Involvement of hippocampal CAMKII/CREB signaling in the spatial memory retention induced by creatine

Amino Acids

Volumn 43, Issue 6, 2012, Pages 2491-2503

  Souza, Mauren Assis ^a   Magni, Danieli Valnes ^a   Guerra, Gustavo Petri ^a   Oliveira, Mauro Schneider ^a,b   Furian, Ana Flavia ^a   Pereira, Leticia ^a   Marquez, Silvia Vacari ^a   Ferreira, Juliano ^a   Fighera, Michele Rechia ^a   Royes, Luiz Fernando Freire ^a  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b Unipampa campus Itaqui   (Brazil)

Author keywords

Creatine; CREB; Hippocampus; Protein kinases; Spatial memory

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CREATINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; INTRACELLULAR SIGNALING; LATENT PERIOD; LOCOMOTION; MALE; MAZE TEST; MEMORY CONSOLIDATION; MENTAL TASK; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SPATIAL MEMORY; WESTERN BLOTTING;

ANIMALS; BENZIMIDAZOLES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CREATINE; CREB-BINDING PROTEIN; HIPPOCAMPUS; MALE; MAZE LEARNING; NAPHTHALIMIDES; RATS; RATS, WISTAR; RETENTION (PSYCHOLOGY); SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84872676782     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-012-1329-4     Document Type: Article

References (51)

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(5):615-626 (Pubitemid 27152404)
2. Ajilore O, Haroon E, Kumaran S, Darwin C, Binesh N, Mintz J, Miller J, Thomas MA, Kumar A (2007) Measurement of brain metabolites in patients with type 2 diabetes and major depression using proton magnetic resonance spectroscopy. Neuropsychopharmacology 32(6):1224-1231 (Pubitemid 46788852)
3. Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89(1):121-145
4. Almeida LS, Salomons GS, Hogenboom F, Jakobs C, Schoffelmeer AN (2006) Exocytotic release of creatine in rat brain. Synapse 60(2):118-123 (Pubitemid 43878120)
5. Andres RH, Ducray AD, Schlattner U, Wallimann T, Widmer HR (2008) Functions and effects of creatine in the central nervous system. Brain Res Bull 76(4):329-343
6. Bach ME, Hawkins RD, Osman M, Kandel ER, Mayford M (1995) Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell 81(6):905-915
7. Bachevalier J, Nemanic S (2008) Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex. Hippocampus 18(1):64-80
8. Barnes CA (1979) Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93(1):74-104 (Pubitemid 9140564)
9. Bernabeu R, Bevilaqua L, Ardenghi P, Bromberg E, Schmitz P, Bianchin M, Izquierdo I, Medina JH (1997) Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc Natl Acad Sci USA 94(13): 7041-7046 (Pubitemid 27281987)
10. Braissant O, Henry H, Beard E, Uldry J (2011) Creatine deficiency syndromes and the importance of creatine synthesis in the brain. Amino Acids 40(5):1315-1324
11. Casu MA, Sanna A, Spada GP, Falzoi M, Mongeau R, Pani L (2007) Effects of acute and chronic valproate treatments on p-CREB levels in the rat amygdala and nucleus accumbens. Brain Res 1141:15-24 (Pubitemid 46394502)
12. Cippitelli A, Zook M, Bell L, Damadzic R, Eskay RL, Schwandt M, Heilig M (2010) Reversibility of object recognition but not spatial memory impairment following binge-like alcohol exposure in rats. Neurobiol Learn Mem 94(4):538-546
13. Colombo PJ, Brightwell JJ, Countryman RA (2003) Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J Neurosci 23(8):3547-3554 (Pubitemid 36531998)
14. Dechent P, Pouwels PJ, Wilken B, Hanefeld F, Frahm J (1999) Increase of total creatine in human brain after oral supplementation of creatine- monohydrate. Am J Physiol 277(3 Pt 2):R698-R704 (Pubitemid 29458141)
15. File SE, Gonzalez LE (1996) Anxiolytic effects in the plus-maze of 5-HT1A-receptor ligands in dorsal raphe and ventral hippocampus. Pharmacol Biochem Behav 54(1):123-128
16. Igaz LM, Vianna MR, Medina JH, Izquierdo I (2002) Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning. J Neurosci 22(15):6781-6789 (Pubitemid 35386435)
17. Izquierdo I, Bevilaqua LR, Rossato JI, Bonini JS, Medina JH, Cammarota M (2006) Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci 29(9):496-505 (Pubitemid 44291818)
18. McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA (1996) Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87(7):1339-1349 (Pubitemid 27010116)
19. McMorris T, Harris RC, Swain J, Corbett J, Collard K, Dyson RJ, Dye L, Hodgson C, Draper N (2006) Effect of creatine supplementation and sleep deprivation, with mild exercise, on cognitive and psychomotor performance, mood state, and plasma concentrations of catecholamines and cortisol. Psychopharmacology 185(1):93-103 (Pubitemid 43289617)
20. McMorris T, Harris RC, Howard AN, Langridge G, Hall B, Corbett J, Dicks M, Hodgson C (2007) Creatine supplementation, sleep deprivation, cortisol, melatonin and behavior. Physiol Behav 90(1):21-28 (Pubitemid 44920426)
21. Medeiros R, Prediger RD, Passos GF, Pandolfo P, Duarte FS, Franco JL, Dafre AL, Di Giunta G, Figueiredo CP, Takahashi RN, Campos MM, Calixto JB (2007) Connecting TNF-Alpha signaling pathways to iNOS expression in a mouse model of Alzheimer's disease: relevance for the behavioral and synaptic deficits induced by amyloid beta protein. J Neurosci 27(20):5394-5404 (Pubitemid 46790177)
22. Mishkin M (1978) Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273(5660):297-298 (Pubitemid 8332881)
23. Miyamoto E (2006) Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 100(5):433-442 (Pubitemid 44609534)
24. Mizuno K, Giese KP (2005) Hippocampus-dependent memory formation: do memory type-specific mechanisms exist? J Pharmacol Sci 98(3):191-197 (Pubitemid 41296396)
25. Mizuno M, Yamada K, Maekawa N, Saito K, Seishima M, Nabeshima T (2002) CREB phosphorylation as a molecular marker of memory processing in the hippocampus for spatial learning. Behav Brain Res 133(2):135-141 (Pubitemid 34754389)
26. Murray EA, Mishkin M (1998) Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J Neurosci 18(16):6568-6582 (Pubitemid 28373258)
27. Oliveira MS, Furian AF, Fighera MR, Fiorenza NG, Ferreira J, Rubin MA, Mello CF, Royes LF (2008) The involvement of the polyamines binding sites at the NMDA receptor in creatineinduced spatial learning enhancement. Behav Brain Res 187(1): 200-204 (Pubitemid 350216199)
28. Paxinos G, Watson C, Pennisi M, Topple A (1985) Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J Neurosci Methods 13(2): 139-143 (Pubitemid 15008633)
29. Persky AM, Brazeau GA (2001) Clinical pharmacology of the dietary supplement creatine monohydrate. Pharmacol Rev 53(2): 161-176 (Pubitemid 32476115)
30. Porte Y, Buhot MC, Mons NE (2008) Spatial memory in the Morris water maze and activation of cyclic AMP response elementbinding (CREB) protein within the mouse hippocampus. Learn Mem 15(12):885-894
31. Rae C, Digney AL, McEwan SR, Bates TC (2003) Oral creatine monohydrate supplementation improves brain performance: A double-blind, placebo-controlled, cross-over trial. Proc Biol Sci 270(1529):2147-2150 (Pubitemid 37289881)
32. Rodrigues SM, Farb CR, Bauer EP, LeDoux JE, Schafe GE (2004) Pavlovian fear conditioning regulates Thr286 autophosphorylation of Ca2 ?/calmodulin-dependent protein kinase II at lateral amygdala synapses. J Neurosci 24(13):3281-3288 (Pubitemid 38451894)
33. Romero-Calvo I, Ocon B, Martinez-Moya P, Suarez MD, Zarzuelo A, Martinez-Augustin O, de Medina FS (2010) Reversible Ponceau staining as a loading control alternative to actin in Western blots. Anal Biochem 401(2):318-320
34. Rongo C (2002) A fresh look at the role of CaMKII in hippocampal synaptic plasticity and memory. BioEssays 24(3):223-233 (Pubitemid 34248688)
35. Rubin MA, Jurach A, Zanolla GR, Boemo RL, Souza DO, de Mello CF (1997) Intrahippocampal GMP administration improves inhibitory avoidance performance through GABAergic and glutamatergic mechanisms in rats. NeuroReport 8(17):3713-3716 (Pubitemid 28004861)
36. Sakimura K, Kutsuwada T, Ito I, Manabe T, Takayama C, Kushiya E, Yagi T, Aizawa S, Inoue Y, Sugiyama H et al (1995) Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit. Nature 373(6510):151-155
37. Sharifzadeh M, Sharifzadeh K, Naghdi N, Ghahremani MH, Roghani A (2005) Posttraining intrahippocampal infusion of a protein kinase AII inhibitor impairs spatial memory retention in rats. J Neurosci Res 79(3):392-400 (Pubitemid 40278354)
38. Silva AJ, Paylor R, Wehner JM, Tonegawa S (1992) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257(5067):206-211
39. Tan SE, Liang KC (1996) Spatial learning alters hippocampal calcium/calmodulin-dependent protein kinase II activity in rats. Brain Res 711(1-2):234-240
40. Todd Roach J, Volmar CH, Dwivedi S, Town T, Crescentini R, Crawford F, Tan J, Mullan M (2004) Behavioral effects of CD40-CD40L pathway disruption in aged PSAPP mice. Brain Res 1015(1-2):161-168 (Pubitemid 38829750)
41. Tokumitsu H, Inuzuka H, Ishikawa Y, Ikeda M, Saji I, Kobayashi R (2002) STO-609, a specific inhibitor of the Ca(2?)/calmodulindependent protein kinase kinase. J Biol Chem 277(18): 15813-15818 (Pubitemid 34967859)
42. Trifilieff P, Herry C, Vanhoutte P, Caboche J, Desmedt A, Riedel G, Mons N, Micheau J (2006) Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learn Mem 13(3):349-358 (Pubitemid 43830682)
43. Valenzuela MJ, Jones M, Wen W, Rae C, Graham S, Shnier R, Sachdev P (2003) Memory training alters hippocampal neurochemistry in healthy elderly. Neuroreport 14(10):1333-1337 (Pubitemid 36936720)
44. Vazquez SI, Vazquez A, Pena de Ortiz S (2000) Different hippocampal activity profiles for PKA and PKC in spatial discrimination learning. Behav Neurosci 114(6):1109-1118 (Pubitemid 32001890)
45. Vianna MR, Izquierdo LA, Barros DM, Medina JH, Izquierdo I (1999) Intrahippocampal infusion of an inhibitor of protein kinase A separates short-from long-term memory. Behav Pharmacol 10(2):223-227 (Pubitemid 29150042)
46. Vianna MR, Izquierdo LA, Barros DM, Ardenghi P, Pereira P, Rodrigues C, Moletta B, Medina JH, Izquierdo I (2000) Differential role of hippocampal cAMP-dependent protein kinase in short-And long-term memory. Neurochem Res 25(5):621-626 (Pubitemid 30421995)
47. Watanabe A, Kato N, Kato T (2002) Effects of creatine on mental fatigue and cerebral hemoglobin oxygenation. Neurosci Res 42(4):279-285 (Pubitemid 34414988)
48. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ (2004) Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 24(26):5901-5908 (Pubitemid 38859387)
49. Winters BD, Saksida LM, Bussey TJ (2008) Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci Biobehav Rev 32(5):1055-1070
50. Wyss M, Kaddurah-Daouk R (2000) Creatine and creatinine metabolism. Physiol Rev 80(3):1107-1213 (Pubitemid 30452013)
51. Zola-Morgan S, Squire LR, Alvarez-Royo P, Clower RP (1991) Independence of memory functions and emotional behavior: separate contributions of the hippocampal formation and the amygdala. Hippocampus 1(2):207-220