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Review Articles

T-cell metabolism in rheumatoid arthritis: focus on mitochondrial and lysosomal dysfunction

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Pages 378-384 | Received 07 Jun 2023, Accepted 08 Mar 2024, Published online: 19 Mar 2024

References

  • Almutairi K, Nossent J, Preen D, et al. The global prevalence of rheumatoid arthritis: a meta-analysis based on a systematic review. Rheumatol Int. 2021;41(5):863–877. doi: 10.1007/s00296-020-04731-0.
  • Edilova MI, Akram A, Abdul-Sater AA. Innate immunity drives pathogenesis of rheumatoid arthritis. Biomed J. 2021;44(2):172–182. doi: 10.1016/j.bj.2020.06.010.[PMC]w
  • José Alcaraz M. New potential therapeutic approaches targeting synovial fibroblasts in rheumatoid arthritis. Biochem Pharmacol. 2021;194:114815. doi: 10.1016/j.bcp.2021.114815.
  • Deane KD, Demoruelle MK, Kelmenson LB, et al. Genetic and environmental risk factors for rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2017;31(1):3–18. doi: 10.1016/j.berh.2017.08.003.
  • Nemtsova MV, Zaletaev DV, Bure IV, et al. Epigenetic changes in the pathogenesis of rheumatoid arthritis. Front Genet. 2019;10:570. doi: 10.3389/fgene.2019.00570.
  • Firestein GS, McInnes IB. Immunopathogenesis of rheumatoid arthritis. Immunity. 2017;46(2):183–196. doi: 10.1016/j.immuni.2017.02.006.
  • Weyand CM, Goronzy JJ. Immunometabolism in early and late stages of rheumatoid arthritis. Nat Rev Rheumatol. 2017;13(5):291–301. doi: 10.1038/nrrheum.2017.49.
  • Yu H-C, Lu M-C. The roles of anti-citrullinated protein antibodies in the immunopathogenesis of rheumatoid arthritis. Ci ji yi Xue za Zhi = Tzu-Chi Med J. 2019;31:5–10.
  • Shuai Z, Zheng S, Wang K, et al. Reestablish immune tolerance in rheumatoid arthritis. Front Immunol. 2022;13:1012868. doi: 10.3389/fimmu.2022.1012868.
  • Imboden JB. The immunopathogenesis of rheumatoid arthritis. Annu Rev Pathol. 2009;4(1):417–434. doi: 10.1146/annurev.pathol.4.110807.092254.
  • Weyand CM, Wu B, Goronzy JJ. The metabolic signature of T cells in rheumatoid arthritis. Curr Opin Rheumatol. 2020;32(2):159–167. doi: 10.1097/BOR.0000000000000683.
  • Weyand CM, Yang Z, Goronzy JJ. T-cell aging in rheumatoid arthritis. Curr Opin Rheumatol. 2014;26(1):93–100. doi: 10.1097/BOR.0000000000000011.
  • Fujii H, Shao L, Colmegna I, et al. Telomerase insufficiency in rheumatoid arthritis. Proc Natl Acad Sci U S A. 2009;106(11):4360–4365. doi: 10.1073/pnas.0811332106.
  • Yang Z, Matteson EL, Goronzy JJ, et al. T-cell metabolism in autoimmune disease. Arthritis Res Ther. 2015;17(1):29. doi: 10.1186/s13075-015-0542-4.
  • Weyand CM, Zeisbrich M, Goronzy JJ. Metabolic signatures of T-cells and macrophages in rheumatoid arthritis. Curr Opin Immunol. 2017;46:112–120. doi: 10.1016/j.coi.2017.04.010.
  • Qiu J, Wu B, Goodman SB, et al. Metabolic control of autoimmunity and tissue inflammation in rheumatoid arthritis. Front Immunol. 2021;12:652771. doi: 10.3389/fimmu.2021.652771.
  • Weyand CM, Wu B, Huang T, et al. Mitochondria as disease-relevant organelles in rheumatoid arthritis. Clin Exp Immunol. 2023;211(3):208–223. doi: 10.1093/cei/uxac107.
  • Collison J. Faulty mitochondrial DNA repair promotes inflammation in RA. Nat Rev Rheumatol. 2019;15(10):576–576. doi: 10.1038/s41584-019-0303-x.
  • Clayton SA, MacDonald L, Kurowska-Stolarska M, et al. Mitochondria as key players in the pathogenesis and treatment of rheumatoid arthritis. Front Immunol. 2021;12:673916. doi: 10.3389/fimmu.2021.673916.
  • Cao M, Luo X, Wu K, et al. Targeting lysosomes in human disease: from basic research to clinical applications. Signal Transduct Target Ther. 2021;6:379.
  • Wen Z, Jin K, Shen Y, et al. N-myristoyltransferase deficiency impairs activation of kinase AMPK and promotes synovial tissue inflammation. Nat Immunol. 2019;20(3):313–325. doi: 10.1038/s41590-018-0296-7.
  • Frauwirth KA, Thompson CB. Regulation of T lymphocyte metabolism. J Immunol. 2004;172(8):4661–4665. doi: 10.4049/jimmunol.172.8.4661.
  • Kvacskay P, Yao N, Schnotz J-H, et al. Increase of aerobic glycolysis mediated by activated T helper cells drives synovial fibroblasts towards an inflammatory phenotype: new targets for therapy? Arthritis Res Ther. 2021;23(1):56. doi: 10.1186/s13075-021-02437-7.
  • Yang Z, Fujii H, Mohan SV, et al. Phosphofructokinase deficiency impairs ATP generation, autophagy, and redox balance in rheumatoid arthritis T cells. J Exp Med. 2013;210(10):2119–2134. doi: 10.1084/jem.20130252.
  • Telang S, Clem BF, Klarer AC, et al. Small molecule inhibition of 6-phosphofructo-2-kinase suppresses t cell activation. J Transl Med. 2012;10(1):95. doi: 10.1186/1479-5876-10-95.
  • Mor I, Cheung EC, Vousden KH. Control of glycolysis through regulation of PFK1: old friends and recent additions. Cold Spring Harb Symp Quant Biol. 2011;76(0):211–216. doi: 10.1101/sqb.2011.76.010868.
  • Yang Z, Shen Y, Oishi H, et al. Restoring oxidant signaling suppresses proarthritogenic T cell effector functions in rheumatoid arthritis. Sci Transl Med. 2016;8(331):331ra38. doi: 10.1126/scitranslmed.aad7151.
  • Howie D, Ten Bokum A, Necula AS, et al. The role of lipid metabolism in T lymphocyte differentiation and survival. Front Immunol. 2017;8:1949. doi: 10.3389/fimmu.2017.01949.
  • O'Sullivan D, van der Windt GJW, Huang SC-C, et al. Memory CD8(+) T cells use cell-intrinsic lipolysis to support the metabolic programming necessary for development. Immunity. 2014;41(1):75–88. doi: 10.1016/j.immuni.2014.06.005.
  • Pietrocola F, Galluzzi L, Bravo-San Pedro JM, et al. Acetyl coenzyme A: a Central metabolite and second messenger. Cell Metab. 2015;21(6):805–821. doi: 10.1016/j.cmet.2015.05.014.
  • Shen Y, Wen Z, Li Y, et al. Metabolic control of the scaffold protein TKS5 in tissue-invasive, proinflammatory T cells. Nat Immunol. 2017;18(9):1025–1034. doi: 10.1038/ni.3808.
  • Schnoor M, Stradal TE, Rottner K. Cortactin: cell functions of a multifaceted Actin-Binding protein. Trends Cell Biol. 2018;28(2):79–98. doi: 10.1016/j.tcb.2017.10.009.
  • Courtneidge SA. Cell migration and invasion in human disease: the tks adaptor proteins. Biochem Soc Trans. 2012;40(1):129–132. doi: 10.1042/BST20110685.
  • Sinenko SA, Starkova TY, Kuzmin AA, et al. Physiological signaling functions of reactive oxygen species in stem cells: from flies to man. Front Cell Dev Biol. 2021;9:714370. doi: 10.3389/fcell.2021.714370.
  • Gelderman KA, Hultqvist M, Pizzolla A, et al. Macrophages suppress T cell responses and arthritis development in mice by producing reactive oxygen species. J Clin Invest. 2007;117(10):3020–3028. doi: 10.1172/JCI31935.
  • Ma C, Wang J, Hong F, et al. Mitochondrial dysfunction in rheumatoid arthritis. Biomolecules. 2022;12(9):1216. doi: 10.3390/biom12091216.
  • Taanman JW. The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta. 1999;1410(2):103–123. doi: 10.1016/s0005-2728(98)00161-3.
  • Ali AT, Boehme L, Carbajosa G, et al. Nuclear genetic regulation of the human mitochondrial transcriptome. McCarthy MI, battle A, arking D, editors. Elife. 2019;8:e41927. doi: 10.7554/eLife.41927.
  • Greaves LC, Reeve AK, Taylor RW, et al. Mitochondrial DNA and disease. J Pathol. 2012;226(2):274–286. doi: 10.1002/path.3028.
  • Pérez-Treviño P, Velásquez M, García N. Mechanisms of mitochondrial DNA escape and its relationship with different metabolic diseases. Biochim Biophys Acta Mol Basis Dis. 2020;1866(6):165761. doi: 10.1016/j.bbadis.2020.165761.
  • Olzmann JA, Carvalho P. Dynamics and functions of lipid droplets. Nat Rev Mol Cell Biol. 2019;20(3):137–155. doi: 10.1038/s41580-018-0085-z.
  • Li Y, Shen Y, Jin K, et al. The DNA repair nuclease MRE11A functions as a mitochondrial protector and prevents T cell pyroptosis and tissue inflammation. Cell Metab. 2019;30(3):477–492.e6. doi: 10.1016/j.cmet.2019.06.016.
  • Lamarche BJ, Orazio NI, Weitzman MD. The MRN complex in double-strand break repair and telomere maintenance. FEBS Lett. 2010;584(17):3682–3695. doi: 10.1016/j.febslet.2010.07.029.
  • Oh J, Symington LS. Role of the Mre11 complex in preserving genome integrity. Genes (Basel). 2018;9(12):9. doi: 10.3390/genes9120589.
  • Weyand CM, Goronzy JJ. Immunometabolism in the development of rheumatoid arthritis. Immunol Rev. 2020;294(1):177–187. doi: 10.1111/imr.12838.
  • Li Y, Shen Y, Hohensinner P, et al. Deficient activity of the nuclease MRE11A induces T cell aging and promotes arthritogenic effector functions in patients with rheumatoid arthritis. Immunity. 2016;45(4):903–916. doi: 10.1016/j.immuni.2016.09.013.
  • Jin J, Zhang H, Weyand CM, et al. Lysosomes in T cell immunity and aging. Front Aging. 2021;2:809539. doi: 10.3389/fragi.2021.809539.
  • Nowosad A, Besson A. Lysosomes at the crossroads of cell metabolism, cell cycle, and stemness. Int J Mol Sci. 2022;23(4):23. doi: 10.3390/ijms23042290.
  • Lawrence RE, Zoncu R. The lysosome as a cellular Centre for signalling, metabolism and quality control. Nat Cell Biol. 2019;21(2):133–142. doi: 10.1038/s41556-018-0244-7.
  • Lamming DW, Bar-Peled L. Lysosome: the metabolic signaling hub. Traffic. 2019;20(1):27–38. doi: 10.1111/tra.12617.
  • Saxton RA, Sabatini DM. mTOR signaling in growth, metabolism, and disease. Cell. 2017;168(6):960–976. doi: 10.1016/j.cell.2017.02.004.
  • Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci. 2009;122(Pt 20):3589–3594. doi: 10.1242/jcs.051011.
  • Huang H, Long L, Zhou P, et al. mTOR signaling at the crossroads of environmental signals and T-cell fate decisions. Immunol Rev. 2020;295(1):15–38. doi: 10.1111/imr.12845.
  • Kim J, Guan K-L. mTOR as a Central hub of nutrient signalling and cell growth. Nat Cell Biol. 2019;21(1):63–71. doi: 10.1038/s41556-018-0205-1.
  • Garcia D, Shaw RJ. AMPK: mechanisms of cellular energy sensing and restoration of metabolic balance. Mol Cell. 2017;66(6):789–800. doi: 10.1016/j.molcel.2017.05.032.
  • Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 2011;25(18):1895–1908. doi: 10.1101/gad.17420111.
  • Yan H, Zhou H-F, Hu Y, et al. Suppression of experimental arthritis through AMP-activated protein kinase activation and autophagy modulation. J Rheum Dis Treat. 2015;1(1):5. doi: 10.23937/2469-5726/1510005.
  • Finlay DK. N-myristoylation of AMPK controls T cell inflammatory function. Nat Immunol. 2019;20(3):252–254. doi: 10.1038/s41590-019-0322-4.
  • Hipolito VEB, Ospina-Escobar E, Botelho RJ. Lysosome remodelling and adaptation during phagocyte activation. Cell Microbiol. 2018;20(4):e12824. doi: 10.1111/cmi.12824.

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