Dietary menhaden fish oil supplementation suppresses lipopolysaccharide-induced neuroinflammation and cognitive impairment in diabetic rats

References

• Afshordel S, Hagl S, Werner D, Röhner N, Kögel D, Bazan NG, Eckert GP. 2015. Omega-3 polyunsaturated fatty acids improve mitochondrial dysfunction in brain aging - impact of Bcl-2 and NPD-1 like metabolites. Prostaglandins Leukot Essent Fatty Acids. 92:23–31. doi: 10.1016/j.plefa.2014.05.008.
   PubMed Web of Science ®Google Scholar
• Agrawal R, Gomez-Pinilla F. 2012. ‘Metabolic syndrome’ in the brain: deficiency in omega-3 fatty acid exacerbates dysfunctions in insulin receptor signalling and cognition. J Physiol. 590(10):2485–2499. doi: 10.1113/jphysiol.2012.230078.
   PubMed Web of Science ®Google Scholar
• Ajmone-Cat MA, Salvatori ML, De Simone R, Mancini M, Biagioni S, Bernardo A, Cacci E, Minghetti L. 2012. Docosahexaenoic acid modulates inflammatory and antineurogenic -functions of activated microglial cells. J Neurosci Res. 90(3):575–587. doi: 10.1002/jnr.22783.
   PubMed Web of Science ®Google Scholar
• Anaeigoudari A, Shafei MN, Soukhtanloo M, Sadeghnia HR, Reisi P, Beheshti F, Mohebbati R, Mousavi SM, Hosseini M. 2015. Lipopolysaccharide-induced memory impairment in rats is preventable using 7-nitroindazole. Arq Neuropsiquiatr. 73(9):784–790. doi: 10.1590/0004-282X20150121.
   PubMed Web of Science ®Google Scholar
• Anand K, Dhikav V. 2012. Hippocampus in health and disease: an overview. Ann Indian Acad Neurol. 15(4):239–246. doi: 10.4103/0972-2327.104323.
   PubMed Web of Science ®Google Scholar
• Anwar MM. 2022. Oxidative stress-A direct bridge to central nervous system homeostatic dysfunction and Alzheimer’s disease. Cell Biochem Funct. 40(1):17–27. doi: 10.1002/cbf.3673.
   PubMed Web of Science ®Google Scholar
• Asari MA, Zulkaflee MH, Sirajudeen KNS, Mohd Yusof NA, Mohd Sairazi NS. 2019. Tualang honey and DHA-rich fish oil reduce the production of pro-inflammatory cytokines in the rat brain following exposure to chronic stress. J Taibah Univ Med Sci. 14(4):317–323. doi: 10.1016/j.jtumed.2019.06.004.
   PubMed Web of Science ®Google Scholar
• Batista CRA, Gomes GF, Candelario-Jalil E, Fiebich BL, de Oliveira ACP. 2019. Lipopolysaccharide-induced neuroinflammation as a bridge to understand neurodegeneration. IJMS. 20(9):2293. doi: 10.3390/ijms20092293.
   Google Scholar
• Bellenger J, Bellenger S, Bataille A, Massey KA, Nicolaou A, Rialland M, Tessier C, Kang JX, Narce M. 2011. High pancreatic n-3 fatty acids prevent stz-induced diabetes in fat-1 mice: inflammatory pathway inhibition. Diabetes. 60(4):1090–1099. doi: 10.2337/db10-0901.
   PubMed Web of Science ®Google Scholar
• Berbudi A, Rahmadika N, Tjahjadi AI, Ruslami R. 2020. Type 2 diabetes and its impact on the immune system. Curr Diabetes Rev. 16(5):442–449. doi: 10.2174/1573399815666191024085838.
   PubMed Web of Science ®Google Scholar
• Bhatia HS, Agrawal R, Sharma S, Huo YX, Ying Z, Gomez-Pinilla F. 2011. Omega-3 fatty acid deficiency during brain maturation reduces neuronal and behavioral plasticity in adulthood. PLOS One. 6(12):e28451. doi: 10.1371/journal.pone.0028451.
   PubMed Web of Science ®Google Scholar
• Brown TJ, Brainard J, Song F, Wang X, Abdelhamid A, Hooper L,. 2019. Omega-3, omega-6, and total dietary polyunsaturated fat for prevention and treatment of type 2 diabetes mellitus: systematic review and meta-analysis of randomised controlled trials. BMJ. 366:l4697. doi: 10.1136/bmj.l4697.
   PubMedGoogle Scholar
• Crabtree T, Altaan S, Tarik A. 2016. Early-onset dementia in type 1 diabetes mellitus. Pract Diab. 33(4):133–134. doi: 10.1002/pdi.2019.
   Google Scholar
• Das M, Banerjee A, Roy R. 2022. A novel in vitro approach to test the effectiveness of fish oil in ameliorating type 1 diabetes. Mol Cell Biochem. 477(8):2121–2132. doi: 10.1007/s11010-022-04424-1.
   PubMed Web of Science ®Google Scholar
• De Felice FG, Ferreira ST. 2014. Inflammation, defective insulin signaling, and mitochondrial dysfunction as common molecular denominators connecting type 2 diabetes to Alzheimer disease. Diabetes. 63(7):2262–2272. doi: 10.2337/db13-1954.
   PubMed Web of Science ®Google Scholar
• De Sousa RAL, Harmer AR, Freitas DA, Mendonça VA, Lacerda ACR, Leite HR. 2020. An update on potential links between type 2 diabetes mellitus and Alzheimer’s disease. Mol Biol Rep. 47(8):6347–6356. doi: 10.1007/s11033-020-05693-z.
   PubMed Web of Science ®Google Scholar
• Devassy JG, Leng S, Gabbs M, Monirujjaman M, Aukema HM. 2016. Omega-3 polyunsaturated fatty acids and oxylipins in neuroinflammation and management of Alzheimer disease. Adv Nutr. 7(5):905–916. doi: 10.3945/an.116.012187.
   PubMed Web of Science ®Google Scholar
• Díaz-Gerevini GT, Daín A, Pasqualini ME, López CB, Eynard AR, Repossi G. 2019. Diabetic encephalopathy: beneficial effects of supplementation with fatty acids ω3 and nordihydroguaiaretic acid in a spontaneous diabetes rat model. Lipids Health Dis. 18(1):43. doi: 10.1186/s12944-018-0938-7.
   PubMedGoogle Scholar
• Dinel AL, André C, Aubert A, Ferreira G, Layé S, Castanon N. 2011. Cognitive and emotional alterations are related to hippocampal inflammation in a mouse model of metabolic syndrome. PLoS One. 6(9):e24325. doi: 10.1371/journal.pone.0024325.
   PubMed Web of Science ®Google Scholar
• Erdogan H, Fadillioglu E, Ozgocmen S, Sogut S, Ozyurt B, Akyol O, Ardicoglu O. 2004. Effect of fish oil supplementation on plasma oxidant/antioxidant status in rats. Prostaglandins Leukot Essent Fatty Acids. 71(3):149–152. doi: 10.1016/j.plefa.2004.02.001.
   PubMed Web of Science ®Google Scholar
• Gao C, Liu Y, Gan Y, Bao W, Peng X, Xing Q, Gao H, Lai J, Liu L, Wang Z, et al. 2020. Effects of fish oil supplementation on glucose control and lipid levels among patients with type 2 diabetes mellitus: a meta-analysis of randomized controlled trials. Lipids Health Dis. 19(1):87. doi: 10.1186/s12944-020-01214-w.
   PubMed Web of Science ®Google Scholar
• Gaspar JM, Baptista FI, MacEdo MP, Ambrósio AF. 2016. Inside the diabetic brain: role of different players involved in cognitive decline. ACS Chem Neurosci. 7(2):131–142. doi: 10.1021/acschemneuro.5b00240.
   PubMed Web of Science ®Google Scholar
• Gholamhosseinian A, Abbasalipourkabir R, Ziamajidi N, Sayadi M, Sayadi K. 2020. The anti-inflammatory effect of omega-3 polyunsaturated fatty acids dramatically decreases by iron in the hippocampus of diabetic rats. Life Sci. 245:117393. doi: 10.1016/j.lfs.2020.117393.
   PubMed Web of Science ®Google Scholar
• Ghule S, Prakash T, Kotresha D, Karki R, Surendra V, Goli D. 2010. Anti-diabetic activity of Celosia argentea root in streptozotocin-induced diabetic rats. Int J Green Pharm. 4(3):206–211. doi: 10.4103/0973-8258.69183.
   Google Scholar
• Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. 2010. Mechanisms underlying inflammation in neurodegeneration. Cell. 140(6):918–934. doi: 10.1016/j.cell.2010.02.016.
   PubMed Web of Science ®Google Scholar
• Gupta M, Pandey S, Rumman M, Singh B, Mahdi AA. 2023. Molecular mechanisms underlying hyperglycaemia associated cognitive decline. IBRO Neurosci Rep. 14:57–63. doi: 10.1016/j.ibneur.2022.12.006.
   PubMedGoogle Scholar
• Habib EK. 2013. Possible role of Omega-3 on the pancreas of streptozotocin-induced diabetes in adult albino rats: histological and immunohistochemical study. Egypt J Histol. 36(3):579–591. doi: 10.1097/01.EHX.0000431956.27366.8f.
   Google Scholar
• Hafandi A, Begg DP, Premaratna SD, Sinclair AJ, Jois M, Weisinger RS. 2014. Dietary repletion with ω3 fatty acid or with COX inhibition reverses cognitive effects in F3 ω3 fatty-acid-deficient mice. Comp Med. 64(2):106–109.
   PubMed Web of Science ®Google Scholar
• Harrison LC. 2021. The dark side of insulin: a primary autoantigen and instrument of self-destruction in type 1 diabetes. Mol Metab. 52:101288. doi: 10.1016/j.molmet.2021.101288.
   PubMed Web of Science ®Google Scholar
• Hikmah N, Dewi A, Shita P, Maulana H. 2015. Diabetic blood glucose level profile with stratified dose streptozotocin (sd-stz) and multi low dose streptozotocin (mld-stz) induction methods. J Trop Life Sci. 5:30–34.
   Google Scholar
• Hu M, Fang Z, Zhang T, Chen Y. 2022. Polyunsaturated fatty acid intake and incidence of type 2 diabetes in adults: a dose response meta-analysis of cohort studies. Diabetol Metab Syndr. 14(1):34. doi: 10.1186/s13098-022-00804-1.
   PubMed Web of Science ®Google Scholar
• Hung HC, Tsai SF, Sie SR, Kuo YM. 2022. High glucose enhances lipopolysaccharide-induced inflammation in cultured BV2 microglial cell line. Immunity, Inflamm Dis. 10:1–9.
   Web of Science ®Google Scholar
• Inoue T, Tanaka M, Masuda S, Ohue-Kitano R, Yamakage H, Muranaka K, Wada H, Kusakabe T, Shimatsu A, Hasegawa K, et al. 2017. Omega-3 polyunsaturated fatty acids suppress the inflammatory responses of lipopolysaccharide-stimulated mouse microglia by activating SIRT1 pathways. Biochim Biophys Acta Mol Cell Biol Lipids. 1862(5):552–560. doi: 10.1016/j.bbalip.2017.02.010.
   PubMed Web of Science ®Google Scholar
• Iwase Y, Kamei N, Takeda-Morishita M. 2015. Antidiabetic effects of omega-3 polyunsaturated fatty acids: from mechanism to therapeutic possibilities. PP. 06(03):190–200. doi: 10.4236/pp.2015.63020.
   Google Scholar
• Jangale NM, Devarshi PP, Dubal AA, Ghule AE, Koppikar SJ, Bodhankar SL, Chougale AD, Kulkarni MJ, Harsulkar AM. 2013. Dietary flaxseed oil and fish oil modulates expression of antioxidant and inflammatory genes with alleviation of protein glycation status and inflammation in liver of streptozotocin-nicotinamide induced diabetic rats. Food Chem. 141(1):187–195. doi: 10.1016/j.foodchem.2013.03.001.
   PubMedGoogle Scholar
• Karges B, Schwandt A, Heidtmann B, Kordonouri O, Binder E, Schierloh U, Boettcher C, Kapellen T, Rosenbauer J, Holl RW. 2017. Association of insulin pump therapy vs. insulin injection therapy with severe hypoglycemia, ketoacidosis, and glycemic control among children, adolescents, and young adults with type 1 diabetes.J Am Med Assoc. 318(14):1358–1366. doi: 10.1001/jama.2017.13994.
   PubMed Web of Science ®Google Scholar
• Keapai W, Apichai S, Amornlerdpison D, Lailerd N. 2016. Evaluation of fish oil-rich in MUFAs for anti-diabetic and antiinflammation potential in experimental type 2 diabetic rats. Korean J Physiol Pharmacol. 20(6):581–593. doi: 10.4196/kjpp.2016.20.6.581.
   PubMed Web of Science ®Google Scholar
• Kim HY. 2014. Neuroprotection by docosahexaenoic acid in brain injury. Mil Med. 179(11 Suppl):106–111. doi: 10.7205/MILMED-D-14-00162.
   PubMed Web of Science ®Google Scholar
• Kobyliak N, Falalyeyeva T, Mykhalchyshyn G, Molochek N, Savchuk O, Kyriienko D, Komisarenko I. 2020. Probiotic and omega-3 polyunsaturated fatty acids supplementation reduces insulin resistance, improves glycemia and obesity parameters in individuals with type 2 diabetes: a randomised controlled trial. Obes Med. 19:100248. doi: 10.1016/j.obmed.2020.100248.
   Google Scholar
• Konsman JP. 2022. Cytokines in the brain and neuroinflammation: we didn’t starve the fire!. Pharmaceuticals . 15(2):140. doi: 10.3390/ph15020140.
   Web of Science ®Google Scholar
• Kwon HS, Koh SH. 2020. Neuroinflammation in neurodegenerative disorders: the roles of microglia and astrocytes. Transl Neurodegener. 9(1):42. doi: 10.1186/s40035-020-00221-2.
   PubMed Web of Science ®Google Scholar
• Laubertová L, Koňariková K, Gbelcová H, Ďuračková Z, Muchová J, Garaiova I, Žitňanová I. 2017. Fish oil emulsion supplementation might improve quality of life of diabetic patients due to its antioxidant and anti-inflammatory properties. Nutr Res. 46:49–58. doi: 10.1016/j.nutres.2017.07.012.
   PubMed Web of Science ®Google Scholar
• Lu DY, Tsao YY, Leung YM, Su KP. 2010. Docosahexaenoic acid suppresses neuroinflammatory responses and induces heme oxygenase-1 expression in BV-2 microglia: implications of antidepressant effects for omega-3 fatty acids. Neuropsychopharmacology. 35(11):2238–2248. doi: 10.1038/npp.2010.98.
   PubMed Web of Science ®Google Scholar
• Lu Y, Zhao LX, Cao DL, Gao YJ. 2013. Spinal injection of docosahexaenoic acid attenuates carrageenan-induced inflammatory pain through inhibition of microglia-mediated neuroinflammation in the spinal cord. Neuroscience. 241:22–31. doi: 10.1016/j.neuroscience.2013.03.003.
   PubMed Web of Science ®Google Scholar
• Luna R, Talanki Manjunatha R, Bollu B, Jhaveri S, Avanthika C, Reddy N, Saha T, Gandhi F. 2021. A comprehensive review of neuronal changes in diabetics. Cureus. 13(10):e19142. doi: 10.7759/cureus.19142.
   PubMed Web of Science ®Google Scholar
• Mahdi O, Baharuldin MTH, Nor NHM, Chiroma SM, Jagadeesan S, Moklas MAM. 2019. Chemicals used for the induction of Alzheimer’s disease-like cognitive dysfunctions in rodents. Biomed Res Ther. 6(11):3460–3484. doi: 10.15419/bmrat.v6i11.575.
   Web of Science ®Google Scholar
• McCrimmon RJ, Ryan CM, Frier BM. 2012. Diabetes and cognitive dysfunction. Lancet. 379(9833):2291–2299. doi: 10.1016/S0140-6736(12)60360-2.
   PubMed Web of Science ®Google Scholar
• Mesa J. 2015. New insulin types in type 1 diabetes mellitus. Med Clin . 145(2):70–75. doi: 10.1016/j.medcle.2014.04.005.
   PubMed Web of Science ®Google Scholar
• Mizuseki K, Diba K, Pastalkova E, Buzsáki G. 2011. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat Neurosci. 14(9):1174–1181. doi: 10.1038/nn.2894.
   PubMed Web of Science ®Google Scholar
• Muramatsu K. 2020. Diabetes mellitus-related dysfunction of the motor system. Int J Mol Sci. 21(20):1–26.
   Web of Science ®Google Scholar
• Murtishaw AS. 2014. [The effect of acute LPS-induced immune activation and brain insulin signaling disruption in a diabetic model of Alzheimer’s disease]. [UNLV Theses, Dissertations, Professional Papers, and Capstones]. p. 2199.
   Google Scholar
• Parveen K, Siddiqui WA, Arif JM, Kuddus M, Shahid SMA, Kausar MA. 2019. Evaluation of vegetables and fish oils for the attenuation of diabetes complications. Cell Mol Biol (Noisy-le-Grand). 65(7):38–45. doi: 10.14715/cmb/2019.65.7.8.
   PubMed Web of Science ®Google Scholar
• Perry VH. 2004. The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav Immun. 18(5):407–413. doi: 10.1016/j.bbi.2004.01.004.
   PubMed Web of Science ®Google Scholar
• Pugazhenthi S, Qin L, Reddy PH. 2017. Common neurodegenerative pathways in obesity, diabetes, and Alzheimer’s disease. Biochim Biophys Acta Mol Basis Dis. 1863(5):1037–1045. doi: 10.1016/j.bbadis.2016.04.017.
   PubMed Web of Science ®Google Scholar
• Purdel C, Ungurianu A, Margina D. 2021. Metabolic and metabolomic insights regarding the omega-3 PUFAs intake in type 1 diabetes mellitus. Front Mol Biosci. 8:783065. doi: 10.3389/fmolb.2021.783065.
   PubMed Web of Science ®Google Scholar
• Rauf A, Badoni H, Abu-Izneid T, Olatunde A, Rahman MM, Painuli S, Semwal P, Wilairatana P, Mubarak MS. 2022. Neuroinflammatory markers: key indicators in the pathology of neurodegenerative diseases. Molecules. 27(10):3194. doi: 10.3390/molecules27103194.
   PubMed Web of Science ®Google Scholar
• Rom S, Zuluaga-Ramirez V, Gajghate S, Seliga A, Winfield M, Heldt NA, Kolpakov MA, Bashkirova YV, Sabri AK, Persidsky Y. 2019. Hyperglycaemia-driven neuroinflammation compromises bbb leading to memory loss in both diabetes mellitus (dm) type 1 and type 2 mouse models. Mol Neurobiol. 56(3):1883–1896. doi: 10.1007/s12035-018-1195-5.
   PubMed Web of Science ®Google Scholar
• Samsulrizal N, Goh YM, Ahmad H, Md Dom S, Azmi NS, NoorMohamad Zin NS, Ebrahimi M. 2021. Ficus deltoidea promotes bone formation in streptozotocin-induced diabetic rats. Pharm Biol. 59(1):66–73. doi: 10.1080/13880209.2020.1865411.
   PubMed Web of Science ®Google Scholar
• Sellers RS, Morton D, Michael B, Roome N, Johnson JK, Yano BL, Perry R, Schafer K. 2007. Society of Toxicologic Pathology position paper: organ weight recommendations for toxicology studies. Toxicol Pathol. 35(5):751–755. doi: 10.1080/01926230701595300.
   Google Scholar
• Soltan SSAM. 2012. The effects of varieties sources of omega-3 fatty acids on diabetes in rats. FNS. 03(10):1404–1412. doi: 10.4236/fns.2012.310184.
   Google Scholar
• Sopian NFA, Ajat M, Shafie NI, Noor MHM, Ebrahimi M, Rajion MA, Meng GY, Ahmad H. 2015. Does short-term dietary omega-3 fatty acid supplementation influence brain hippocampus gene expression of zinc transporter-3? Int J Mol Sci. 16(7):15800–15810. doi: 10.3390/ijms160715800.
   PubMed Web of Science ®Google Scholar
• Takada A, Shimizu F, Ishii Y, Ogawa M, Takao T. 2021. Roles of glucose and sucrose intakes on the brain functions measured by the working ability and Morris maze. In: Takada A and Hubertus Himmerich H, ed. Psychology and pathophysiological outcomes of eating. London, United Kingdom: IntechOpen. doi: 10.5772/intechopen.99203.
   Google Scholar
• Ventura-Sobrevilla J, Boone-Villa VD, Aguilar CN, Román-Ramos R, Vega-Ávila E, Campos-Sepúlveda E, Alarcón-Aguilar F. 2011. Effect of varying dose and administration of streptozotocin on blood sugar in male CD1 mice. Proc West Pharmacol Soc. 54:5–9.
   PubMedGoogle Scholar
• Wang G, Zhang X, Lu X, Liu J, Zhang Z, Wei Z, Wu Z, Wang J. 2020. Fish oil supplementation attenuates cognitive impairment by inhibiting neuroinflammation in STZ-induced diabetic rats. Aging. 12(15):15281–15289. doi: 10.18632/aging.103426.
   PubMedGoogle Scholar
• Wang H, Deng JL, Chen L, Ding K, Wang Y. 2021. Acute glucose fluctuation induces inflammation and neurons apoptosis in hippocampal tissues of diabetic rats. J Cell Biochem. 122(9):1239–1247. doi: 10.1002/jcb.29523.
   PubMed Web of Science ®Google Scholar
• Yang RH, Wang F, Hou XH, Cao ZP, Wang B, Xu XN, Hu SJ. 2012. Dietary omega-3 polyunsaturated fatty acids improves learning performance of diabetic rats by regulating the neuron excitability. Neuroscience. 212:93–103. doi: 10.1016/j.neuroscience.2012.04.005.
   PubMed Web of Science ®Google Scholar
• Zakaria R, Wan Yaacob WMH, Othman Z, Long I, Ahmad AH, Al-Rahbi B. 2017. Lipopolysaccharide-induced memory impairment in rats: a model of Alzheimer’s disease. Physiol Res. 66(4):553–565. doi: 10.33549/physiolres.933480.
   PubMed Web of Science ®Google Scholar
• Zhu B, Wang ZG, Ding J, Liu N, Wang DM, Ding LC, Yang C. 2014. Chronic lipopolysaccharide exposure induces cognitive dysfunction without affecting BDNF expression in the rat hippocampus. Exp Ther Med. 7(3):750–754. doi: 10.3892/etm.2014.1479.
   PubMed Web of Science ®Google Scholar