eISSN: 1509-572x
ISSN: 1641-4640
Folia Neuropathologica
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SCImago Journal & Country Rank
1/2018
vol. 56
 
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abstract:
Original paper

Interactive involvement of hippocampal cAMP/PKA and cyclooxygenase-2 signaling pathways in spatial learning in the Morris water maze

Kaveh Tabrizian, Mahmoud Hashemzaei, Ali Akbar Nasiri, Sheyda Najafi, Fatemeh Amelinia, Mehdi Sanati, Farzaneh Shamshirgaran, Sahar Fanoudi

Folia Neuropathol 2018; 56 (1): 58-66
Online publish date: 2018/03/28
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Introduction
Accumulated evidence shows that the cAMP-PKA signaling pathway plays a key role in memory functions. Cyclooxygenase-2, a critical player in neuroinflammation, has been confirmed in the pathogenesis of neurodegenerative diseases. This study is aimed to assess the effect of the interaction of cAMP-PKA and cyclooxygenase pathways on spatial memory acquisition in animal models.

Material and methods
In the present study, the effects of the four-day bilateral intra-hippocampal infusions of H-89 as a protein kinase AII inhibitor (10 µM/side), celecoxib (0.1 M/side) as a selective cyclooxygenase-2 inhibitor, cele­coxib/H-89 and bucladesine (10 µM/side)/celecoxib/H-89 on spatial memory acquisition in the Morris water maze were investigated. Control animals received bilateral intra-hippocampal infusions of dimethyl sulfoxide. Rats were trained for 4 days; each day included one block of four trials. Post-training probe trial tests were performed on day five.

Results
A bilateral intra-hippocampal infusion of H-89 and celecoxib led to a significant impairment in spatial learning compared to the controls through a notable decrease in escape latency and traveled distance. But, combination treatment of animals with celecoxib/H-89 and bucladesine/celecoxib/H-89 could considerably reverse celecoxib and H-89-induced spatial memory acquisition impairments in the Morris water maze.

Conclusions
These results indicate the probable regulatory effects of cAMP/PKA and cyclooxygenase-2 signaling pathways on spatial memory acquisition in the Morris water maze.

keywords:

COX-2, cAMP/PKA, Morris water maze, spatial memory acquisition, hippocampus

references:
Andrade C, Singh NM, Thyagarajan S, Nagaraja N, Rao NSK, Chandra JS. Possible glutamatergic and lipid signalling mechanisms in ECT-induced retrograde amnesia: experimental evidence for involvement of COX-2, and review of literature. J Psychiat Res 2008; 42: 837-850.
Azami K, Etminani M, Tabrizian K, Salar F, Belaran M, Hosseini A, Hosseini-Sharifabad A, Sharifzadeh M. The quantitative evaluation of cholinergic markers in spatial memory improvement induced by nicotine–bucladesine combination in rats. Eur J Pharmacol 2010; 636: 102-107.
Azami K, Tabrizian K, Hosseini R, Seyedabadi M, Shariatpanahi M, Noorbakhsh F, Kebriaeezadeh A, Ostad SN, Sharifzadeh M. Nicotine attenuates spatial learning deficits induced by sodium metavanadate. Neurotoxicology 2012; 33: 44-52.
Azimi L, Kachooeian M, Khodagholi F, Yans A, Heysieattalab S, Vakilzadeh G, Vosoughi N, Sanati M, Taghizadeh G, Sharifzadeh M. Protective effects of salicylate on PKA inhibitor (H-89)-induced spatial memory deficit via lessening autophagy and apoptosis in rats. Pharmacol Biochem Be 2016; 150: 158-169.
Cao Y, Prescott SM. Many actions of cyclooxygenase-2 in cellular dynamics and in cancer. J Cell Physiol 2002; 190: 279-286.
Chen C, Magee JC, Bazan NG. Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity. J Neurophysiol 2002; 87: 2851-2857.
Cowley T, Fahey B, O’Mara S. COX-2, but not COX-1, activity is necessary for the induction of perforant path long-term potentiation and spatial learning in vivo. Eur J Neurosci 2008; 27: 2999-3008.
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.
George P, Charles W. The rat brain in stereotaxic coordinates. Qingchuan Zhuge translate (People’s Medical Publishing House, Beijing, China, 2007) 1998; 32.
Gopez JJ, Yue H, Vasudevan R, Malik AS, Fogelsanger LN, Lewis S, Panikashvili D, Shohami E, Jansen SA, Narayan RK. Cyclooxygenase-2-specific inhibitor improves functional outcomes, provides neuroprotection, and reduces inflammation in a rat model of traumatic brain injury. Neurosurgery 2005; 56: 590-604.
Greenamyre JT, Porter R. Anatomy and physiology of glutamate in the CNS. Neurology 1994; 44: S7-13.
Guerra GP, Mello CF, Bochi GV, Pazini AM, Fachinetto R, Dutra RC, Calixto JB, Ferreira J, Rubin MA. Hippocampal PKA/CREB pathway is involved in the improvement of memory induced by spermidine in rats. Neurobiol Learn Mem 2011; 96: 324-332.
Hewett SJ, Bell SC, Hewett JA. Contributions of cyclooxygenase-2 to neuroplasticity and neuropathology of the central nervous system. Pharmacol Therapeut 2006; 112: 335-357.
Inoue H, Hase K, Segawa A, Takita T. H89 (N-[2-p-bromocinnamylamino-ethyl]-5-isoquinolinesulphonamide) induces autophagy independently of protein kinase A inhibition. Eur J Pharmacol 2013; 714: 170-177.
Jiang J, Dingledine R. Prostaglandin receptor EP2 in the crosshairs of anti-inflammation, anti-cancer, and neuroprotection. Trends Pharmacol Sci 2013; 34: 413-423.
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.
Lin TY, Lu CW, Wang CC, Huang SK, Wang SJ. Cyclooxygenase 2 inhibitor celecoxib inhibits glutamate release by attenuating the PGE2/EP2 pathway in rat cerebral cortex endings. J Pharmacol Exp Ther 2014; 351: 134-145
Luo Y, Kuang S, Li H, Ran D, Yang J. cAMP/PKA-CREB-BDNF signaling pathway in hippocampus mediates cyclooxygenase 2-induced learning/memory deficits of rats subjected to chronic unpredictable mild stress. Oncotarget 2017; 8: 35558.
Millán C, Sánchez-Prieto J. Differential coupling of N- and P/Q-type calcium channels to glutamate exocytosis in the rat cerebral cortex. Neurosci Lett 2002; 330: 29-32.
Murray H, O’Connor J. A role for COX-2 and p38 mitogen activated protein kinase in long-term depression in the rat dentate gyrus in vitro. Neuropharmacology 2003; 44: 374-380.
Najafi S, Payandemehr B, Tabrizian K, Shariatpanahi M, Nassireslami E, Azami K, Mohammadi M, Asadi F, Roghani A, Sharif­zadeh M. The role of nitric oxide in the PKA inhibitor induced spatial memory deficits in rat: involvement of choline acetyltransferase. Eur J Pharmacol 2013; 714: 478-485.
Nishiham I, Toshiaki M, Watanabe Y, Ito S, Hayaishi O. Prostaglandin E 2 stimulates glutamate release from synaptosomes of rat spinal cord. Neurosci Lett 1995; 196: 57-60.
O’Neill LA, Kaltschmidt C. NF-B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 1997; 20: 252-258.
Paxinos G, Watson C. The rat brain atlas. Academic Press, San Diego 1986.
Rall JM, Mach SA, Dash PK. Intrahippocampal infusion of a cyclooxygenase-2 inhibitor attenuates memory acquisition in rats. Brain Res 2003; 968: 273-276.
Sharifzadeh M, Naghdi N, Khosrovani S, Ostad SN, Sharifzadeh K, Roghani A. Post-training intrahippocampal infusion of the COX-2 inhibitor celecoxib impaired spatial memory retention in rats. Eur J Pharmacol 2005; 511: 159-166.
Sharifzadeh M, Sharifzadeh K, Naghdi N, Ghahremani MH, Roghani A. Posttraining intrahippocampal infusion of a protein kinase AII inhibitor impairs spatial memory retention in rats. J Neurosci Res 2005; 79: 392-400.
Sharifzadeh M, Tavasoli M, Naghdi N, Ghanbari A, Amini M, Roghani A. Post-training intrahippocampal infusion of nicotine prevents spatial memory retention deficits induced by the cyclo-oxygenase-2-specific inhibitor celecoxib in rats. J Neurochem 2005; 95: 1078-1090.
Sharifzadeh M, Tavasoli M, Soodi M, Mohammadi-Eraghi S, Ghahremani MH, Roghani A. A time course analysis of cyclo­oxygenase-2 suggests a role in spatial memory retrieval in rats. Neurosci Res 2006; 54: 171-179.
Sharifzadeh M, Zamanian A-R, Gholizadeh S, Tabrizian K, Etminani M, Khalaj S, Zarrindast M-R, Roghani A. Post-training intrahippocampal infusion of nicotine–bucladesine combination causes a synergistic enhancement effect on spatial memory retention in rats. Eur J Pharmacol 2007; 562: 212-220.
Shrager Y, Bayley PJ, Bontempi B, Hopkins RO, Squire LR. Spatial memory and the human hippocampus. Proceedings of the National Academy of Sciences 2007; 104: 2961-2966.
Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF. Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 1993; 11: 371-386.
Yang H, Chen C. Cyclooxygenase-2 in synaptic signaling. Curr Pharm Design 2008; 14: 1443.
Yang Y, Gao L. Celecoxib Alleviates Memory Deficits by Downregulation of COX-2 Expression and Upregulation of the BDNF-TrkB Signaling Pathway in a Diabetic Rat Model. J Mol Neurosci 2017; 62: 188-198.
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