Leaf extract of Anacardium occidentale ameliorates biomarkers of neuroinflammation, memory loss, and neurobehavioral deficit in N(ω)-nitro-L-arginine methyl ester (L-NAME) treated rats

References

• Abdel-Salam, E.R., et al., 2017. Nitric oxide synthase inhibitors protect against brain and liver damage caused by acute malathion intoxication. Asian pacific journal of tropical medicine, 10 (8), 773–786.
   PubMed Web of Science ®Google Scholar
• Arshiany, H., et al., 2022. Psychiatric onset alexander disease: an important challenge in neuropsychiatric diagnosis: a case report. Basic and clinical neuroscience, 13 (2), 269–274.
   PubMed Web of Science ®Google Scholar
• Balez, R., and Ooi, L., 2016. Getting to NO Alzheimer’s disease: neuroprotection versus neurotoxicity mediated by nitric oxide. Oxidative medicine and cellular longevity, 2016, 3806157.
   PubMed Web of Science ®Google Scholar
• Baloglu, M., and Atasoy, M.A., 2022. Effect of MCI-186 on lipid peroxidation in experimental traumatic brain damage in rats. Korean journal of neurotrauma, 18 (2), 188–197.
   PubMedGoogle Scholar
• Baluchnejadmojarad, T., Mohamadi-Zarch, S.M., and Roghani, M., 2019. Safranal, an active ingredient of saffron, attenuates cognitive deficits in amyloid β-induced rat model of Alzheimer’s disease: underlying mechanisms. Metabolic brain disease, 34 (6), 1747–1759.
   PubMed Web of Science ®Google Scholar
• Baptista, A., et al., 2018. Antioxidant and antimicrobial activities of crude extracts and fractions of Cashew (Anacardium occidentale L.), Cajui (Anacardium microcarpum), and Pequi (Caryocar brasiliense C.): a systematic review. Oxidative medicine and cellular longevity, 2018, 3753562.
   PubMed Web of Science ®Google Scholar
• Beutler, E., Duron, O., and Kelly, B.M., 1963. Improved method for the determination of blood glutathione. Journal of laboratory clinical medicine, 61, 882–888.
   PubMed Web of Science ®Google Scholar
• Bodhinathan, K., Kumar, A., and Foster, T.C., 2010. Redox sensitive calcium stores underlie enhanced after hyperpolarization of aged neurons: role for ryanodine receptor mediated calcium signaling. Journal of neurophysiology, 104 (5), 2586–2593.
   PubMed Web of Science ®Google Scholar
• Bromley-Brits, K., Deng, Y., and Song, W., 2011. Morris water maze test for learning and memory deficits in Alzheimer’s disease model mice. Journal of visualized experiments, 53, 2920.
   Google Scholar
• Chen, S.D., et al., 2023. Alternative role of glucagon-like Peptide-1 receptor agonists in neurodegenerative diseases. European journal of pharmacology, 938, 175439.
   PubMed Web of Science ®Google Scholar
• Chen, H., et al., 2022. Research progress of targeting neuro-immune inflammation in the treatment of Alzheimer’s disease. Frontiers in bioscience (landmark edition), 27 (11), 312.
   PubMed Web of Science ®Google Scholar
• Chen, K.Z., et al., 2023. Vimentin as a potential target for diverse nervous system diseases. Neural regeneration research, 18 (5), 969–975.
   PubMed Web of Science ®Google Scholar
• Christensen, S.H., et al., 2022. Short-term biological variation of serum glial fibrillary acidic protein. Clinical chemistry and laboratory medicine, 60 (11), 1813–1819.
   PubMed Web of Science ®Google Scholar
• Cifuentes, D., et al., 2017. Inactivation of nitric oxide synthesis exacerbates the development of Alzheimer disease pathology in APPPS1 mice (amyloid precursor protein/presenilin-1). Hypertension (Dallas, Tex. : 1979), 70 (3), 613–623.
   PubMed Web of Science ®Google Scholar
• da Costa, C.D.F., et al., 2018. Hypotensive, vasorelaxant and antihypertensive activities of the hexane extract of Anacardium occidentale Linn. Archives of biological sciences, 70 (3), 459–468.
   Web of Science ®Google Scholar
• de Munter, J., et al., 2021. Increased oxidative stress in the prefrontal cortex as a shared feature of depressive- and PTSD-like syndromes: effects of a standardized herbal antioxidant. Frontiers in nutrition, 8, 661455.
   PubMed Web of Science ®Google Scholar
• de Siqueira, E.A., et al., 2023. Vitamin D3 actions on astrocyte cells: a target for therapeutic strategy in Parkinson’s disease? Neuroscience letters, 793, 136997.
   PubMed Web of Science ®Google Scholar
• Demir, C.F., et al., 2021. Protective effect of pregabalin on the brain tissue of diabetic rats. Diabetology international, 12 (2), 207–216.
   PubMed Web of Science ®Google Scholar
• Dong, L.R., et al., 2022. Effects of chronic restraint stress on apoptosis of amygdala cells in rats. Fa Yi xue Za zhi, 38 (4), 459–467.
   PubMedGoogle Scholar
• Duangjan, C., et al., 2021. Anacardium Occidentale L. leaf extracts protect against glutamate/H2O2-induced oxidative toxicity and induce neurite outgrowth: the involvement of SIRT1/Nrf2 signaling pathway and teneurin 4 transmembrane protein. Frontiers in pharmacology, 12, 627738.
   PubMed Web of Science ®Google Scholar
• Dubey, H., Gulati, K., and Ray, A., 2017. Effects of nitric oxide (NO) modulators on cognitive function and brain oxidative stress in experimental model of Alzheimer’s disease in rats. Journal of pharmacological reports, 2 (2), 1000126.
   Google Scholar
• Ellman, G.L., 1959. Tissue sulfhydryl groups. Archives of biochemistry and biophysics, 82 (1), 70–77.
   PubMed Web of Science ®Google Scholar
• Fatma, G., Houda, B., and Ahmed, L., 2018. H2O2-induced oxidative stress, AChE inhibition and mediated brain injury attenuated by Thymus algeriensis. Applied physiology, nutrition and metabolism, 43 (12), 1275–1281.
   PubMed Web of Science ®Google Scholar
• Förstermann, U., 2010. Nitric oxide and oxidative stress in vascular disease. Pflugers archiv: European journal of physiology, 459 (6), 923–939.
   PubMed Web of Science ®Google Scholar
• Fuhrich, D.G., Lessey, B.A., and Savaris, R.F., 2013. Comparison of HSCORE assessment of endometrial beta3 integrin subunit expression with digital HSCORE using computerized image analysis (ImageJ). Analytical and quantitative cytopathology and histpathology, 35 (4), 210–216.
   PubMedGoogle Scholar
• Garry, P.S., et al., 2015. The role of the nitric oxide pathway in brain injury and its treatment—from bench to bedside. Experimental neurology, 263, 235–243.
   PubMed Web of Science ®Google Scholar
• Gonçalves, J.S., et al., 2022. Impairment of neurovascular coupling in the hippocampus due to decreased nitric oxide bioavailability supports early cognitive dysfunction in type 2 diabetic rats. Free radical biology & medicine, 193 (Pt 2), 669–675.
   PubMedGoogle Scholar
• Gornal, A.G., Bardawill, C., and David, M.M., 1949. Determination of serum proteins by means of biuret reaction. The journal of biological chemistry, 177 (2), 751–766.
   PubMed Web of Science ®Google Scholar
• Habig, W.H., Pabst, M.J., and Jakoby, W.B., 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of biol chem, 25, 7130–7139.
   Google Scholar
• Han, Y., et al., 2022. Ferrous ions doped calcium carbonate nanoparticles potentiate chemotherapy by inducing ferroptosis. Journal of controlled release: official journal of the controlled release society, 348, 346–356.
   PubMed Web of Science ®Google Scholar
• Hazut, N., et al., 2019. Nitric oxide and l-arginine regulate feeding in satiated rats. Appetite, 132, 44–54.
   PubMed Web of Science ®Google Scholar
• Hol, E.M., and Pekny, M., 2015. Glial fibrillary acidic protein (GFAP) and the astrocyte intermediate filament system in diseases of the central nervous system. Current opinion in cell biology, 32, 121–130.
   PubMed Web of Science ®Google Scholar
• Hollenberg, S.M., and Cinel, I., 2009. Bench-to-bedside review: nitric oxide in critical illness – update 2008. Critical care (london, England), 13 (4), 218.
   PubMed Web of Science ®Google Scholar
• Hoogland, I.C., et al., 2015. Systemic inflammation and microglial activation: systematic review of animal experiments. Journal of neuroinflammation, 12, 114.
   PubMed Web of Science ®Google Scholar
• Iadecola, C., et al., 1994. Prolonged inhibition of brain nitric oxide synthase by short-term systemic administration of nitro-L-arginine methyl ester. Neurochemical research, 19 (4), 501–505.
   PubMed Web of Science ®Google Scholar
• Jacques-Silva, M.C., et al., 2001. Diphenyl diselenide and ascorbic acid changes deposition of selenium and ascorbic acid in liver and brain of mice. Pharmacology & toxicology, 88 (3), 119–125.
   PubMedGoogle Scholar
• Jollow, D.J., et al., 1974. Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology, 11 (3), 151–169. PMID: 4831804.
   PubMed Web of Science ®Google Scholar
• Khan, H.B.H., et al., 2013. Anti-inflammatory and anti-hyperlipidemic effect of semecarpus anacardium in a high fat diet: STZ-induced type 2 diabetic rat model. Inflammopharmacology, 21 (1), 37–46.
   PubMed Web of Science ®Google Scholar
• Kim, H.N., et al., 2017. Comparative analysis of the beneficial effects of treadmill training and electroacupuncture in a rat model of neonatal hypoxia-ischemia. International journal of molecular medicine, 39 (6), 1393–1402.
   PubMed Web of Science ®Google Scholar
• Kishida, K.T., and Klann, E., 2007. Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antioxidants & redox signaling, 9 (2), 233–244.
   PubMed Web of Science ®Google Scholar
• Kopincová, J., Púzserová, A., and Bernátová, I., 2012. L-NAME in the cardiovascular system - nitric oxide synthase activator? Pharmacological reports: PR, 64 (3), 511–520.
   PubMed Web of Science ®Google Scholar
• Lazarus, J.E., et al., 2015. Protein carbonylation after traumatic brain injury: cell specificity, regional susceptibility, and gender differences. Free radical biology & medicine, 78, 89–100.
   PubMed Web of Science ®Google Scholar
• Li, M., et al., 2022. Mitofusin 2 confers the suppression of microglial activation by cannabidiol: Insights from in vitro and in vivo models. Brain, behavior, and immunity, 104, 155–170.
   PubMed Web of Science ®Google Scholar
• Li, S., et al., 2018. Impaired cognitive performance in endothelial nitric oxide synthase knockout mice after ischemic stroke: a pilot study. American journal of physical medicine & rehabilitation, 97 (7), 492–499.
   PubMed Web of Science ®Google Scholar
• Lima, A.T., et al., 2022. Release of 6-nitrodopamine modulates vascular reactivity of Pantherophis guttatus aortic rings. Comparative biochemistry and physiology. Toxicology & pharmacology : CBP, 262, 109471.
   PubMed Web of Science ®Google Scholar
• Liu, Z., et al., 2021. The main mechanisms of trimethyltin chloride-induced neurotoxicity: Energy metabolism disorder and peroxidation damage. Toxicology letters, 345, 67–76.
   PubMed Web of Science ®Google Scholar
• Malinski, T., 2007. Nitric oxide and nitroxidative stress in Alzheimer’s disease. Journal of alzheimer’s disease : JAD, 11 (2), 207–218.
   PubMed Web of Science ®Google Scholar
• Martins, I.K., et al., 2018. Anacardium microcarpum promotes neuroprotection dependently of AKT and ERK phosphorylation but does not prevent mitochondrial damage by 6-OHDA. Oxidative medicine and cellular longevity, 2018, 2131895.
   PubMed Web of Science ®Google Scholar
• Michel, T.M., et al., 2007. Evidence for oxidative stress in the frontal cortex in patients with recurrent depressive disorder—a postmortem study. Psychiatry research, 151 (1-2), 145–150.
   PubMed Web of Science ®Google Scholar
• Middeldorp, J., and Hol, E.M., 2011. Progress in neurobiology GFAP in health and disease. Progress in neurobiology, 93 (3), 421–443.
   PubMed Web of Science ®Google Scholar
• Misra, H.P., and Fridovich, I., 1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of biological chemistry, 247 (10), 3170–3175.
   PubMed Web of Science ®Google Scholar
• Morris, R., 1984. Developments of a water-maze procedure for studying spatial learning in the rat. Journal of neuroscience methods, 11 (1), 47–60.
   PubMed Web of Science ®Google Scholar
• Olajide, O.A., Aderogba, M.A., and Fiebich, B.L., 2013. Mechanisms of anti-inflammatory property of Anacardium occidentale stem bark: inhibition of NF-κB and MAPK signalling in the microglia. Journal of ethnopharmacology, 145 (1), 42–49.
   PubMed Web of Science ®Google Scholar
• Olaleye, S.B., et al., 2007. Lead exposure increases oxidative stress in the gastric mucosa of HCl/ethanol-exposed rats. World journal of gastroenterology, 13 (38), 5121–5126.
   PubMed Web of Science ®Google Scholar
• Oyagbemi, A.A., et al., 2020. Antihypertensive power of Naringenin is mediated via attenuation of mineralocorticoid receptor (MCR)/angiotensin converting enzyme (ACE)/kidney injury molecule (Kim-1) signaling pathway. European journal of pharmacology, 880, 173142. Epub 2020 May 16. PMID: 32422184.
   PubMed Web of Science ®Google Scholar
• Oyagbemi, A.A., et al., 2015. Lack of reversal of oxidative damage in renal tissues of lead acetate-treated rats. Environmental toxicology, 30 (11), 1235–1243.
   PubMed Web of Science ®Google Scholar
• Oyagbemi, A.A., et al., 2019. Cobalt chloride toxicity elicited hypertension and cardiac complication via induction of oxidative stress and upregulation of COX-2/Bax signaling pathway. Human & experimental toxicology, 38 (5), 519–532.
   PubMed Web of Science ®Google Scholar
• Paul, R., and Borah, A., 2017. Global loss of acetylcholinesterase activity with mitochondrial complexes inhibition and inflammation in brain of hypercholesterolemic mice. Scientific reports, 7 (1), 17922.
   PubMedGoogle Scholar
• Paul, V., and Ekambaram, P., 2011. Involvement of nitric oxide in learning & memory processes. Indian journal of medical research, 133, 471–478.
   PubMed Web of Science ®Google Scholar
• Reznick, A.Z., and Packer, L., 1994. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods in enzymology, 233, 357–363.
   PubMed Web of Science ®Google Scholar
• Rossi, M., et al., 2021. Sustainable drug discovery of multi-target-directed ligands for Alzheimer’s disease. Journal of medicinal chemistry, 64 (8), 4972–4990.
   PubMed Web of Science ®Google Scholar
• Rumman, M., et al., 2022. Genistein suppresses microglial activation and inhibits apoptosis in different brain regions of hypoxia-exposed mice model of amnesia. Metabolic brain disease, 37 (7), 2521–2532. Epub 2022 Jul 27. PMID: 35895244.
   PubMed Web of Science ®Google Scholar
• Savareh, E., et al., 2022. Prenatal zinc supplementation ameliorates hippocampal astrocytes activation and inflammatory cytokines expression induced by lipopolysaccharide in a rat model of maternal immune activation. Basic and clinical neuroscience, 13 (3), 335–347.
   PubMedGoogle Scholar
• Sesti, F., Liu, S., and Cai, S.Q., 2010. Oxidation of potassium channels by ROS: a general mechanism of aging and neurodegeneration? Trends in cell biology, 20 (1), 45–51.
   PubMed Web of Science ®Google Scholar
• Sharma, P., et al., 2021. Neuroprotective potential of hydroethanolic hull extract of Juglans regia L. on isoprenaline induced oxidative damage in brain of Wistar rats. Toxicology reports, 2021 8, 223–229.
   Google Scholar
• Shi, F.J., et al., 2021. Is Iba-1 protein expression a sensitive marker for microglia activation in experimental diabetic retinopathy? International journal of ophthalmology, 14 (2), 200–208.
   PubMed Web of Science ®Google Scholar
• Shinotoh, H., et al., 2003. The amygdala and Alzheimer’s disease: positron emission tomographic study of the cholinergic system. Annals of the New York academy of sciences, 85, 411–419.
   Google Scholar
• Sofroniew, M.V., 2014. Astrogliosis. Cold spring harbor perspectives in biology, 7 (2), a020420.
   PubMed Web of Science ®Google Scholar
• Souza, N.C., et al., 2017. Antioxidant and anti-inflammatory properties of Anacardium occidentale leaf extract. Evidence-based complementary and alternative medicine: eCAM, 2017, 2787308.
   PubMed Web of Science ®Google Scholar
• Steinert, J.R., Chernova, T., and Forsythe, I.D., 2010. Nitric oxide signaling in brain function, dysfunction, and dementia. The neuroscientist: a review journal bringing neurobiology, neurology and psychiatry, 16 (4), 435–452.
   PubMed Web of Science ®Google Scholar
• Stephan, B., et al., 2017. Cardiovascular disease, the nitric oxide pathway and risk of cognitive impairment and dementia. Current cardiology reports, 19 (9), 87.
   PubMed Web of Science ®Google Scholar
• Stevanović, I.D., et al., 2009. Effects of L-NAME, a non-specific nitric oxide synthase inhibitor, on AlCl3-induced toxicity in the rat forebrain cortex. Journal of veterinary science, 10 (1), 15–22.
   PubMed Web of Science ®Google Scholar
• Tan, X., et al., 2019. A multifunctional bis-(-)-nor-meptazinol-oxalamide hybrid with metal-chelating property ameliorates Cu(II)-induced spatial learning and memory deficits via preventing neuroinflammation and oxido-nitrosative stress in mice. Journal of trace elements in medicine and biology : organ of the society for minerals and trace elements (GMS), 52, 199–208.
   PubMed Web of Science ®Google Scholar
• Tchikaya, F.O., et al., 2011. Anacardium occidentale Linn. (Anacardiaceae) stem bark extract induces hypotensive and cardio-inhibitory effects in experimental animal models. African journal of traditional complementary and alternative medicines, 8 (4), 452–461.
   PubMedGoogle Scholar
• Thomas, D.D., et al., 2008. The chemical biology of nitric oxide: implications in cellular signaling. Free radical biology & medicine, 45 (1), 18–31.
   PubMed Web of Science ®Google Scholar
• Tinning, A.R., et al., 2018. Pazopanib-induced hypertension in patients with renal cell carcinoma is associated with low urine excretion of NO metabolites. Hypertension (Dallas, Tex.: 1979), 71 (3), 473–480.
   PubMed Web of Science ®Google Scholar
• Toda, N., Ayajiki, K., and Okamura, T., 2009. Cerebral blood flow regulation by nitric oxide in neurological disorders. Canadian journal of physiology and pharmacology, 87 (8), 581–594.
   PubMed Web of Science ®Google Scholar
• Tropea, M.R., et al., 2022. Nitric oxide/cGMP/CREB pathway and amyloid-beta crosstalk: from physiology to Alzheimer’s disease. Free radical biology & medicine, 193 (Pt 2), 657–668.
   PubMedGoogle Scholar
• Varshney, R., and Kale, K.K., 1990. Effect of calmodulin antagonists on radiation induced lipid peroxidation in microsomes. International journal of radiation biology, 58 (5), 733–743.
   PubMed Web of Science ®Google Scholar
• Vasconcelos, M.D., et al., 2015. Anti-inflammatory and wound healing potential of cashew apple juice (Anacardium occidentale L.) in mice. Experimental biology and medicine (Maywood, N.J.), 240 (12), 1648–1655.
   PubMed Web of Science ®Google Scholar
• Veal, E.A., Day, A.M., and Morgan, B.A., 2007. Hydrogen peroxide sensing and signalling. Molecular cell, 26 (1), 1–14.
   PubMed Web of Science ®Google Scholar
• Velagapudi, R., et al., 2018. Agathisflavone isolated from Anacardium occidentale suppresses SIRT1-mediated neuroinflammation in BV2 microglia and neurotoxicity in APPSwe-transfected SH-SY5Y cells. Phytotherapy research : PTR, 32 (10), 1957–1966.
   PubMed Web of Science ®Google Scholar
• Vorhees, C.V., and Williams, M.T., 2006. Morris’s water maze: procedures for assessing spatial and related forms of learning and memory. Nature protocols, 1 (2), 848–858.
   PubMed Web of Science ®Google Scholar
• Wang, W.E., et al., 2023. Association of longitudinal cognitive decline with diffusion MRI in Gray Matter, Amyloid, and Tau deposition. Neurobiology of aging, 121, 166–178.
   PubMed Web of Science ®Google Scholar
• Wattanathorn, J., et al., 2017. Preventive effect of cashew-derived protein hydrolysate with high fiber on cerebral ischemia. BioMed research international, 2017, 6135023.
   PubMed Web of Science ®Google Scholar
• Wittekindt, M., et al., 2022. Different methods for evaluating microglial activation using anti-ionized calcium-binding adaptor protein-1 immunohistochemistry in the cuprizone model. Cells, 11 (11), 1723.
   PubMed Web of Science ®Google Scholar
• Wolff, S.F., 1994. Ferrous ion oxidation in the presence of ferric ion indicator xylenol orange for measurement of hydrogen peroxides. Methods in enzymology, 233, 182–189.
   Web of Science ®Google Scholar
• Xia, Y., and Zweier, J.L., 1997. Measurement of myeloperoxidase in leukocyte-containing tissues. Analytical biochemistry, 245 (1), 93–96.
   PubMed Web of Science ®Google Scholar
• Xie, Z., et al., 2023. Activated AMPK mitigates diabetes-related cognitive dysfunction by inhibiting hippocampal ferroptosis. Biochemical pharmacology, 207, 115374.
   PubMed Web of Science ®Google Scholar
• Yan, L., et al., 2022. Lanthanum impairs learning and memory by activating microglia in the hippocampus of mice. Biological trace element research, 200 (4), 1640–1649.
   PubMed Web of Science ®Google Scholar
• Yang, Y., et al., 2021. Iron-doxorubicin prodrug loaded liposome nanogenerator programs multimodal ferroptosis for efficient cancer therapy. Asian journal of pharmaceutical sciences, 16 (6), 784–793.
   PubMed Web of Science ®Google Scholar
• Yang, Z., and Wang, K.K., 2015. Glial fibrillary acidic protein: from intermediate filament assembly and gliosis to neurobiomarker. Trends in neurosciences, 38 (6), 364–374.
   PubMed Web of Science ®Google Scholar
• Yang, Z., et al., 2022. Methylglyoxal in the brain: from glycolytic metabolite to signalling molecule. Molecules, 27 (22), 7905.
   PubMed Web of Science ®Google Scholar
• Yogini, J., et al., 2012. Pharmacognostic and preliminary phytochemical investigations of Anacardium occidentale (Linn.) leaves. International journal of pharmacy and pharmaceutical sciences, 4, 625–631.
   Google Scholar
• Younis, W., et al., 2020. Role of the NO/cGMP pathway and renin-angiotensin system in the hypotensive and diuretic effects of aqueous soluble fraction from Crataegus songarica K. Koch. Journal of ethnopharmacology, 249, 112400.
   PubMed Web of Science ®Google Scholar
• Zarinfard, G., et al., 2022. Upregulation of neurotrophic factors and myelin basic protein in Schwann-like cells by T3 hormone following transdifferentiation of human adipose-derived stem cells. International journal of molecular and cellular medicine, 11 (1), 41–54.
   PubMedGoogle Scholar
• Zhou, Z.Y., et al., 2019. Endothelial-dependent and independent vascular relaxation effect of tetrahydropalmatine on rat aorta. Frontiers in pharmacology, 10, 336.
   PubMed Web of Science ®Google Scholar