Sodium chloride promotes pro-inflammatory macrophage polarization thereby aggravating CNS autoimmunity

Journal of Autoimmunity

Volumn 67, Issue , 2016, Pages 90-101

  Hucke, Stephanie ^a   Eschborn, Melanie ^a   Liebmann, Marie ^a   Herold, Martin ^a   Freise, Nicole ^a   Engbers, Annika ^a   Ehling, Petra ^a   Meuth, Sven G ^a   Roth, Johannes ^a   Kuhlmann, Tanja ^a   Wiendl, Heinz ^a   Klotz, Luisa ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

CNS autoimmunity; Dietary salt intake; Multiple sclerosis; Myeloid cells; Pro inflammatory M1 macrophages

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; SODIUM CHLORIDE; BIOLOGICAL MARKER; SALT INTAKE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MACROPHAGE ACTIVATION; MONOCYTE; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; SALT INTAKE; SIGNAL TRANSDUCTION; ADMINISTRATION AND DOSAGE; ANIMAL; AUTOIMMUNITY; CENTRAL NERVOUS SYSTEM; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MULTIPLE SCLEROSIS; PATHOLOGY; PHENOTYPE;

ANIMALS; AUTOIMMUNITY; BIOMARKERS; CENTRAL NERVOUS SYSTEM; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; IMMUNOPHENOTYPING; MACROPHAGE ACTIVATION; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; MONOCYTES; MULTIPLE SCLEROSIS; PHENOTYPE; SODIUM CHLORIDE, DIETARY;

EID: 84957554992     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2015.11.001     Document Type: Article

References (48)

1. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683-747.
2. Hewer S., Lucas R., van der Mei I., Taylor B.V. Vitamin D and multiple sclerosis. J. Clin. Neurosci. Off. J. Neurosurg. Soc. Australas. 2013, 20:634-641.
3. Alonso A., Hernan M.A. Temporal trends in the incidence of multiple sclerosis: a systematic review. Neurology 2008, 71:129-135.
4. Olival G.S., Lima B.M., Sumita L.M., Serafim V., Fink M.C., Nali L.H., et al. Multiple sclerosis and herpesvirus interaction. Arq. Neuro-psiquiatr. 2013, 71:727-730.
5. Schmitz K., Barthelmes J., Stolz L., Beyer S., Diehl O., Tegeder I. "Disease modifying nutricals" for multiple sclerosis. Pharmacol. Ther. 2015 Apr, 148:85-113. Epub 2014 Nov 27. 10.1016/j.pharmthera.2014.11.015.
6. Kleinewietfeld M., Manzel A., Titze J., Kvakan H., Yosef N., Linker R.A., et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 2013, 496:518-522.
7. Farez M.F., Fiol M.P., Gaitán M.I., Quintana F.J., Correale J. Sodium intake is associated with increased disease activity in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 2015 Jan, 86(1):26-31. Epub 2014 Aug 28. 10.1136/jnnp-2014-307928.
8. Reboldi A., Coisne C., Baumjohann D., Benvenuto F., Bottinelli D., Lira S., et al. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 2009, 10:514-523.
9. Kebir H., Kreymborg K., Ifergan I., Dodelet-Devillers A., Cayrol R., Bernard M., et al. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 2007, 13:1173-1175.
10. Codarri L., Gyulveszi G., Tosevski V., Hesske L., Fontana A., Magnenat L., et al. RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 2011, 12:560-567.
11. Prineas J.W., Graham J.S. Multiple sclerosis: capping of surface immunoglobulin G on macrophages engaged in myelin breakdown. Ann. Neurol. 1981, 10:149-158.
12. Barnett M.H., Henderson A.P., Prineas J.W. The macrophage in MS: just a scavenger after all? Pathology and pathogenesis of the acute MS lesion. Mult. Scler. 2006, 12:121-132.
13. Mildner A., Mack M., Schmidt H., Bruck W., Djukic M., Zabel M.D., et al. CCR2+Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain J. Neurol. 2009, 132:2487-2500.
14. King I.L., Dickendesher T.L., Segal B.M. Circulating Ly-6C+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 2009, 113:3190-3197.
15. Hendriks J.J., Teunissen C.E., de Vries H.E., Dijkstra C.D. Macrophages and neurodegeneration. Brain Res. Brain Res. Rev. 2005, 48:185-195.
16. Breuer J., Schwab N., Schneider-Hohendorf T., Marziniak M., Mohan H., Bhatia U., et al. Ultraviolet B light attenuates the systemic immune response in central nervous system autoimmunity. Ann. Neurol. 2014, 75:739-758.
17. Hucke S., Flossdorf J., Grutzke B., Dunay I.R., Frenzel K., Jungverdorben J., et al. Licensing of myeloid cells promotes central nervous system autoimmunity and is controlled by peroxisome proliferator-activated receptor gamma. Brain J. Neurol. 2012, 135:1586-1605.
18. Fassl S.K., Austermann J., Papantonopoulou O., Riemenschneider M., Xue J., Bertheloot D., et al. Transcriptome assessment reveals a dominant role for TLR4 in the activation of human monocytes by the alarmin MRP8. J. Immunol. 2015, 194:575-583.
19. Schwab N., Waschbisch A., Wrobel B., Lochmuller H., Sommer C., Wiendl H. Human myoblasts modulate the function of antigen-presenting cells. J. Neuroimmunol. 2008, 200:62-70.
20. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11:723-737.
21. Vaknin I., Kunis G., Miller O., Butovsky O., Bukshpan S., Beers D.R., et al. Excess circulating alternatively activated myeloid (M2) cells accelerate ALS progression while inhibiting experimental autoimmune encephalomyelitis. PloS One 2011, 6:e26921.
22. Murray P.J., Allen J.E., Biswas S.K., Fisher E.A., Gilroy D.W., Goerdt S., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014, 41:14-20.
23. Binger K.J., Linker R.A., Muller D.N., Kleinewietfeld M. Sodium chloride, SGK1, and Th17 activation. Pflug. Arch. Eur. J. Physiol. 2015, 467:543-550.
24. Wu C., Yosef N., Thalhamer T., Zhu C., Xiao S., Kishi Y., et al. Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 2013, 496:513-517.
25. Schmid E., Xuan N.T., Zahir N., Russo A., Yang W., Kuhl D., et al. Serum- and glucocorticoid-inducible kinase 1 sensitive NF-kappaB signaling in dendritic cells. Cell. Physiol. Biochem. Int. J. Exp. Cell. Physiol. Biochem. Pharmacol. 2014, 34:943-954.
26. Schernthaner-Reiter M.H., Kiefer F., Zeyda M., Stulnig T.M., Luger A., Vila G. Strong association of serum- and glucocorticoid-regulated kinase 1 with peripheral and adipose tissue inflammation in obesity. Int. J. Obes. 2015, 39:1143-1150.
27. Ackermann T.F., Boini K.M., Beier N., Scholz W., Fuchss T., Lang F. EMD638683, a novel SGK inhibitor with antihypertensive potency. Cell. Physiol. Biochem. Int. J. Exp. Cell. Physiol. Biochem. Pharmacol. 2011, 28:137-146.
28. Lang F., Bohmer C., Palmada M., Seebohm G., Strutz-Seebohm N., Vallon V. (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol. Rev. 2006, 86:1151-1178.
29. Eder C. Ion channels in microglia (brain macrophages). Am. J. Physiol. 1998, 275:C327-C342.
30. Roselli F., Livrea P., Jirillo E. Voltage-gated sodium channel blockers as immunomodulators. Recent Pat. CNS Drug Discov. 2006, 1:83-91.
31. Craner M.J., Damarjian T.G., Liu S., Hains B.C., Lo A.C., Black J.A., et al. Sodium channels contribute to microglia/macrophage activation and function in EAE and MS. Glia 2005, 49:220-229.
32. Lee P.Y., Tsai P.S., Huang Y.H., Huang C.J. Inhibition of toll-like receptor-4, nuclear factor-kappaB and mitogen-activated protein kinase by lignocaine may involve voltage-sensitive sodium channels. Clin. Exp. Pharmacol. Physiol. 2008, 35:1052-1058.
33. Huang Y.H., Tsai P.S., Kai Y.F., Yang C.H., Huang C.J. Lidocaine inhibition of inducible nitric oxide synthase and cationic amino acid transporter-2 transcription in activated murine macrophages may involve voltage-sensitive Na+ channel. Anesth. Analg. 2006, 102:1739-1744.
34. Schwartz L., Guais A., Pooya M., Abolhassani M. Is inflammation a consequence of extracellular hyperosmolarity?. J. Inflamm. 2009, 6:21.
35. Wang C., Shi X., Chen X., Wu H., Zhang H., Xie J., et al. 17-beta-estradiol inhibits hyperosmolarity-induced proinflammatory cytokine elevation via the p38 MAPK pathway in human corneal epithelial cells. Mol. Vis. 2012, 18:1115-1122.
36. Liu Y., Shepherd E.G., Nelin L.D. MAPK phosphatases-regulating the immune response. Nat. Rev. Immunol. 2007, 7:202-212.
37. Jantsch J., Schatz V., Friedrich D., Schroder A., Kopp C., Siegert I., et al. Cutaneous Na+ storage strengthens the antimicrobial barrier function of the skin and boosts macrophage-driven host defense. Cell Metab. 2015, 21:493-501.
38. Sorgi C.A., Rose S., Court N., Carlos D., Paula-Silva F.W., Assis P.A., et al. GM-CSF priming drives bone marrow-derived macrophages to a pro-inflammatory pattern and downmodulates PGE2 in response to TLR2 ligands. PloS One 2012, 7:e40523.
39. Jiang Z., Jiang J.X., Zhang G.X. Macrophages: a double-edged sword in experimental autoimmune encephalomyelitis. Immunol. Lett. 2014, 160:17-22.
40. Arnold C.E., Whyte C.S., Gordon P., Barker R.N., Rees A.J., Wilson H.M. A critical role for suppressor of cytokine signalling 3 in promoting M1 macrophage activation and function in vitro and in vivo. Immunology 2014, 141:96-110.
41. Zhu W., Yu J., Nie Y., Shi X., Liu Y., Li F., et al. Disequilibrium of M1 and M2 macrophages correlates with the development of experimental inflammatory bowel diseases. Immunol. Invest. 2014, 43:638-652.
42. Miron V.E., Boyd A., Zhao J.W., Yuen T.J., Ruckh J.M., Shadrach J.L., et al. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat. Neurosci. 2013, 16:1211-1218.
43. Jiang H.R., Milovanovic M., Allan D., Niedbala W., Besnard A.G., Fukada S.Y., et al. IL-33 attenuates EAE by suppressing IL-17 and IFN-gamma production and inducing alternatively activated macrophages. Eur. J. Immunol. 2012, 42:1804-1814.
44. Liu C., Li Y., Yu J., Feng L., Hou S., Liu Y., et al. Targeting the shift from M1 to M2 macrophages in experimental autoimmune encephalomyelitis mice treated with fasudil. PloS One 2013, 8:e54841.
45. Kerby G.S., Cottin V., Accurso F.J., Hoffmann F., Chan E.D., Fadok V.A., et al. Impairment of macrophage survival by NaCl: implications for early pulmonary inflammation in cystic fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 283:L188-L197.
46. Ip W.K., Medzhitov R. Macrophages monitor tissue osmolarity and induce inflammatory response through NLRP3 and NLRC4 inflammasome activation. Nat. Commun. 2015, 6:6931.
47. Zhang W.C., Zheng X.J., Du L.J., Sun J.Y., Shen Z.X., Shi C., et al. High salt primes a specific activation state of macrophages, M(Na). Cell Res. 2015, 25:893-910.
48. Yi B., Titze J., Rykova M., Feuerecker M., Vassilieva G., Nichiporuk I., et al. Effects of dietary salt levels on monocytic cells and immune responses in healthy human subjects: a longitudinal study. Transl. Res. J. Lab. Clin. Med. 2015, 166:103-110.