Agaricus blazei extract abrogates rotenone-induced dopamine depletion and motor deficits by its anti-oxidative and anti-inflammatory properties in Parkinsonic mice

References

• Connolly BS, Lang AE. Pharmacological treatment of Parkinson disease: a review. JAMA 2014;311:1670–83. doi: 10.1001/jama.2014.3654
   PubMed Web of Science ®Google Scholar
• Natale G, Kastsiushenka O, Fulceri F, Ruggieri S, Paparelli A, Fornai F. MPTP-induced parkinsonism extends to a subclass of TH-positive neurons in the gut. Brain Res 2010;355:195–206. doi: 10.1016/j.brainres.2010.07.076
   Web of Science ®Google Scholar
• Maslin P. Rotenone. Pesticide News 2001;54:20–1.
   Google Scholar
• Hisata JS. Lake and stream rehabilitation: rotenone use and health risks. Final supplemental environmental impact statement. Olympia, WA: Department of Fish and Wildlife; 2002.
   Google Scholar
• Horgan DJ, Ohno H, Singer TP. Studies on the respiratory chain-linked reduced nicotinamide adenine dinucleotide dehydrogenase. XV. interactions of piericidin with the mitochondrial respiratory chain. J Biol Chem 1968;243:5967–76.
   PubMed Web of Science ®Google Scholar
• Schuler F, Casida JE. Functional coupling of PSST and ND1 subunits in NADH: ubiquinone oxidoreductase established by photo affinity labeling. Biochim Biophys Acta 2001;1506:79–87. doi: 10.1016/S0005-2728(01)00183-9
   PubMed Web of Science ®Google Scholar
• Dhanalakshmi C, Janakiraman U, Manivasagam T, Thenmozhi AJ, Essa MM, Kalandar A, et al. Vanillin attenuated behavioural impairments, neurochemical deficts, oxidative stress and apoptosis against rotenone induced rat model of Parkinson’s disease. Neurochem Res 2016;41:1899–910. doi: 10.1007/s11064-016-1901-5
   PubMed Web of Science ®Google Scholar
• Corona JC, Gimenez-Cassina A, Lim F, Diaz-Nido J. Hexokinase II gene transfer protects against neurodegeneration in the rotenone and MPTP mouse models of Parkinson’s disease. J Neurosci Res. 2010;88:1943–50.
   PubMed Web of Science ®Google Scholar
• Gao HM, Liu B, Hong JS. Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J Neurosci 2003;23:6181–7.
   PubMed Web of Science ®Google Scholar
• Hirsch EC, Hunot S. Neuroinflammation in Parkinson’s disease: a target for neuroprotection? Lancet Neurol 2009;8:382–97. doi: 10.1016/S1474-4422(09)70062-6
   PubMed Web of Science ®Google Scholar
• Wang H, Fu Z, Han C. The medicinal values of culinary-medicinal royal sun mushroom (Agaricus blazei Murrill). Evid Based Complement Alternat Med 2013;2013:842619.
   PubMedGoogle Scholar
• Val CH, Brant F, Miranda AS, Rodrigues FG, Oliveira BC, Santos EA, et al. Effect of mushroom agaricus blazei on immune response and development of experimental cerebral malaria. Malar J 2015;4:311. doi: 10.1186/s12936-015-0832-y
   Web of Science ®Google Scholar
• Soares AA, de Oliveira AL, de Sá-Nakanishi AB, Comar JF, Rampazzo AP, Vicentini FA, et al. Effects of an Agaricus blazei aqueous extract pretreatment on paracetamol-induced brain and liver injury in rats. Biomed Res Int 2013;2013:469180.
   PubMedGoogle Scholar
• deSá-Nakanishi AB, Soares AA, Natali MRM, Comar JF, Peralta RM, Bracht A. Effects of the continuous administration of an Agaricus blazei extract to rats on oxidative parameters of the brain and liver during aging. Molecules 2014;19:18590–603. doi: 10.3390/molecules191118590
   PubMed Web of Science ®Google Scholar
• Johnson E, Forland DT, Saetre L, Bernardshaw SV, Lyberg T, Hetland G. Effect of an extract based on the medicinal mushroom Agaricus blazei murill on release of cytokines, chemokines and leukocyte growth factors in human blood ex vivo and in vivo. Scand J Immunol 2009;69:242–50. doi: 10.1111/j.1365-3083.2008.02218.x
   PubMed Web of Science ®Google Scholar
• Richter F, Hamann M, Richter A. Chronic rotenone treatment induces behavioral effects but no pathological signs of parkinsonism in mice. J Neurosci Res 2007;85:681–91. doi: 10.1002/jnr.21159
   PubMed Web of Science ®Google Scholar
• Santosa JR, Cunhaa JA, Dierschnabela AL, Campeloa CLC, Leaoa AHF, Silva AH, et al. Cognitive, motor and tyrosine hydroxylase temporal impairment in a model of parkinsonism induced by reserpine. Behav Brain Res 2013;253:68–77. doi: 10.1016/j.bbr.2013.06.031
   PubMed Web of Science ®Google Scholar
• Abdelkader NF, Arafa NM, Attia AS, Ain-Shoka AA, Abdallah DM. Pyrrolidinedithiocarbamate ameliorates rotenone-induced Parkinson’s disease in rats. Bulletin Facult Pharmacy Cairo Univ 2016;55:107–13. doi: 10.1016/j.bfopcu.2016.11.003
   Google Scholar
• Rajasankar S, Manivasagam T, Surendran S. Ashwagandha leaf extract: A potential agent in treating oxidative damage and physiological abnormalities seen in a mouse model of Parkinson’s disease. Neurosci Lett 2009;454:11–5. doi: 10.1016/j.neulet.2009.02.044
   PubMed Web of Science ®Google Scholar
• Rozas G, Guerra MJ, Labandeira-García JL. An automated rotarod method for quantitative drug–free evaluation of overall motor deficits in rat models of parkinsonism. Brain Res. Brain Res Protoc 1997;2:75–84. doi: 10.1016/S1385-299X(97)00034-2
   PubMedGoogle Scholar
• Tillerson JL, Miller GW. Grid performance test to measure behavioral impairment in the MPTP-treated mouse model of Parkinsonism. J Neurosci Methods 2003;123:189–200. doi: 10.1016/S0165-0270(02)00360-6
   PubMed Web of Science ®Google Scholar
• Muralikrishnan D, Mohanakumar KP. Neuroprotection by bromocriptine against 1-methyl 4-phenyl 1,2,3,6 tetrahydropyridine induced neurotoxicity in mice. FASEB J 1998;12:905–12. doi: 10.1096/fasebj.12.10.905
   PubMed Web of Science ®Google Scholar
• Utley HC, Bernheim F, Hochslein P. Effect of sulfhydryl reagent on peroxidation in microsome. Arch Biochem Biophys 1967;118:29–32. doi: 10.1016/0003-9861(67)90273-1
   Web of Science ®Google Scholar
• Tamilselvam K, Nataraj J, Janakiraman U, Manivasagam T, Essa MM. Antioxidant and anti-inflammatory potential of hesperidin against 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced experimental Parkinson's disease in mice. Int J Nutr Pharmacol Neurol Dis 2013;3:294–302. doi: 10.4103/2231-0738.114875
   Google Scholar
• Jollow DJ, Mitchell JR, Zampagloine N, Gillette JR. Bromobenzene-induced liver necrosis: protective role of glutathione and evidence for 3, 4 bromobenzeneoxide as the hepatotoxic intermediate. Pharmacol 1974;11:151–69. doi: 10.1159/000136485
   PubMed Web of Science ®Google Scholar
• Mohandas J, Marshall JJ, Duggin GG, Horvath JS, Tiller D. Differential distribution of glutathione and glutathione related enzymes in rabbit kidneys: Possible implication in analgesic neuropathy. Biochem Pharmacol 1984;33:1801–7. doi: 10.1016/0006-2952(84)90353-8
   PubMed Web of Science ®Google Scholar
• Claiborne A. Catalase activity. In: RA Greenwald, (eds.) CRC handbook of methods for oxygen radical research. Boca Raton, FL: CRC Press; 1985. p. 283–4.
   Google Scholar
• Oberley LW, Spitz DR. Assay of superoxide dismutase activity in tumor tissue. Methods Enzymol 1984;l05:457–64. doi: 10.1016/S0076-6879(84)05064-3
   Google Scholar
• Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265–75.
   PubMed Web of Science ®Google Scholar
• Anandhan A, Tamilselvam K, Radhiga T, Rao S, Essa MM, Manivasagam T. Theaflavin, a black tea polyphenol, protects nigral dopaminergic neurons against chronic MPTP/probenecid induced Parkinson’s disease. Brain Res 2012;1433:104–13. doi: 10.1016/j.brainres.2011.11.021
   PubMed Web of Science ®Google Scholar
• Fernagut PO, Diguet E, Stefanova N, Biran M, Wenning GK, Canioni P, et al. Subacute systemic 3-nitropro-pionic acid intoxication induces a distinct motor disorder in adult C57Bl/6 mice: behavioural and histopathological characterisation. Neuroscience 2002;114:1005–17. doi: 10.1016/S0306-4522(02)00205-1
   PubMed Web of Science ®Google Scholar
• Sedelis M, Schwarting RK, Huston JP. Behavioral phenotyping of the MPTP mouse model of Parkinson’s disease. Behav Brain Res 2001;125:109–25. doi: 10.1016/S0166-4328(01)00309-6
   PubMed Web of Science ®Google Scholar
• Recchia A, Rota D, Debetto P, Peroni D, Guidolin D, Negro A, et al. Generation of a alpha-synuclein-based rat model of Parkinson’s disease. Neurobiol Dis 2008;30:8–18. doi: 10.1016/j.nbd.2007.11.002
   PubMed Web of Science ®Google Scholar
• Thiffault C, Langston JW, Di Monte DA. Increased striatal dopamine turnover following acute administration of rotenone to mice. Brain Res 2000;885(2):283–8. doi: 10.1016/S0006-8993(00)02960-7
   PubMed Web of Science ®Google Scholar
• Gao ZG, Cui WY, Zhang HT, Liu CG. Effects of nicotine on 1-methyl, 4-phenyl 1,2,3,6 tetrahydropyridine induced depression of striatal dopamine content and spontaneous locomotor activity in C57 black mice. Pharmacol Res 1998;38:101–6. doi: 10.1006/phrs.1998.0337
   PubMed Web of Science ®Google Scholar
• Zhang C, Gao X, Sun Y, Sun X, Wu Y, Liu Y, et al. Anxiolytic effects of royal sun medicinal mushroom, Agaricus brasiliensis (Higher Basidiomycetes) on Ischemia-induced anxiety in rats. Int J Med Mushrooms 2015;17:1–10. doi: 10.1615/IntJMedMushrooms.v17.i1.10
   PubMed Web of Science ®Google Scholar
• Floyd RA. Antioxidants, oxidative stress, and degenerative neurological disorders. Proc Soc Exp Biol Med 1999;222:236–45. doi: 10.1046/j.1525-1373.1999.d01-140.x
   PubMed Web of Science ®Google Scholar
• Seaton TA, Cooper JM, Schapira AH. Free radical scavengers protect dopaminergic cell lines from apoptosis induced by complex I inhibitors. Brain Res 1997;777:110–8. doi: 10.1016/S0006-8993(97)01034-2
   PubMed Web of Science ®Google Scholar
• Dexter DT, Carter CJ, Wells FR, Javoy-Agid F, Agid Y, Lees A, et al. Basal lipid peroxidation in substantia nigra is increased in Parkinson’s disease. J Neurochem 1989;52:381–9. doi: 10.1111/j.1471-4159.1989.tb09133.x
   PubMed Web of Science ®Google Scholar
• Saravanan KS, Sindhu KM, Mohanakumar KP. Melatonin protects against rotenone-induced oxidative stress in a hemiparkinsonian rat model. J Pineal Res 2007;42:247–53. doi: 10.1111/j.1600-079X.2006.00412.x
   PubMed Web of Science ®Google Scholar
• Carneiro AAJ, Ferreira ICFR, Dueñas M, Barros L, da Silva R, Gomes E, et al. Chemical composition and antioxidant activity of dried powder formulations of Agaricus blazei and Lentinusedodes. Food Chem 2013;138:2168–73. doi: 10.1016/j.foodchem.2012.12.036
   PubMed Web of Science ®Google Scholar
• Hakime-silva RA, Vellosa JC, Khalil NM, Khalil OA, Brunetti IL, Oliveira OM. Chemical, enzymatic and cellular antioxidant activity studies of Agaricus blazei Murrill. An Acad Bras Cienc 2013;85:1073–81. doi: 10.1590/S0001-37652013005000044
   PubMed Web of Science ®Google Scholar
• Greenwood B. Review: intermittent preventive treatment – A new approach to the prevention of malaria in children in areas with seasonal malaria transmission. Trop Med Int Health 2006;11:983–91. doi: 10.1111/j.1365-3156.2006.01657.x
   PubMed Web of Science ®Google Scholar
• Abrahamsson PA. Potential benefits of intermittent androgen suppression therapy in the treatment of prostate cancer: a systematic review of the literature. Eur Urol 2010;57:49–59. doi: 10.1016/j.eururo.2009.07.049
   PubMed Web of Science ®Google Scholar
• Hissin PJ, Hilf RA. Fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976;74:214–26. doi: 10.1016/0003-2697(76)90326-2
   PubMed Web of Science ®Google Scholar
• Sedlak J, Lindsay RH. Estimation of total, protein-bound and non-protein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 1968;25:192–205. doi: 10.1016/0003-2697(68)90092-4
   PubMed Web of Science ®Google Scholar
• de Sá-Nakanishi AB, Soares AA, de Oliveira AL, Comar JF, Peralta RM, Bracht A. Effects of treating old rats with an aqueous Agaricus blazei extract on oxidative and functional parameters of the brain tissue and brain mitochondria. Oxid Med Cell Longev 2014;2014:563179. doi: 10.1155/2014/563179
   PubMed Web of Science ®Google Scholar
• Subash S, Essa MM, Al-Asmi A, Al-Adawi S, Vaishnav R, Braidy N, et al. Pomegranate from Oman alleviates the brain oxidative damage in transgenic mouse model of Alzheimer’s disease. J Trad Complemen Med 2014;4:232–8. doi: 10.4103/2225-4110.139107
   PubMedGoogle Scholar
• Muthaiyah B, Essa MM, Lee M, Chauhan V, Kaur K, Chauhan A. Dietary supplementation of walnuts improves memory deficits and learning skills in transgenic mouse model of Alzheimer's disease. J Alz Dis 2014;42:1397–405.
   PubMed Web of Science ®Google Scholar
• Rausch WD, Hirata Y, Nagatsu T, Riederer P, Jellinger K. Tyrosine hydroxylase activity in caudate nucleus from Parkinson’s disease: effects of iron and phophorylating agents. J Neurochem. 1988;50:202–8. doi: 10.1111/j.1471-4159.1988.tb13250.x
   PubMed Web of Science ®Google Scholar
• Borges CR, Geddes T, Watson JT, Kuhn DM. Dopamine biosynthesis is regulated by S-glutathionylation potential mechanism of tyrosine hydroxylase inhibition during oxidative stress. J Biol Chem. 2002;277:48295–302. doi: 10.1074/jbc.M209042200
   PubMed Web of Science ®Google Scholar
• Giustarini D, Rossi R, Milzani A, Colombo R, Dalle-Donne I. S-glutathionylation: from redox regulation of protein functions to human diseases. J Cell Mol Med. 2004;8:201–12. doi: 10.1111/j.1582-4934.2004.tb00275.x
   PubMed Web of Science ®Google Scholar
• Oyagi A, Oida Y, Hara H, Izuta H, Shimazawa M, Matsunaga N, et al. Protective effect of SUN N8075, a novel agent with antioxidant properties, in in vitro and in vivo madels of Parkinson’s disease. Brain Res. 2008;1214:169–76. doi: 10.1016/j.brainres.2008.02.073
   PubMed Web of Science ®Google Scholar
• McGeer PL, McGeer EG. Glial reactions in Parkinson’s disease. Mov Disord 2008;23:474–83. doi: 10.1002/mds.21751
   PubMed Web of Science ®Google Scholar
• Sawada M, Imamura K, Nagatsu T. Role of cytokines in inflammatory process in Parkinson's disease. J Neural Transm Suppl 2006;70:373–81. doi: 10.1007/978-3-211-45295-0_57
   PubMedGoogle Scholar
• Khan MM, Kempuraj D, Thangavel R, Zaheer A. Protection of MPTP-induced neuroinflammation and neurodegeneration by pycnogenol. Neurochem. Int 2006;62:379–88. doi: 10.1016/j.neuint.2013.01.029
   Web of Science ®Google Scholar
• Damier P, Hirsch EC, Zhang P, Agid Y, Javoy-Agid F. Glutathione peroxidase, glial cells and Parkinson’s disease. Neuroscience. 1993;52:1–6. doi: 10.1016/0306-4522(93)90175-F
   PubMed Web of Science ®Google Scholar
• Niranjan R. The role of inflammatory and oxidative stress mechanisms in the pathogenesis of Parkinson's disease: focus on astrocytes. Mol Neurobiol 2014;49:28–38. doi: 10.1007/s12035-013-8483-x
   PubMed Web of Science ®Google Scholar
• Litteljohn D, Mangano E, Clarke M, Bobyn J, Moloney K, Hayley S. Inflammatory mechanisms of neurodegeneration in toxin-based models of Parkinson's disease. Parkinsons Dis 2010;2011:713517.
   PubMedGoogle Scholar
• Mogi M, Harada M, Kondo T, Mizuno Y, Narabayashi H, Riederer P. Bcl-2 protein is increased in the brain from parkinsonian patients. Neurosci Lett 1996;215:137–9. doi: 10.1016/0304-3940(96)12961-X
   PubMed Web of Science ®Google Scholar
• Forland DT, Johnson E, Saetre L, Lyberg T, Lygren I, Hetland G. Effect of an extract based on the medicinal mushroom Agaricus blazei Murill on expression of cytokines and calprotectin in patients with ulcerative colitis and Crohn’s disease. Scand J Immunol 2011;73:66–75. doi: 10.1111/j.1365-3083.2010.02477.x
   PubMed Web of Science ®Google Scholar
• Selvakumar GP, Janakiraman U, Essa MM, Justin Thenmozhi A, Manivasagam T. Escin attenuates behavioral impairments, oxidative stress and inflammation in a chronic MPTP/probenecid mouse model of Parkinson's disease. Brain Res 2014;1585:23–36. doi: 10.1016/j.brainres.2014.03.010
   PubMed Web of Science ®Google Scholar
• Ohja S, Javed H, Azimullah S, AbulKhair SB, Haque MH. Glycyrrhizic acid attenuates neuroinflammation and oxidative stress in rotenone model of Parkinson’s disease. Neurotox Res 2016;29:275–87. doi: 10.1007/s12640-015-9579-z
   PubMed Web of Science ®Google Scholar
• Wang P, Li XT, Sun L, Shen L. Anti-Inflammatory activity of water soluble polysaccharide of Agaricus blazei Murill on ovariectomized osteopenic rats. Evid Based Complement Alternat Med 2013;2013:164817.
   PubMedGoogle Scholar
• Yu L, Yang S, Sun L, Jiang YF, Zhu LY. Effects of selenium-enriched Agaricus blazei Murill on liver metabolic dysfunction in mice, a comparison with selenium-deficient Agaricus blazei Murill and sodium selenite. Biol Trace Elem Res 2014;160:79–84. doi: 10.1007/s12011-014-0022-8
   PubMed Web of Science ®Google Scholar
• Numakawa T, Matsumoto T, Numakawa Y, Richards M, Yamawaki S. Protective action of neurotrophic factors and estrogen against oxidative stress-mediated neurodegeneration. J Toxicol 2011;2011:405194. doi: 10.1155/2011/405194
   PubMedGoogle Scholar
• Venkatesh Gobi V, Rajasankar S, Ramkumar M, Dhanalakshmi C, Manivasagam T, Justin Thenmozhi A, et al. Agaricus blazei extract attenuates rotenone-induced apoptosis through its mitochondrial protective and antioxidant properties in SH-SY5Y neuroblastoma cells. Nutr Neurosci 2016:1–11 (in press).
   Google Scholar