Rescue of Impaired Long-Term Facilitation at Sensorimotor Synapses of Aplysia Following siRNA Knockdown of CREB1

Journal of Neuroscience

Volumn 35, Issue 4, 2015, Pages 1617-1626

  Zhou, Lian ^a   Zhang, Xyili ^a   Liu, Rong Yu ^a   Smolen, Paul ^a   Cleary, Xleonard J ^a   Byrne, John H ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CCAAT ENHANCER BINDING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; ROLIPRAM; SEROTONIN; SMALL INTERFERING RNA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN;

ANIMAL CELL; APLYSIA; ARTICLE; BRAIN ELECTROPHYSIOLOGY; COCULTURE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; GENE SILENCING; LONG TERM FACILITATION; MATHEMATICAL MODEL; MEMORY DISORDER; NERVE CELL PLASTICITY; NONHUMAN; PHARMACOLOGICAL STIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SENSORIMOTOR CORTEX; SIGNAL TRANSDUCTION; SIMULATION; SYNAPSE; TRAINING; TRANSCRIPTION REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; BIOPHYSICS; COMPUTER SIMULATION; CYTOLOGY; DRUG EFFECTS; ELECTROSTIMULATION; LONG TERM POTENTIATION; METABOLISM; MOTONEURON; PHYSIOLOGY; SENSORY NERVE CELL; TIME;

ANIMALS; APLYSIA; BIOPHYSICS; COCULTURE TECHNIQUES; COMPUTER SIMULATION; CREB-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MODELS, NEUROLOGICAL; MOTOR NEURONS; RNA, SMALL INTERFERING; SENSORY RECEPTOR CELLS; SEROTONIN; SYNAPSES; TIME FACTORS;

EID: 84921903076     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3330-14.2015     Document Type: Article

References (50)

1. Alarco´n JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, Barco A (2004) Chromatin acetylation, memory, and LTP are impaired in CBP_/_ mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42:947–959. CrossRef Medline
2. Alberini CM, Ghirardi M, Metz R, Kandel ER (1994) C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76:1099–1114. CrossRef Medline
3. Aytan N, Choi JK, Carreras I, Kowall NW, Jenkins BG, Dedeoglu A (2013) Combination therapy in a transgenic model of Alzheimer’s disease. Exp Neurol 250:228–238. CrossRef Medline
4. 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 U S A 95:15020–15025. CrossRef Medline
5. Barrett RM, Malvaez M, Kramer E, Matheos DP, Arrizon A, Cabrera SM, Lynch G, Greene W, Wood MA (2011) Hippocampal focal knockout of CBP affects specific histone modifications, long-term potentiation, and long-term memory. Neuropsychopharmacology 26:1545–1556. CrossRef Medline
6. Bartsch D, Ghirardi M, Skehel PA, Karl KA, Herder SP, Chen M, Bailey CH, Kandel ER (1995) Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83:979–992. CrossRef Medline
7. Bartsch D, Casadio A, Karl KA, Serodio P, Kandel ER (1998) CREB1 encodes a nuclear activator, a repressor, and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation. Cell 95:211–223. CrossRef Medline
8. Bourtchouladze R, Lidge R, Catapano R, Stanley J, Gossweiler S, Romashko D, Scott R, Tully T (2003) A mouse model of Rubinstein-Taybi syndrome: defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proc Natl Acad Sci U S A 100:10518–10522. CrossRef Medline
9. Bourtchuladze 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. CrossRef Medline
10. Cai D, Pearce K, Chen S, Glanzman DL (2011) Protein kinaseMmaintains long-term sensitization and long-term facilitation in Aplysia. J Neurosci 31:6421– 6431. CrossRef Medline
11. Chain DG, Casadio A, Schacher S, Hegde AN, Valbrun M, Yamamoto N, Goldberg AL, Bartsch D, Kandel ER, Schwartz JH (1999) Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysia. Neuron 22:147–156. CrossRef Medline
12. Dash PK, Hochner B, Kandel ER (1990) Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345:718–721. CrossRef Medline
13. Gong B, Vitolo OV, Trinchese F, Liu S, Shelanski M, Arancio O (2004) Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J Clin Invest 114:1624–1634. CrossRef Medline
14. Guan Z, Giustetto M, Lomvardas S, Kim JH, Miniaci MC, Schwartz JH, Thanos D, Kandel ER (2002) Integration of long-term memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111:483–493. CrossRef Medline
15. Guan Z, Kim JH, Lomvardas S, Holick K, Xu S, Kandel ER, Schwartz JH (2003) p38 MAP kinase mediates both short-term and long-term synaptic depression in Aplysia. J Neurosci 23:7317–7325. Medline
16. Josselyn SA, Shi C, Carlezon WA Jr, Neve RL, Nestler EJ, Davis M (2001) Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J Neurosci 21:2404–2412. Medline
17. Kawahara K, Seunobu M, Ohtsuka H, Kuniyasu A, Sugimoto Y, Nakagomi M, Fukasawa H, Shudo K, Nakayama H (2014) Cooperative therapeutic action of retinoic acid receptor and retinoid X receptor agonists in a mouse model of Alzheimer’s disease. J Alzheimers Dis 42:587–605.CrossRef
18. Korzus E, Rosenfeld MG, Mayford M (2004) CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42:961–972. CrossRef Medline
19. Liu RY, Cleary LJ, Byrne JH (2011a) The requirement for enhanced CREB1 expression in consolidation of long-term synaptic facilitation and longterm excitability in sensory neurons of Aplysia. J Neurosci 31:6871–6879. CrossRef Medline
20. Liu RY, Shah S, Cleary LJ, Byrne JH (2011b) Serotonin- and traininginduced dynamic regulation of CREB2 in Aplysia. Learn Mem 18:245–249. CrossRef Medline
21. Liu RY, Zhang Y, Baxter DA, Smolen P, Cleary LJ, Byrne JH (2013) Deficit in long-term synaptic plasticity is rescued by a computationally predicted stimulus protocol. J Neurosci 33:6944–6949. CrossRef Medline
22. Loewe S (1953) The problem of synergism and antagonism of combined drugs. Arzneimittel-Forschung 3:285–290. Medline
23. MacKenzie SJ, Houslay MD (2000) Action of rolipram on specific PDE4 cAMP phosphodiesterase isoforms and on the phosphorylation of cAMPresponse-element-binding protein (CREB) and p38 mitogen-activated protein (MAP) kinase in U937 monocytic cells. Biochem J 347:571–578. CrossRef Medline
24. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899–912. CrossRef Medline
25. Mohamed HA, Yao W, Fioravante D, Smolen PD, Byrne JH (2005) cAMPresponse elements in Aplysia creb1, creb2, and Ap-uch promoters: implications for feedback loops modulating long term memory. J Biol Chem 280:27035–27043. CrossRef Medline
26. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234:1249–1254. CrossRef Medline
27. Müller U, Carew TJ (1998) Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons. Neuron 21:1423–1434. CrossRef Medline
28. Novick SJ (2013) A simple test for synergy for a small number of combinations. Stat Med 32:5145–5155. CrossRef Medline
29. Park H, Lee JA, Lee C, Kim MJ, Chang DJ, Kim H, Lee SH, Lee YS, Kaang BK (2005) An Aplysia type 4 phosphodiesterase homolog localizes at the presynaptic terminals of Aplysia neuron and regulates synaptic facilitation. J Neurosci 25:9037–9045. CrossRef Medline
30. Peters M, Bletsch M, Catapano R, Zhang X, Tully T, Bourtchouladze R (2009) RNA interference in hippocampus demonstrates opposing roles for CREB and PP1_ in contextual and temporal long-term memory. Genes Brain Behav 8:320–329. CrossRef Medline
31. Philips GT, Kopec AM, Carew TJ (2013) Pattern and predictability in memory formation: from molecular mechanisms to clinical relevance. Neurobiol Learn Mem 105:117–124. CrossRef Medline
32. Pittenger C, Huang YY, Paletzki RF, Bourtchouladze R, Scanlin H, Vronskaya S, Kandel ER (2002) Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampusdependent spatial memory. Neuron 34:447–462. CrossRef Medline
33. Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T, Kandel ER (2012) A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 149:693–707. CrossRef Medline
34. Raymond FL, Tarpey P (2006) The genetics of mental retardation. Hum Mol Genet 15 [Suppl 2]:R110–R116. Medline
35. Restivo L, Tafi E, Ammassari-Teule M, Marie H (2009) Viral-mediated expression of a constitutively active form of CREB in hippocampal neurons increases memory. Hippocampus 19:228–234. CrossRef Medline
36. Roelfsema JH, Peters DJ (2007) Rubinstein-Taybi syndrome: clinical and molecular overview. Expert Rev Mol Med 9:1–16. Medline
37. Saura CA, Valero J (2011) The role of CREB signaling in Alzheimer’s disease and other cognitive disorders. Rev Neurosci 22:153–169. Medline
38. Sharma SK, Sherff CM, Shobe J, Bagnall MW, Sutton MA, Carew TJ (2003) Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. J Neurosci 23:3899–3907. Medline
39. Song H, Smolen P, Av-Ron E, Baxter DA, Byrne JH (2007) Dynamics of a minimal model of interlocked positive and negative feedback loops of transcriptional regulation by cAMP-response element binding proteins. Biophys J 92:3407–3424. CrossRef Medline
40. Stenberg JH, Terevnikov V, Joffe M, Tiihonen J, Tchoukhine E, Burkin M, Joffe G (2011) More evidence on proneurocognitive effects of add-on mirtazapine in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 35:1080–1086. CrossRef Medline
41. Stornetta RL, Zhu JJ (2011) Ras and Rap signaling in synaptic plasticity and mental disorders. Neuroscientist 17:54–78. CrossRef Medline
42. Titus DJ, Sakurai A, Kang Y, Furones C, Jergova S, Santos R, Sick TJ, Atkins CM (2013) Phosphodiesterase inhibition rescues chronic cognitive deficits induced by traumatic brain injury. J Neurosci 33:5216–5226. CrossRef Medline
43. Wijetunge LS, Chattarji S, Wyllie DJ, KindPC (2013) FragileXsyndrome: from targets to treatments. Neuropharmacology 68:83–96. CrossRef Medline
44. Wood MA, Kaplan MP, Park A, Blanchard EJ, Oliveira AM, Lombardi TL, Abel T (2005) Transgenic mice expressing a truncated form of CREBbinding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn Mem 12:111–119. CrossRef Medline
45. Xiao S, Xue H, Li G, Yuan C, Li X, Chen C, Wu HZ, Mitchell P, Zhang M (2012) Therapeutic effects of cerebrolysin added to risperidone in patients with schizophrenia dominated by negative symptoms. Aust N Z J Psychiatry 46:153–160. CrossRef Medline
46. Yamamoto N, Hegde AN, Chain DG, Schwartz JH (1999) Activation and degradation of the transcription factor C/EBP during long-term facilitation in Aplysia. J Neurochem 73:2415–2423. Medline
47. Yin N, Ma W, Pei J, Ouyang Q, Tang C, Lai L (2014) Synergistic and antagonistic drug combinations depend on network topology. PLoS One 9:e93960. CrossRef Medline
48. Zhang Y, Liu RY, Heberton GA, Smolen P, Baxter DA, Cleary LJ, Byrne JH (2012) Computational design of enhanced learning protocols. Nat Neurosci 15:294–297. Medline
49. Zhang Y, Smolen P, Baxter DA, Byrne JH (2014) Computational analysis of synergism in small molecular network motifs. PLoS Comput Biol 10: e1003524. CrossRef Medline
50. Zimmermann GR, Lehar J, Keith CT (2007) Multi-target therapeutics: when the whole is greater than the sum of the parts. Drug Discov Today 12:34–42. CrossRef Medline