Mitochondria as a key player in systemic lupus erythematosus

References

• Kaul A, Gordon C, Crow MK, et al. Systemic lupus erythematosus. Nat Rev Di Prim. 2016;2:1–21.
   Web of Science ®Google Scholar
• Goulielmos GN, Zervou MI, Vazgiourakis VM, et al. The genetics and molecular pathogenesis of systemic lupus erythematosus (SLE) in populations of different ancestry. Gene. 2018;668:59–72.
   PubMed Web of Science ®Google Scholar
• Hurtado C, Acevedo Sáenz LY, Vásquez Trespalacios EM, et al. DNA methylation changes on immune cells in systemic lupus erythematosus. Autoimmunity. 2020;53(3):114–121.
   PubMed Web of Science ®Google Scholar
• Long H, Yin H, Wang L, et al. The critical role of epigenetics in systemic lupus erythematosus and autoimmunity. J Autoimmun. 2016;74:118–138.
   PubMed Web of Science ®Google Scholar
• Parks CG, Espindola Santos A, Barbhaiya M, et al. Understanding the role of environmental factors in the development of systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 2017;31(3):306–320.
   PubMed Web of Science ®Google Scholar
• Christou EAA, Banos A, Kosmara D, et al. Sexual dimorphism in SLE: above and beyond sex hormones. Lupus. 2019;28(1):3–10.
   PubMed Web of Science ®Google Scholar
• Honarpisheh M, Köhler P, Rauchhaupt E, et al. The involvement of microRNAs in modulation of innate and adaptive immunity in systemic lupus erythematosus and lupus nephritis. J Immunol Res. 2018;2018:4126106–4126115.
   PubMed Web of Science ®Google Scholar
• Assad S, Khan HH, Ghazanfar H, et al. Role of sex hormone levels and psychological stress in the pathogenesis of autoimmune diseases. Cureus. 2017;9(6):e1315.
   PubMed Web of Science ®Google Scholar
• Wincup C, Radziszewska A. Abnormal mitochondrial physiology in the pathogenesis of systemic lupus erythematosus. Rheum Dis Clin North Am. 2021;47(3):427–439.
   PubMed Web of Science ®Google Scholar
• Javinani A, Ashraf-Ganjouei A, Aslani S, et al. Exploring the etiopathogenesis of systemic lupus erythematosus: a genetic perspective. Immunogenetics. 2019;71(4):283–297.
   PubMed Web of Science ®Google Scholar
• Tsokos GC. Autoimmunity and organ damage in systemic lupus erythematosus. Nat Immunol. 2020;21(6):605–614.
   PubMed Web of Science ®Google Scholar
• Labbé K, Murley A, Nunnari J. Determinants and functions of mitochondrial behavior. Annu Rev Cell Dev Biol. 2014;30:357–391.
   PubMed Web of Science ®Google Scholar
• Osellame LD, Blacker TS, Duchen MR. ç Cellular and molecular mechanisms of mitochondrial function. Best Pract Res Clin Endocrinol Metab. 2012;26(6):711–723.
   PubMed Web of Science ®Google Scholar
• Chaban Y, Boekema EJ, Dudkina NV. Structures of mitochondrial oxidative phosphorylation supercomplexes and mechanisms for their stabilisation. Biochim Biophys Acta. 2014;1837(4):418–426.
   PubMed Web of Science ®Google Scholar
• Sinha K, Das J, Bikash Pal P, et al. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol. 2013;87(7):1157–1180.
   PubMed Web of Science ®Google Scholar
• West A, Shadel GS. Mitochondrial DNA in innate immune responses and inflammatory pathology. Nat Rev Immunol. 2017;17(6):363–375.
   PubMed Web of Science ®Google Scholar
• Lee HT, Lin CS, Lee CS, et al. Increased 8-hydroxy-2’-deoxyguanosine in plasma and decreased mRNA expression of human 8-oxoguanine DNA glycosylase 1, anti-oxidant enzymes, mitochondrial biogenesis-related proteins and glycolytic enzymes in leucocytes in patients with systemic lupus erythematosus. Clin Exp Immunol. 2014;176(1):66–77.
   PubMed Web of Science ®Google Scholar
• Zamponi N, Zamponi E, Cannas SA, et al. Mitochondrial network complexity emerges from fission/fusion dynamics. Sci Rep. 2018;8(1):1–10.
   PubMedGoogle Scholar
• Rambold AS, Pearce e Mitochondrial dynamics at the interface of immune cell metabolism and function. Trends Immunol. 2018;39(1):6–18.
   PubMed Web of Science ®Google Scholar
• Yang F, He Y, Zhai Z, et al. Programmed cell death pathways in the pathogenesis of systemic lupus erythematosus. J Immunol Res. 2019;2019:3638562.
   PubMed Web of Science ®Google Scholar
• Mutua V, Gershwin LJ. A review of neutrophil extracellular traps (NETs) in disease: potential anti-NETs therapeutics. Clin Rev Allergy Immunol. 2021;61(2):194–211.
   PubMed Web of Science ®Google Scholar
• Ma K, Chen G, Li W, et al. Mitophagy, mitochondrial homeostasis, and cell fate. Front Cell Dev. Biol. 2020;8:1–14.
   PubMed Web of Science ®Google Scholar
• Jacobs SR, Herman CE, MacIver NJ, et al. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J Immunol. 2008;180(7):4476–4486.
   PubMed Web of Science ®Google Scholar
• Yin Y, Choi SC, Xu Z, et al. Normalization of CD4+ T cell metabolism reverses lupus. Sci. Transl. Med. 2015;7(274):1–13.
   Web of Science ®Google Scholar
• Faas MM, de Vos P. Mitochondrial function in immune cells in health and disease. Biochim Biophys Acta Mol Basis Dis. 2020;1866(10):165845.
   PubMed Web of Science ®Google Scholar
• Yang J, Yang X, Zou H, et al. Oxidative stress and Treg and Th17 dysfunction in systemic lupus erythematosus. Oxid Med Cell Longev. 2016;2016:2526174.
   PubMed Web of Science ®Google Scholar
• Lu Z, Tian Y, Bai Z, et al. Increased oxidative stress contributes to impaired peripheral CD56(dim)CD57(+) NK cells from patients with systemic lupus erythematosus. Arthritis Res Ther. 2022;24(1):48.
   PubMed Web of Science ®Google Scholar
• Li KJ, Wu CH, Hsieh SC, et al. Deranged bioenergetics and defective redox capacity in T lymphocytes and neutrophils are related to cellular dysfunction and increased oxidative stress in patients with active systemic lupus erythematosus. Clin Dev Immunol. 2012;2012:1–12.
   Google Scholar
• Pravda J. Systemic lupus erythematosus: pathogenesis at the functional limit of redox homeostasis. Oxid Med Cell Longev. 2019;2019:1–11.
   Web of Science ®Google Scholar
• Lee HT, Lin CS, Pan SC, et al. Alterations of oxygen consumption and extracellular acidification rates by glutamine in PBMCs of SLE patients. Mitochondrion. 2019;44:65–74.
   PubMed Web of Science ®Google Scholar
• Perl A, Hanczko R, Doherty E. Assessment of mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Methods Mol Biol. 2012;900:61–89.
   PubMedGoogle Scholar
• Ohl K, Tenbrock K. Oxidative stress in SLE T cells, is NRF2 really the target to treat? Front Immunol. 2021;12:633845.
   PubMed Web of Science ®Google Scholar
• Barati MT, Caster DJ. The potential of Nrf2 activation as a therapeutic target in systemic lupus erythematosus. Metabolites. 2022;12(2):151.
   PubMed Web of Science ®Google Scholar
• Zhao M, Chen H, Ding Q, et al. Nuclear factor erythroid 2-related factor 2 deficiency exacerbates lupus nephritis in B6/lpr mice by regulating Th17 cell function. Sci Rep. 2016;6:38619.
   PubMed Web of Science ®Google Scholar
• Jiang T, Tian F, Zheng H, et al. Nrf2 suppresses lupus nephritis through inhibition of oxidative injury and the NF-κB-mediated inflammatory response. Kidney Int. 2014;85(2):333–343.
   PubMed Web of Science ®Google Scholar
• Han S, Zhuang H, Lee PY, et al. NF-E2–related factor 2 regulates interferon receptor expression and alters macrophage polarization in lupus. Arthritis Rheumatol. 2020;72(10):1707–1720.
   PubMed Web of Science ®Google Scholar
• Gergely PJ, Grossman C, Niland B, et al. Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus. Arthritis Rheum. 2002;46(1):175–190.
   PubMed Web of Science ®Google Scholar
• Leishangthem BD, Sharma A, Bhatnagar A. Role of altered mitochondria functions in the pathogenesis of systemic lupus erythematosus. Lupus. 2016;25(3):272–281.
   PubMed Web of Science ®Google Scholar
• Doherty E, Oaks Z, Perl A. Increased mitochondrial electron transport chain activity at complex i is regulated by N-acetylcysteine in lymphocytes of patients with systemic lupus erythematosus. Antioxid Redox Signal. 2014;21(1):56–65.
   PubMed Web of Science ®Google Scholar
• Zhang H, Fu R, Guo C, et al. Anti-dsDNA antibodies bind to TLR4 and activate NLRP3 inflammasome in lupus monocytes/macrophages. J Transl Med. 2016;14(1):1–12.
   PubMedGoogle Scholar
• Casciola-Rosen LA, Anhalt G, Rosen A. Autoantigens targeted in systemic lupus erythematmus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med. 1994;179(4):1317–1330.
   PubMed Web of Science ®Google Scholar
• Shruthi S, Thabah MM, Zachariah B, et al. Association of oxidative stress with disease activity and damage in systemic lupus erythematosus: a cross sectional study from a tertiary care centre in Southern India. Indian J Clin Biochem. 2021;36(2):185–193.
   PubMed Web of Science ®Google Scholar
• Caielli S, Athale S, Domic B, et al. Oxidized mitochondrial nucleoids released by neutrophils drive type I interferon production in human lupus. J Exp Med. 2016;213(5):697–713.
   PubMed Web of Science ®Google Scholar
• Alarcon F, McLaren Z, Wright HL. Neutrophils in the pathogenesis of rheumatoid arthritis and systemic lupus erythematosus: same foe different M.O. Front Immunol. 2021;12:649693.
   PubMed Web of Science ®Google Scholar
• Gehrke N, Mertens C, Zillinger T, et al. Oxidative damage of DNA confers resistance to cytosolic nuclease TREX1 degradation and potentiates STING-dependent immune sensing. Immunity. 2013;39(3):482–495.
   PubMed Web of Science ®Google Scholar
• McArthur K, Whitehead LW, Heddleston JM, et al. BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis. Science. 2018;359(6378):eaa6047.
   Web of Science ®Google Scholar
• Kim J, Gupta R, Blanco LP, et al. VDAC oligomers form mitochondrial pores to release mtDNA fragments and promote lupus-like disease. Science. 2019;366(6472):1531–1536.
   PubMed Web of Science ®Google Scholar
• Yan J, Liu W, Feng F, et al. VDAC oligomer pores: a mechanism in disease triggered by mtDNA release. Cell Biol Int. 2020;44(11):2178–2181.
   PubMed Web of Science ®Google Scholar
• Varughese JT, Buchanan SK, Pitt AS. The role of voltage-dependent anion channel in mitochondrial dysfunction and human disease. Cells. 2021;10(7):1737.
   PubMed Web of Science ®Google Scholar
• Buskiewicz IA, Montgomery T, Yasewicz EC, et al. Reactive oxygen species induce virus-independent MAVS oligomerization in systemic lupus erythematosus. Sci Signal. 2016;9(456):ra115.
   PubMed Web of Science ®Google Scholar
• Wang G, Pierangeli SS, Papalardo E, et al. Markers of oxidative and nitrosative stress in systemic lupus erythematosus: correlation with disease activity. Arthritis Rheum. 2010;62:NA–2072.
   Google Scholar
• Scavuzzi BM, Simão AN, Veiga TM, et al. Increased lipid and protein oxidation and lowered anti-oxidant defenses in systemic lupus erythematosus are associated with severity of illness, autoimmunity, increased adhesion molecules, and Th1 and Th17 immune shift. Immunol Res. 2018;66(1):158–171.
   PubMed Web of Science ®Google Scholar
• Toyoda K, Nagae R, Akagawa M, et al. Protein-bound 4-hydroxy-2-nonenal: an endogenous triggering antigen of anti-DNA response. J Biol Chem. 2007;282(35):25769–25778.
   PubMed Web of Science ®Google Scholar
• Iriyoda TM, Stadtlober VN, Lozovoy MAB, et al. Reduction of nitric oxide and DNA/RNA oxidation products are associated with active disease in systemic lupus erythematosus patients. Lupus. 2017;26(10):1106–1111.
   PubMed Web of Science ®Google Scholar
• Wincup C, Sawford N, Rahman A. Pathological mechanisms of abnormal iron metabolism and mitochondrial dysfunction in systemic lupus erythematosus. Expert Rev Clin Immunol. 2021;17(9):957–967.
   PubMed Web of Science ®Google Scholar
• Chen QC, Wang J, Xiang M, et al. The potential role of ferroptosis in systemic lupus erythematosus. Front Immunol. 2022;13:1–7.
   Web of Science ®Google Scholar
• Li P, Jiang M, Li K, et al. Glutathione peroxidase 4–regulated neutrophil ferroptosis induces systemic autoimmunity. Nat Immunol. 2021;22(9):1107–1117.
   PubMed Web of Science ®Google Scholar
• Gao X, Song Y, Lu S, et al. Insufficient iron improves pristane-induced lupus by promoting treg cell expansion. Front Immunol. 2022;13:1–10.
   Web of Science ®Google Scholar
• Hu C, Zhang J, Hong S, et al. Oxidative stress-induced aberrant lipid metabolism is an important causal factor for dysfunction of immunocytes from patients with systemic lupus erythematosus. Free Radic Biol Med. 2021;163:210–219.
   PubMed Web of Science ®Google Scholar
• Lood C, Blanco LP, Purmalek MM, et al. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat Med. 2016;22(2):146–153.
   PubMed Web of Science ®Google Scholar
• Julian MW, Shao G, VanGundy ZC, et al. Mitochondrial transcription factor A, an endogenous danger signal, promotes TNFα release via RAGE- and TLR9-Responsive plasmacytoid dendritic cells. PLoS One. 2013;8(8):e72354–16.
   PubMed Web of Science ®Google Scholar
• Zhou Z, Yazdi AS, Menu P, et al. A role for mitochondria in NLRP3 inflammasome activation. Nature. 2011;469(7329):221–226.
   PubMed Web of Science ®Google Scholar
• Chen L, Duvvuri B, Grigull J, et al. Experimental evidence that mutated-self peptides derived from mitochondrial DNA somatic mutations have the potential to trigger autoimmunity. Hum Immunol. 2014;75(8):873–879.
   PubMed Web of Science ®Google Scholar
• Ivanova VV, Khaiboullina SF, Cherenkova EE, et al. Differential immuno-reactivity to genomic DNA, RNA and mitochondrial DNA is associated with auto-immunity. Cell Physiol Biochem. 2014;34(6):2200–2208.
   PubMedGoogle Scholar
• Becker Y, Loignon RC, Julien AS, et al. Anti-mitochondrial autoantibodies in systemic lupus erythematosus and their association with disease manifestations. Sci Rep. 2019;9(1):4530.
   PubMedGoogle Scholar
• Becker Y, Marcoux G, Allaeys I, et al. Autoantibodies in systemic lupus erythematosus target mitochondrial RNA. Front Immunol. 2019;10:1026.
   PubMed Web of Science ®Google Scholar
• Mobarrez F, Fuzzi E, Gunnarsson I, et al. Microparticles in the blood of patients with SLE: Size, content of mitochondria and role in circulating immune complexes. J Autoimmun. 2019;102:142–149.
   PubMed Web of Science ®Google Scholar
• Pisetsky DS, Spencer DM, Mobarrez F, et al. The binding of SLE autoantibodies to mitochondria. Clin Immunol. 2020;212:108349.
   PubMed Web of Science ®Google Scholar
• Melki I, Allaeys I, Tessandier N, et al. Platelets release mitochondrial antigens in systemic lupus erythematosus. Sci Transl Med. 2021;13(581):eaav5928.
   PubMed Web of Science ®Google Scholar
• Lee HT, Lin CS, Chen WS, et al. Leukocyte mitochondrial DNA alteration in systemic lupus erythematosus and its relevance to the susceptibility to lupus nephritis. Int J Mol Sci. 2012;13(7):8853–8868.
   PubMed Web of Science ®Google Scholar
• Lai R, Zhang X, Qiao K, et al. Identification of sequence polymorphisms in the mitochondrial deoxyribonucleic acid displacement-loop region as risk factors for systemic lupus erythematosus. Arch Rheumatol. 2020;36(3):375–380.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Lai R, Peng C, et al. Risk related single nucleotide polymorphisms in mitochondrial D-loops promotes the levels of reactive oxygen species in systemic lupus erythematosus. Int J Clin Exp Med. 2021;14:2636–2640.
   Web of Science ®Google Scholar
• Yu X, Wieczorek S, Franke A, et al. Association of UCP2 - 866 G/a polymorphism with chronic inflammatory diseases. Genes Immun. 2009;10(6):601–605.
   PubMed Web of Science ®Google Scholar
• Vyshkina T, Sylvester A, Sadiq S, et al. Association of common mitochondrial DNA variants with multiple sclerosis and systemic lupus erythematosus. Clin Immunol. 2008;129(1):31–35.
   PubMed Web of Science ®Google Scholar
• Tang Y, Wang L, Zhu M, et al. Association of mtDNA M/N haplogroups with systemic lupus erythematosus: a case-control study of Han Chinese women. Sci Rep. 2015;5:10817–10816.
   PubMed Web of Science ®Google Scholar
• Caza TN, Fernandez DR, Talaber G, et al. HRES-1/Rab4-mediated depletion of Drp1 impairs mitochondrial homeostasis and represents a target for treatment in SLE. Ann Rheum Dis. 2014;73(10):1888–1897.
   PubMed Web of Science ®Google Scholar
• Nagy G, Barcza M, Gonchoroff N, et al. Nitric oxide-dependent mitochondrial biogenesis generates Ca2+ signaling profile of lupus T cells. J Immunol. 2004;173(6):3676–3683.
   PubMed Web of Science ®Google Scholar
• Bengtsson AA, Gullstrand B, Truedsson L, et al. SLE serum induces classical caspase-dependent apoptosis independent of death receptors. Clin Immunol. 2008;126(1):57–66.
   PubMed Web of Science ®Google Scholar
• Su YJ, Cheng TT, Chen CJ, et al. Investigation of the caspase-dependent mitochondrial apoptotic pathway in mononuclear cells of patients with systemic lupus erythematosus. J Transl Med. 2014;12:303.
   PubMed Web of Science ®Google Scholar
• Li X, Liu L, Meng D, et al. Enhanced apoptosis and senescence of bone-marrow-derived mesenchymal stem cells in patients with systemic lupus erythematosus. Stem Cells Dev. 2012;21(13):2387–2394.
   PubMed Web of Science ®Google Scholar
• Nicotera P, Leist M, Ferrando-May E. Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol Lett. 1998;102-103:139–142.
   PubMed Web of Science ®Google Scholar
• Pruchniak MP, Ostafin M, Wachowska M, et al. Neutrophil extracellular traps generation and degradation in patients with granulomatosis with polyangiitis and systemic lupus erythematosus. Autoimmunity. 2019;52(3):126–135.
   PubMed Web of Science ®Google Scholar
• Lee KH, Kronbichler A, Park DD, et al. Neutrophil extracellular traps (NETs) in autoimmune diseases: a comprehensive review. Autoimmun Rev. 2017;16(11):1160–1173.
   PubMed Web of Science ®Google Scholar
• Muller S, Radic M. Oxidation and mitochondrial origin of NET DNA in the pathogenesis of lupus. Nat Med. 2016;22(2):126–127.
   PubMed Web of Science ®Google Scholar
• Linge P, Arve S, Olsson LM, et al. NCF1-339 polymorphism is associated with altered formation of neutrophil extracellular traps, high serum interferon activity and antiphospholipid syndrome in systemic lupus erythematosus. Ann Rheum Dis. 2020;79(2):254–261.
   PubMed Web of Science ®Google Scholar
• Liu G, Sabatini DM. mTOR at the nexus of nutrition, growth, ageing and disease. Nat Rev Mol Cell Biol. 2020;21(4):183–203.
   PubMed Web of Science ®Google Scholar
• Perl A. Systems biology of lupus: Mapping the impact of genomic and environmental factors on gene expression signatures, cellular signaling, metabolic pathways, hormonal and cytokine imbalance, and selecting targets for treatment. Autoimmunity. 2010;43(1):32–47.
   PubMed Web of Science ®Google Scholar
• Fernandez DR, Telarico T, Bonilla E, et al. Activation of mammalian target of rapamycin controls the loss of TCRζ in lupus T cells through HRES-1/Rab4-regulated lysosomal degradation. J Immunol. 2009;182(4):2063–2073.
   PubMed Web of Science ®Google Scholar
• Gkirtzimanaki K, Kabrani E, Nikoleri D, et al. IFNα impairs autophagic degradation of mtDNA promoting autoreactivity of SLE monocytes in a STING-dependent fashion. Cell Rep. 2018;25(4):921–933.e5.
   PubMed Web of Science ®Google Scholar
• Morel L. Erythrocyte-derived mitochondria: an unexpected interferon inducer in lupus. Trends Immunol. 2021;42(12):1054–1056.
   PubMed Web of Science ®Google Scholar
• Caielli S, Cardenas J, de Jesus AA, et al. Erythroid mitochondrial retention triggers myeloid-dependent type I interferon in human SLE. Cell. 2021;184(17):4464–4479.e19.
   PubMed Web of Science ®Google Scholar
• Liao P, He Y, Yang F, et al. Polydatin effectively attenuates disease activity in lupus-prone mouse models by blocking ROS-mediated NET formation. Arthritis Res Ther. 2018;20(1):1–11.
   PubMedGoogle Scholar
• Fortner KA, Blanco LP, Buskiewicz I, et al. Targeting mitochondrial oxidative stress with MitoQ reduces NET formation and kidney disease in lupus-prone MRL- lpr mice. Lupus Sci Med. 2020;7(1):e000387corr1.
   PubMed Web of Science ®Google Scholar
• Blanco LP, Pedersen HL, Wang X, et al. Improved mitochondrial metabolism and reduced inflammation following attenuation of murine lupus with coenzyme Q10 analog idebenone. Arthritis Rheumatol. 2020;72(3):454–464.
   PubMed Web of Science ®Google Scholar
• Wang H, Li T, Chen S, et al. Extracellular trap mitochondrial DNA and its autoantibody in systemic lupus erythematosus and a proof-of-concept trial of metformin. Arthritis Rheumatol. 2015;67(12):3190–3200.
   PubMed Web of Science ®Google Scholar
• Ruiz-Limon P, Barbarroja N, Perez-Sanchez C, et al. Atherosclerosis and cardiovascular disease in systemic lupus erythematosus: effects of in vivo statin treatment. Ann Rheum Dis. 2015;74(7):1450–1458.
   PubMed Web of Science ®Google Scholar
• dos Santos M, Poletti PT, Favero G, et al. Protective effects of quercetin treatment in a pristane-induced mouse model of lupus nephritis. Autoimmunity. 2018;51(2):69–80.
   PubMed Web of Science ®Google Scholar
• Lai ZW, Kelly R, Winans T, et al. Sirolimus in patients with clinically active systemic lupus erythematosus resistant to, or intolerant of, conventional medications: a single-arm, open-label, phase 1/2 trial. Lancet. 2018;391(10126):1186–1196.
   PubMed Web of Science ®Google Scholar