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Omega-3 Attenuates Disrupted Neurotransmission and Partially Protects Metabolic Dysfunction Caused by Obesity in Wistar Rats.

التفاصيل البيبلوغرافية
العنوان: Omega-3 Attenuates Disrupted Neurotransmission and Partially Protects Metabolic Dysfunction Caused by Obesity in Wistar Rats.
المؤلفون: de Farias Fraga G; Graduate Program in Biosciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., da Silva Rodrigues F; Graduate Program in Biosciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Jantsch J; Graduate Program in Biosciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Silva Dias V; Biomedical Science Undergraduate Program, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Milczarski V; Biomedical Science Undergraduate Program, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Wickert F; Biomedical Science Undergraduate Program, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Pereira Medeiros C; Biomedical Science Undergraduate Program, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Eller S; Graduate Program in Health Sciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Gatto Barschak A; Graduate Program in Health Sciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Giovenardi M; Graduate Program in Biosciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil.; Graduate Program in Health Sciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil., Padilha Guedes R; Graduate Program in Biosciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil. renata.guedes@ufcspa.edu.br.; Graduate Program in Health Sciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil. renata.guedes@ufcspa.edu.br.
المصدر: Neurochemical research [Neurochem Res] 2024 Oct; Vol. 49 (10), pp. 2763-2773. Date of Electronic Publication: 2024 Jul 03.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Kluwer Academic/Plenum Publishers Country of Publication: United States NLM ID: 7613461 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-6903 (Electronic) Linking ISSN: 03643190 NLM ISO Abbreviation: Neurochem Res Subsets: MEDLINE
أسماء مطبوعة: Publication: 1999- : New York, NY : Kluwer Academic/Plenum Publishers
Original Publication: New York, Plenum Press
مواضيع طبية MeSH: Rats, Wistar* , Fatty Acids, Omega-3*/pharmacology , Fatty Acids, Omega-3*/metabolism , Obesity*/metabolism , Synaptic Transmission*/drug effects, Animals ; Male ; Rats ; Dietary Supplements ; Muscle, Skeletal/metabolism ; Muscle, Skeletal/drug effects
مستخلص: Omega-3 (n3) is a polyunsaturated fatty acid well known for its anti-inflammatory and neuroprotective properties. Obesity is linked to chronic inflammation that disrupts metabolism, the intestine physiology and the central nervous system functioning. This study aims to determine if n3 supplementation can interfere with the effects of obesity on the mitochondrial activity, intestinal barrier, and neurotransmitter levels in the brain of Wistar rats that received cafeteria diet (CAF). We examined adipose tissue, skeletal muscle, plasma, intestine, and the cerebral cortex of four groups: CT (control diet), CTn3 (control diet with n3 supplementation), CAF, and CAFn3 (CAF and n3). Diets were offered for 13 weeks, with n3 supplementation in the final 5 weeks. Adipose tissue Electron Transport Chain complexes I, II, and III showed higher activity in CAF groups, as did complexes III and IV in skeletal muscle. Acetate levels in plasma were reduced in CAF groups, and Lipopolysaccharide (LPS) was higher in the CAF group but reduced in CAFn3 group. Claudin-5 in the intestine was lower in CAF groups, with no n3 supplementation effect. In the cerebral cortex, dopamine levels were decreased with CAF, which was reversed by n3. DOPAC, a dopamine metabolite, also showed a supplementation effect, and HVA, a diet effect. Serotonin levels increased in the CAF group that received supplementation. Therefore, we demonstrate disturbances in mitochondria, plasma, intestine and brain of rats submitted to CAF and the potential benefit of n3 supplementation in endotoxemia and neurotransmitter levels.
(© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)
References: Djuricic I, Calder PC (2021) Beneficial outcomes of omega-6 and omega-3 polyunsaturated fatty acids on human health: an update for 2021. Nutrients 13:2421. https://doi.org/10.3390/nu13072421. (PMID: 10.3390/nu13072421343719308308533)
Chalon S (2006) Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot Essent Fatty Acids 75:259–269. https://doi.org/10.1016/j.plefa.2006.07.005. (PMID: 10.1016/j.plefa.2006.07.00516963244)
Devarshi PP, Grant RW, Ikonte CJ, Hazels Mitmesser S (2019) Maternal omega-3 nutrition, placental transfer and fetal brain development in gestational diabetes and preeclampsia. Nutrients 11:1107. https://doi.org/10.3390/nu11051107. (PMID: 10.3390/nu11051107311090596567027)
Shahidi F, Ambigaipalan P (2018) Omega-3 polyunsaturated fatty acids and their health benefits. Annu Rev Food Sci Technol 9:345–381. https://doi.org/10.1146/annurev-food-111317-095850. (PMID: 10.1146/annurev-food-111317-09585029350557)
Liao Y, Xie B, Zhang H et al (2019) Efficacy of omega-3 PUFAs in depression: a meta-analysis. Transl Psychiatry 9:190. https://doi.org/10.1038/s41398-019-0515-5. (PMID: 10.1038/s41398-019-0515-5313838466683166)
Neto J, Jantsch J, de Oliveira S et al (2022) DHA/EPA supplementation decreases anxiety-like behaviour, but it does not ameliorate metabolic profile in obese male rats. Br J Nutr 128:964–974. https://doi.org/10.1017/S0007114521003998. (PMID: 10.1017/S000711452100399834605386)
Caballero B (2019) Humans against obesity: Who will win? Adv Nutr 10:S4–S9. https://doi.org/10.1093/advances/nmy055. (PMID: 10.1093/advances/nmy055307219566363526)
de Vos WM, Tilg H, Van Hul M, Cani PD (2022) Gut microbiome and health: mechanistic insights. Gut 71:1020–1032. https://doi.org/10.1136/gutjnl-2021-326789. (PMID: 10.1136/gutjnl-2021-32678935105664)
Aron-Wisnewsky J, Warmbrunn MV, Nieuwdorp M, Clément K (2021) Metabolism and metabolic disorders and the microbiome: the intestinal microbiota associated with obesity, lipid metabolism, and metabolic health—pathophysiology and therapeutic strategies. Gastroenterology 160:573–599. https://doi.org/10.1053/j.gastro.2020.10.057. (PMID: 10.1053/j.gastro.2020.10.05733253685)
Mengeste AM, Rustan AC, Lund J (2021) Skeletal muscle energy metabolism in obesity. Obesity 29:1582–1595. https://doi.org/10.1002/oby.23227. (PMID: 10.1002/oby.2322734464025)
Kawai T, Autieri MV, Scalia R (2021) Adipose tissue inflammation and metabolic dysfunction in obesity. Am J Physiol Cell Physiol 320:C375–C391. https://doi.org/10.1152/ajpcell.00379.2020. (PMID: 10.1152/ajpcell.00379.202033356944)
Sabaratnam R, Hansen DR, Svenningsen P (2023) White adipose tissue mitochondrial bioenergetics in metabolic diseases. Rev Endocr Metab Disord. https://doi.org/10.1007/s11154-023-09827-z. (PMID: 10.1007/s11154-023-09827-z37558853)
Labban RSM, Alfawaz H, Almnaizel AT et al (2020) High-fat diet-induced obesity and impairment of brain neurotransmitter pool. Transl Neurosci 11:147–160. https://doi.org/10.1515/tnsci-2020-0099. (PMID: 10.1515/tnsci-2020-0099333127207705990)
Hersey M, Woodruff JL, Maxwell N et al (2021) High-fat diet induces neuroinflammation and reduces the serotonergic response to escitalopram in the hippocampus of obese rats. Brain Behav Immun 96:63–72. https://doi.org/10.1016/j.bbi.2021.05.010. (PMID: 10.1016/j.bbi.2021.05.010340107138319113)
de Macedo IC, de Freitas JS, da Silva Torres IL (2016) The influence of palatable diets in reward system activation: a mini review. Adv Pharmacol Sci 2016:7238679. https://doi.org/10.1155/2016/7238679. (PMID: 10.1155/2016/7238679270878064818794)
Leigh S-J, Kendig MD, Morris MJ (2019) Palatable western-style cafeteria diet as a reliable method for modeling diet-induced obesity in rodents. J Vis Exp. https://doi.org/10.3791/60262. (PMID: 10.3791/6026231736485)
Spinazzi M, Casarin A, Pertegato V et al (2012) Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat Protoc 7:1235–1246. https://doi.org/10.1038/nprot.2012.058. (PMID: 10.1038/nprot.2012.05822653162)
Teixeira PC, Dorneles GP, Santana Filho PC et al (2021) Increased LPS levels coexist with systemic inflammation and result in monocyte activation in severe COVID-19 patients. Int Immunopharmacol 100:108125. https://doi.org/10.1016/j.intimp.2021.108125. (PMID: 10.1016/j.intimp.2021.108125345439808426217)
Viana RR, Pego AMF, de Oliveira TF et al (2022) Liquid chromatography-tandem mass spectrometry method for simultaneous quantification of neurotransmitters in rat brain tissue exposed to 4’-fluoro-α-PHP. Biomed Chromatogr 36:e5487. https://doi.org/10.1002/bmc.5487. (PMID: 10.1002/bmc.548736001303)
Brestoff JR, Wilen CB, Moley JR et al (2021) Intercellular mitochondria transfer to macrophages regulates white adipose tissue homeostasis and is impaired in obesity. Cell Metab 33:270-282.e8. https://doi.org/10.1016/j.cmet.2020.11.008. (PMID: 10.1016/j.cmet.2020.11.00833278339)
Sarparanta J, García-Macia M, Singh R (2017) Autophagy and mitochondria in obesity and type 2 diabetes. Curr Diabetes Rev 13:352–369. https://doi.org/10.2174/1573399812666160217122530. (PMID: 10.2174/157339981266616021712253026900135)
Heinonen S, Jokinen R, Rissanen A, Pietiläinen KH (2020) White adipose tissue mitochondrial metabolism in health and in obesity. Obes Rev 21:e12958. https://doi.org/10.1111/obr.12958. (PMID: 10.1111/obr.1295831777187)
Pileggi CA, Parmar G, Harper M-E (2021) The lifecycle of skeletal muscle mitochondria in obesity. Obes Rev 22:e13164. https://doi.org/10.1111/obr.13164. (PMID: 10.1111/obr.1316433442950)
Chattopadhyay M, Guhathakurta I, Behera P et al (2011) Mitochondrial bioenergetics is not impaired in nonobese subjects with type 2 diabetes mellitus. Metabolism 60:1702–1710. https://doi.org/10.1016/j.metabol.2011.04.015. (PMID: 10.1016/j.metabol.2011.04.01521663924)
Turner N, Bruce CR, Beale SM et al (2007) Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56:2085–2092. https://doi.org/10.2337/db07-0093. (PMID: 10.2337/db07-009317519422)
Garcia-Roves P, Huss JM, Han D-H et al (2007) Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle. Proc Natl Acad Sci U S A 104:10709–10713. https://doi.org/10.1073/pnas.0704024104. (PMID: 10.1073/pnas.0704024104175488281965577)
Levak-Frank S, Radner H, Walsh A et al (1995) Muscle-specific overexpression of lipoprotein lipase causes a severe myopathy characterized by proliferation of mitochondria and peroxisomes in transgenic mice. J Clin Invest 96:976–986. https://doi.org/10.1172/JCI118145. (PMID: 10.1172/JCI1181457635990185285)
González LPF, da Rodrigues F, S, Jantsch J, et al (2023) Effects of omega-3 supplementation on anxiety-like behaviors and neuroinflammation in Wistar rats following cafeteria diet-induced obesity. Nutr Neurosci. https://doi.org/10.1080/1028415X.2023.2168229. (PMID: 10.1080/1028415X.2023.216822936657165)
Di Meo S, Iossa S, Venditti P (2017) Skeletal muscle insulin resistance: role of mitochondria and other ROS sources. J Endocrinol 233:R15–R42. https://doi.org/10.1530/JOE-16-0598. (PMID: 10.1530/JOE-16-059828232636)
Hernández MAG, Canfora EE, Jocken JWE, Blaak EE (2019) The short-chain fatty acid acetate in body weight control and insulin sensitivity. Nutrients 11:1943. https://doi.org/10.3390/nu11081943. (PMID: 10.3390/nu1108194331426593)
Cummings JH, Pomare EW, Branch WJ et al (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28:1221–1227. https://doi.org/10.1136/gut.28.10.1221. (PMID: 10.1136/gut.28.10.122136789501433442)
Perry RJ, Peng L, Barry NA et al (2016) Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature 534:213–217. https://doi.org/10.1038/nature18309. (PMID: 10.1038/nature18309272792144922538)
Neto J, Jantsch J, Rodrigues F et al (2023) Impact of cafeteria diet and n3 supplementation on the intestinal microbiota, fatty acids levels, neuroinflammatory markers and social memory in male rats. Physiol Behav 260:114068. https://doi.org/10.1016/j.physbeh.2022.114068. (PMID: 10.1016/j.physbeh.2022.11406836567032)
Squizani S, Jantsch J, da Rodrigues F, S, et al (2022) Zinc supplementation partially decreases the harmful effects of a cafeteria diet in rats but does not prevent intestinal dysbiosis. Nutrients 14:3921. https://doi.org/10.3390/nu14193921. (PMID: 10.3390/nu14193921362355749571896)
Fuke N, Nagata N, Suganuma H, Ota T (2019) Regulation of gut microbiota and metabolic endotoxemia with dietary factors. Nutrients 11:2277. https://doi.org/10.3390/nu11102277. (PMID: 10.3390/nu11102277315475556835897)
Stouffer MA, Woods CA, Patel JC et al (2015) Insulin enhances striatal dopamine release by activating cholinergic interneurons and thereby signals reward. Nat Commun 6:8543. https://doi.org/10.1038/ncomms9543. (PMID: 10.1038/ncomms954326503322)
Kleinridders A, Pothos EN (2019) Impact of brain insulin signaling on dopamine function, food intake, reward, and emotional behavior. Curr Nutr Rep 8:83–91. https://doi.org/10.1007/s13668-019-0276-z. (PMID: 10.1007/s13668-019-0276-z31001792)
Jantsch J, da Rodrigues F, S, Fraga G de F, et al (2023) Calorie restriction mitigates metabolic, behavioral and neurochemical effects of cafeteria diet in aged male rats. J Nutr Biochem 119:109371. https://doi.org/10.1016/j.jnutbio.2023.109371. (PMID: 10.1016/j.jnutbio.2023.10937137169228)
Soares-da-Silva P, Garrett MC (1990) A kinetic study of the rate of formation of dopamine, 3,4-dihydroxyphenylacetic acid (DOPAC) and homovanillic acid (HVA) in the brain of the rat: implications for the origin of DOPAC. Neuropharmacology 29:869–874. https://doi.org/10.1016/0028-3908(90)90135-e. (PMID: 10.1016/0028-3908(90)90135-e1979427)
Jiménez-Jiménez FJ, Alonso-Navarro H, García-Martín E, Agúndez JAG (2014) Cerebrospinal fluid biochemical studies in patients with Parkinson’s disease: toward a potential search for biomarkers for this disease. Front Cell Neurosci 8:369. https://doi.org/10.3389/fncel.2014.00369. (PMID: 10.3389/fncel.2014.00369254260234227512)
Wallace CW, Fordahl SC (2022) Obesity and dietary fat influence dopamine neurotransmission: exploring the convergence of metabolic state, physiological stress, and inflammation on dopaminergic control of food intake. Nutr Res Rev 35:236–251. https://doi.org/10.1017/S0954422421000196. (PMID: 10.1017/S095442242100019634184629)
Zhou L, Xiong J-Y, Chai Y-Q et al (2022) Possible antidepressant mechanisms of omega-3 polyunsaturated fatty acids acting on the central nervous system. Front Psychiat. https://doi.org/10.3389/fpsyt.2022.933704. (PMID: 10.3389/fpsyt.2022.933704)
Patrick RP, Ames BN (2015) Vitamin D and the omega-3 fatty acids control serotonin synthesis and action, part 2: relevance for ADHD, bipolar disorder, schizophrenia, and impulsive behavior. FASEB J 29:2207–2222. https://doi.org/10.1096/fj.14-268342. (PMID: 10.1096/fj.14-26834225713056)
DiNicolantonio JJ, O’Keefe JH (2020) The importance of marine omega-3s for brain development and the prevention and treatment of behavior, mood, and other brain disorders. Nutrients 12:2333. https://doi.org/10.3390/nu12082333. (PMID: 10.3390/nu12082333327598517468918)
Günther J, Schulte K, Wenzel D et al (2010) Prostaglandins of the E series inhibit monoamine release via EP3 receptors: proof with the competitive EP3 receptor antagonist L-826,266. Naunyn Schmiedebergs Arch Pharmacol 381:21–31. https://doi.org/10.1007/s00210-009-0478-9. (PMID: 10.1007/s00210-009-0478-920012265)
Hibbeln JR, Linnoila M, Umhau JC et al (1998) Essential fatty acids predict metabolites of serotonin and dopamine in cerebrospinal fluid among healthy control subjects, and early-and late-onset alcoholics. Biol Psychiat 44:235–242. https://doi.org/10.1016/s0006-3223(98)00141-3. (PMID: 10.1016/s0006-3223(98)00141-39715354)
Li P, Song C (2022) Potential treatment of Parkinson’s disease with omega-3 polyunsaturated fatty acids. Nutr Neurosci 25:180–191. https://doi.org/10.1080/1028415X.2020.1735143. (PMID: 10.1080/1028415X.2020.173514332124682)
Carabelli B, Delattre AM, Waltrick APF et al (2020) Fish-oil supplementation decreases Indoleamine-2,3-Dioxygenase expression and increases hippocampal serotonin levels in the LPS depression model. Behav Brain Res 390:112675. https://doi.org/10.1016/j.bbr.2020.112675. (PMID: 10.1016/j.bbr.2020.11267532407816)
Heinrichs SC (2010) Dietary omega-3 fatty acid supplementation for optimizing neuronal structure and function. Mol Nutr Food Res 54:447–456. https://doi.org/10.1002/mnfr.200900201. (PMID: 10.1002/mnfr.20090020120112300)
Pinot M, Vanni S, Pagnotta S et al (2014) Lipid cell biology. Polyunsaturated phospholipids facilitate membrane deformation and fission by endocytic proteins. Science 345:693–697. https://doi.org/10.1126/science.1255288. (PMID: 10.1126/science.125528825104391)
Jahangard L, Sadeghi A, Ahmadpanah M et al (2018) Influence of adjuvant omega-3-polyunsaturated fatty acids on depression, sleep, and emotion regulation among outpatients with major depressive disorders—Results from a double-blind, randomized and placebo-controlled clinical trial. J Psychiatr Res 107:48–56. https://doi.org/10.1016/j.jpsychires.2018.09.016. (PMID: 10.1016/j.jpsychires.2018.09.01630317101)
Emery S, Häberling I, Berger G et al (2020) Verbal memory performance in depressed children and adolescents: associations with epa but not dha and depression severity. Nutrients 12:3630. https://doi.org/10.3390/nu12123630. (PMID: 10.3390/nu12123630332558197761519)
فهرسة مساهمة: Keywords: Cafeteria diet; Claudin-5; Electron transport chain; LPS; Neurotransmitters; Polyunsaturated fatty acids
المشرفين على المادة: 0 (Fatty Acids, Omega-3)
تواريخ الأحداث: Date Created: 20240703 Date Completed: 20240831 Latest Revision: 20240831
رمز التحديث: 20240901
DOI: 10.1007/s11064-024-04201-0
PMID: 38960951
قاعدة البيانات: MEDLINE
الوصف
تدمد:1573-6903
DOI:10.1007/s11064-024-04201-0