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Cellular and Molecular Links between Autoimmunity and Lipid Metabolism

  • Ryu, Heeju (Laboratory of Immune Regulation, Institute of Pharmaceutical Sciences, Seoul National University) ;
  • Kim, Jiyeon (Laboratory of Immune Regulation, Institute of Pharmaceutical Sciences, Seoul National University) ;
  • Kim, Daehong (Laboratory of Immune Regulation, Institute of Pharmaceutical Sciences, Seoul National University) ;
  • Lee, Jeong-Eun (Laboratory of Immune Regulation, Institute of Pharmaceutical Sciences, Seoul National University) ;
  • Chung, Yeonseok (Laboratory of Immune Regulation, Institute of Pharmaceutical Sciences, Seoul National University)
  • 투고 : 2019.08.29
  • 심사 : 2019.11.03
  • 발행 : 2019.11.30

초록

The incidence of atherosclerosis is higher among patients with several autoimmune diseases such as psoriasis, rheumatoid arthritis (RA) and systemic lupus erythematosus (SLE). It is well documented that innate immune cells including macrophages and dendritic cells sense lipid species such as saturated fatty acids and oxidized low-density lipoprotein and produce pro-inflammatory cytokines and chemokines. However, whether a hyperlipidemic environment also impacts autoimmune T cell responses has been unclear. Among $CD4^+$ T cells, Th17 and follicular helper T (Tfh) cells are known to play pathogenic roles in the development of hyperlipidemia-associated autoimmune diseases. This review gives an overview of the cellular and molecular mechanisms by which dysregulated lipid metabolism impacts the pathogenesis of autoimmune diseases, with specific emphasis on Th17 and Tfh cells.

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참고문헌

  1. A-Gonzalez, N., Bensinger, S.J., Hong, C., Beceiro, S., Bradley, M.N., Zelcer, N., Deniz, J., Ramirez, C., Diaz, M., Gallardo, G., et al. (2009). Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 31, 245-258. https://doi.org/10.1016/j.immuni.2009.06.018
  2. Ait-Oufella, H., Salomon, B.L., Potteaux, S., Robertson, A.K.L., Gourdy, P., Zoll, J., Merval, R., Esposito, B., Cohen, J.L., Fisson, S., et al. (2006). Natural regulatory T cells control the development of atherosclerosis in mice. Nat. Med. 12, 178-180. https://doi.org/10.1038/nm1343
  3. Aktas, O., Waiczies, S., Smorodchenko, A., Dorr, J., Seeger, B., Prozorovski, T., Sallach, S., Endres, M., Brocke, S., Nitsch, R., et al. (2003). Treatment of relapsing paralysis in experimental encephalomyelitis by targeting Th1 cells through atorvastatin. J. Exp. Med. 197, 725-733. https://doi.org/10.1084/jem.20021425
  4. Anaya, J.M. (2012). Common mechanisms of autoimmune diseases (the autoimmune tautology). Autoimmun. Rev. 11, 781-784. https://doi.org/10.1016/j.autrev.2012.02.002
  5. Bao, Y.K., Weide, L.G., Ganesan, V.C., Jakhar, I., McGill, J.B., Sahil, S., Cheng, A.L., Gaddis, M., and Drees, B.M. (2019). High prevalence of comorbid autoimmune diseases in adults with type 1 diabetes from the HealthFacts database. J. Diabetes 11, 273-279. https://doi.org/10.1111/1753-0407.12856
  6. Baptista, D., Mach, F., and Brandt, K.J. (2018). Follicular regulatory T cell in atherosclerosis. J. Leukoc. Biol. 104, 925-930. https://doi.org/10.1002/JLB.MR1117-469R
  7. Batten, M., Ramamoorthi, N., Kljavin, N.M., Ma, C.S., Cox, J.H., Dengler, H.S., Danilenko, D.M., Caplazi, P., Wong, M., Fulcher, D.A., et al. (2010). IL-27 supports germinal center function by enhancing IL-21 production and the function of T follicular helper cells. J. Exp. Med. 207, 2895. https://doi.org/10.1084/jem.20100064
  8. Berod, L., Friedrich, C., Nandan, A., Freitag, J., Hagemann, S., Harmrolfs, K., Sandouk, A., Hesse, C., Castro, C.N., Bähre, H., et al. (2014). De novo fatty acid synthesis controls the fate between regulatory T and T helper 17 cells. Nat. Med. 20, 1327. https://doi.org/10.1038/nm.3704
  9. Canavan, M., McCarthy, C., Larbi, N.B., Dowling, J.K., Collins, L., O'Sullivan, F., Hurley, G., Murphy, C., Quinlan, A., Moloney, G., et al. (2013). Activation of liver X receptor suppresses the production of the IL-12 family of cytokines by blocking nuclear translocation of NF-${\kappa}Bp50$. Innate Immun. 20, 675-687. https://doi.org/10.1177/1753425913501915
  10. Carr, T.M., Wheaton, J.D., Houtz, G.M., and Ciofani, M. (2017). JunB promotes Th17 cell identity and restrains alternative CD4(+) T-cell programs during inflammation. Nat. Commun. 8, 301. https://doi.org/10.1038/s41467-017-00380-3
  11. Choi, J.Y., Ho, J.H., Pasoto, S.G., Bunin, V., Kim, S.T., Carrasco, S., Borba, E.F., Goncalves, C.R., Costa, P.R., Kallas, E.G., et al. (2015). Circulating follicular helper-like T cells in systemic lupus erythematosus: association with disease activity. Arthritis Rheumatol. 67, 988-999. https://doi.org/10.1002/art.39020
  12. Choi, J.Y., Seth, A., Kashgarian, M., Terrillon, S., Fung, E., Huang, L., Wang, L.C., and Craft, J. (2017). Disruption of pathogenic cellular networks by IL-21 blockade leads to disease amelioration in murine lupus. J. Immunol. 198, 2578-2588. https://doi.org/10.4049/jimmunol.1601687
  13. Chung, Y., Tanaka, S., Chu, F., Nurieva, R., Martinez, G.J., Rawal, S., Wang, Y.H., Lim, H.Y., Reynolds, J.M., Zhou, X.H., et al. (2011). Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat. Med. 17, 983-988. https://doi.org/10.1038/nm.2426
  14. Cua, D.J., Sherlock, J., Chen, Y., Murphy, C.A., Joyce, B., Seymour, B., Lucian, L., To, W., Kwan, S., Churakova, T., et al. (2003). Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744-748. https://doi.org/10.1038/nature01355
  15. Cui, G., Qin, X., Wu, L., Zhang, Y., Sheng, X., Yu, Q., Sheng, H., Xi, B., Zhang, J.Z., and Zang, Y.Q. (2011). Liver X receptor (LXR) mediates negative regulation of mouse and human Th17 differentiation. J. Clin. Invest. 121, 658-670. https://doi.org/10.1172/JCI42974
  16. De Nardo, D., Labzin, L.I., Kono, H., Seki, R., Schmidt, S.V., Beyer, M., Xu, D., Zimmer, S., Lahrmann, C., Schildberg, F.A., et al. (2014). High-density lipoprotein mediates anti-inflammatory reprogramming of macrophages via the transcriptional regulator ATF3. Nat. Immunol. 15, 152-160. https://doi.org/10.1038/ni.2784
  17. Diani, M., Altomare, G., and Reali, E. (2015). T cell responses in psoriasis and psoriatic arthritis. Autoimmun. Rev. 14, 286-292. https://doi.org/10.1016/j.autrev.2014.11.012
  18. Dickhout, J.G., Basseri, S., and Austin R.C. (2008). Macrophage function and its impact on atherosclerotic lesion composition, progression, and stability. Arterioscler. Thromb. Vasc. Biol. 28, 1413-1415. https://doi.org/10.1161/ATVBAHA.108.169144
  19. Duewell, P., Kono, H., Rayner, K.J., Sirois, C.M., Vladimer, G., Bauernfeind, F.G., Abela, G.S., Franchi, L., Nunez, G., Schnurr, M., et al. (2010). NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361. https://doi.org/10.1038/nature08938
  20. DuPage, M. and Bluestone, J.A. (2016). Harnessing the plasticity of CD4+ T cells to treat immune-mediated disease. Nat. Rev. Immunol. 16, 149. https://doi.org/10.1038/nri.2015.18
  21. Durante, A. and Bronzato, S. (2015). The increased cardiovascular risk in patients affected by autoimmune diseases: review of the various manifestations. J. Clin. Med. Res. 7, 379-384. https://doi.org/10.14740/jocmr2122w
  22. Finkelman, F.D., Holmes, J., Katona, I.M., Urban, J.F., Jr., Beckmann, M.P., Park, L.S., Schooley, K.A., Coffman, R.L., Mosmann, T.R., and Paul, W.E. (1990). Lymphokine control of in vivo immunoglobulin isotype selection. Annu. Rev. Immunol. 8, 303-333. https://doi.org/10.1146/annurev.iy.08.040190.001511
  23. Fitch, E., Harper, E., Skorcheva, I., Kurtz, S.E., and Blauvelt, A. (2007). Pathophysiology of psoriasis: recent advances on IL-23 and Th17 cytokines. Curr. Rheumatol. Rep. 9, 461-467. https://doi.org/10.1007/s11926-007-0075-1
  24. Gaddis, D.E., Padgett, L.E., Wu, R., McSkimming, C., Romines, V., Taylor, A.M., McNamara, C.A., Kronenberg, M., Crotty, S., Thomas, M.J., et al. (2018). Apolipoprotein AI prevents regulatory to follicular helper T cell switching during atherosclerosis. Nat. Commun. 9, 1095. https://doi.org/10.1038/s41467-018-03493-5
  25. Ghazizadeh, R., Tosa, M., and Ghazizadeh, M. (2011). Clinical improvement in psoriasis with treatment of associated hyperlipidemia. Am. J. Med. Sci. 341, 394-398. https://doi.org/10.1097/MAJ.0b013e3181ff8eeb
  26. Gong, Y., Tong, J., and Wang, S. (2017). Are follicular regulatory T cells involved in autoimmune diseases? Front. Immunol. 8, 1790. https://doi.org/10.3389/fimmu.2017.01790
  27. Goodson, N., Marks, J., Lunt, M., and Symmons, D. (2005). Cardiovascular admissions and mortality in an inception cohort of patients with rheumatoid arthritis with onset in the 1980s and 1990s. Ann. Rheum. Dis. 64, 1595-1601. https://doi.org/10.1136/ard.2004.034777
  28. Heine, G., Dahten, A., Hilt, K., Ernst, D., Milovanovic, M., Hartmann, B., and Worm, M. (2009). Liver X receptors control IgE expression in B cells. J. Immunol. 182, 5276-5282. https://doi.org/10.4049/jimmunol.0801804
  29. Hsu, H.C., Yang, P., Wang, J., Wu, Q., Myers, R., Chen, J., Yi, J., Guentert, T., Tousson, A., Stanus, A.L., et al. (2008). Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. 9, 166-175. https://doi.org/10.1038/ni1552
  30. Hu, X., Wang, Y., Hao, L.Y., Liu, X., Lesch, C.A., Sanchez, B.M., Wendling, J.M., Morgan, R.W., Aicher, T.D., Carter, L.L., et al. (2015). Sterol metabolism controls TH17 differentiation by generating endogenous $ROR{\gamma}$ agonists. Nat. Chem. Biol. 11, 141-147. https://doi.org/10.1038/nchembio.1714
  31. Iacano, A.J., Lewis, H., Hazen, J.E., Andro, H., Smith, J.D., and Gulshan, K. (2019). Miltefosine increases macrophage cholesterol release and inhibits NLRP3-inflammasome assembly and IL-$1{\beta}$ release. Sci. Rep. 9, 11128. https://doi.org/10.1038/s41598-019-47610-w
  32. Ito, A., Hong, C., Oka, K., Salazar, J.V., Diehl, C., Witztum, J.L., Diaz, M., Castrillo, A., Bensinger, S.J., Chan, L., et al. (2016). Cholesterol accumulation in CD11c+ immune cells is a causal and targetable factor in autoimmune disease. Immunity 45, 1311-1326. https://doi.org/10.1016/j.immuni.2016.11.008
  33. Jeon, J.Y., Nam, J.Y., Kim, H.A., Park, Y.B., Bae, S.C., and Suh, C.H. (2014). Liver X receptors alpha gene (NR1H3) promoter polymorphisms are associated with systemic lupus erythematosus in Koreans. Arthritis Res. Ther. 16, R112. https://doi.org/10.1186/ar4563
  34. Joseph, S.B., Castrillo, A., Laffitte, B.A., Mangelsdorf, D.J., and Tontonoz, P. (2003). Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat. Med. 9, 213. https://doi.org/10.1038/nm820
  35. Kiss, M., Czimmerer, Z., and Nagy, L. (2013). The role of lipid-activated nuclear receptors in shaping macrophage and dendritic cell function: from physiology to pathology. J. Allergy Clin. Immunol. 132, 264-286. https://doi.org/10.1016/j.jaci.2013.05.044
  36. Lancaster, G.I., Langley, K.G., Berglund, N.A., Kammoun, H.L., Reibe, S., Estevez, E., Weir, J., Mellett, N.A., Pernes, G., Conway, J.R.W., et al. (2018). Evidence that TLR4 is not a receptor for saturated fatty acids but mediates lipid-induced inflammation by reprogramming macrophage metabolism. Cell Metab. 27, 1096-1110.e5. https://doi.org/10.1016/j.cmet.2018.03.014
  37. Lee, K.H., Lee, C.H., Woo, J., Jeong, J., Jang, A.H., and Yoo, C.G. (2018). Cigarette smoke extract enhances IL-17A-induced IL-8 production via upregulation of IL-17R in human bronchial epithelial cells. Mol. Cells 41, 282-289. https://doi.org/10.14348/molcells.2018.2123
  38. Lerner, A., Jeremias, P., and Matthias, T. (2015). The world incidence and prevalence of autoimmune diseases is increasing. Int. J. Celiac Dis. 3, 151-155.
  39. Li, J., Lu, E., Yi, T., and Cyster, J.G. (2016). EBI2 augments Tfh cell fate by promoting interaction with IL-2-quenching dendritic cells. Nature 533, 110-114. https://doi.org/10.1038/nature17947
  40. Lim, H., Kim, Y.U., Sun, H., Lee, J.H., Reynolds, J.M., Hanabuchi, S., Wu, H., Teng, B.B., and Chung, Y. (2014). Proatherogenic conditions promote autoimmune T helper 17 cell responses in vivo. Immunity 40, 153-165. https://doi.org/10.1016/j.immuni.2013.11.021
  41. Liu, X., Chen, X., Zhong, B., Wang, A., Wang, X., Chu, F., Nurieva, R.I., Yan, X., Chen, P., van der Flier, L.G., et al. (2014). Transcription factor achaete-scute homologue 2 initiates follicular T-helper-cell development. Nature 507, 513. https://doi.org/10.1038/nature12910
  42. Mitsdoerffer, M., Lee, Y., Jäger, A., Kim, H.J., Korn, T., Kolls, J.K., Cantor, H., Bettelli, E., and Kuchroo, V.K. (2010). Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc. Nat. Acad. Sci. U. S. A. 107, 14292. https://doi.org/10.1073/pnas.1009234107
  43. Mountz, J.D., Yang, P., Wu, Q., Zhou, J., Tousson, A., Fitzgerald, A., Allen, J., Wang, X., Cartner, S., Grizzle, W.E., et al. (2005). Genetic segregation of spontaneous erosive arthritis and generalized autoimmune disease in the BXD2 recombinant inbred strain of mice. Scand. J. Immunol. 61, 128-138. https://doi.org/10.1111/j.0300-9475.2005.01548.x
  44. Nickel, T., Schmauss, D., Hanssen, H., Sicic, Z., Krebs, B., Jankl, S., Summo, C., Fraunberger, P., Walli, A.K., Pfeiler, S., et al. (2009). oxLDL uptake by dendritic cells induces upregulation of scavenger-receptors, maturation and differentiation. Atherosclerosis 205, 442-450. https://doi.org/10.1016/j.atherosclerosis.2009.01.002
  45. Nistala, K., Moncrieffe, H., Newton, K.R., Varsani, H., Hunter, P., and Wedderburn, L.R. (2008). Interleukin-17-producing T cells are enriched in the joints of children with arthritis, but have a reciprocal relationship to regulatory T cell numbers. Arthritis Rheum. 58, 875-887. https://doi.org/10.1002/art.23291
  46. Nurieva, R.I., Chung, Y., Hwang, D., Yang, X.O., Kang, H.S., Ma, L., Wang, Y.H., Watowich, S.S., Jetten, A.M., Tian, Q., et al. (2008). Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29, 138-149. https://doi.org/10.1016/j.immuni.2008.05.009
  47. Nus, M., Sage, A.P., Lu, Y., Masters, L., Lam, B.Y.H., Newland, S., Weller, S., Tsiantoulas, D., Raffort, J., Marcus, D., et al. (2017). Marginal zone B cells control the response of follicular helper T cells to a high-cholesterol diet. Nat. Med. 23, 601. https://doi.org/10.1038/nm.4315
  48. Papp, K.A., Langley, R.G., Sigurgeirsson, B., Abe, M., Baker, D.R., Konno, P., Haemmerle, S., Thurston, H.J., Papavassilis, C., and Richards, H.B. (2013). Efficacy and safety of secukinumab in the treatment of moderate-tosevere plaque psoriasis: a randomized, double-blind, placebo-controlled phase II dose-ranging study. Br. J. Dermatol. 168, 412-421. https://doi.org/10.1111/bjd.12110
  49. Papp, K.A., Leonardi, C., Menter, A., Ortonne, J.P., Krueger, J.G., Kricorian, G., Aras, G., Li, J., Russell, C.B., Thompson, E.H.Z., et al. (2012). Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N. Engl. J. Med. 366, 1181-1189. https://doi.org/10.1056/NEJMoa1109017
  50. Pereira, J.P., Kelly, L.M., Xu, Y., and Cyster, J.G. (2009). EBI2 mediates B cell segregation between the outer and centre follicle. Nature 460, 1122. https://doi.org/10.1038/nature08226
  51. Pesce, B., Soto, L., Sabugo, F., Wurmann, P., Cuchacovich, M., Lopez, M.N., Sotelo, P.H., Molina, M.C., Aguillon, J.C., and Catalan, D. (2013). Effect of interleukin-6 receptor blockade on the balance between regulatory T cells and T helper type 17 cells in rheumatoid arthritis patients. Clin. Exp. Immunol. 171, 237-242. https://doi.org/10.1111/cei.12017
  52. Pourcet, B., Gage, M.C., Leon, T.E., Waddington, K.E., Pello, O.M., Steffensen, K.R., Castrillo, A., Valledor, A.F., and Pineda-Torra, I. (2016). The nuclear receptor LXR modulates interleukin-18 levels in macrophages through multiple mechanisms. Sci. Rep. 6, 25481. https://doi.org/10.1038/srep25481
  53. Reinhardt, R.L., Liang, H.E., and Locksley, R.M. (2009). Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 10, 385-393. https://doi.org/10.1038/ni.1715
  54. Reynolds, C.M., McGillicuddy, F.C., Harford, K.A., Finucane, O.M., Mills, K.H.G., and Roche, H.M. (2012). Dietary saturated fatty acids prime the NLRP3 inflammasome via TLR4 in dendritic cells-implications for dietinduced insulin resistance. Mol. Nutr. Food Res. 56, 1212-1222. https://doi.org/10.1002/mnfr.201200058
  55. Roman, M.J., Shanker, B.A., Davis, A., Lockshin, M.D., Sammaritano, L., Simantov, R., Crow, M.K., Schwartz, J.E., Paget, S.A., Devereux, R.B., et al. (2003). Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N. Engl. J. Med. 349, 2399-2406. https://doi.org/10.1056/NEJMoa035471
  56. Ryu, H., Lim, H., Choi, G., Park, Y.J., Cho, M., Na, H., Ahn, C.W., Kim, Y.C., Kim, W.U., Lee, S.H., et al. (2018). Atherogenic dyslipidemia promotes autoimmune follicular helper T cell responses via IL-27. Nat. Immunol. 19, 583-593. https://doi.org/10.1038/s41590-018-0102-6
  57. Santori, F.R., Huang, P., van de Pavert, S.A., Douglass, E.F., Jr., Leaver, D.J., Haubrich, B.A., Keber, R., Lorbek, G., Konijn, T., Rosales, B.N., et al. (2015). Identification of natural $ROR{\gamma}$ ligands that regulate the development of lymphoid cells. Cell Metab. 21, 286-298. https://doi.org/10.1016/j.cmet.2015.01.004
  58. Smith, J.P., Burton, G.F., Tew, J.G., and Szakal, A.K. (1998). Tingible body macrophages in regulation of germinal center reactions. Dev. Immunol. 6, 285-294. https://doi.org/10.1155/1998/38923
  59. Soroosh, P., Wu, J., Xue, X., Song, J., Sutton, S.W., Sablad, M., Yu, J., Nelen, M.I., Liu, X., Castro, G., et al. (2014). Oxysterols are agonist ligands of $ROR{\gamma}t$ and drive Th17 cell differentiation. Proc. Nat. Acad. Sci. U. S. A. 111, 12163. https://doi.org/10.1073/pnas.1322807111
  60. Stelzner, K., Herbert, D., Popkova, Y., Lorz, A., Schiller, J., Gericke, M., Kloting, N., Blüher, M., Franz, S., Simon, J.C., et al. (2016). Free fatty acids sensitize dendritic cells to amplify TH1/TH17-immune responses. Eur. J. Immunol. 46, 2043-2053. https://doi.org/10.1002/eji.201546263
  61. Taghavie-Moghadam, P.L., Waseem, T.C., Hattler, J., Glenn, L.M., Dobrian, A.D., Kaplan, M.H., Yang, Y., Nurieva, R., Nadler, J.L., and Galkina, E.V. (2017). STAT4 regulates the CD8+ regulatory T cell/T follicular helper cell axis and promotes atherogenesis in insulin-resistant Ldlr-/- Mice. J. Immunol. 199, 3453-3465. https://doi.org/10.4049/jimmunol.1601429
  62. Tangye, S.G., Ma, C.S., Brink, R., and Deenick, E.K. (2013). The good, the bad and the ugly - TFH cells in human health and disease. Nat. Rev. Immunol. 13, 412. https://doi.org/10.1038/nri3447
  63. Thomas, D.G., Doran, A.C., Fotakis, P., Westerterp, M., Antonson, P., Jiang, H., Jiang, X.C., Gustafsson, J.A., Tabas, I., and Tall, A.R. (2018). LXR suppresses inflammatory gene expression and neutrophil migration through cis-repression and cholesterol efflux. Cell Rep. 25, 3774-3785.e4. https://doi.org/10.1016/j.celrep.2018.11.100
  64. Tsilingiri, K., de la Fuente, H., Relano, M., Sanchez-Diaz, R., Rodriguez, C., Crespo, J., Sanchez-Cabo, F., Dopazo, A., Alonso-Lebrero Jose, L., Vara, A., et al. (2019). Oxidized low-density lipoprotein receptor in lymphocytes prevents atherosclerosis and predicts subclinical disease. Circulation 139, 243-255. https://doi.org/10.1161/CIRCULATIONAHA.118.034326
  65. Varshney, P., Narasimhan, A., Mittal, S., Malik, G., Sardana, K., and Saini, N. (2016). Transcriptome profiling unveils the role of cholesterol in IL-17A signaling in psoriasis. Sci. Rep. 6, 19295. https://doi.org/10.1038/srep19295
  66. Volpe, E., Battistini, L., and Borsellino, G. (2015). Advances in T helper 17 cell biology: pathogenic role and potential therapy in multiple sclerosis. Mediators Inflamm. 2015, 475158.
  67. Westerterp, M., Gautier, E.L., Ganda, A., Molusky, M.M., Wang, W., Fotakis, P., Wang, N., Randolph, G.J., D'Agati, V.D., Yvan-Charvet, L., et al. (2017). Cholesterol accumulation in dendritic cells links the inflammasome to acquired immunity. Cell Metab. 25, 1294-1304.e6. https://doi.org/10.1016/j.cmet.2017.04.005
  68. Wilson, C.S., Elizer, S.K., Marshall, A.F., Stocks, B.T., and Moore, D.J. (2016). Regulation of B lymphocyte responses to Toll-like receptor ligand binding during diabetes prevention in non-obese diabetic (NOD) mice. J. Diabetes 8, 120-131. https://doi.org/10.1111/1753-0407.12263
  69. Xu, J., Wagoner, G., Douglas, J.C., and Drew, P.D. (2009). Liver X receptor agonist regulation of Th17 lymphocyte function in autoimmunity. J. Leukoc. Biol. 86, 401-409. https://doi.org/10.1189/jlb.1008600
  70. Youssef, S., Stuve, O., Patarroyo, J.C., Ruiz, P.J., Radosevich, J.L., Hur, E.M., Bravo, M., Mitchell, D.J., Sobel, R.A., Steinman, L., et al. (2002). The HMGCoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature 420, 78-84. https://doi.org/10.1038/nature01158
  71. Yu, H.H., Chen, P.C., Yang, Y.H., Wang, L.C., Lee, J.H., Lin, Y.T., and Chiang, B.L. (2015). Statin reduces mortality and morbidity in systemic lupus erythematosus patients with hyperlipidemia: A nationwide populationbased cohort study. Atherosclerosis 243, 11-18. https://doi.org/10.1016/j.atherosclerosis.2015.08.030
  72. Yuan, J., Li, L.I., Wang, Z., Song, W., and Zhang, Z. (2016). Dyslipidemia in patients with systemic lupus erythematosus: Association with disease activity and B-type natriuretic peptide levels. Biomed. Rep. 4, 68-72. https://doi.org/10.3892/br.2015.544
  73. Zhang, M., Yu, G., Chan, B., Pearson, J.T., Rathanaswami, P., Delaney, J., Ching Lim, A., Babcook, J., Hsu, H., and Gavin, M.A. (2015). Interleukin-21 receptor blockade inhibits secondary humoral responses and halts the progression of preestablished disease in the (NZB $\times$ NZW)F1 systemic lupus erythematosus model. Arthritis Rheumatol. 67, 2723-2731. https://doi.org/10.1002/art.39233

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  4. The Effect of a Persian Herbal Medicine Compound on the Lipid Profiles of Patients with Dyslipidemia: A Randomized Double-Blind Placebo-Controlled Clinical Trial vol.2021, 2019, https://doi.org/10.1155/2021/6631963
  5. Clinical Characteristics of Lipid Metabolism in Untreated Patients with Anti-MDA5 Antibody-Positive vol.14, 2019, https://doi.org/10.2147/ijgm.s315885
  6. Association of the ENPP1/ENTPD1 Polymorphisms in Hemodialysis Patients vol.14, 2021, https://doi.org/10.2147/ijgm.s332911
  7. Inhibition of phospholipases suppresses progression of psoriasis through modulation of inflammation vol.246, pp.11, 2019, https://doi.org/10.1177/1535370221993424
  8. Dexamethasone reduces autoantibody levels in MRL/lpr mice by inhibiting Tfh cell responses vol.25, pp.17, 2021, https://doi.org/10.1111/jcmm.16785
  9. The role of high‐density lipoprotein in the regulation of the immune response: implications for atherosclerosis and autoimmunity vol.164, pp.2, 2019, https://doi.org/10.1111/imm.13348