Exacerbation of autoimmune neuroinflammation by dietary sodium is genetically controlled and sex specific

FASEB Journal

Volumn 29, Issue 8, 2015, Pages 3446-3457

  Krementsov, Dimitry N ^a   Case, Laure K ^a   Hickey, William F ^b   Teuscher, Cory ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Environment; Experimental autoimmune encephalomyelitis; Mouse model; Multiple sclerosis; Risk factor

Indexed keywords

SODIUM; SODIUM INTAKE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CHROMOSOME 17; CONTROLLED STUDY; DISEASE COURSE; DISEASE EXACERBATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENDER; GENETIC REGULATION; HELPER CELL; MALE; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RISK FACTOR; SODIUM INTAKE; TH17 CELL; ADVERSE EFFECTS; ANIMAL; BLOOD BRAIN BARRIER; C57BL MOUSE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMAN; IMMUNOLOGY; INFLAMMATION; METABOLISM; SEXUAL DEVELOPMENT; TH1 CELL;

ANIMALIA; MUS;

ANIMALS; BLOOD-BRAIN BARRIER; CHROMOSOMES, HUMAN, PAIR 17; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HUMANS; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; RISK FACTORS; SEX CHARACTERISTICS; SODIUM, DIETARY; TH1 CELLS; TH17 CELLS;

EID: 84940102196     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-272542     Document Type: Article

References (48)

1. Gourraud, P. A., Harbo, H. F., Hauser, S. L., and Baranzini, S. E. (2012) The genetics of multiple sclerosis: an up-to-date review. Immunol. Rev. 248, 87-103
2. Ebers, G. C. (2008) Environmental factors and multiple sclerosis. Lancet Neurol. 7, 268-277
3. Ramagopalan, S. V., and Sadovnick, A. D. (2011) Epidemiology of multiple sclerosis. Neurol. Clin. 29, 207-217
4. Kleinewietfeld, M., Manzel, A., Titze, J., Kvakan, H., Yosef, N., Linker, R. A., Muller, D. N., and Hafler, D. A. (2013) Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496, 518-522
5. Wu, C., Yosef, N., Thalhamer, T., Zhu, C., Xiao, S., Kishi, Y., Regev, A., and Kuchroo, V. K. (2013) Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 496, 513-517
6. Farez, M. F., Fiol, M. P., Gaitan, M. I., Quintana, F. J., and Correale, J. (2015) Sodium intake is associated with increased disease activity in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 86, 26-31
7. Clausen, B. E., Burkhardt, C., Reith, W., Renkawitz, R., and Förster, I. (1999) Conditional genetargetinginmacrophagesandgranulocytes using LysMcre mice. Transgenic Res. 8, 265-277
8. Caton, M. L., Smith-Raska, M. R., and Reizis, B. (2007) Notch-RBP-J signaling controls the homeostasis of CD8-dendritic cells in the spleen. J. Exp. Med. 204, 1653-1664
9. Nishida, K., Yamaguchi, O., Hirotani, S., Hikoso, S., Higuchi, Y., Watanabe, T., Takeda, T., Osuka, S., Morita, T., Kondoh, G., Uno, Y., Kashiwase, K., Taniike, M., Nakai, A., Matsumura, Y., Miyazaki, J., Sudo, T., Hongo, K., Kusakari, Y., Kurihara, S., Chien, K. R., Takeda, J., Hori, M., and Otsu, K. (2004) p38alpha Mitogen-activated protein kinaseplaysacritical roleincardiomyocytesurvivalbut notincardiac hypertrophic growth inresponsetopressure overload. Mol. Cell. Biol. 24, 10611-10620
10. Lee, P. P., Fitzpatrick, D. R., Beard, C., Jessup, H. K., Lehar, S., Makar, K. W., Pérez-Melgosa, M., Sweetser, M. T., Schlissel, M. S., Nguyen, S., Cherry, S. R., Tsai, J. H., Tucker, S. M., Weaver, W. M., Kelso, A., Jaenisch, R., and Wilson, C. B. (2001) A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15, 763-774
11. Machnik, A., Neuhofer, W., Jantsch, J., Dahlmann, A., Tammela, T., Machura, K., Park, J. K., Beck, F. X., Müller, D. N., Derer, W., Goss, J., Ziomber, A., Dietsch, P., Wagner, H., van Rooijen, N., Kurtz, A., Hilgers, K. F., Alitalo, K., Eckardt, K. U., Luft, F. C., Kerjaschki, D., and Titze, J. (2009) Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat. Med. 15, 545-552
12. Noubade, R., Milligan, G., Zachary, J. F., Blankenhorn, E. P., del Rio, R., Rincon, M., and Teuscher, C. (2007) Histamine receptor H1 is required for TCR-mediated p38 MAPK activation and optimal IFN-gamma production in mice. J. Clin. Invest. 117, 3507-3518
13. Mostafavi, S., Ortiz-Lopez, A., Bogue, M. A., Hattori, K., Pop, C., Koller, D., Mathis, D., and Benoist, C.; Immunological Genome Consortium. (2014) Variation and genetic control of gene expression in primary immunocytes across inbred mouse strains. J. Immunol. 193, 4485-4496
14. Liu, L., and Duff, K. (2008) A technique for serial collection of cerebrospinal fluid from the cisterna magna in mouse. J. Vis. Exp. (21)
15. Butterfield, R. J., Blankenhorn, E. P., Roper, R. J., Zachary, J. F., Doerge, R. W., and Teuscher, C. (2000) Identification ofgenetic loci controlling the characteristics and severity of brain and spinal cord lesions in experimental allergic encephalomyelitis. Am. J. Pathol. 157, 637-645
16. Friedman, M. (1937) The use of ranks to avoid the assumption of normality implicit in the analysis of variance. J. Am. Stat. Assoc. 32, 675-701
17. Friedman, M. (1939) A correction: the use of ranks to avoid the assumption of normality implicit in the analysis of variance. J. Am. Stat. Assoc. 34, 109
18. Friedman, M. (1940) Acomparisonofalternative testsofsignificance for the problem of m rankings. Ann. Math. Stat. 11, 86-92
19. Glass, G. V., Peckham, P. D., and Sanders, J. R. (1972) Consequences offailuretomeetassumptionsunderlying thefixed effects analyses of variance and covariance. Rev. Educ. Res. 42, 237-288
20. Blankenhorn, E. P., Butterfield, R. J., Rigby, R., Cort, L., Giambrone, D., McDermott, P., McEntee, K., Solowski, N., Meeker, N. D., Zachary, J. F., Doerge, R. W., and Teuscher, C. (2000) Genetic analysis of the influence of pertussis toxin on experimental allergic encephalomyelitis susceptibility: an environmental agent can override genetic checkpoints. J. Immunol. 164, 3420-3425
21. Matsuki, T., Nakae, S., Sudo, K., Horai, R., and Iwakura, Y. (2006) Abnormal T cell activation caused by the imbalance of the IL-1/IL-1R antagonist system is responsible for the development of experimental autoimmune encephalomyelitis. Int. Immunol. 18, 399-407
22. Spach, K. M., Noubade, R., McElvany, B., Hickey, W. F., Blankenhorn, E. P., and Teuscher, C. (2009) A single nucleotide polymorphism in Tyk2 controls susceptibility to experimental allergic encephalomyelitis. J. Immunol. 182, 7776-7783
23. Bearoff, F., Case, L. K., Krementsov, D. N., Wall, E. H., Saligrama, N., Blankenhorn, E. P., and Teuscher, C. (2015) Identification of genetic determinants of the sexual dimorphism in CNS autoimmunity. PLoS ONE 10, e0117993
24. Krementsov, D. N., Noubade, R., Dragon, J. A., Otsu, K., Rincon, M., and Teuscher, C. (2014) Sex-specific control of central nervous system autoimmunitybyp38mitogen-activated protein kinasesignaling in myeloid cells. Ann. Neurol. 75, 50-66
25. Artzt, K. (1986) Genetic analysis of the T/t complex. Hum. Immunol. 15, 374-380
26. Hammer, M. F., Schimenti, J., and Silver, L. M. (1989) Evolution of mouse chromosome 17and the origin of inversions associated with t haplotypes. Proc. Natl. Acad. Sci. USA 86, 3261-3265
27. Lyon, M. F., and Searle, A. G., eds. (1989) Genetic Variants and Strains of the Laboratory Mouse. Oxford University Press, New York
28. Alvarez, J. I., Cayrol, R., and Prat, A. (2011) Disruption of central nervous system barriers in multiple sclerosis. Biochim. Biophys. Acta 1812, 252-264
29. Schulz, M., and Engelhardt, B. (2005) The circumventricular organs participate in the immunopathogenesis of experimental autoimmune encephalomyelitis. Cerebrospinal Fluid Res. 2, 8
30. Wuerfel, E., Infante-Duarte, C., Glumm, R., and Wuerfel, J. T. (2010) Gadofluorine M-enhanced MRI shows involvement of circumventricular organs in neuroinflammation. J. Neuroinflammation 7, 70
31. Miller, R. L., Wang, M. H., Gray, P. A., Salkoff, L. B., and Loewy, A. D. (2013) ENaC-expressing neurons in the sensory circumventricular organs become c-Fos activated following systemic sodium changes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 305, R1141-R1152
32. Noda, M., and Hiyama, T. Y. (2015) Sodium sensing in the brain. Pflugers Arch.
33. Brown, I. J., Tzoulaki, I., Candeias, V., and Elliott, P. (2009) Salt intakes around the world: implications for public health. Int. J. Epidemiol. 38, 791-813 467, 465-474
34. Jew, S., AbuMweis, S. S., and Jones, P. J. (2009) Evolution of the human diet: linking our ancestral diet to modern functional foods as a means of chronic disease prevention. J. Med. Food 12, 925-934
35. McGuire, S. (2010) Institute of Medicine. 2010. Strategies to reduce sodium intake in the United States. Washington, DC: National Academies Press. Adv Nutr 1, 49-50
36. Weinberger, M. H. (1996) Salt sensitivity of blood pressure in humans. Hypertension 27, 481-490
37. Cowley, A. W., Jr. (2006) The genetic dissection of essential hypertension. Nat. Rev. Genet. 7, 829-840
38. Holbrook, J. T., Patterson, K. Y., Bodner, J. E., Douglas, L. W., Veillon, C., Kelsay, J. L., Mertz, W., and Smith, J. C., Jr. (1984) Sodium and potassium intake and balanceinadultsconsuming self-selected diets. Am. J. Clin. Nutr. 40, 786-793
39. Drenjančević-Perić, I., Jelaković, B., Lombard, J. H., Kunert, M. P., Kibel, A., and Gros, M. (2011) High-salt diet and hypertension: focus on the renin-angiotensin system. Kidney Blood Press. Res. 34, 1-11
40. Lanz, T. V., Ding, Z., Ho, P. P., Luo, J., Agrawal, A. N., Srinagesh, H., Axtell, R., Zhang, H., Platten, M., Wyss-Coray, T., and Steinman, L. (2010) Angiotensin II sustains brain inflammation in mice via TGF-beta. J. Clin. Invest. 120, 2782-2794
41. Stegbauer, J., Lee, D. H., Seubert, S., Ellrichmann, G., Manzel, A., Kvakan, H., Muller, D. N., Gaupp, S., Rump, L. C., Gold, R., and Linker, R. A. (2009) Role of the renin-angiotensin system in autoimmune inflammation of the central nervous system. Proc. Natl. Acad. Sci. USA 106, 14942-14947
42. Platten, M., Youssef, S., Hur, E. M., Ho, P. P., Han, M. H., Lanz, T. V., Phillips, L. K., Goldstein, M. J., Bhat, R., Raine, C. S., Sobel, R. A., and Steinman, L. (2009) Blocking angiotensin-converting enzyme induces potent regulatory T cells and modulates TH1- and TH17-mediated autoimmunity. Proc. Natl. Acad. Sci. USA 106, 14948-14953
43. +/- mice with low nephron number. Kidney Blood Press. Res. 37, 379-391
44. Engelhardt, B. (2008) The blood-central nervous system barriers actively control immune cell entry into the central nervous system. Curr. Pharm. Des. 14, 1555-1565
45. Inglese, M., Madelin, G., Oesingmann, N., Babb, J. S., Wu, W., Stoeckel, B., Herbert, J., and Johnson, G. (2010) Brain tissue sodium concentration in multiple sclerosis: a sodium imaging study at 3 tesla. Brain 133, 847-857
46. Paling, D., Solanky, B. S., Riemer, F., Tozer, D. J., Wheeler-Kingshott, C. A., Kapoor, R., Golay, X., and Miller, D. H. (2013) Sodium accumulation is associated with disability and a progressive course in multiple sclerosis. Brain 136, 2305-2317
47. Ochoa-Repáraz, J., Mielcarz, D. W., Begum-Haque, S., and Kasper, L. H. (2011) Gut, bugs, and brain: role of commensal bacteria in the control of central nervous system disease. Ann. Neurol. 69, 240-247
48. Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R. D., Shanahan, F., Dinan, T. G., and Cryan, J. F. (2013) The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol. Psychiatry 18, 666-673