Paradoxical role of PKA inhibitor on amyloidβ-induced memory deficit

Physiology and Behavior

Volumn 149, Issue , 2015, Pages 76-85

  Amini, Elham ^a   Nassireslami, Ehsan ^a   Payandemehr, Borna ^a   Khodagholi, Fariba ^b   Foolad, Forough ^b   Khalaj, Sara ^a   Hamedani, Mostafa Pirali ^a   Azimi, Leyla ^a   Sharifzadeh, Mohammad ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Alzheimer's disease; Caspase 3; Fear conditioning; NF B; P CREB; Protein kinase A inhibitor

Indexed keywords

AMYLOID BETA PROTEIN; CASPASE 3; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; TRANSCRIPTION FACTOR NRF2; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; ISOQUINOLINE DERIVATIVE; N-(2-(4-BROMOCINNAMYLAMINO)ETHYL)-5-ISOQUINOLINESULFONAMIDE; NFE2L2 PROTEIN, RAT; SULFONAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FEAR; HIPPOCAMPAL CA1 REGION; LOW DRUG DOSE; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; STEREOTAXIC SURGERY; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CATALEPSY; CHEMICALLY INDUCED; CONDITIONED REFLEX; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; MALE; MEMORY DISORDERS; METABOLISM; TIME; WISTAR RAT;

AMYLOID BETA-PEPTIDES; ANIMALS; CASPASE 3; CONDITIONING, CLASSICAL; CREB-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEAR; FREEZING REACTION, CATALEPTIC; HEME OXYGENASE-1; ISOQUINOLINES; MALE; MEMORY DISORDERS; NF-E2-RELATED FACTOR 2; RATS; RATS, WISTAR; SULFONAMIDES; TIME FACTORS;

EID: 84930648970     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2015.05.029     Document Type: Article

References (67)

1. Koffie R.M., Hyman B.T., Spires-Jones T.L. Alzheimer's disease: synapses gone cold. Mol. Neurodegener. 2011, 6:63.
2. Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
3. Shankar G.M., Walsh D.M. Alzheimer's disease: synaptic dysfunction and Aβ. Mol. Neurodegener. 2009, 4:48.
4. Zola-Morgan S., Squire L.R., Amaral D.G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 1986, 6:2950-2967.
5. Abel T., Nguyen P.V. Regulation of hippocampus-dependent memory by cyclic AMP-dependent protein kinase. Prog. Brain Res. 2008, 169:97-115.
6. Michel M., Kemenes I., Muller U., Kemenes G. Different phases of long-term memory require distinct temporal patterns of PKA activity after single-trial classical conditioning. Learn. Mem. 2008, 15:694-702.
7. Schafe G.E., Atkins C.M., Swank M.W., Bauer E.P., Sweatt J.D., LeDoux J.E. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J Neurosci 2000, 20:8177-8187.
8. Eftekharzadeh B., Ramin M., Khodagholi F., Moradi S., Tabrizian K., Sharif R., Azami K., Beyer C., Sharifzadeh M. Inhibition of PKA attenuates memory deficits induced by beta-amyloid (1-42), and decreases oxidative stress and NF-kappaB transcription factors. Behav. Brain Res. 2012, 226:301-308.
9. Khorshidahmad T., Tabrizian K., Vakilzadeh G., Nikbin P., Moradi S., Hosseini-Sharifabad A., Roghani A., Naghdi N., Sharifzadeh M. Interactive effects of a protein kinase AII inhibitor and testosterone on spatial learning in the Morris water maze. Behav. Brain Res. 2012, 228:432-439.
10. Lochner A., Moolman J.A. The many faces of H89: a review. Cardiovasc Drug Rev 2006, 24:261-274.
11. Ghosh A., Greenberg M.E. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 1995, 268:239-247. New York, N.Y.
12. Deisseroth K., Bito H., Tsien R.W. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 1996, 16:89-101.
13. Gonzalez G.A., Montminy M.R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989, 59:675-680.
14. Impey S., Obrietan K., Storm D.R. Making new connections: role of ERK/MAP kinase signaling in neuronal plasticity. Neuron 1999, 23:11-14.
15. Roberson E.D., English J.D., Adams J.P., Selcher J.C., Kondratick C., Sweatt J.D. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 1999, 19:4337-4348.
16. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., Oyake T., Hayashi N., Satoh K., Hatayama I., Yamamoto M., Nabeshima Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 1997, 236:313-322.
17. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999, 13:76-86.
18. Abraham N.G., Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol. Rev. 2008, 60:79-127.
19. Pappolla M.A., Chyan Y.J., Omar R.A., Hsiao K., Perry G., Smith M.A., Bozner P. Evidence of oxidative stress and in vivo neurotoxicity of beta-amyloid in a transgenic mouse model of Alzheimer's disease: a chronic oxidative paradigm for testing antioxidant therapies in vivo. Am J Pathol 1998, 152:871-877.
20. Zandi E., Rothwarf D.M., Delhase M., Hayakawa M., Karin M. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 1997, 91:243e252.
21. Ellis H.M., Horvitz H.R. Genetic control of programmed cell death in the nematode C. elegans. Cell 1986, 44:817-829.
22. Porter A.G., Janicke R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999, 6:99-104.
23. Yuan J., Shaham S., Ledoux S., Ellis H.M., Horvitz H.R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 1993, 75:641-652.
24. D'Amelio M., Cavallucci V., Middei S., Marchetti C., Pacioni S., Ferri A., Diamantini A., De Zio D., Carrara P., Battistini L., Moreno S., Bacci A., Ammassari-Teule M., Marie H., Cecconi F. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat. Neurosci. 2011, 14:69-76.
25. de Calignon A., Fox L.M., Pitstick R., Carlson G.A., Bacskai B.J., Spires-Jones T.L., Hyman B.T. Caspase activation precedes and leads to tangles. Nature 2010, 464:1201-1204.
26. Maren S. Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. 2001, 24:897-931.
27. Maren S. Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. Eur. J. Neurol. 2008, 28:1661-1666.
28. Bradford M.A. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
29. 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 1997, 88:615-626.
30. Bourtchouladze R., Abel T., Berman N., Gordon R., Lapidus K., Kandel E.R. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn. Mem. 1998, 5:365-374.
31. Lynch M.A. Long-term potentiation and memory. Physiol. Rev. 2004, 84:87-136.
32. Mondragón-Rodríguez S., Perry G., Zhu X., Boehm J. Amyloid beta and tau proteins as therapeutic targets for Alzheimer's disease treatment: rethinking the current strategy. Int. J. Alzheimers Dis. 2012, 2012:630182.
33. Zhang H., Gong B., Liu S., Fa M., Ninan I., Staniszewski A., Arancio O. Synaptic fatigue is more pronounced in the APP/PS1 transgenic mouse model of Alzheimer's disease. Curr Alzheimer Res 2005, 2:137-140.
34. Wang H.Y., Lee D.H., Davis C.B., Shank R.P. Amyloid peptide Abeta(1-42) binds selectively and with picomolar affinity to alpha7 nicotinic acetylcholine receptors. J. Neurochem. 2000, 75:1155-1161.
35. Su Y., Ryder J., Ni B. Inhibition of A[beta] production and APP maturation by a specific PKA inhibitor. FEBS Lett. 2003, 546:407-410.
36. Ran I., Laplante I., Lacaille J.C. CREB-dependent transcriptional control and quantal changes in persistent long-term potentiation in hippocampal interneurons. J Neurosci 2012, 32:6335-6350.
37. Yin J.C., Tully T. CREB and the formation of long-term memory. Curr. Opin. Neurobiol. 1996, 6:264-268.
38. Porte Y., Buhot M.C., Mons N.E. Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus. Learn. Mem. 2008, 15:885-894.
39. Vitolo O.V., Sant'Angelo A., Costanzo V., Battaglia F., Arancio O., Shelanski M. Amyloid beta -peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13217-13221.
40. Barlow C.A., Kitiphongspattana K., Siddiqui N., Roe M.W., Mossman B.T., Lounsbury K.M. Protein kinase A-mediated CREB phosphorylation is an oxidant-induced survival pathway in alveolar type II cells. Apoptosis 2008, 13:681-692.
41. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 1998, 21:869-883.
42. Daniels W.M., Hendricks J., Salie R., Taljaard J.J. The role of the MAP-kinase superfamily in beta-amyloid toxicity. Metab. Brain Dis. 2001, 16:175-185.
43. Ma Q.L., Harris-White M.E., Ubeda O.J., Simmons M., Beech W., Lim G.P., Teter B., Frautschy S.A., Cole G.M. Evidence of Abeta- and transgene-dependent defects in ERK-CREB signaling in Alzheimer's models. J. Neurochem. 2007, 103:1594-1607.
44. Axelsen P.H., Komatsu H., Murray I.V.J. Oxidative stress and cell membranes in the pathogenesis of Alzheimer's disease. Physiology 2011, 26:54-69.
45. Calkins M.J., Johnson D.A., Townsend J.A., Vargas M.R., Dowell J.A., Williamson T.P., Kraft A.D., Lee J.M., Li J., Johnson J.A. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid. Redox Signal. 2009, 11:497-508.
46. Kanninen K., Malm T.M., Jyrkkanen H.K., Goldsteins G., Keksa-Goldsteine V., Tanila H., Yamamoto M., Yla-Herttuala S., Levonen A.L., Koistinaho J. Nuclear factor erythroid 2-related factor 2 protects against beta amyloid. Mol. Cell. Neurosci. 2008, 39:302-313.
47. Kanninen K., Heikkinen R., Malm T., Rolova T., Kuhmonen S., Leinonen H., Yla-Herttuala S., Tanila H., Levonen A.L., Koistinaho M., Koistinaho J. Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:16505-16510.
48. Tomobe K., Shinozuka T., Kuroiwa M., Nomura Y. Age-related changes of Nrf2 and phosphorylated GSK-3beta in a mouse model of accelerated aging (SAMP8). Arch. Gerontol. Geriatr. 2012, 54:e1-e7.
49. Wruck C.J., Gotz M.E., Herdegen T., Varoga D., Brandenburg L.O., Pufe T. Kavalactones protect neural cells against amyloid beta peptide-induced neurotoxicity via extracellular signal-regulated kinase 1/2-dependent nuclear factor erythroid 2-related factor 2 activation. Mol. Pharmacol. 2008, 73:1785-1795.
50. Zhang J., Hosoya T., Maruyama A., Nishikawa K., Maher J.M., Ohta T., Motohashi H., Fukamizu A., Shibahara S., Itoh K., Yamamoto M. Nrf2 Neh5 domain is differentially utilized in the transactivation of cytoprotective genes. Biochem. J. 2007, 404:459-466.
51. Itoh K., Mimura J., Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid. Redox Signal. 2010, 13:1665-1678.
52. Ghattas M.H., Chuang L.T., Kappas A., Abraham N.G. Protective effect of HO-1 against oxidative stress in human hepatoma cell line (HepG2) is independent of telomerase enzyme activity. Int. J. Biochem. Cell Biol. 2002, 34:1619-1628.
53. Poss K.D., Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:10925-10930.
54. Smith M.A., Perry G., Richey P.L., Sayrec L.M., Anderson V.E., Beal M.F., Kowall N. Oxidative damage in Alzheimer's. Nature 1996, 382:120-121.
55. Olszanecki R., Rezzani R., Omura S., Stec D.E., Rodella L., Botros F.T., Goodman A.I., Drummond G., Abraham N.G. Genetic suppression of HO-1 exacerbates renal damage: reversed by an increase in the antiapoptotic signaling pathway. Am. J. Physiol. Ren. Physiol. 2007, 292:F148-F157.
56. Krönke G., Bochkov V.N., Huber J., Gruber F., Blüml S., Fürnkranz A., Kadl A., Binder B.R., Leitinger N. Oxidized phospholipids induce expression of human heme oxygenase-1 involving activation of cAMP-responsive element-binding protein. J BiolChem 2003, 278:51006-51014.
57. Lee B., Cao R., Choi Y.S., Cho H.Y., Rhee A.D., Hah C.K., Hoyt K.R., Obrietan K. The CREB/CRE transcriptional pathway: protection against oxidative stress-mediated neuronal cell death. J. Neurochem. 2009, 108:1251-1265.
58. Elbirt K.K., Bonkovsky H.L. Heme oxygenase: recent advances in understanding its regulation and role. Proc. Assoc. Am. Physicians 1999, 111:438-447.
59. Lavrovsky Y., Schwartzman M.L., Levere R.D., Kappas A., Abraham N.G. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:5987-5991.
60. Kaltschmidt B., Kaltschmidt C. NF-kB in the nervous system. Nuclear factor kB: regulation and role in disease 2003, 373.
61. Kaltschmidt B., Uherek M., Volk B., Baeuerle P.A., Kaltschmidt C. Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:2642-2647.
62. Koistinaho J., Malm T., Goldsteins G. Glycogen synthase kinase-3beta: a mediator of inflammation in Alzheimer's disease?. Int. J. Alzheimers Dis. 2011, 2011:129753.
63. Mincheva-Tasheva S., Soler R.M. NF-κB signaling pathways: role in nervous system physiology and pathology. Neuroscientist 2013, 19:175-194.
64. Terwel D., Muyllaert D., Dewachter I., Borghgraef P., Croes S., Devijver H., Van Leuven F. Amyloid activates GSK-3beta to aggravate neuronal tauopathy in bigenic mice. Am J Pathol 2008, 172:786-798.
65. Fang X., Yu S.X., Lu Y., Bast R.C., Woodgett J.R., Mills G.B. Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase a. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11960-11965.
66. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 2000, 351:95-105.
67. Gholizadeh S., Tharmalingam S., MacAldaz M.E., Hampson D.R. Transduction of the central nervous system after intracerebroventricular injection of adeno-associated viral vectors in neonatal and juvenile mice. Human Gene Therapy Methods. 2013, 24:205-213.