Selol, an organic selenium donor, prevents lipopolysaccharide-induced oxidative stress and inflammatory reaction in the rat brain

Neurochemistry International

Volumn 108, Issue , 2017, Pages 66-77

  Dominiak, Agnieszka ^a   Wilkaniec, Anna ^b   Jęśko, Henryk ^b   Czapski, Grzegorz A ^b   Lenkiewicz, Anna M ^b   Kurek, Eliza ^c   Wroczyński, Piotr ^a   Adamczyk, Agata ^b  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

^b MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

^c UNIVERSITY OF WARSAW   (Poland)

Author keywords

Lipopolysaccharide; Neurodegenerative disease; Neuroinflammation; Organic selenium compound; Selenoenzyme; Selol

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTIOXIDANT; BETA ACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; GAMMA INTERFERON; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE REDUCTASE; INTERLEUKIN 6; LIPID PEROXIDE; MALONALDEHYDE; MESSENGER RNA; NEUROPROTECTIVE AGENT; ORGANOSELENIUM DERIVATIVE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SELENIUM; SELOL; THIOBARBITURIC ACID REACTIVE SUBSTANCE; THIOREDOXIN REDUCTASE; THIOREDOXIN REDUCTASE 1; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AUTACOID; LIPOPOLYSACCHARIDE; SELENIUM DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; BRAIN TISSUE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; EX VIVO STUDY; FEMALE; GENE EXPRESSION; LIPID PEROXIDATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SINGLE DRUG DOSE; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; DRUG EFFECTS; INFLAMMATION; METABOLISM; PHYSIOLOGY; RANDOMIZATION; WISTAR RAT;

ANIMALS; BRAIN; FEMALE; INFLAMMATION; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; OXIDATIVE STRESS; RANDOM ALLOCATION; RATS; RATS, WISTAR; SELENIUM; SELENIUM COMPOUNDS;

EID: 85014496002     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2017.02.014     Document Type: Article

References (120)

1. Abdo, K.M., NTP toxicity studies of sodium selenate and sodium selenite (CAS nos. 13410-01-0 and 10102-18-8) administered in drinking water to F344/N rats and B6C3F1 mice. Toxic. Rep. Ser. 38 (1994), 1–e5.
2. Akil, M., Bicer, M., Menevse, E., Baltaci, A.K., Mogulkoc, R., Selenium supplementation prevents lipid peroxidation caused by arduous exercise in rat brain tissue. Bratisl. Lek. Listy 112 (2011), 314–317.
3. Al-Amin, M.M., Sultana, R., Sultana, S., Rahman, M.M., Reza, H.M., Astaxanthin ameliorates prenatal LPS-exposed behavioral deficits and oxidative stress in adult offspring. BMC Neurosci., 17, 2016, 11.
4. Aleryani, S., Milo, E., Kostka, P., Formation of peroxynitrite during thiol-mediated reduction of sodium nitroprusside. Biochim. Biophys. Acta 1472 (1999), 181–190.
5. Aoyama, K., Nakaki, T., Impaired glutathione synthesis in neurodegeneration. Int. J. Mol. Sci. 14 (2013), 21021–21044.
6. Autry, A.E., Monteggia, L.M., Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol. Rev. 64 (2012), 238–258.
7. Beishuizen, A., Thijs, L.G., Endotoxin and the hypothalamo-pituitary-adrenal (HPA) axis. J. Endotoxin Res. 9 (2003), 3–24.
8. Berg, B.M., Godbout, J.P., Chen, J., Kelley, K.W., Johnson, R.W., alpha-Tocopherol and selenium facilitate recovery from lipopolysaccharide-induced sickness in aged mice. J. Nutr. 135 (2005), 1157–1163.
9. Berlett, B.S., Stadtman, E.R., Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272 (1997), 20313–20316.
10. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254.
11. Bruning, C.A., Prigol, M., Luchese, C., Jesse, C.R., Duarte, M.M., Roman, S.S., Nogueira, C.W., Protective effect of diphenyl diselenide on ischemia and reperfusion-induced cerebral injury: involvement of oxidative stress and pro-inflammatory cytokines. Neurochem. Res. 37 (2012), 2249–2258.
12. Cheng, W.H., Ho, Y.S., Valentine, B.A., Ross, D.A., Combs, G.F. Jr., Lei, X.G., Cellular glutathione peroxidase is the mediator of body selenium to protect against paraquat lethality in transgenic mice. J. Nutr. 128 (1998), 1070–1076.
13. Chez, M.G., Dowling, T., Patel, P.B., Khanna, P., Kominsky, M., Elevation of tumor necrosis factor-alpha in cerebrospinal fluid of autistic children. Pediatr. Neurol. 36 (2007), 361–365.
14. Colucci, D.G., Puig, N.R., Hernandez-Pando, R., Influence of anaesthetic drugs on immune response: from inflammation to immunosuppression. OA Anaesth., 30, 2013, 21.
15. Comim, C.M., Cassol, O.J. Jr., Constantino, L.S., Felisberto, F., Petronilho, F., Rezin, G.T., Scaini, G., Daufenbach, J.F., Streck, E.L., Quevedo, J., Dal-Pizzol, F., Alterations in inflammatory mediators, oxidative stress parameters and energetic metabolism in the brain of sepsis survivor rats. Neurochem. Res. 36 (2011), 304–311.
16. Czapski, G.A., Cakala, M., Kopczuk, D., Kaminska, M., Strosznajder, J.B., Inhibition of nitric oxide synthase prevents energy failure and oxidative damage evoked in the brain by lipopolysaccharide. Pol. J. Pharmacol. 56 (2004), 643–646.
17. Czapski, G.A., Gajkowska, B., Strosznajder, J.B., Systemic administration of lipopolysaccharide induces molecular and morphological alterations in the hippocampus. Brain Res. 1356 (2010), 85–94.
18. Dandona, P., Ghanim, H., Bandyopadhyay, A., Korzeniewski, K., Ling Sia, C., Dhindsa, S., Chaudhuri, A., Insulin suppresses endotoxin-induced oxidative, nitrosative, and inflammatory stress in humans. Diabetes Care 33 (2010), 2416–2423.
19. Deponte, M., Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim. Biophys. Acta 1830 (2013), 3217–3266.
20. Dobashi, K., Aihara, M., Araki, T., Shimizu, Y., Utsugi, M., Iizuka, K., Murata, Y., Hamuro, J., Nakazawa, T., Mori, M., Regulation of LPS induced IL-12 production by IFN-gamma and IL-4 through intracellular glutathione status in human alveolar macrophages. Clin. Exp. Immunol. 124 (2001), 290–296.
21. Dominiak, A., Wilkaniec, A., Wroczynski, P., Adamczyk, A., Selenium in the therapy of neurological diseases. Where is it going?. Curr. Neuropharmacol. 14 (2016), 282–299.
22. Dominiak, A., Wilkaniec, A., Wroczynski, P., Jesko, H., Adamczyk, A., Protective effects of selol against sodium nitroprusside-induced cell death and oxidative stress in PC12 cells. Neurochem Res. 41 (2016), 3215–3226.
23. Dominiak, A., Wilkaniec, A., Wroczynski, P., Jesko, H., Adamczyk, A., Protective effects of selol against sodium nitroprusside-induced cell death and oxidative stress in PC12 cells. Neurochem. Res., 2016.
24. Dringen, R., Oxidative and antioxidative potential of brain microglial cells. Antioxid. Redox Signal 7 (2005), 1223–1233.
25. Du, X., Wang, Z., Zheng, Y., Li, H., Ni, J., Liu, Q., Inhibitory effect of selenoprotein P on Cu(+)/Cu(2+)-induced Abeta42 aggregation and toxicity. Inorg. Chem. 53 (2014), 1672–1678.
26. Galter, D., Mihm, S., Droge, W., Distinct effects of glutathione disulphide on the nuclear transcription factor kappa B and the activator protein-1. Eur. J. Biochem. 221 (1994), 639–648.
27. Garousi, Farzaneh, The toxicity of different selenium forms and compounds – Review. Acta Agrar. Debreceniensis, 64, 2015.
28. Gasmi, A., Garnier, R., Galliot-Guilley, M., Gaudillat, C., Quartenoud, B., Buisine, A., Djebbar, D., Acute selenium poisoning. Vet. Hum. Toxicol. 39 (1997), 304–308.
29. Gianfranceschi, L., Siciliano, R., Walls, J., Morales, B., Kirkwood, A., Huang, Z.J., Tonegawa, S., Maffei, L., Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 12486–12491.
30. Glass, C.K., Saijo, K., Winner, B., Marchetto, M.C., Gage, F.H., Mechanisms underlying inflammation in neurodegeneration. Cell 140 (2010), 918–934.
31. Goraca, A., Aslanowicz-Antkowiak, K., Prophylaxis with alpha-lipoic acid against lipopolysaccharide-induced brain injury in rats. Arch. Immunol. Ther. Exp. Warsz. 57 (2009), 141–146.
32. Gordon, R., Singh, N., Lawana, V., Ghosh, A., Harischandra, D.S., Jin, H., Hogan, C., Sarkar, S., Rokad, D., Panicker, N., Anantharam, V., Kanthasamy, A.G., Kanthasamy, A., Protein kinase Cdelta upregulation in microglia drives neuroinflammatory responses and dopaminergic neurodegeneration in experimental models of Parkinson's disease. Neurobiol. Dis. 93 (2016), 96–114.
33. Gu, F., Chauhan, V., Chauhan, A., Impaired synthesis and antioxidant defense of glutathione in the cerebellum of autistic subjects: alterations in the activities and protein expression of glutathione-related enzymes. Free Radic. Biol. Med. 65 (2013), 488–496.
34. Guan, Z., Fang, J., Peripheral immune activation by lipopolysaccharide decreases neurotrophins in the cortex and hippocampus in rats. Brain Behav. Immun. 20 (2006), 64–71.
35. Gubba, E.M., Fawcett, J.W., Herbert, J., The effects of corticosterone and dehydroepiandrosterone on neurotrophic factor mRNA expression in primary hippocampal and astrocyte cultures. Brain Res. Mol. Brain Res. 127 (2004), 48–59.
36. Haddad, J.J., Saade, N.E., Safieh-Garabedian, B., Cytokines and neuro-immune-endocrine interactions: a role for the hypothalamic-pituitary-adrenal revolving axis. J. Neuroimmunol. 133 (2002), 1–19.
37. Hansson, A.C., Sommer, W., Rimondini, R., Andbjer, B., Stromberg, I., Fuxe, K., c-fos reduces corticosterone-mediated effects on neurotrophic factor expression in the rat hippocampal CA1 region. J. Neurosci. 23 (2003), 6013–6022.
38. Halliwell, B., Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18 (2001), 685–716.
39. Ho, Y.H., Lin, Y.T., Wu, C.W., Chao, Y.M., Chang, A.Y., Chan, J.Y., Peripheral inflammation increases seizure susceptibility via the induction of neuroinflammation and oxidative stress in the hippocampus. J. Biomed. Sci., 22, 2015, 46.
40. Hoffmann, P.R., Berry, M.J., The influence of selenium on immune responses. Mol. Nutr. Food Res. 52 (2008), 1273–1280.
41. Holman, D.W., Klein, R.S., Ransohoff, R.M., The blood-brain barrier, chemokines and multiple sclerosis. Biochim. Biophys. Acta 1812 (2011), 220–230.
42. Hozyen, H.F., Eldebaky, H.A., Soror, A.H., Desouky, H.M., Shalaby, S.I.A., Protective role of selenium against adverse effects of atrazine toxicity in male rats: biochemical, histopathological and molecular changes. Glob. Veterinaria 15 (2015), 357–365.
43. Huang, Z., Rose, A.H., Hoffmann, P.R., The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal 16 (2012), 705–743.
44. Hyman, C., Hofer, M., Barde, Y.A., Juhasz, M., Yancopoulos, G.D., Squinto, S.P., Lindsay, R.M., BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350 (1991), 230–232.
45. Itami, C., Kimura, F., Kohno, T., Matsuoka, M., Ichikawa, M., Tsumoto, T., Nakamura, S., Brain-derived neurotrophic factor-dependent unmasking of “silent” synapses in the developing mouse barrel cortex. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 13069–13074.
46. Jacewicz, M., Czapski, G.A., Katkowska, I., Strosznajder, R.P., Systemic administration of lipopolysaccharide impairs glutathione redox state and object recognition in male mice. The effect of PARP-1 inhibitor. Folia Neuropathol. 47 (2009), 321–328.
47. Jastrzebski, Z., Czyzewska-Szafran, H., Fijatek, Z., Suchocki, P., Fitak, B.A., Toxicity studies of a new selenium compound, Selol, in rats. Drugs Exp. Clin. Res. 21 (1995), 217–220.
48. Jastrzebski, Z., Czyzewska-Szafran, H., Remiszewska, M., Fijalek, Z., Fitak, B.A., Suchocki, P., Pharmacokinetics of selol, a new agent containing selenium, in rats. Drugs Exp. Clin. Res. 23 (1997), 7–11.
49. Jeong, H.K., Jou, I., Joe, E.H., Systemic LPS administration induces brain inflammation but not dopaminergic neuronal death in the substantia nigra. Exp. Mol. Med. 42 (2010), 823–832.
50. Jones, J.J., Fan, J., Nathens, A.B., Kapus, A., Shekhman, M., Marshall, J.C., Parodo, J., Rotstein, O.D., Redox manipulation using the thiol-oxidizing agent diethyl maleate prevents hepatocellular necrosis and apoptosis in a rodent endotoxemia model. Hepatology 30 (1999), 714–724.
51. Kasarpalkar, N.J., Kothari, S.T., Dave, U.P., Brain-derived neurotrophic factor in children with autism spectrum disorder. Ann. Neurosci. 21 (2014), 129–133.
52. Kaul, N., Forman, H.J., Activation of NF kappa B by the respiratory burst of macrophages. Free Radic. Biol. Med. 21 (1996), 401–405.
53. Kaur, G., Tirkey, N., Bharrhan, S., Chanana, V., Rishi, P., Chopra, K., Inhibition of oxidative stress and cytokine activity by curcumin in amelioration of endotoxin-induced experimental hepatoxicity in rodents. Clin. Exp. Immunol. 145 (2006), 313–321.
54. Kefer, J., Rahman, A., Anwar, K.N., Malik, A.B., Decreased oxidant buffering impairs NF-kappaB activation and ICAM-1 transcription in endothelial cells. Shock 15 (2001), 11–15.
55. Kielczykowska, M., Kocot, J., Lewandowska, A., Zelazowska, R., Musik, I., The protective influence of selenium on oxidant disturbances in brain of rats exposed to lithium. Physiol. Res. 64 (2015), 739–746.
56. Kim, W.G., Mohney, R.P., Wilson, B., Jeohn, G.H., Liu, B., Hong, J.S., Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 20 (2000), 6309–6316.
57. Kirsten, T.B., Chaves-Kirsten, G.P., Chaible, L.M., Silva, A.C., Martins, D.O., Britto, L.R., Dagli, M.L., Torrao, A.S., Palermo-Neto, J., Bernardi, M.M., Hypoactivity of the central dopaminergic system and autistic-like behavior induced by a single early prenatal exposure to lipopolysaccharide. J. Neurosci. Res. 90 (2012), 1903–1912.
58. Kirsten, T.B., Galvao, M.C., Reis-Silva, T.M., Queiroz-Hazarbassanov, N., Bernardi, M.M., Zinc prevents sickness behavior induced by lipopolysaccharides after a stress challenge in rats. PLoS One, 10, 2015, e0120263.
59. Kirsten, T.B., Taricano, M., Maiorka, P.C., Palermo-Neto, J., Bernardi, M.M., Prenatal lipopolysaccharide reduces social behavior in male offspring. Neuroimmunomodulation 17 (2010), 240–251.
60. Knusel, B., Winslow, J.W., Rosenthal, A., Burton, L.E., Seid, D.P., Nikolics, K., Hefti, F., Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin 3. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 961–965.
61. Koyanagi, T., Nakamuta, M., Enjoji, M., Iwamoto, H., Motomura, K., Sakai, H., Nawata, H., The selenoorganic compound ebselen suppresses liver injury induced by Propionibacterium acnes and lipopolysaccharide in rats. Int. J. Mol. Med. 7 (2001), 321–327.
62. Laye, S., Gheusi, G., Cremona, S., Combe, C., Kelley, K., Dantzer, R., Parnet, P., Endogenous brain IL-1 mediates LPS-induced anorexia and hypothalamic cytokine expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (2000), R93–R98.
63. Lehnardt, S., Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 58 (2010), 253–263.
64. Leite, M.R., Cechella, J.L., Mantovani, A.C., Duarte, M.M., Nogueira, C.W., Zeni, G., Swimming exercise and diphenyl diselenide-supplemented diet affect the serum levels of pro- and anti-inflammatory cytokines differently depending on the age of rats. Cytokine 71 (2015), 119–123.
65. Lenczowski, M.J., Van Dam, A.M., Poole, S., Larrick, J.W., Tilders, F.J., Role of circulating endotoxin and interleukin-6 in the ACTH and corticosterone response to intraperitoneal LPS. Am. J. Physiol. 273 (1997), R1870–R1877.
66. Leszek, J., Barreto, G.E., Gasiorowski, K., Koutsouraki, E., Avila-Rodrigues, M., Aliev, G., Inflammatory mechanisms and oxidative stress as key factors responsible for progression of neurodegeneration: role of brain innate immune system. CNS Neurol. Disord. Drug Targets 15 (2016), 329–336.
67. Letavayova, L., Vlasakova, D., Spallholz, J.E., Brozmanova, J., Chovanec, M., Toxicity and mutagenicity of selenium compounds in Saccharomyces cerevisiae. Mutat. Res. 638 (2008), 1–10.
68. Li, X., Chauhan, A., Sheikh, A.M., Patil, S., Chauhan, V., Li, X.M., Ji, L., Brown, T., Malik, M., Elevated immune response in the brain of autistic patients. J. Neuroimmunol. 207 (2009), 111–116.
69. Liaudet, L., Murthy, K.G., Mabley, J.G., Pacher, P., Soriano, F.G., Salzman, A.L., Szabo, C., Comparison of inflammation, organ damage, and oxidant stress induced by Salmonella enterica serovar Muenchen flagellin and serovar Enteritidis lipopolysaccharide. Infect. Immun. 70 (2002), 192–198.
70. Limongi, D., Baldelli, S., Redox imbalance and viral infections in neurodegenerative diseases. Oxid. Med. Cell Longev., 2016, 2016, 6547248.
71. Lopategui Cabezas, I., Herrera Batista, A., Penton Rol, G., The role of glial cells in Alzheimer disease: potential therapeutic implications. Neurologia 29 (2014), 305–309.
72. Mamounas, L.A., Blue, M.E., Siuciak, J.A., Altar, C.A., Brain-derived neurotrophic factor promotes the survival and sprouting of serotonergic axons in rat brain. J. Neurosci. 15 (1995), 7929–7939.
73. Manu, P., Correll, C.U., Wampers, M., Mitchell, A.J., Probst, M., Vancampfort, D., De Hert, M., Markers of inflammation in schizophrenia: association vs. causation. World Psychiatry 13 (2014), 189–192.
74. Mehlhase, J., Gieche, J., Ullrich, O., Sitte, N., Grune, T., LPS-induced protein oxidation and proteolysis in BV-2 microglial cells. IUBMB Life 50 (2000), 331–335.
75. Mitchell, J.H., Nicol, F., Beckett, G.J., Arthur, J.R., Selenoprotein expression and brain development in preweanling selenium- and iodine-deficient rats. J. Mol. Endocrinol. 20 (1998), 203–210.
76. Muller, L.G., Borsoi, M., Stolz, E.D., Herzfeldt, V., Viana, A.F., Ravazzolo, A.P., Rates, S.M., Diene valepotriates from valeriana glechomifolia prevent lipopolysaccharide-induced sickness and depressive-like behavior in mice. Evid. Based Complement. Altern. Med., 2015, 2015, 145914.
77. Murata, Y., Shimamura, T., Hamuro, J., The polarization of T(h)1/T(h)2 balance is dependent on the intracellular thiol redox status of macrophages due to the distinctive cytokine production. Int. Immunol. 14 (2002), 201–212.
78. Nagatsu, T., Sawada, M., Inflammatory process in Parkinson's disease: role for cytokines. Curr. Pharm. Des. 11 (2005), 999–1016.
79. Nathens, A.B., Bitar, R., Watson, R.W., Issekutz, T.B., Marshall, J.C., Dackiw, A.P., Rotstein, O.D., Thiol-mediated regulation of ICAM-1 expression in endotoxin-induced acute lung injury. J. Immunol. 160 (1998), 2959–2966.
80. Nava Catorce, M., Acero, G., Pedraza-Chaverri, J., Fragoso, G., Govezensky, T., Gevorkian, G., Alpha-mangostin attenuates brain inflammation induced by peripheral lipopolysaccharide administration in C57BL/6J mice. J. Neuroimmunol. 297 (2016), 20–27.
81. Norden, D.M., Trojanowski, P.J., Villanueva, E., Navarro, E., Godbout, J.P., Sequential activation of microglia and astrocyte cytokine expression precedes increased Iba-1 or GFAP immunoreactivity following systemic immune challenge. Glia 64 (2016), 300–316.
82. Olson, J.K., Miller, S.D., Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J. Immunol. 173 (2004), 3916–3924.
83. Paglia, D.E., Valentine, W.N., Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70 (1967), 158–169.
84. Pasqualetti, G., Brooks, D.J., Edison, P., The role of neuroinflammation in dementias. Curr. Neurol. Neurosci. Rep., 15, 2015, 17.
85. Peterson, L.J., Flood, P.M., Oxidative stress and microglial cells in Parkinson's disease. Mediat. Inflamm., 2012, 2012, 401264.
86. Picq, C.A., Clarencon, D., Sinniger, V.E., Bonaz, B.L., Mayol, J.F., Impact of anesthetics on immune functions in a rat model of vagus nerve stimulation. PLoS One, 8, 2013, e67086.
87. Pullen, R.G., Schofield, M., Markham, A., Lough, J., Menton, K., Selenium homeostasis in the central nervous system of the rat. Life Sci. 58 (1996), 2125–2135.
88. Rahden-Staron, I., Suchocki, P., Czeczot, H., Evaluation of mutagenic activity of the organo-selenium compound Selol by use of the Salmonella typhimurium mutagenicity assay. Mutat. Res. 699 (2010), 44–46.
89. Rossignol, D.A., Frye, R.E., Evidence linking oxidative stress, mitochondrial dysfunction, and inflammation in the brain of individuals with autism. Front. Physiol., 5, 2014, 150.
90. Sah, S.P., Tirkey, N., Kuhad, A., Chopra, K., Effect of quercetin on lipopolysaccharide induced-sickness behavior and oxidative stress in rats. Indian J. Pharmacol. 43 (2011), 192–196.
91. Santamaria, A., Salvatierra-Sanchez, R., Vazquez-Roman, B., Santiago-Lopez, D., Villeda-Hernandez, J., Galvan-Arzate, S., Jimenez-Capdeville, M.E., Ali, S.F., Protective effects of the antioxidant selenium on quinolinic acid-induced neurotoxicity in rats: in vitro and in vivo studies. J. Neurochem. 86 (2003), 479–488.
92. Schrauzer, G.N., The nutritional significance, metabolism and toxicology of selenomethionine. Adv. Food Nutr. Res. 47 (2003), 73–112.
93. Sebai, H., Gadacha, W., Sani, M., Aouani, E., Ghanem-Boughanmi, N., Ben-Attia, M., Protective effect of resveratrol against lipopolysaccharide-induced oxidative stress in rat brain. Brain Inj. 23 (2009), 1089–1094.
94. Selamoglu Talas, Z., Ozdemir, I., Yilmaz, I., Gok, Y., Orun, I., The investigation of the antioxidative properties of the novel synthetic organoselenium compounds in some rat tissues. Exp. Biol. Med. (Maywood) 233 (2008), 575–579.
95. Senol, N., Naziroglu, M., Yuruker, V., N-acetylcysteine and selenium modulate oxidative stress, antioxidant vitamin and cytokine values in traumatic brain injury-induced rats. Neurochem. Res. 39 (2014), 685–692.
96. Shilo, S., Pardo, M., Aharoni-Simon, M., Glibter, S., Tirosh, O., Selenium supplementation increases liver MnSOD expression: molecular mechanism for hepato-protection. J. Inorg. Biochem. 102 (2008), 110–118.
97. Sochacka, M., Giebultowicz, J., Remiszewska, M., Suchocki, P., Wroczynski, P., Effects of Selol 5% supplementation on the activity or concentration of antioxidants and malondialdehyde level in the blood of healthy mice. Pharmacol. Rep. 66 (2014), 301–310.
98. Song, E., Su, C., Fu, J., Xia, X., Yang, S., Xiao, C., Lu, B., Chen, H., Sun, Z., Wu, S., Song, Y., Selenium supplementation shows protective effects against patulin-induced brain damage in mice via increases in GSH-related enzyme activity and expression. Life Sci. 109 (2014), 37–43.
99. Song, M., Kellum, J.A., Kaldas, H., Fink, M.P., Evidence that glutathione depletion is a mechanism responsible for the anti-inflammatory effects of ethyl pyruvate in cultured lipopolysaccharide-stimulated RAW 264.7 cells. J. Pharmacol. Exp. Ther. 308 (2004), 307–316.
100. Soudani, N., Troudi, A., Amara, I.B., Bouaziz, H., Boudawara, T., Zeghal, N., Ameliorating effect of selenium on chromium (VI)-induced oxidative damage in the brain of adult rats. J. Physiol. Biochem. 68 (2012), 397–409.
101. Spallholz, J.E., Selenium and glutathione peroxidase: essential nutrient and antioxidant component of the immune system. Adv. Exp. Med. Biol. 262 (1990), 145–158.
102. Su, X., Federoff, H.J., Immune responses in Parkinson's disease: interplay between central and peripheral immune systems. Biomed. Res. Int., 2014, 2014, 275178.
103. Tandon, P., Yang, Y., Das, K., Holmes, G.L., Stafstrom, C.E., Neuroprotective effects of brain-derived neurotrophic factor in seizures during development. Neuroscience 91 (1999), 293–303.
104. Tang, Y.L., Wang, S.W., Lin, S.M., Both inorganic and organic selenium supplements can decrease brain monoamine oxidase B enzyme activity in adult rats. Br. J. Nutr. 100 (2008), 660–665.
105. Tonges, L., Gunther, R., Suhr, M., Jansen, J., Balck, A., Saal, K.A., Barski, E., Nientied, T., Gotz, A.A., Koch, J.C., Mueller, B.K., Weishaupt, J.H., Sereda, M.W., Hanisch, U.K., Bahr, M., Lingor, P., Rho kinase inhibition modulates microglia activation and improves survival in a model of amyotrophic lateral sclerosis. Glia 62 (2014), 217–232.
106. Tsiotou, A.G., Sakorafas, G.H., Anagnostopoulos, G., Bramis, J., Septic shock; current pathogenetic concepts from a clinical perspective. Med. Sci. Monit. 11 (2005), Ra76–85.
107. Uttara, B., Singh, A.V., Zamboni, P., Mahajan, R.T., Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr. Neuropharmacol. 7 (2009), 65–74.
108. Victoria, F.N., Martinez, D.M., Castro, M., Casaril, A.M., Alves, D., Lenardao, E.J., Salles, H.D., Schneider, P.H., Savegnago, L., Antioxidant properties of (R)-Se-aryl thiazolidine-4-carboselenoate. Chem. Biol. Interact. 205 (2013), 100–107.
109. von Bernhardi, R., Eugenin-von Bernhardi, L., Eugenin, J., Microglial cell dysregulation in brain aging and neurodegeneration. Front. Aging Neurosci., 7, 2015, 124.
110. Wang, J., Wu, W.Y., Huang, H., Li, W.Z., Chen, H.Q., Yin, Y.Y., Biochanin a protects against lipopolysaccharide-induced damage of dopaminergic neurons both in vivo and in vitro via inhibition of microglial activation. Neurotox Res., 2016.
111. Wendel, A., Glutathione peroxidase. Methods Enzymol. 77 (1981), 325–333.
112. Whitton, P.S., Inflammation as a causative factor in the aetiology of Parkinson's disease. Br. J. Pharmacol. 150 (2007), 963–976.
113. Wirth, M.J., Brun, A., Grabert, J., Patz, S., Wahle, P., Accelerated dendritic development of rat cortical pyramidal cells and interneurons after biolistic transfection with BDNF and NT4/5. Development 130 (2003), 5827–5838.
114. Wrobel, J.K., Power, R., Toborek, M., Biological activity of selenium: Revisited. IUBMB Life 68 (2016), 97–105.
115. Xing, B., Xin, T., Hunter, R.L., Bing, G., Pioglitazone inhibition of lipopolysaccharide-induced nitric oxide synthase is associated with altered activity of p38 MAP kinase and PI3K/Akt. J. Neuroinflammation, 5, 2008, 4.
116. Xu, S.Z., Lee, S.H., Lillehoj, H.S., Bravo, D., Dietary sodium selenite affects host intestinal and systemic immune response and disease susceptibility to necrotic enteritis in commercial broilers. Br. Poult. Sci. 56 (2015), 103–112.
117. Xue, B., Wu, Y., Yin, Z., Zhang, H., Sun, S., Yi, T., Luo, L., Regulation of lipopolysaccharide-induced inflammatory response by glutathione S-transferase P1 in RAW264.7 cells. FEBS Lett. 579 (2005), 4081–4087.
118. Yanamoto, H., Xue, J.H., Miyamoto, S., Nagata, I., Nakano, Y., Murao, K., Kikuchi, H., Spreading depression induces long-lasting brain protection against infarcted lesion development via BDNF gene-dependent mechanism. Brain Res. 1019 (2004), 178–188.
119. Zhang, L.P., Wang, Q.S., Guo, X., Zhu, Y.J., Zhou, G.Z., Xie, K.Q., Time-dependent changes of lipid peroxidation and antioxidative status in nerve tissues of hens treated with tri-ortho-cresyl phosphate (TOCP). Toxicology 239 (2007), 45–52.
120. Zuccato, C., Cattaneo, E., Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 5 (2009), 311–322.