High salt reduces the activation of IL-4- and IL-13-stimulated macrophages

Journal of Clinical Investigation

Volumn 125, Issue 11, 2015, Pages 4223-4238

  Binger, Katrina J ^a,l   Gebhardt, Matthias ^a   Heinig, Matthias ^a   Rintisch, Carola ^a   Schroeder, Agnes ^b   Neuhofer, Wolfgang ^c   Hilgers, Karl ^b   Manzel, Arndt ^b   Schwartz, Christian ^b   Kleinewietfeld, Markus ^d,e   Voelkl, Jakob ^f   Schatz, Valentin ^g   Linker, Ralf A ^b   Lang, Florian ^f   Voehringer, David ^b   Wright, Mark D ^h   Hubner, Norbert ^a   Dechend, Ralf ^a,i   Jantsch, Jonathan ^g   Titze, Jens ^b,j   Müller, Dominik N ^a,k   more..

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^e CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^f UNIVERSITY OF TÜBINGEN   (Germany)

^g UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^h MONASH UNIVERSITY   (Australia)

ⁱ HELIOS Klinikum Berlin   (Germany)

^j VANDERBILT UNIVERSITY   (United States)

^k DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^l BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; INTERLEUKIN 13; INTERLEUKIN 4; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; SODIUM CHLORIDE; STAT6 PROTEIN; AKT1 PROTEIN, MOUSE; MTOR PROTEIN, MOUSE; SALT INTAKE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL POLARITY; CELL STIMULATION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EFFECTOR CELL; GLYCOLYSIS; IMMUNOREGULATION; IN VITRO STUDY; INFLAMMATION; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MACROPHAGE ACTIVATION; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SALT INTAKE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH17 CELL; WOUND HEALING IMPAIRMENT; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CLASSIFICATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HISTONE CODE; IMMUNOLOGY; MACROPHAGE; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; PHARMACOLOGY; PHYSIOLOGY; RANDOMIZATION; TOXICITY; TRANSGENIC MOUSE; WOUND HEALING;

ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; CHITIN; GENE EXPRESSION REGULATION; GLYCOLYSIS; HISTONE CODE; IMMUNITY, INNATE; INFLAMMATION; INTERLEUKIN-13; INTERLEUKIN-4; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; SODIUM CHLORIDE, DIETARY; TOR SERINE-THREONINE KINASES; WOUND HEALING;

EID: 84946763057     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI80919     Document Type: Article

References (64)

1. Mozaffarian D, et al. Global sodium consumption and death from cardiovascular causes. N Engl J Med. 2014;371(7):624-634.
2. He FJ, Li J, Macgregor GA. Effect of longer-term modest salt reduction on blood pressure. Cochrane Database Syst Rev. 2013;4:CD004937.
3. Sundstrom B, Johansson I, Rantapaa-Dahlqvist S. Interaction between dietary sodium and smoking increases the risk for rheumatoid arthritis: results from a nested case-control study. Rheumatology (Oxford). 2014;54(3):487-493.
4. Farez MF, Fiol MP, Gaitán MI, Quintana FJ, Correale J. Sodium intake is associated with increased disease activity in multiple sclerosis. J Neurol Neurosurg Psychiatry. 2015;86(1):26-31.
5. D'Elia L, Galletti F, Strazzullo P. Dietary salt intake and risk of gastric cancer. Cancer Treat Res. 2014;159:83-95.
6. Mente A, et al. Association of urinary sodium and potassium excretion with blood pressure. N Engl J Med. 2014;371(7):601-611.
7. O'Donnell M, et al. Urinary sodium and potassium excretion, mortality, and cardiovascular events. N Engl J Med. 2014;371(7):612-623.
8. Wain LV, et al. Genome-wide association study identifies six new loci influencing pulse pressure and mean arterial pressure. Nat Genet. 2011;43(10):1005-1011.
9. Ehret GB, et al. Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk. Nature. 2011;478(7367):103-109.
10. Deloukas P, et al. Large-scale association analysis identifies new risk loci for coronary artery disease. Nat Genet. 2013;45(1):25-33.
11. Beecham AH, et al. Analysis of immune-related loci identifies 48 new susceptibility variants for multiple sclerosis. Nat Genet. 2013;45(11):1353-1360.
12. Titze J. Sodium balance is not just a renal affair. Curr Opin Nephrol Hypertens. 2014;23(2):101-105.
13. Dahlmann A, et al. Magnetic resonance-determined sodium removal from tissue stores in hemodialysis patients. Kidney Int. 2015;87(2):434-441.
14. Kopp C, et al. 23Na magnetic resonance imag-ing-determined tissue sodium in healthy subjects and hypertensive patients. Hypertension. 2013;61(3):635-640.
15. Kopp C, et al. (23)Na magnetic resonance imaging of tissue sodium. Hypertension. 2012;59(1):167-172.
16. Machnik A, et al. Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat Med. 2009;15(5):545-552.
17. Wiig H, et al. Immune cells control skin lymphatic electrolyte homeostasis and blood pressure. J Clin Invest. 2013;123(7):2803-2815.
18. + storage strengthens the antimicrobial barrier function of the skin and boosts macrophage-driven host defense. Cell Metab. 2015;21(3):493-501.
19. Szabo G, Magyar Z. Electrolyte concentrations in subcutaneous tissue fluid and lymph. Lymphol-ogy. 1982;15(4):174-177.
20. Titze J, et al. Glycosaminoglycan polymerization may enable osmotically inactive Na+ storage in the skin. Am J Physiol Heart Circ Physiol. 2004;287(1):H203-H208.
21. Go WY, Liu X, Roti MA, Liu F, Ho SN. NFAT5/TonEBP mutant mice define osmotic stress as a critical feature of the lymphoid microenvironment. Proc Natl Acad Sci USA. 2004;101(29):10673-10678.
22. Kleinewietfeld M, et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature. 2013;496(7446):518-522.
23. Muller S, et al. Salt-dependent chemotaxis of macrophages. PLoS O ne. 2013;8(9):e73439.
24. Wu C, et al. Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature. 2013;496(7446):513-517.
25. Xue J, et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity. 2014;40(2):274-288.
26. Murray PJ, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41(1):14-20.
27. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8(12):958-969.
28. Parsa R, et al. Adoptive transfer of immunomod-ulatory M2 macrophages prevents type 1 diabetes in NOD mice. Diabetes. 2012;61(11):2881-2892.
29. Jiang HR, et al. IL-33 attenuates EAE by suppressing IL-17 and IFN-γ production and inducing alternatively activated macrophages. Eur J Immunol. 2012;42(7):1804-1814.
30. Mikita J, et al. Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. Mult Scler. 2011;17(1):2-15.
31. Szanto A, et al. STAT6 transcription factor is a facilitator of the nuclear receptor PPARγ-regu-lated gene expression in macrophages and dendritic cells. Immunity. 2010;33(5):699-712.
32. Huber S, Hoffmann R, Muskens F, Voehringer D. Alternatively activated macrophages inhibit T-cell proliferation by Stat6-dependent expression of PD-L2. Blood. 2010;116(17):3311-3320.
33. Bouhlel MA, et al. PPARγ activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab. 2007;6(2):137-143.
34. Odegaard JI, et al. Macrophage-specific PPARγ controls alternative activation and improves insulin resistance. Nature. 2007;447(7148):1116-1120.
35. Haschemi A, et al. The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism. Cell Metab. 2012;15(6):813-826.
36. Huang SC, et al. Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat Immunol. 2014;15(9):846-855.
37. Byles V, et al. The TSC-mTOR pathway regulates macrophage polarization. Nat Commun. 2013;4:2834.
38. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007;117(1):175-184.
39. Li L, et al. Role of myeloid-derived suppressor cells in glucocorticoid-mediated amelioration of FSGS. J Am Soc Nephrol. 2015;26(9):2183-2197.
40. Marigo I, et al. Tumor-induced tolerance and immune suppression depend on the C/EBPβ transcription factor. Immunity. 2010;32(6):790-802.
41. Reese TA, et al. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature. 2007;447(7140):92-96.
42. Satoh T, et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol. 2010;11(10):936-944.
43. Martin P. Wound healing-aiming for perfect skin regeneration. Science. 1997;276(5309):75-81.
44. Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med. 1999;341(10):738-746.
45. Deonarine K, et al. Gene expression profiling of cutaneous wound healing. J Transl Med. 2007;5:11.
46. Martin P, et al. Wound healing in the PU. Curr Biol. 2003;13(13):1122-1128.
47. Liao X, et al. Kruppel-like factor 4 regulates macrophage polarization. J Clin Invest. 2011;121(7):2736-2749.
48. Heikamp EB, et al. The AGC kinase SGK1 regulates TH1 and TH2 differentiation downstream of the mTORC2 complex. Nat Immunol. 2014;15(5):457-464.
49. Lang F. Effect of cell hydration on metabolism. Nestle Nutr Ins t Workshop Ser. 2011;69:115-126.
50. Pearce EL, Poffenberger MC, Chang CH, Jones RG. Fueling immunity: insights into metabolism and lymphocyte function. Science. 2013;342(6155):1242454.
51. O'Sullivan D, et al. Memory CD8(+) T cells use cell-intrinsic lipolysis to support the metabolic programming necessary for development. Immunity. 2014;41(1):75-88.
52. van der Windt GJ, et al. CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc Natl Acad Sci USA. 2013;110(35):14336-14341.
53. Man K, et al. The transcription factor IRF4 is essential for TCR affinity-mediated metabolic programming and clonal expansion of T cells. Nat Immunol. 2013;14(11):1155-1165.
54. Everts B, et al. TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKvars supports the anabolic demands of dendritic cell activation. Nat Immunol. 2014;15(4):323-332.
55. Everts B, et al. Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells. Blood. 2012;120(7):1422-1431.
56. Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell Res. 2005;15(1):11-18.
57. Ip WK, Medzhitov R. Macrophages monitor tissue osmolarity and induce inflammatory response through NLRP3 and NLRC4 inflammasome activation. Nat Commun. 2015;6:6931.
58. Chang CH, et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell. 2013;153(6):1239-1251.
59. Colegio OR, et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature. 2014;513(7519):559-563.
60. Tannahill GM, et al. Succinate is an inflammatory signal that induces IL-1ß through HIF-1a. Nature. 2013;496(7444):238-242.
61. Shi LZ, et al. HIF1a-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med. 2011;208(7):1367-1376.
62. Ganeshan K, Chawla A. Metabolic regulation of immune responses. Annu Rev Immunol. 2014;32:609-634.
63. Wulff P, et al. Impaired renal Na(+) retention in the sgk1-knockout mouse. J Clin Invest 2002;110(9):1263-1268.
64. Kueper C, Beck FX, Neuhofer W. Generation of a conditional knockout allele for the NFAT5 gene in mice. Front Physiol. 2015;5:507