Deletion of the mineralocorticoid receptor in myeloid cells attenuates central nervous system autoimmunity

Frontiers in Immunology

Volumn 8, Issue OCT, 2017, Pages

  Montes Cobos, Elena ^a   Schweingruber, Nils ^a   Li, Xiao ^a   Fischer, Henrike J ^a   Reichardt, Holger M ^a   Lühder, Fred ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

Experimental autoimmune encephalomyelitis; M2 polarization; Mineralocorticoid receptor; Myeloid cells; Neuroinflammation

Indexed keywords

CHLORIDE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 17; MINERALOCORTICOID RECEPTOR; SODIUM; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; BONE MARROW CELL; CELL ACTIVATION; CELL FUNCTION; CELL ISOLATION; CELL PROLIFERATION; CELL SEPARATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE DELETION; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHENOTYPE; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; WESTERN BLOTTING;

EID: 85032859467     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.01319     Document Type: Article

References (61)

1. Milligan NM, Newcombe R, Compston DAS. A double-blind controlled trial of high-dose methylprednisolone in patients with multiple-sclerosis. 1. Clinical effects. J Neurol Neurosurg Psychiatry (1987) 50:511-6. doi:10.1136/jnnp.50.5.511
2. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the Diagnosis of Multiple Sclerosis. Ann Neurol (2001) 50:121-7. doi:10.1002/ana.1032
3. Haghikia A, Hohlfeld R, Gold R, Fugger L. Therapies for multiple sclerosis: translational achievements and outstanding needs. Trends Mol Med (2013) 19:309-19. doi:10.1016/j.molmed.2013.03.004
4. Arriza JL, Weinberger C, Cerelli G, Glaser TM, Handelin BL, Housman DE, et al. Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science (1987) 237:268-75. doi:10.1126/science.3037703
5. Funder JW. Mineralocorticoid receptor antagonists: emerging roles in cardiovascular medicine. Integr Blood Press Control (2013) 6:129-38. doi:10.2147/IBPC.S13783
6. Yang J, Young MJ. The mineralocorticoid receptor and its coregulators. J Mol Endocrinol (2009) 43:53-64. doi:10.1677/JME-09-0031
7. Bene NC, Alcaide P, Wortis HH, Jaffe IZ. Mineralocorticoid receptors in immune cells: emerging role in cardiovascular disease. Steroids (2014) 91:38-45. doi:10.1016/j.steroids.2014.04.005
8. Funder JW. Mineralocorticoid receptors: distribution and activation. Heart Fail Rev (2005) 10:15-22. doi:10.1007/s10741-005-2344-2
9. Usher MG, Duan SZ, Ivaschenko CY, Frieler RA, Berger S, Schütz G, et al. Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J Clin Invest (2010) 120:3350-64. doi:10.1172/JCI41080
10. Chantong B, Kratschmar DV, Nashev LG, Balazs Z, Odermatt A. Mineralocorticoid and glucocorticoid receptors differentially regulate NF-kappaB activity and pro-inflammatory cytokine production in murine BV-2 microglial cells. J Neuroinflammation (2012) 9:260. doi:10.1186/1742-2094-9-260
11. Lühder F, Reichardt HM. Traditional concepts and future avenues of glucocorticoid action in experimental autoimmune encephalomyelitis and multiple sclerosis therapy. Crit Rev Immunol (2009) 29:255-73. doi:10.1615/CritRevImmunol.v29.i3.50
12. Wüst S, van den BJ, Tischner D, Kleiman A, Tuckermann JP, Gold R, et al. Peripheral T cells are the therapeutic targets of glucocorticoids in experimental autoimmune encephalomyelitis. J Immunol (2008) 180:8434-43. doi:10.4049/jimmunol.180.12.8434
13. Wüst S, Tischner D, John M, Tuckermann JP, Menzfeld C, Hanisch UK, et al. Therapeutic and adverse effects of a non-steroidal glucocorticoid receptor ligand in a mouse model of multiple sclerosis. PLoS One (2009) 4:e8202. doi:10.1371/journal.pone.0008202
14. Schweingruber N, Fischer HJ, Fischer L, van den Brandt J, Karabinskaya A, Labi V, et al. Chemokine-mediated redirection of T cells constitutes a critical mechanism of glucocorticoid therapy in autoimmune CNS responses. Acta Neuropathol (2014) 127:713-29. doi:10.1007/s00401-014-1248-4
15. Schweingruber N, Haine A, Tiede K, Karabinskaya A, van den Brandt J, Wüst S, et al. Liposomal encapsulation of glucocorticoids alters their mode of action in the treatment of experimental autoimmune encephalomyelitis. J Immunol (2011) 187:4310-8. doi:10.4049/jimmunol.1101604
16. Montes-Cobos E, Ring S, Fischer HJ, Heck J, Strauss J, Schwaninger M, et al. Targeted delivery of glucocorticoids to macrophages in a mouse model of multiple sclerosis using inorganic-organic hybrid nanoparticles. J Control Release (2016) 245:157-69. doi:10.1016/j.jconrel.2016.12.003
17. Herrada AA, Contreras FJ, Marini NP, Amador CA, Gonzalez PA, Cortes CM, et al. Aldosterone promotes autoimmune damage by enhancing Th17-mediated immunity. J Immunol (2010) 184:191-202. doi:10.4049/jimmunol.0802886
18. Bechmann L, Busse K, Stoppe M, Cotte S, Ettrich B, Then BF. Corticosteroid receptor expression and in vivo glucocorticoid sensitivity in multiple sclerosis. J Neuroimmunol (2014) 276:159-65. doi:10.1016/j.jneuroim.2014.07.004
19. Berger S, Wolfer DP, Selbach O, Alter H, Erdmann G, Reichardt HM, et al. Loss of the limbic mineralocorticoid receptor impairs behavioral plasticity. Proc Natl Acad Sci U S A (2006) 103:195-200. doi:10.1073/pnas.0503878102
20. Ronzaud C, Loffing J, Gretz N, Schütz G, Berger S. Inducible renal principal cell-specific mineralocorticoid receptor gene inactivation in mice. Am J Physiol Renal Physiol (2011) 300:F756-60. doi:10.1152/ajprenal.00728.2009
21. Fraccarollo D, Berger S, Galuppo P, Kneitz S, Hein L, Schütz G, et al. Deletion of cardiomyocyte mineralocorticoid receptor ameliorates adverse remodeling after myocardial infarction. Circulation (2011) 123:400-8. doi:10.1161/CIRCULATIONAHA.110.983023
22. Montes-Cobos E, Li X, Fischer HJ, Sasse A, Kügler S, Didie M, et al. Inducible knock-down of the mineralocorticoid receptor in mice disturbs regulation of the renin-angiotensin-aldosterone system and attenuates heart failure induced by pressure overload. PLoS One (2015) 10:e0143954. doi:10.1371/journal.pone.0143954
23. Frieler RA, Meng H, Duan SZ, Berger S, Schütz G, He Y, et al. Myeloid-specific deletion of the mineralocorticoid receptor reduces infarct volume and alters inflammation during cerebral ischemia. Stroke (2011) 42:179-85. doi:10.1161/STROKEAHA.110.598441
24. Li C, Sun XN, Zeng MR, Zheng XJ, Zhang YY, Wan Q, et al. Mineralocorticoid receptor deficiency in T cells attenuates pressure overload-induced cardiac hypertrophy and dysfunction through modulating T-cell activation. Hypertension (2017) 70:137-47. doi:10.1161/HYPERTENSIONAHA.117.09070
25. Sun XN, Li C, Liu Y, Du LJ, Zeng MR, Zheng XJ, et al. T-cell mineralocorticoid receptor controls blood pressure by regulating interferon-gamma. Circ Res (2017) 120:1584-97. doi:10.1161/CIRCRESAHA.116.310480
26. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Förster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res (1999) 8:265-77. doi:10.1023/A:1008942828960
27. Bettelli E, Pagany M, Weiner HL, Linington C, Sobel RA, Kuchroo AK. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J Exp Med (2003) 197:1073-81. doi:10.1084/jem.20021603
28. Litchfield S, Nagy Z. New temperature modification makes the Bielschowsky silver stain reproducible. Acta Neuropathol (2001) 101:17-21
29. Flach AC, Litke T, Strauss J, Haberl M, Gomez CC, Reindl M, et al. Autoantibody-boosted T-cell reactivation in the target organ triggers manifestation of autoimmune CNS disease. Proc Natl Acad Sci U S A (2016) 113:3323-8. doi:10.1073/pnas.1519608113
30. Kleiman A, Hübner S, Rodriguez Parkitna JM, Neumann A, Hofer S, Weigand MA, et al. Glucocorticoid receptor dimerization is required for survival in septic shock via suppression of interleukin-1 in macrophages. FASEB J (2012) 26:722-9. doi:10.1096/fj.11-192112
31. Mildner A, Mack M, Schmidt H, Brück W, Djukic M, Zabel MD, et al. CCR2 + Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain (2009) 132:2487-500. doi:10.1093/brain/awp144
32. Rose S, Misharin A, Perlman H. A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry A (2012) 81:343-50. doi:10.1002/cyto.a.22012
33. Heppner FL, Greter M, Marino D, Falsig J, Raivich G, Hovelmeyer N, et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med (2005) 11:146-52. doi:10.1038/nm1177
34. Friese MA, Fugger L. T cells and microglia as drivers of multiple sclerosis pathology. Brain (2007) 130:2755-7. doi:10.1093/brain/awm246
35. Martin-Fernandez B, Rubio-Navarro A, Cortegano I, Ballesteros S, Alia M, Cannata-Ortiz P, et al. Aldosterone induces renal fibrosis and inflammatory M1-macrophage subtype via mineralocorticoid receptor in rats. PLoS One (2016) 11:e0145946. doi:10.1371/journal.pone.0145946
36. Bienvenu LA, Morgan J, Rickard AJ, Tesch GH, Cranston GA, Fletcher EK, et al. Macrophage mineralocorticoid receptor signaling plays a key role in aldosterone-independent cardiac fibrosis. Endocrinology (2012) 153:3416-25. doi:10.1210/en.2011-2098
37. Hendriks JJ, Teunissen CE, de Vries HE, Dijkstra CD. Macrophages and neurodegeneration. Brain Res Brain Res Rev (2005) 48:185-95. doi:10.1016/j.brainresrev.2004.12.008
38. van der Goes A, Brouwer J, Hoekstra K, Roos D, van den Berg TK, Dijkstra CD. Reactive oxygen species are required for the phagocytosis of myelin by macrophages. J Neuroimmunol (1998) 92:67-75. doi:10.1016/S0165-5728(98)00175-1
39. Mosley K, Cuzner ML. Receptor-mediated phagocytosis of myelin by macrophages and microglia: effect of opsonization and receptor blocking agents. Neurochem Res (1996) 21:481-7. doi:10.1007/BF02527713
40. Brück W, Sommermeier N, Bergmann M, Zettl U, Goebel HH, Kretzschmar HA, et al. Macrophages in multiple sclerosis. Immunobiology (1996) 195:588-600. doi:10.1016/S0171-2985(96)80024-6
41. Huitinga I, van RN, de Groot CJ, Uitdehaag BM, Dijkstra CD. Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J Exp Med (1990) 172:1025-33. doi:10.1084/jem.172.4.1025
42. Tran EH, Hoekstra K, van RN, Dijkstra CD, Owens T. Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice. J Immunol (1998) 161:3767-75
43. Mikita J, Dubourdieu-Cassagno N, Deloire MSA, Vekris A, Biran M, Raffard G, et al. Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. amelioration of clinical status by M2 activated monocyte administration. Mult Scler (2011) 17:2-15. doi:10.1177/1352458510379243
44. Vaknin I, Kunis G, Miller O, Butovsky O, Bukshpan S, Beers DR, et al. Excess circulating alternatively activated myeloid (M2) cells accelerate ALS progression while inhibiting experimental autoimmune encephalomyelitis. PLoS One (2011) 6:e26921. doi:10.1371/journal.pone.0026921
45. Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, et al. Differential roles of microglia and monocytes in the inflamed central nervous system. J Exp Med (2014) 211:1533-49. doi:10.1084/jem.20132477
46. Starossom SC I, Mascanfroni D, Imitola J, Cao L, Raddassi K, Hernandez SF, et al. Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration. Immunity (2012) 37:249-63. doi:10.1016/j.immuni.2012.05.023
47. Lim HY, Müller N, Herold MJ, van den Brandt J, Reichardt HM. Glucocorticoids exert opposing effects on macrophage function dependent on their concentration. Immunology (2007) 122:47-53. doi:10.1111/j.1365-2567.2007.02611.x
48. Jäger A, Dardalhon V, Sobel RA, Bettelli E, Kuchroo VK. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J Immunol (2009) 183:7169-77. doi:10.4049/jimmunol.0901906
49. Domingues HS, Mues M, Lassmann H, Wekerle H, Krishnamoorthy G. Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLoS One (2010) 5:e15531. doi:10.1371/journal.pone.0015531
50. 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) 12:560-7. doi:10.1038/ni.2027
51. El-Behi M, Ciric B, Dai H, Yan Y, Cullimore M, Safavi F, et al. The encephalitogenicity of T(H)17 cells is dependent on IL-1-and IL-23-induced production of the cytokine GM-CSF. Nat Immunol (2011) 12:568-75. doi:10.1038/ni.2031
52. Waisman A, Hauptmann J, Regen T. The role of IL-17 in CNS diseases. Acta Neuropathol (2015) 129:625-37. doi:10.1007/s00401-015-1402-7
53. Rodriguez PC, Zea AH, DeSalvo J, Culotta KS, Zabaleta J, Quiceno DG, et al. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J Immunol (2003) 171:1232-9. doi:10.4049/jimmunol.171.3.1232
54. Bronte V, Serafini P, Mazzoni A, Segal DM, Zanovello P. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol (2003) 24:302-6. doi:10.1016/S1471-4906(03)00132-7
55. Armanini D, Endres S, Kuhnle U, Weber PC. Parallel determination of mineralocorticoid and glucocorticoid receptors in T-and B-lymphocytes of human spleen. Acta Endocrinol (Copenh) (1988) 118:479-82
56. Kleinewietfeld M, Manzel A, Titze J, Kvakan H, Yosef N, Linker RA, et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature (2013) 496:518-22. doi:10.1038/nature11868
57. Jörg S, Kissel J, Manzel A, Kleinewietfeld M, Haghikia A, Gold R, et al. High salt drives Th17 responses in experimental autoimmune encephalomyelitis without impacting myeloid dendritic cells. Exp Neurol (2016) 279:212-22. doi:10.1016/j.expneurol.2016.03.010
58. Hucke S, Eschborn M, Liebmann M, Herold M, Freise N, Engbers A, 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
59. Edelmann F, Wachter R, Schmidt AG, Kraigher-Krainer E, Colantonio C, Kamke W, et al. Effect of spironolactone on diastolic function and exercise capacity in patients with heart failure with preserved ejection fraction: the aldo-DHF randomized controlled trial. JAMA (2013) 309:781-91. doi:10.1001/jama.2013.905
60. Bärfacker L, Kuhl A, Hillisch A, Grosser R, Figueroa-Perez S, Heckroth H, et al. Discovery of BAY 94-8862: a nonsteroidal antagonist of the mineralocorticoid receptor for the treatment of cardiorenal diseases. ChemMedChem (2012) 7:1385-403. doi:10.1002/cmdc.201200081
61. Kolkhof P, Delbeck M, Kretschmer A, Steinke W, Hartmann E, Bärfacker L, et al. Finerenone, a novel selective nonsteroidal mineralocorticoid receptor antagonist protects from rat cardiorenal injury. J Cardiovasc Pharmacol (2014) 64:69-78. doi:10.1097/FJC.0000000000000091