Neuroprotective effects of curcumin and apocynin on spatial memory performance in an animal model of acute neuroinflammation / Efeitos neuroprotetores de curcumina e apocinina sobre o desempenho em memória espacial em modelo animal de neuroinflamação aguda

Authors

  • Paola Fernanda de Souza
  • Maria Vaitsa L. Haskel
  • Elizama de Gregório
  • Daniele de Paula
  • Emilaynne R. Bensberg
  • Carlos Ricardo M. Malfatti
  • Juliana Sartori Bonini
  • Weber Cláudio da Silva

DOI:

https://doi.org/10.34117/bjdv7n4-521

Keywords:

Neuroinflammation, Curcumin, Apocynin, Cognition, Spatial Memory.

Abstract

Neuroinflammation is closely related to the etiology of several neurological/neurodegenerative diseases. These disorders cause cognitive impairment and sensitization of the immune system to internal and/or external stimuli. This work aims to evaluate the neuroprotective effects of the phytochemical compounds curcumin and apocynin on the spatial memory of rats in a model of acute neuroinflammation. For this, the study was divided into two phases. First, the dose of lipopolysaccharide (LPS) able to cause neuroinflammation and consequently mnemonic damage to the animals was tested. In the second phase, the neuroprotective effect of curcumin and apocynin was assessed. At two days after the surgery, the treatment with curcumin 50 mg/kg dissolved in vegetable oil was administered by gavage to saline + curcumin and LPS + curcumin groups. On the same day, animals from groups saline + apocynin and LPS + apocynin received by gavage apocynin 50 mg/kg suspended in distilled water. Rats of saline + vehicle and LPS + vehicle groups received vegetable oil or distilled water. The gavage treatment was given for 30 days for all groups. The spatial memory evaluation was assessed by Morris Water Maze (MWM) task, performed 30 days after the surgery in the first phase of the study and 1 day after the last gavage treatment in the second phase, both for 5 consecutive days. The MWM test trial was conducted 24 hours after the last training session. We found that the intra-hippocampal infusion of LPS, performed 30 days before training in the MWW task, impaired the retention of spatial memory acquired in this task. It also caused histopathological alterations in the infusion region, which are compatible with both acute and chronic neuroinflammation. Oral administration of apocynin, but not curcumin, reversed the mnemonic deficit and mitigated the histopathological alterations caused by the intra-hippocampal infusion of LPS.

References

Akaishi, T., & Abe, K. (2017). CNB-001, a synthetic pyrazole derivative of curcumin, suppresses lipopolysaccharide-induced nitric oxide production through the inhibition of NF-?B and p38 MAPK pathways in microglia. European Journal of Pharmacology. doi:10.1016/j.ejphar.2017.12.008

Bassani, T. B., Turnes, J. M., Moura, E. L., Bonato, J. M., Cóppola-Segovia, V., Zanata, S. M., Oliveira, R. M., & Vital, M. A. (2017). Effects of curcumin on short-term spatial and recognition memory, adult neurogenesis and neuroinflammation in a streptozotocin-induced rat model of dementia of Alzheimer’s type. Behavioural Brain Research, 335, 41-54. doi:10.1016/j.bbr.2017.08.014

Baufeld, C., O’Loughlin, E., Calcagno, N., Madore, C., & Butovsky, O. (2017). Differential contribution of microglia and monocytes in neurodegenerative diseases. Journal of Neural Transmission, 1-18. doi:10.1007/s00702-017-1795-7

Bonini, J.S., Da Silva, W.C., Bevilaqua, L.R.M., Medina, J.H., Izquierdo, I., Cammarota, M. (2007). On the participation of hippocampal pkc in acquisition, consolidation and reconsolidation of spatial memory. Neuroscience 147, 37-45. doi:10.1016/j.neuroscience.2007.04.013

Feng, Y., Cui, C., Liu, X., Wu, Q., Hu, F., Ma, Z., Zhang, H., & Wang, L. (2017). Protective Role of Apocynin via Suppression of Neuronal Autophagy and TLR4/NF-?B Signaling Pathway in a Rat Model of Traumatic Brain Injury. Neurochemical Research, 42(11), 3296-3309. doi:10.1007/s11064-017-2372-z

Hosseini, A., Razavi, B. M., & Hosseinzadeh, H. (2017). Pharmacokinetic Properties of Saffron and its Active Components. European Journal of Drug Metabolism and Pharmacokinetics. doi:10.1007/s13318-017-0449-3

Hou, L., Wang, K., Zhang, C., Sun, F., Che, Y., Zhao, X., Zhang, D., Li, H., & Wang, Q. (2018). Complement receptor 3 mediates NADPH oxidase activation and dopaminergic neurodegeneration through a Src-Erk-dependent pathway. Redox Biology, 14, 250-260. doi:10.1016/j.redox.2017.09.017

Hui-Guo, L., Kui, L., Yan-Ning, Z., & Yong-Jian, X. (2010). Apocynin attenuate spatial learning deficits and oxidative responses to intermittent hypoxia. Sleep Medicine, 11(2), 205-212. doi:10.1016/j.sleep.2009.05.015

Jin, M., Park, S.Y., Shen, Q., Lai, Y., Ou, X., Mao, Z. Lin, D., Yu, Y., & Zhang, W. (2018). Anti-neuroinflammatory effect of curcumin on Pam3CSK4-stimulated microglial cells. International Journal of Molecular Medicine, 41, 521-530. https://doi.org/10.3892/ijmm.2017.3217

Kapoor, M., Sharma, N., Sandhir, R., & Nehru, B. (2018). Effect of the NADPH oxidase inhibitor apocynin on ischemia-reperfusion hippocampus injury in rat brain. Biomedicine & Pharmacotherapy, 97, 458-472. doi:10.1016/j.biopha.2017.10.123

Kaur, H., Patro, I., Tikoo, K., & Sandhir, R. (2015). Curcumin attenuates inflammatory response and cognitive deficits in experimental model of chronic epilepsy. Neurochemistry International, 89, 40-50. doi:10.1016/j.neuint.2015.07.009

Kim, J., & Kang, T. (2017). P47Phox/CDK5/DRP1-Mediated Mitochondrial Fission Evokes PV Cell Degeneration in the Rat Dentate Gyrus Following Status Epilepticus. Frontiers in Cellular Neuroscience, 11. doi:10.3389/fncel.2017.00267

Kishida, K. T., Hoeffer, C. A., Hu, D., Pao, M., Holland, S. M., & Klann, E. (2006). Synaptic Plasticity Deficits and Mild Memory Impairments in Mouse Models of Chronic Granulomatous Disease. Molecular and Cellular Biology, 26(15), 5908-5920. doi:10.1128/mcb.00269-06

Ma, M. W., Wang, J., Zhang, Q., Wang, R., Dhandapani, K. M., Vadlamudi, R. K., & Brann, D. W. (2017). NADPH oxidase in brain injury and neurodegenerative disorders. Molecular Neurodegeneration, 12(1). doi:10.1186/s13024-017-0150-7

Molteni, M., & Rossetti, C. (2017). Neurodegenerative diseases: The immunological perspective. Journal of Neuroimmunology, 313, 109-115. doi:10.1016/j.jneuroim.2017.11.002

Neal, M., & Richardson, J. R. (2018). Epigenetic regulation of astrocyte function in neuroinflammation and neurodegeneration. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1864(2), 432-443. doi:10.1016/j.bbadis.2017.11.004

Poulose, S. M., Miller, M. G., Scott, T., & Shukitt-Hale, B. (2017). Nutritional Factors Affecting Adult Neurogenesis and Cognitive Function. Advances in Nutrition, 8, 804-811. doi:10.3945/an.117.016261

Radtke, F. A., Chapman, G., Hall, J., & Syed, Y. A. (2017). Modulating Neuroinflammation to Treat Neuropsychiatric Disorders. BioMed Research International, 2017, 5071786. http://doi.org/10.1155/2017/5071786

Rajasekar, N., Dwivedi, S., Tota, S. K., Kamat, P. K., Hanif, K., Nath, C., & Shukla, R. (2013). Neuroprotective effect of curcumin on okadaic acid induced memory impairment in mice. European Journal of Pharmacology, 715(1-3), 381-394. doi:10.1016/j.ejphar.2013.04.033

Ravelli, K. G., Rosário, B. D., Vasconcelos, A. R., Scavone, C., Camarini, R., Hernandes, M. S., & Britto, L. R. (2017). NADPH oxidase contributes to streptozotocin-induced neurodegeneration. Neuroscience, 358, 227-237. doi:10.1016/j.neuroscience.2017.06.050

Sarkar, S., Malovic, E., Harishchandra, D. S., Ghaisas, S., Panicker, N., Charli, A., Palanisamy, B. N., Rokad, D., Jin, H., Anantharam, V., & Kanthasamy, A. G. (2017). Mitochondrial impairment in microglia amplifies NLRP3 inflammasome proinflammatory signaling in cell culture and animal models of Parkinson’s disease. Npj Parkinsons Disease, 3(1). doi:10.1038/s41531-017-0032-2

Seo, E., Fischer, N., & Efferth, T. (2017). Phytochemicals as inhibitors of NF-?B for treatment of Alzheimer’s disease. Pharmacological Research. doi:10.1016/j.phrs.2017.11.030

Sevastre-Berghian, A. C., F?g?r?san, V., Toma, V. A., Bâldea, I., Olteanu, D., Moldovan, R., Decea, N., Filip, G. A., & Clichici, S. V. (2017). Curcumin Reverses the Diazepam-Induced Cognitive Impairment by Modulation of Oxidative Stress and ERK 1/2/NF-?B Pathway in Brain. Oxidative Medicine and Cellular Longevity, 2017, 1-16. doi:10.1155/2017/3037876

Sorce, S., Stocker, R., Seredenina, T., Holmdahl, R., Aguzzi, A., Chio, A., Depaulis, A., Heitz, F., Olofsson, P., Olsson, T. and Duveau, V., Sanoudou, D., Skosgater, S., Vlahou, A., Wasquel, D., Krause, K-H., & Jaquet, V. (2017). NADPH oxidases as drug targets and biomarkers in neurodegenerative diseases: What is the evidence? Free Radical Biology and Medicine, 112, 387-396. doi:10.1016/j.freeradbiomed.2017.08.006

Sundaram, J. R., Poore, C. P., Sulaimee, N. H., Pareek, T., Cheong, W. F., Wenk, M. R., Pant, H. C., Frautschy, S. A., Low, C. M., & Kesavapany, S. (2017). Curcumin Ameliorates Neuroinflammation, Neurodegeneration, and Memory Deficits in p25 Transgenic Mouse Model that Bears Hallmarks of Alzheimer’s Disease. Journal of Alzheimers Disease, 60(4), 1429-1442. doi:10.3233/jad-170093

Tanriverdi, L. H., Parlakpinar, H., Ozhan, O., Ermis, N., Polat, A., Vardi, N., Tanbek, K., Yildiz, A., & Acet, A. (2017). Inhibition of NADPH oxidase by apocynin promotes myocardial antioxidant response and prevents isoproterenol-induced myocardial oxidative stress in rats. Free Radical Research, 51(9-10), 772-786. doi:10.1080/10715762.2017.1375486

The Rat Brain in Stereotaxic Coordinates. (1982). doi:10.1016/c2009-0-63235-9

Ullah, F., Liang, A., Rangel, A., Gyengesi, E., Niedermayer, G., & Münch, G. (2017). High bioavailability curcumin: an anti-inflammatory and neurosupportive bioactive nutrient for neurodegenerative diseases characterized by chronic neuroinflammation. Archives of Toxicology, 91(4), 1623-1634. doi:10.1007/s00204-017-1939-4

Zhang, J., Malik, A., Choi, H., Ko, R., Dissing-Olesen, L., & Macvicar, B. (2014). Microglial CR3 Activation Triggers Long-Term Synaptic Depression in the Hippocampus via NADPH Oxidase. Neuron, 82(1), 195-207. doi:10.1016/j.neuron.2014.01.043

Published

2021-04-20

How to Cite

Souza, P. F. de, Haskel, M. V. L., Gregório, E. de, Paula, D. de, Bensberg, E. R., Malfatti, C. R. M., Bonini, J. S., & Silva, W. C. da. (2021). Neuroprotective effects of curcumin and apocynin on spatial memory performance in an animal model of acute neuroinflammation / Efeitos neuroprotetores de curcumina e apocinina sobre o desempenho em memória espacial em modelo animal de neuroinflamação aguda. Brazilian Journal of Development, 7(4), 40975–40992. https://doi.org/10.34117/bjdv7n4-521

Issue

Section

Original Papers