends Neurosci 28:37-43.
56. Merlo E, Romano A. 2007. Long-term memory consolidation depends on proteasome activity in the crab Chasmagnathus. Neuroscience 147:46-52.
57. Merlo E, Freudenthal R, Romano A. 2002. The IkappaB kinase inhibitor sulfasalazine impairs long-term memory in the crab Chasmagnathus. Neuroscience 112:161-172.
58. Merlo E, Freudenthal R, Maldonado H, Romano A. 2005. Activation of the transcription factor NF-kappaB by retrieval is required for long-term memory reconsolidation. Learn Mem 12:23-29.
59. Mulkey RM, Endo S, Shenolikar S, Malenka RC. 1994. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369:486-488.
60. Myers KM, Davis M. 2007. Mechanisms of fear extinction. Mol Psychiatry 12:120-150.
61. Nader K. 2003. Memory traces unbound. Trends Neurosci 26:65-72.
62. Nader K, Schafe GE, Le Doux JE. 2000. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722-726.
63. Paterson JM, Smith SM, Harmar AJ, Antoni FA. 1995. Control of a novel adenylyl cyclase by calcineurin. Biochem Biophys Res Commun 214:1000-1008.
64. Pedreira ME, Maldonado H. 2003. Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38:863-869.
65. Pedreira ME, Perez-Cuesta LM, Maldonado H. 2004. Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction. Learn Mem 11:579-585.
66. Pons S, Torres-Aleman I. 2000. Insulin-like growth factor-I stimulates dephosphorylation of ikappa B through the serine phosphatase calcineurin (protein phosphatase 2B). J Biol Chem 275:38620-38625.
67. Price CJ, Kim P, Raymond LA. 1999. D1 dopamine receptor-induced cyclic AMP-dependent protein kinase phosphorylation and potentiation of striatal glutamate receptors. J Neurochem 73:2441-2446.
68. Raman IM, Tong G, Jahr CE. 1996. Beta-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase. Neuron 16:415-421.
69. Schwaninger M, Blume R, Krüger M, Lux G, Oetjen E, Knepel W. 1995. Involvement of the Ca(2+)-dependent phosphatase calcineurin in gene transcription that is stimulated by cAMP through cAMP response elements. J Biol Chem 270:8860-8866.
70. Sheridan CM, Heist EK, Beals CR, Crabtree GR, Gardner P. 2002. Protein kinase A negatively modulates the nuclear accumulation of NF-ATc1 by priming for subsequent phosphorylation by glycogen synthase kinase-3. J Biol Chem 277:48664-48676.
71. Si J, Yang J, Xue L, Yang C, Luo Y, Shi H, Lu L. 2012. Activation of NF-κB in basolateral amygdala is required for memory reconsolidation in auditory fear conditioning. PloS One 7:e43973.
72. Silva AJ, Josselyn SA. 2002. The molecules of forgetfulness. Nature 418:929-930.
73. Sweatt JD. 2003. Mechanisms of memory. San Diego, California: Academic Press. http://www.loc.gov/catdir/toc/els051/2003107470.html http://www.loc.gov/catdir/description/els051/2003107470.html.
74. Tong G, Shepherd D, Jahr CE. 1995. Synaptic desensitization of NMDA receptors by calcineurin. Science 267:1510-1512.
75. Traynelis SF, Wahl P. 1997. Control of rat GluR6 glutamate receptor open probability by protein kinase A and calcineurin. J Physiol 503 (Pt 3):513-531.
76. Von Hertzen LSJ, Giese KP. 2005. Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci Off J Soc Neurosci 25:1935-1942.
77. Wahl C, Liptay S, Adler G, Schmid RM. 1998. Sulfasalazine: a potent and specific inhibitor of nuclear factor kappa B. J Clin Invest 101:1163-1174.
78. Wang JH, Kelly PT. 1996. The balance between postsynaptic Ca(2+)-dependent protein kinase and phosphatase activities controlling synaptic strength. Learn Mem 3:170-181.
79. Weber CK, Liptay S, Wirth T, Adler G, Schmid RM. 2000. Suppression of NF-kappaB activity by sulfasalazine is mediated by direct inhibition of IkappaB kinases alpha and beta. Gastroenterology 119:1209-1218.
80. Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER. 1998. Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell 92:25-37.
81. Yang J, Yu J, Jia X, Zhu W, Zhao L, Li S, Xu C, Yang C, Wu P, Lu L. 2011. Inhibition of nuclear factor-κB impairs reconsolidation of morphine reward memory in rats. Behav Brain Res 216:592-596.
82. Yeh SH, Lin CH, Lee CF, Gean PW. 2002. A requirement of nuclear factor-kappaB activation in fear-potentiated startle. J Biol Chem 277:46720-46729.
83. Zhong H, SuYang H, Erdjument-Bromage H, Tempst P, Ghosh S. 1997. The transcriptional activity of NF-kappaB is regulated by the IkappaB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89:413-424.
84. Zhong H, Voll RE, Ghosh S. 1998. Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1:661-671.
85. Zhong H, May MJ, Jimi E, Ghosh S. 2002. The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol Cell 9:625-636.