Phosphodiesterase 10A inhibition attenuates sleep deprivation-induced deficits in long-term fear memory

Neuroscience Letters

Volumn 635, Issue , 2016, Pages 44-50

  Guo, Lengqiu ^a,b   Guo, Zhuangli ^c   Luo, Xiaoqing ^b   Liang, Rui ^b   Yang, Shui ^b   Ren, Haigang ^b   Wang, Guanghui ^a   Zhen, Xuechu ^a  

^a SOOCHOW UNIVERSITY   (China)

^b Suzhou Health College   (China)

^c QINGDAO UNIVERSITY   (China)

Author keywords

Fear memory; Phosphodiesterase 10; REM sleep deprivation

Indexed keywords

2 [4 [1 METHYL 4 (4 PYRIDINYL) 3 PYRAZOLYL]PHENOXYMETHYL]QUINOLINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; NOOTROPIC AGENT; PHOSPHODIESTERASE; PHOSPHODIESTERASE 10A; UNCLASSIFIED DRUG; 2-((4-(1-METHYL-4-PYRIDIN-4-YL-1H-PYRAZOL-3-YL)PHENOXY)METHYL)QUINOLINE; PDE10A PROTEIN, HUMAN; PHOSPHODIESTERASE INHIBITOR; PYRAZOLE DERIVATIVE; QUINOLINE DERIVATIVE;

ADULT; AMNESIA; AMYGDALA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DOSE RESPONSE; ENZYME INHIBITION; FEAR; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REM SLEEP DEPRIVATION; STARTLE REFLEX; ANIMAL; BRAIN; COMPLICATION; DRUG EFFECTS; MEMORY DISORDERS; METABOLISM; PHOSPHORYLATION; PSYCHOLOGY; REM SLEEP; SLEEP DEPRIVATION; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEAR; MALE; MEMORY DISORDERS; MEMORY, LONG-TERM; PHOSPHODIESTERASE INHIBITORS; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORYLATION; PYRAZOLES; QUINOLINES; RATS, SPRAGUE-DAWLEY; REFLEX, STARTLE; SLEEP DEPRIVATION; SLEEP, REM;

EID: 84994005178     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2016.10.017     Document Type: Article

References (63)

1. [1] Yang, R.H., Hu, S.J., Wang, Y., Zhang, W.B., Luo, W.J., Chen, J.Y., Paradoxical sleep deprivation impairs spatial learning and affects membrane excitability and mitochondrial protein in the hippocampus. Brain Res. 1230 (2008), 224–232.
2. [2] Bjorness, T.E., Riley, B.T., Tysor, M.K., Poe, G.R., REM restriction persistently alters strategy used to solve a spatial task. Learn. Mem. 12 (2005), 352–359.
3. [3] Siegel, J.M., The REM sleep-memory consolidation hypothesis. Science 294 (2001), 1058–1063.
4. [4] Stickgold, R., Walker, M.P., Sleep-dependent memory consolidation and reconsolidation. Sleep Med. 8 (2007), 331–343.
5. [5] Gais, S., Plihal, W., Wagner, U., Born, J., Early sleep triggers memory for early visual discrimination skills. Nat. Neurosci. 3 (2000), 1335–1339.
6. [6] Born, J., Rasch, B., Gais, S., Sleep to remember. Neurosci.: Rev. J. Bring. Neurobiol. Neurol. Psychiatry 12 (2006), 410–424.
7. [7] Walker, M.P., Stickgold, R., Sleep-dependent learning and memory consolidation. Neuron 44 (2004), 121–133.
8. [8] Ishikawa, A., Kanayama, Y., Matsumura, H., Tsuchimochi, H., Ishida, Y., Nakamura, S., Selective rapid eye movement sleep deprivation impairs the maintenance of long-term potentiation in the rat hippocampus. Eur. J. Neurosci. 24 (2006), 243–248.
9. [9] Walker, M.P., Stickgold, R., Sleep, memory, and plasticity. Annu. Rev. Psychol. 57 (2006), 139–166.
10. [10] Backhaus, J., Hoeckesfeld, R., Born, J., Hohagen, F., Junghanns, K., Immediate as well as delayed post learning sleep but not wakefulness enhances declarative memory consolidation in children. Neurobiol. Learn. Mem. 89 (2008), 76–80.
11. [11] Alhaider, I.A., Aleisa, A.M., Tran, T.T., Alzoubi, K.H., Alkadhi, K.A., Chronic caffeine treatment prevents sleep deprivation-induced impairment of cognitive function and synaptic plasticity. Sleep 33 (2010), 437–444.
12. [12] Alhaider, I.A., Aleisa, A.M., Tran, T.T., Alkadhi, K.A., Caffeine prevents sleep loss-induced deficits in long-term potentiation and related signaling molecules in the dentate gyrus. Eur. J. Neurosci. 31 (2010), 1368–1376.
13. [13] Aleisa, A.M., Helal, G., Alhaider, I.A., Alzoubi, K.H., Srivareerat, M., Tran, T.T., Al-Rejaie, S.S., Alkadhi, K.A., Acute nicotine treatment prevents REM sleep deprivation-induced learning and memory impairment in rat. Hippocampus 21 (2011), 899–909.
14. [14] Alberini, C.M., Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev. 89 (2009), 121–145.
15. [15] Hernandez, P.J., Abel, T., The role of protein synthesis in memory consolidation: progress amid decades of debate. Neurobiol. Learn. Mem. 89 (2008), 293–311.
16. [16] Kandel, E.R., The molecular biology of memory storage: a dialogue between genes and synapses. Science 294 (2001), 1030–1038.
17. [17] Josselyn, S.A., Shi, C., Carlezon, W.A. Jr., Neve, R.L., Nestler, E.J., Davis, M., Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J. Neurosci.: Offi. J. Soc. Neurosc. 21 (2001), 2404–2412.
18. [18] Zhou, Y., Won, J., Karlsson, M.G., Zhou, M., Rogerson, T., Balaji, J., Neve, R., Poirazi, P., Silva, A.J., CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat. Neurosci. 12 (2009), 1438–1443.
19. [19] Han, J.H., Kushner, S.A., Yiu, A.P., Cole, C.J., Matynia, A., Brown, R.A., Neve, R.L., Guzowski, J.F., Silva, A.J., Josselyn, S.A., Neuronal competition and selection during memory formation. Science 316 (2007), 457–460.
20. [20] Vecsey, C.G., Baillie, G.S., Jaganath, D., Havekes, R., Daniels, A., Wimmer, M., Huang, T., Brown, K.M., Li, X.Y., Descalzi, G., Kim, S.S., Chen, T., Shang, Y.Z., Zhuo, M., Houslay, M.D., Abel, T., Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461 (2009), 1122–1125.
21. [21] Abel, T., Nguyen, P.V., Barad, M., Deuel, T.A., Kandel, E.R., Bourtchouladze, R., Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88 (1997), 615–626.
22. [22] Havekes, R., Abel, T., Genetic dissection of neural circuits and behavior in Mus musculus. Adv. Genet. 65 (2009), 1–38.
23. [23] Havekes, R., Vecsey, C.G., Abel, T., The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cell. Signal. 24 (2012), 1251–1260.
24. [24] Seeger, T.F., Bartlett, B., Coskran, T.M., Culp, J.S., James, L.C., Krull, D.L., Lanfear, J., Ryan, A.M., Schmidt, C.J., Strick, C.A., Varghese, A.H., Williams, R.D., Wylie, P.G., Menniti, F.S., Immunohistochemical localization of PDE10A in the rat brain. Brain Res. 985 (2003), 113–126.
25. [25] Hebb, A.L., Robertson, H.A., Denovan-Wright, E.M., Striatal phosphodiesterase mRNA and protein levels are reduced in Huntington's disease transgenic mice prior to the onset of motor symptoms. Neuroscience 123 (2004), 967–981.
26. [26] Soderling, S.H., Bayuga, S.J., Beavo, J.A., Identification and characterization of a novel family of cyclic nucleotide phosphodiesterases. J. Biol. Chem. 273 (1998), 15553–15558.
27. [27] Fujishige, K., Kotera, J., Michibata, H., Yuasa, K., Takebayashi, S., Okumura, K., Omori, K., Cloning and characterization of a novel human phosphodiesterase that hydrolyzes both cAMP and cGMP (PDE10A). J. Biol. Chem. 274 (1999), 18438–18445.
28. [28] Fujishige, K., Kotera, J., Omori, K., Striatum- and testis-specific phosphodiesterase PDE10A isolation and characterization of a rat PDE10A. Eur. J. Biochem./FEBS 266 (1999), 1118–1127.
29. [29] Siuciak, J.A., Chapin, D.S., Harms, J.F., Lebel, L.A., McCarthy, S.A., Chambers, L., Shrikhande, A., Wong, S., Menniti, F.S., Schmidt, C.J., Inhibition of the striatum-enriched phosphodiesterase PDE10A: a novel approach to the treatment of psychosis. Neuropharmacology 51 (2006), 386–396.
30. [30] Simson, E., Gascon-Lema, M.G., Brown, D.L., Performance of automated slidemakers and stainers in a working laboratory environment – routine operation and quality control. Int. J. Lab. Hematol. 32 (2010), e64–e76.
31. [31] Schmidt, C.J., Chapin, D.S., Cianfrogna, J., Corman, M.L., Hajos, M., Harms, J.F., Hoffman, W.E., Lebel, L.A., McCarthy, S.A., Nelson, F.R., Proulx-LaFrance, C., Majchrzak, M.J., Ramirez, A.D., Schmidt, K., Seymour, P.A., Siuciak, J.A., Tingley, F.D. 3rd, Williams, R.D., Verhoest, P.R., Menniti, F.S., Preclinical characterization of selective phosphodiesterase 10A inhibitors: a new therapeutic approach to the treatment of schizophrenia. J. Pharmacol. Exp. Ther. 325 (2008), 681–690.
32. [32] Grauer, S.M., Pulito, V.L., Navarra, R.L., Kelly, M.P., Kelley, C., Graf, R., Langen, B., Logue, S., Brennan, J., Jiang, L., Charych, E., Egerland, U., Liu, F., Marquis, K.L., Malamas, M., Hage, T., Comery, T.A., Brandon, N.J., Phosphodiesterase 10A inhibitor activity in preclinical models of the positive, cognitive, and negative symptoms of schizophrenia. J. Pharmacol. Exp. Ther. 331 (2009), 574–590.
33. [33] Zhang, H.T., Phosphodiesterase targets for cognitive dysfunction and schizophrenia – a New York academy of sciences meeting. IDrugs: Invest. Drugs J. 13 (2010), 166–168.
34. [34] Reneerkens, O.A., Rutten, K., Bollen, E., Hage, T., Blokland, A., Steinbusch, H.W., Prickaerts, J., Inhibition of phoshodiesterase type 2 or type 10 reverses object memory deficits induced by scopolamine or MK-801. Behav. Brain Res. 236 (2013), 16–22.
35. [35] Mu, Y., Ren, Z., Jia, J., Gao, B., Zheng, L., Wang, G., Friedman, E., Zhen, X., Inhibition of phosphodiesterase10A attenuates morphine-induced conditioned place preference. Mol. Brain, 7, 2014, 70.
36. [36] Davis, M., Schlesinger, L.S., Sorenson, C.A., Temporal specificity of fear conditioning: effects of different conditioned stimulus-unconditioned stimulus intervals on the fear-potentiated startle effect, Journal of experimental psychology. Anim. Behav. Processes 15 (1989), 295–310.
37. [37] Falls, W.A., Miserendino, M.J., Davis, M., Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. J. Neurosci.: Offi. J. Soc. Neurosci. 12 (1992), 854–863.
38. [38] Mendelson, W.B., Guthrie, R.D., Frederick, G., Wyatt, R.J., The flower pot technique of rapid eye movement (REM) sleep deprivation. Pharmacol. Biochem. Behav. 2 (1974), 553–556.
39. [39] Grahnstedt, S., Ursin, R., Platform sleep deprivation affects deep slow wave sleep in addition to REM sleep. Behav. Brain Res. 18 (1985), 233–239.
40. [40] Machado, R.B., Hipolide, D.C., Benedito-Silva, A.A., Tufik, S., Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery. Brain Res. 1004 (2004), 45–51.
41. [41] Jin, Q., Cheng, J., Liu, Y., Wu, J., Wang, X., Wei, S., Zhou, X., Qin, Z., Jia, J., Zhen, X., Improvement of functional recovery by chronic metformin treatment is associated with enhanced alternative activation of microglia/macrophages and increased angiogenesis and neurogenesis following experimental stroke. Brain Behav. Immun. 40 (2014), 131–142.
42. [42] Kida, S., Josselyn, S.A., de Ortiz, S. Pena, Kogan, J.H., Chevere, I., Masushige, S., Silva, A.J., CREB required for the stability of new and reactivated fear memories. Nat. Neurosci. 5 (2002), 348–355.
43. [43] Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., Silva, A.J., Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79 (1994), 59–68.
44. [44] Han, J.H., Kushner, S.A., Yiu, A.P., Hsiang, H.L., Buch, T., Waisman, A., Bontempi, B., Neve, R.L., Frankland, P.W., Josselyn, S.A., Selective erasure of a fear memory. Science 323 (2009), 1492–1496.
45. [45] Alonso, M., Vianna, M.R., Depino, A.M., Mello e Souza, T., Pereira, P., Szapiro, G., Viola, H., Pitossi, F., Izquierdo, I., Medina, J.H., BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12 (2002), 551–560.
46. [46] Yamada, K., Nabeshima, T., Brain-derived neurotrophic factor/TrkB signaling in memory processes. J. Pharmacol. Sci. 91 (2003), 267–270.
47. [47] Bekinschtein, P., Cammarota, M., Igaz, L.M., Bevilaqua, L.R., Izquierdo, I., Medina, J.H., Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus. Neuron 53 (2007), 261–277.
48. [48] Alhaider, I.A., Aleisa, A.M., Tran, T.T., Alkadhi, K.A., Sleep deprivation prevents stimulation-induced increases of levels of P-CREB and BDNF: protection by caffeine. Mol. Cell. Neurosci. 46 (2011), 742–751.
49. [49] LeDoux, J.E., Cicchetti, P., Xagoraris, A., Romanski, L.M., The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J. Neurosci.: Offi. J. Soc. Neurosci. 10 (1990), 1062–1069.
50. [50] Sananes, C.B., Davis, M., N-methyl-D-aspartate lesions of the lateral and basolateral nuclei of the amygdala block fear-potentiated startle and shock sensitization of startle. Behav. Neurosci. 106 (1992), 72–80.
51. [51] Maren, S., Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditional fear in rats. J. Neurosci.: Offi. J. Soc. Neurosci. 19 (1999), 8696–8703.
52. [52] Maren, S., Neurotoxic or electrolytic lesions of the ventral subiculum produce deficits in the acquisition and expression of Pavlovian fear conditioning in rats. Behav. Neurosci. 113 (1999), 283–290.
53. [53] Quirk, G.J., Repa, C., LeDoux, J.E., Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 15 (1995), 1029–1039.
54. [54] Maren, S., Holt, W., The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav. Brain Res. 110 (2000), 97–108.
55. [55] Pinho, N., Moreira, K.M., Hipolide, D.C., Sinigaglia-Coimbra, R., Ferreira, T.L., Nobrega, J.N., Tufik, S., Oliveira, M.G., Sleep deprivation alters phosphorylated CREB levels in the amygdala: relationship with performance in a fear conditioning task. Behav. Brain Res. 236 (2013), 221–224.
56. [56] Xie, Z., Adamowicz, W.O., Eldred, W.D., Jakowski, A.B., Kleiman, R.J., Morton, D.G., Stephenson, D.T., Strick, C.A., Williams, R.D., Menniti, F.S., Cellular and subcellular localization of PDE10A, a striatum-enriched phosphodiesterase. Neuroscience 139 (2006), 597–607.
57. [57] O'Connor, V., Genin, A., Davis, S., Karishma, K.K., Doyere, V., De Zeeuw, C.I., Sanger, G., Hunt, S.P., Richter-Levin, G., Mallet, J., Laroche, S., Bliss, T.V., French, P.J., Differential amplification of intron-containing transcripts reveals long term potentiation-associated up-regulation of specific Pde10A phosphodiesterase splice variants. J. Biol. Chem. 279 (2004), 15841–15849.
58. [58] Rattiner, L.M., Davis, M., French, C.T., Ressler, K.J., Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. J. Neurosci.: Offi. J. Soc. Neurosci. 24 (2004), 4796–4806.
59. [59] Ferreira, T.L., Shammah-Lagnado, S.J., Bueno, O.F., Moreira, K.M., Fornari, R.V., Oliveira, M.G., The indirect amygdala-dorsal striatum pathway mediates conditioned freezing: insights on emotional memory networks. Neuroscience 153 (2008), 84–94.
60. [60] McNish, K.A., Gewirtz, J.C., Davis, M., Evidence of contextual fear after lesions of the hippocampus: a disruption of freezing but not fear-potentiated startle. J. Neurosci.: Offi. J. Soc. Neurosci. 17 (1997), 9353–9360.
61. [61] Silva, A.J., Kogan, J.H., Frankland, P.W., Kida, S., CREB and memory. Annu. Rev. Neurosci. 21 (1998), 127–148.
62. [62] Ghosh, A., Ginty, D.D., Bading, H., Greenberg, M.E., Calcium regulation of gene expression in neuronal cells. J. Neurobiol. 25 (1994), 294–303.
63. [63] Robertson, H.A., Immediate-early genes, neuronal plasticity, and memory. Biochem. Cell Biol. = Biochim. Biol. Cell. 70 (1992), 729–737.