Abstract
Parkinson disease (PD) is a chronic progressive neurodegenerative disease characterized by both motor and non-motor features. Numerous risk factors (oxidative stress, free radical formation, and several environmental toxins) have been associated with PD. The experimental studies were carried out under in vivo conditions. Biochemical data analysis indicated that compared with the parameters of control (C) rats, rotenone-induced PD rats showed a significant decrease in the specific content of the total fraction of isoforms of O2−-producing, heat-stable, NADPH-containing associates (NLP-Nox) from membrane formations of tissues (brain, liver, lung, and small intestine). Compared with the C group indices, in the PD and PD + curcumin (PD + CU) groups there is some change in the shape of the optical absorption spectra of isoforms associated with a change in the amount of Nox in the isoform composition of the total fraction of the NLP-Nox associate. Thus, daily administration of CU (200 mg/kg, i.p.) to PD rats for 63 days had a regulatory effect, bringing the specific content and O2−-producing activity of the total fraction of NLP-Nox isoforms closer to the norm. CU has membrane-stabilizing effects in rotenone-induced PD.
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References
Ak T, Gülçin I (2008) Antioxidant and radical scavenging properties of curcumin. Chem Biol Interact 174(1):27–37
Amano S, Ohashi M, Kirihara M, Yang XH, Hazama F (1994) Alpha-tocopherol protects against radical-induced injury in cultured neurons. Neurosci Lett 170:55–58
Amer SA, El-Araby DA, Tartor H, Farahat M, Goda NIA, Farag MFM, Fahmy EM, Hassan AM, Abo El-Maati MF, Osman A (2022) Long-Term Feeding with Curcumin Affects the Growth, Antioxidant Capacity, Immune Status, Tissue Histoarchitecture, Immune Expression of Proinflammatory Cytokines, and Apoptosis Indicators in Nile Tilapia, Oreochromis niloticus. Antioxidants 11(5):937
Andrés CMC, Pérez de la Lastra JM, Andrés Juan C, Plou FJ, Pérez-Lebeña E (2023) Superoxide Anion Chemistry-Its Role at the Core of the Innate Immunity. Int J Mol Sci 24(3):1841
Banach T, Zurowski D, Kania D, Thor PJ (2005) Myoelectrical activity of small intestine in rats with experimental Parkinson’s disease. Folia Med Cracov 46(3–4):119–124
Belarbi K, Cuvelier E, Destée A, Gressier B, Chartier-Harlin MC (2017) NADPH oxidases in Parkinson’s disease: a systematic review. Mol Neurodegener 12(1):84
Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT (2000) Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat Neurosci 3:1301–1306
Bolam JP, Pissadaki EK (2012) Living on the edge with too many mouths to feed: Why dopamine neurons die. Mov Disord 27:1478–1483
Boroumand N, Saeed S, Seyed I (2018) Immunomodulatory, anti-inflammatory, and antioxidant effects of curcumin. J Herbmed Pharmacol 7:211–219
Cannon JR, Tapias V, Na HM, Honick AS, Drolet RE, Greenamyre JT (2009) A highly reproducible rotenone model of Parkinson’s disease. Neurobiol Dis 34:279–290
Cersosimo MG, Benarroch EE (2012) Pathological correlates of gastrointestinal dysfunction in Parkinson’s disease. Neurobiol Dis 46(3):559–564
Chang KH, Chen CM (2020) The Role of Oxidative Stress in Parkinson’s Disease. Antioxidants (Basel) 9(7):597
Darbinyan L, Hambardzumyan L, Manukyan L, Simonyan K, Sarkisian V (2022) Curcumin prevented electrophysiological and behavioral alterations in a rotenone model of Parkinson’s disease. MovDisord 37(S2):S614. https://doi.org/10.1002/mds.29223
Darbinyan LV, Simonyan KV, Hambardzumyan LE, Manukyan LP, Badalyan SH, Sarkisian VH (2022) Protective effect of curcumin against rotenone-induced substantianigra pars compacta neuronal dysfunction. Metab Brain Dis 37(4):1111–1118
Farombi EO, Awogbindin IO, Olorunkalu PD, Ogbuewu E, Oyetunde BF, Agedah AE, Adeniyi PA (2020) Kolaviron protects against nigrostriatal degeneration and gut oxidative damage in a stereotaxic rotenone model of Parkinson’s disease. Psychopharmacology 237(11):3225–3236
Goldstein NI, Goldstein RN, Merzlyak MN (1992) Negative air ions as a source of superoxide. Int J Biometeorol 36:118–122
Greene JG, Noorian AR, Srinivasan S (2009) Delayed gastric emptying and enteric nervous system dysfunction in the rotenone model of Parkinson’s disease. Exp Neurol 218:154–161
Gupta RC (2014) Biomarkers in toxicology. Elsevier, Academic Press, Kentucky
Haddad D, Nakamura K (2015) Understanding the susceptibility of dopamine neurons to mitochondrial stressors in Parkinson’s disease. FEBS Lett 589:3702–3713
Hocking AJ, Elliot D, Hua J, Klebe S (2018) Administering Fixed Oral Doses of Curcumin to Rats through Voluntary Consumption. J Am Assoc Lab Anim Sci 57(5):508–512
Hunn BH, Cragg SJ, Bolam JP, Spillantini MG, Wade-Martins R (2015) Impaired intracellular trafficking defines early Parkinson’s disease. Trends Neurosci 38:178–188
Jakubczyk K, Drużga A, Katarzyna J, Skonieczna-Żydecka K (2020) Antioxidant Potential of Curcumin-A Meta-Analysis of Randomized Clinical Trials. Antioxidants (Basel) 9(11):1092
Jha NS, Mishra S, Jha SK, Surolia A (2015) Antioxidant Activity and Electrochemical Elucidation of the Enigmatic Redox Behavior of Curcumin and Its Structurally Modified Analogues. Electrochim Acta 151:574–583
Kim TY, Leem E, Lee JM, Kim SR (2020) Control of Reactive Oxygen Species for the Prevention of Parkinson’s Disease: The Possible Application of Flavonoids. Antioxidants (Basel) 9(7):583
Kocaadam B, Şanlier N (2017) Curcumin, an active component of turmeric (Curcuma longa), and its effects on health. Crit Rev Food SciNutr 57(13):2889–2895
Lin KJ, Lin KL, Chen SD, Liou CW, Chuang YC, Lin HY, Lin TK (2019) The Overcrowded Crossroads: Mitochondria, Alpha-Synuclein, and the Endo-Lysosomal System Interaction in Parkinson’s Disease. Int J Mol Sci 20(21):5312
Martín-Aragón S, Benedí JM, Villar AM (1997) Modifications on antioxidant capacity and lipid peroxidation in mice under fraxetin treatment. J Pharm Pharmacol 49(1):49–52
Meiser J, Weindl D, Hiller K (2013) Complexity of dopamine metabolism. Cell Commun Signal 11:34
Motterlini R, Foresti R, Bassi R, Green CJ (2000) Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Radic Biol Med 28:1303–1312
Nuzzo G, Senese G, Gallo C, Albiani F, Romano L, d’Ippolito G, Manzo E, Fontana A (2022) Antitumor Potential of Immunomodulatory Natural Products. Mar Drugs 20(6):386
Ojha S, Javed H, Azimullah S, Abul Khair SB, Haque ME (2016) Glycyrrhizic acid Attenuates Neuroinflammation and Oxidative Stress in Rotenone Model of Parkinson’s Disease. Neurotox Res 29(2):275–287
Panov A, Dikalov S, Shalbuyeva N, Taylor G, Sherer T, Greenamyre JT (2005) Rotenone model of Parkinson disease: Multiple brain mitochondria dysfunctions after short term systemic rotenone intoxication. J Biol Chem 280:42026–42035
Patel BA, Arundell M, Parker KH, Yeoman MS, OHare D (2005) Simple and rapid determination of serotonin and catecholamines in biolog-ical tissue using high-performance liquid chromatography with elec-trochemical detection. J Chromatogr B 818(2):269–276
Picca A, Guerra F, Calvani R, Romano R, Coelho-Júnior HJ, Bucci C, Marzetti E (2021) Mitochondrial Dysfunction, Protein Misfolding and Neuroinflammation in Parkinson’s Disease: Roads to Biomarker Discovery. Biomolecules 11(10):1508
Quigley EM (1996) Gastrointestinal dysfunction in Parkinson’s disease. Semin Neurol 16(3):245–250
Requejo-Aguilar R, Bolaños JP (2016) Mitochondrial control of cell bioenergetics in Parkinson’s disease. Free RadicBiol Med 100:123–137
Russo R, Cristiano C, Avagliano C, De Caro C, La Rana G, Raso GM, Canani RB, Meli R, Calignano A (2018) Gut-brain Axis: Role of Lipids in the Regulation of Inflammation, Pain and CNS Diseases. Curr Med Chem 25(32):3930–3952
Simonyan MA, Karapetyan AV, Babayan MA, Simonyan RM (1996) NADPH-containing superoxide-producing lipoprotein fraction of Blood Serum. Isolation, purification, brief characterization and mechanism of action. Biochemistry (Moscow) 61(5):932–938
Simonyan RM, Simonyan KV, Simonyan GM, Khachatryan HS, Babayan MA, Danielyan MH, Darbinyan LV, Simonyan MA (2022) Superoxide-producing thermostable associate from the small intestines of control and alloxan-induced diabetic rats: quantitative and qualitative changes. BMC Endocr Disord 22(1):250
Simonyan RM, Simonyan MA (2021) Method of preparation of superoxide producing thermostable systems from biomembranes and biofluids. Licence of Invention AM, N 618 Y,Yerevan, Armenia
Spielman LJ, Gibson DL, Klegeris A (2018) Unhealthy gut, unhealthy brain: The role of the intestinal microbiota in neurodegenerative diseases. Neurochem Int 120:149–163
Steel BC, McKenzie DR, Bilek MM, Nosworthy NJ, dos Remedios CG (2006) Nanosecond responses of proteins to ultra-high temperature pulses. Biophys J 91(6):L66–L68
Su LJ, Zhang JH, Gomez H, Murugan R, Hong X, Xu D, Jiang F, Peng ZY (2019) Reactive Oxygen Species-Induced Lipid Peroxidation in Apoptosis, Autophagy, and Ferroptosis. Oxid Med Cell Longev 13(2019):5080843
Sun MF, Shen YQ (2018) Dysbiosis of gut microbiota and microbial metabolites in Parkinson’s Disease. Ageing Res Rev 45:53–61
Tanner CM (1991) Liver enzyme abnormalities in Parkinson’s disease. Geriatrics 46(Suppl 1):60–63
Ursell LK, Metcalf JL, Parfrey LW, Knight R (2012) Defining the human microbiome. Nutr Rev 70 Suppl 1(Suppl 1):S38–44
van Kessel SP, Bullock A, van Dijk G, El Aidy S (2022) Parkinson’s Disease Medication Alters Small Intestinal Motility and Microbiota Composition in Healthy Rats. mSystems 7(1):e0119121
Varesi A, Campagnoli LIM, Fahmideh F, Pierella E, Romeo M, Ricevuti G, Nicoletta M, Chirumbolo S, Pascale A (2022) The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment. Int J Mol Sci 23(20):12289
Vitek L, Schwertner HA (2007) The heme catabolic pathway and its protective effects on oxidative stress-mediated diseases. Adv Clin Chem 43:1–57
Wang H, Huo M, Jin Y, Wang Y, Wang X, Yu W, Jiang X (2022) Rotenone induces hepatotoxicity in rats by activating the mitochondrial pathway of apoptosis. ToxicolMech Methods 32(7):510–517
Wright JS (2002) Predicting the Antioxidant Activity of Curcumin and Curcuminoids. J Mol Struct THEOCHEM 591:207–217
Xin WJ, Zhao BL, Li XJ et al (1990) Scavenging effects of chinese herbs and natural health products on active oxygen radicals. Res ChemIntermed 14:171
Yuandani JI, Rohani AS, Sumantri IB (2021) Immunomodulatory Effects and Mechanisms of Curcuma Species and Their Bioactive Compounds: A Review. Front Pharmacol 12:643119
Zhang H, Chen Y, Wang Z, Xie G, Liu M, Yuan B, Chai H, Wang W, Cheng P (2022) Implications of Gut Microbiota in Neurodegenerative Diseases. Front Immunol 13:785644
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All authors contributed to the study conception and design. LVD, MAS, RMS, KVS, LEH and LPM designed the study and conducted the experiment. KVS, LVD and MAS wrote the manuscript. All authors contributed to the revision final version of the manuscript.
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This study was performed in accordance with the principles of laboratory animal care of the Ethics Committee of Yerevan State Medical University (Yerevan, Armenia) and in accordance with the decision of 22 September 2010 of the Council of European Communities [2010/63/EU] and with “ARRIVE” guidelines (Animals in Research Reporting in vivo Experiments). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All methods were carried out in accordance with relevant guidelines and regulations.
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Darbinyan, L.V., Simonyan, K.V., Hambardzumyan, L.E. et al. Membrane-stabilizing and protective effects of curcumin in a rotenone-induced rat model of Parkinson disease. Metab Brain Dis 38, 2457–2464 (2023). https://doi.org/10.1007/s11011-023-01237-z
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DOI: https://doi.org/10.1007/s11011-023-01237-z