Sodium chloride-induced changes in oxidative stress, inflammation, and dysbiosis in experimental multiple sclerosis

References

• Krementsov DN, Case LK, Hickey WF, Teuscher C. Exacerbation of autoimmune neuroinflammation by dietary sodium is genetically controlled and sex specific. FASEB J. 2015;29:3446. doi:10.1096/FJ.15-272542.
   PubMed Web of Science ®Google Scholar
• Farez MF, Mascanfroni ID, Méndez-Huergo SP, et al. Melatonin contributes to the seasonality of multiple sclerosis relapses. Cell. 2015;162:1338–1352. doi:10.1016/j.cell.2015.08.025.
   PubMed Web of Science ®Google Scholar
• Long T, Yang Y, Peng L, Li Z. Neuroprotective effects of melatonin on experimental allergic encephalomyelitis mice via anti-oxidative stress activity. J Mol Neurosci. 2018;64:233–241. doi:10.1007/s12031-017-1022-x.
   PubMed Web of Science ®Google Scholar
• Soto-Brambila AP, Gabriel Ortiz G, Rivero-Moragrega P, et al. Relapsing remitting multiple sclerosis and its relationship with the immune system and oxidative stress. Curr Immunol Rev. 2017;14:15–23. doi:10.2174/1573395514666171226154300.
   Google Scholar
• Gunata M, Parlakpinar H, Acet HA. Melatonin: a review of its potential functions and effects on neurological diseases. Rev Neurol (Paris). 2020;176:148–165. doi:10.1016/j.neurol.2019.07.025.
   PubMed Web of Science ®Google Scholar
• Chen D, Zhang T, Lee TH. Cellular mechanisms of melatonin: insight from neurodegenerative diseases. Biomolecules. 2020;10:1–26. doi:10.3390/biom10081158.
   Web of Science ®Google Scholar
• Zeydan B, Atkinson EJ, Weis DM, et al. Reproductive history and progressive multiple sclerosis risk in women. Brain Commun. 2020;2:fcaa185, doi:10.1093/braincomms/fcaa185.
   PubMedGoogle Scholar
• Hucke S, Eschborn M, Liebmann M, et al. Sodium chloride promotes pro-inflammatory macrophage polarization thereby aggravating CNS autoimmunity. J Autoimmun. 2016;67:90–101. doi:10.1016/J.JAUT.2015.11.001.
   PubMed Web of Science ®Google Scholar
• Hammer A, Schliep A, Jörg S, et al. Impact of combined sodium chloride and saturated long-chain fatty acid challenge on the differentiation of T helper cells in neuroinflammation. J Neuroinflammation. 2017;14:1–9. doi:10.1186/S12974-017-0954-Y/FIGURES/3.
   PubMed Web of Science ®Google Scholar
• Matveeva O, Bogie JFJ, Hendriks JJA, et al. Western lifestyle and immunopathology of multiple sclerosis. Ann N Y Acad Sci. 2018;1417:71–86. doi:10.1111/NYAS.13583.
   PubMed Web of Science ®Google Scholar
• Na SY, Janakiraman M, Leliavski A, Krishnamoorthy G. High-salt diet suppresses autoimmune demyelination by regulating the blood–brain barrier permeability. Proc Natl Acad Sci U S A. 2021;118:2025944118, doi:10.1073/PNAS.2025944118/-/DCSUPPLEMENTAL.
   Web of Science ®Google Scholar
• Matthias J, Heink S, Picard F, et al. Salt generates antiinflammatory Th17 cells but amplifies pathogenicity in proinflammatory cytokine microenvironments. J Clin Invest. 2020;130:4587–4600. doi:10.1172/JCI137786.
   PubMed Web of Science ®Google Scholar
• Heras-Garvin A, Refolo V, Reindl M, et al. High-salt diet does not boost neuroinflammation and neurodegeneration in a model of α-synucleinopathy. J Neuroinflammation. 2020;17; doi:10.1186/S12974-020-1714-Y.
   PubMed Web of Science ®Google Scholar
• Gallardo JM, de Carmen Prado-Uribe M, Amato D, Paniagua R. Inflammation and oxidative stress markers by pentoxifylline treatment in rats with chronic renal failure and high sodium intake. Arch Med Res. 2007;38:34–38. doi:10.1016/J.ARCMED.2006.08.010.
   PubMed Web of Science ®Google Scholar
• Hu L, Zhu S, Peng X, et al. High salt elicits brain inflammation and cognitive dysfunction, accompanied by alternations in the Gut microbiota and decreased SCFA production. J Alzheimers Dis. 2020;77:629–640. doi:10.3233/JAD-200035.
   PubMed Web of Science ®Google Scholar
• Ferguson JF, Aden LA, Barbaro NR, et al. High dietary salt–induced DC activation underlies microbial dysbiosis-associated hypertension. JCI Insight. 2019;4; doi:10.1172/JCI.INSIGHT.126241.
   PubMed Web of Science ®Google Scholar
• Smiljanec K, Lennon SL. Sodium, hypertension, and the gut: does the gut microbiota go salty? Am J Physiol Heart Circ Physiol. 2019;317:H1173–H1182. doi:10.1152/AJPHEART.00312.2019.
   PubMed Web of Science ®Google Scholar
• Janakiraman M, Krishnamoorthy G. Emerging role of diet and microbiota interactions in neuroinflammation. Front Immunol. 2018;9:2067, doi:10.3389/FIMMU.2018.02067.
   PubMed Web of Science ®Google Scholar
• Boziki MK, Kesidou E, Theotokis P, et al. Microbiome in multiple sclerosis: where are we, what we know and do not know. Brain Sci. 2020;10:234. doi:10.3390/BRAINSCI10040234.
   PubMed Web of Science ®Google Scholar
• Berer K, Mues M, Koutrolos M, et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature. 2011. doi:10.1038/nature10554.
   PubMed Web of Science ®Google Scholar
• Conde C, Escribano BM, Luque E, et al. Extra-virgin olive oil modifies the changes induced in non-nervous organs and tissues by experimental autoimmune encephalomyelitis models. Nutrients. 2019;11:2448, doi:10.3390/nu11102448.
   PubMed Web of Science ®Google Scholar
• Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4615–4622. doi:10.1073/PNAS.1000082107.
   PubMed Web of Science ®Google Scholar
• Miyauchi E, Kim SW, Suda W, et al. Gut microorganisms act together to exacerbate inflammation in spinal cords. Nature. 2020;585:102–106. doi:10.1038/s41586-020-2634-9.
   PubMed Web of Science ®Google Scholar
• Binger KJ, Gebhardt M, Heinig M, et al. High salt reduces the activation of IL-4– and IL-13–stimulated macrophages. J Clin Invest. 2015;125:4223, doi:10.1172/JCI80919.
   PubMed Web of Science ®Google Scholar
• Pérez-Nievas BG, García-Bueno B, Madrigal JLM, Leza JC. Chronic immobilisation stress ameliorates clinical score and neuroinflammation in a MOG-induced EAE in dark agouti rats: mechanisms implicated. J Neuroinflammation. 2010;7:60, doi:10.1186/1742-2094-7-60.
   PubMed Web of Science ®Google Scholar
• Escribano BM, Medina-Fernández FJ, Aguilar-Luque M, et al. Lipopolysaccharide binding protein and oxidative stress in a multiple sclerosis model. Neurotherapeutics. 2017;14:199–211. doi:10.1007/s13311-016-0480-0.
   PubMed Web of Science ®Google Scholar
• Stosic-Grujicic S, Ramic Z, Bumbasirevic V, et al. Induction of experimental autoimmune encephalomyelitis in dark agouti rats without adjuvant. Clin Exp Immunol. 2004;136:49–55. doi:10.1111/j.1365-2249.2004.02418.x.
   PubMed Web of Science ®Google Scholar
• Escribano BM, Muñoz-Jurado A, Luque E, et al. Lactose and casein cause changes on biomarkers of oxidative damage and dysbiosis in an experimental model of multiple sclerosis. CNS Neurol Disord Drug Targets. 2021;21:680–692. doi:10.2174/1871527320666211207101113.
   Web of Science ®Google Scholar
• Escribano BM, Muñoz-Jurado A, Caballero-Villarraso J, et al. Protective effects of melatonin on changes occurring in the experimental autoimmune encephalomyelitis model of multiple sclerosis. Mult Scler Relat Disord. 2022;58; doi:10.1016/J.MSARD.2022.103520.
   PubMed Web of Science ®Google Scholar
• Levine RL, Garland D, Oliver CN, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464–78. doi:10.1016/0076-6879(90)86141-H.
   PubMed Web of Science ®Google Scholar
• Ricart-Jané D, Llobera M, López-Tejero MD. Anticoagulants and other preanalytical factors interfere in plasma nitrate/nitrite quantification by the Griess method. Nitric Oxide - Biol Chem. 2002;6:178–185. doi:10.1006/niox.2001.0392.
   PubMed Web of Science ®Google Scholar
• Flohé L, Günzler WA. Assays of glutathione peroxidase. Methods Enzymol. 1984;105:114–21. doi:10.1016/S0076-6879(84)05015-1.
   PubMed Web of Science ®Google Scholar
• Cortese M, Yuan C, Chitnis T, et al. No association between dietary sodium intake and the risk of multiple sclerosis. Neurology. 2017;89:1322, doi:10.1212/WNL.0000000000004417.
   PubMedGoogle Scholar
• Faraco G, Hochrainer K, Segarra SG, et al. Dietary salt promotes cognitive impairment through tau phosphorylation. Nature. 2019;574:686, doi:10.1038/S41586-019-1688-Z.
   PubMed Web of Science ®Google Scholar
• Fitzgerald KC, Munger KL, Hartung HP, et al. Sodium intake and multiple sclerosis activity and progression in BENEFIT. Ann Neurol. 2017;82:20, doi:10.1002/ANA.24965.
   PubMed Web of Science ®Google Scholar
• Nourbakhsh B, Graves J, Casper TC, et al. Dietary salt intake and time to relapse in paediatric multiple sclerosis. J Neurol Neurosurg Psychiatry. 2016;87:1350–1353. doi:10.1136/JNNP-2016-313410.
   PubMedGoogle Scholar
• Amara S, Ivy MT, Myles EL, Tiriveedhi V. Sodium channel γENaC mediates IL-17 synergized high salt induced inflammatory stress in breast cancer cells. Cell Immunol. 2016;302:1, doi:10.1016/J.CELLIMM.2015.12.007.
   PubMed Web of Science ®Google Scholar
• Wilck N, Matus MG, Kearney SM, et al. Salt-responsive gut commensal modulates TH17 axis and disease. Nature. 2017;551:585–589. doi:10.1038/nature24628.
   PubMed Web of Science ®Google Scholar
• Gilman TL, Mitchell NC, Daws LC, Toney GM. Neuroinflammation contributes to high salt intake-augmented neuronal activation and active coping responses to acute stress. Int J Neuropsychopharmacol. 2019;22:137, doi:10.1093/IJNP/PYY099.
   PubMed Web of Science ®Google Scholar
• Schweda F. Salt feedback on the renin-angiotensin-aldosterone system. Pflugers Arch. 2015;467:565–576. doi:10.1007/S00424-014-1668-Y.
   PubMed Web of Science ®Google Scholar
• Platten M, Youssef S, Eun MH, et al. Blocking angiotensin-converting enzyme induces potent regulatory T cells and modulates TH1- and TH17-mediated autoimmunity. Proc Natl Acad Sci U S A. 2009;106:14948–14953. doi:10.1073/PNAS.0903958106/SUPPL_FILE/0903958106SI.PDF.
   PubMed Web of Science ®Google Scholar
• Živković M, Kolaković A, Stojković L, et al. Renin-angiotensin system gene polymorphisms as risk factors for multiple sclerosis. J Neurol Sci. 2016;363:29–32. doi:10.1016/J.JNS.2016.02.026.
   PubMed Web of Science ®Google Scholar
• Stegbauer J, Lee DH, Seubert S, et al. Role of the renin-angiotensin system in autoimmune inflammation of the central nervous system. Proc Natl Acad Sci U S A. 2009;106:14942–14947. doi:10.1073/PNAS.0903602106.
   PubMed Web of Science ®Google Scholar
• Biancardi VC, Stranahan AM, Krause EG, et al. Cross talk between AT1 receptors and toll-like receptor 4 in microglia contributes to angiotensin II-derived ROS production in the hypothalamic paraventricular nucleus. Am J Physiol Heart Circ Physiol. 2016;310:H404–H415. doi:10.1152/AJPHEART.00247.2015.
   PubMed Web of Science ®Google Scholar
• Guo X, Namekata K, Kimura A, et al. The renin-angiotensin system regulates neurodegeneration in a mouse model of optic neuritis. Am J Pathol. 2017;187:2876–2885. doi:10.1016/J.AJPATH.2017.08.012.
   PubMed Web of Science ®Google Scholar
• Wu J, Yang X, Zhang YF, et al. Angiotensin II upregulates Toll-like receptor 4 and enhances lipopolysaccharide-induced CD40 expression in rat peritoneal mesothelial cells. Inflamm Res. 2009;58:473–482. doi:10.1007/S00011-009-0012-Z/FIGURES/4.
   PubMed Web of Science ®Google Scholar
• Bondeva T, Roger T, Wolf G. Differential regulation of Toll-like receptor 4 gene expression in renal cells by angiotensin II: dependency on AP1 and PU.1 transcriptional sites. Am J Nephrol. 2007;27:308–314. doi:10.1159/000102551.
   PubMed Web of Science ®Google Scholar
• Wolf G, Bohlender J, Bondeva T, et al. Angiotensin II upregulates toll-like receptor 4 on mesangial cells. J Am Soc Nephrol. 2006;17:1585–1593. doi:10.1681/ASN.2005070699.
   PubMed Web of Science ®Google Scholar
• Ji Y, Liu J, Wang Z, Liu N. Angiotensin II induces inflammatory response partly via Toll-like receptor 4-dependent signaling pathway in vascular smooth muscle cells. Cell Physiol Biochem. 2009;23:265–276. doi:10.1159/000218173.
   PubMed Web of Science ®Google Scholar
• Saito Y, Berk BC. Transactivation: a novel signaling pathway from angiotensin II to tyrosine kinase receptors. J Mol Cell Cardiol. 2001;33:3–7. doi:10.1006/JMCC.2000.1272.
   PubMed Web of Science ®Google Scholar
• De S, Zhou H, DeSantis D, et al. Erlotinib protects against LPS-induced endotoxicity because TLR4 needs EGFR to signal. Proc Natl Acad Sci U S A. 2015;112:9680–9685. doi:10.1073/PNAS.1511794112.
   PubMed Web of Science ®Google Scholar
• Semba K, Namekata K, Guo X, et al. Renin-angiotensin system regulates neurodegeneration in a mouse model of Normal tension glaucoma. Cell Death Dis. 2014;5; doi:10.1038/CDDIS.2014.296.
   Web of Science ®Google Scholar
• Gelen V, Kükürt A, Şengül E. Role of the renin-angiotensin-aldosterone system in various disease processes: an overview. Renin-Angiotensin Aldosterone Syst. 2021;1; doi:10.5772/INTECHOPEN.97354.
   Google Scholar
• Stone RE, Liu S, Levy AM, et al. Activation of the protective arm of the renin angiotensin system in demyelinating disease. J Neuroimmune Pharmacol. 2020;15:249–263. doi:10.1007/S11481-019-09894-7.
   PubMed Web of Science ®Google Scholar
• Tikellis C, Pickering RJ, Tsorotes D, et al. Activation of the renin-angiotensin system mediates the effects of dietary salt intake on atherogenesis in the apolipoprotein E knockout mouse. Hypertension. 2012;60:98–105. doi:10.1161/HYPERTENSIONAHA.112.191767.
   PubMed Web of Science ®Google Scholar
• Shimosawa T. Salt, the renin–angiotensin–aldosterone system and resistant hypertension. Hypertens Res. 2013;36:657–660. doi:10.1038/hr.2013.69.
   PubMed Web of Science ®Google Scholar
• Angelis E, Tse MY, Pang SC. Interactions between atrial natriuretic peptide and the renin-angiotensin system during salt-sensitivity exhibited by the proANP gene-disrupted mouse. Mol Cell Biochem. 2005;276:121–131. doi:10.1007/S11010-005-3672-1.
   PubMed Web of Science ®Google Scholar
• Shimoura CG, Lincevicius GS, Nishi EE, et al. Increased dietary salt changes baroreceptor sensitivity and intrarenal renin-angiotensin system in Goldblatt hypertension. Am J Hypertens. 2017;30:28–36. doi:10.1093/AJH/HPW107.
   PubMed Web of Science ®Google Scholar
• Bayorh DMA, Ganafa AA, Emmett N, et al. Alterations in aldosterone and angiotensin II levels in salt-induced hypertension. Clin Exp Hypertens. 2009;27:355–367. doi:10.1081/CEH-57423.
   Google Scholar
• Parodi B, Kerlero de Rosbo N. The Gut-brain axis in multiple sclerosis. Is its dysfunction a pathological trigger or a consequence of the disease? Front Immunol. 2021;12:718220, doi:10.3389/FIMMU.2021.718220/BIBTEX.
   PubMed Web of Science ®Google Scholar
• Fellner L, Irschick R, Schanda K, et al. Toll-like receptor 4 is required for α-synuclein dependent activation of microglia and astroglia. Glia. 2013;61:349–360. doi:10.1002/GLIA.22437.
   PubMed Web of Science ®Google Scholar
• Perez-Pardo P, Dodiya HB, Engen PA, et al. Role of TLR4 in the gut-brain axis in Parkinson’s disease: a translational study from men to mice. Gut. 2019;68:829–843. doi:10.1136/GUTJNL-2018-316844.
   PubMed Web of Science ®Google Scholar
• Dasu MR, Riosvelasco AC, Jialal I. Candesartan inhibits Toll-like receptor expression and activity both in vitro and in vivo. Atherosclerosis. 2009;202:76, doi:10.1016/J.ATHEROSCLEROSIS.2008.04.010.
   PubMed Web of Science ®Google Scholar
• Burgueno J, Fritsch J, Santander A, et al. P164 EPITHELIAL TLR4-INDUCED DYSBIOSIS INCREASES SUSCEPTIBILITY TO TUMORIGENESIS. Gastroenterology. 2020;158:S66, doi:10.1053/J.GASTRO.2019.11.169.
   Web of Science ®Google Scholar
• Dange RB, Agarwal D, Masson GS, et al. Central blockade of TLR4 improves cardiac function and attenuates myocardial inflammation in angiotensin II-induced hypertension. Cardiovasc Res. 2014;103:17–27. doi:10.1093/CVR/CVU067.
   PubMed Web of Science ®Google Scholar
• Benicky J, Sánchez-Lemus E, Honda M, et al. Angiotensin II AT1 receptor blockade ameliorates brain inflammation. Neuropsychopharmacology. 2011;36:857, doi:10.1038/NPP.2010.225.
   PubMed Web of Science ®Google Scholar
• Dange RB, Agarwal D, Teruyama R, Francis J. Toll-like receptor 4 inhibition within the paraventricular nucleus attenuates blood pressure and inflammatory response in a genetic model of hypertension. J Neuroinflammation. 2015;12; doi:10.1186/S12974-015-0242-7.
   PubMed Web of Science ®Google Scholar
• Nair AR, Ebenezer PJ, Saini Y, Francis J. Angiotensin II-induced hypertensive renal inflammation is mediated through HMGB1-TLR4 signaling in rat tubulo-epithelial cells. Exp Cell Res. 2015;335:238–247. doi:10.1016/J.YEXCR.2015.05.011.
   PubMed Web of Science ®Google Scholar
• Liu M, Deng M, Luo Q, Dou X, Jia Z. High-salt loading downregulates Nrf2 expression in a sodium-dependent manner in renal collecting duct cells. Front Physiol. 2020;10:1565. doi:10.3389/FPHYS.2019.01565/BIBTEX.
   PubMed Web of Science ®Google Scholar