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Endocrine, Metabolic & Immune Disorders - Drug Targets

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ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

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Mini-Review Article

Autoimmune Responses and Therapeutic Interventions for Systemic Lupus Erythematosus: A Comprehensive Review

Author(s): Surya Prakash Pandey, Rakesh Bhaskar, Sung Soo Han* and Kannan Badri Narayanan*

Volume 24, Issue 5, 2024

Published on: 15 September, 2023

Page: [499 - 518] Pages: 20

DOI: 10.2174/1871530323666230915112642

Price: $65

Abstract

Systemic Lupus Erythematosus (SLE) or Lupus is a multifactorial autoimmune disease of multiorgan malfunctioning of extremely heterogeneous and unclear etiology that affects multiple organs and physiological systems. Some racial groups and women of childbearing age are more susceptible to SLE pathogenesis. Impressive progress has been made towards a better understanding of different immune components contributing to SLE pathogenesis. Recent investigations have uncovered the detailed mechanisms of inflammatory responses and organ damage. Various environmental factors, pathogens, and toxicants, including ultraviolet light, drugs, viral pathogens, gut microbiome metabolites, and sex hormones trigger the onset of SLE pathogenesis in genetically susceptible individuals and result in the disruption of immune homeostasis of cytokines, macrophages, T cells, and B cells. Diagnosis and clinical investigations of SLE remain challenging due to its clinical heterogeneity and hitherto only a few approved antimalarials, glucocorticoids, immunosuppressants, and some nonsteroidal anti-inflammatory drugs (NSAIDs) are available for treatment. However, the adverse effects of renal and neuropsychiatric lupus and late diagnosis make therapy challenging. Additionally, SLE is also linked to an increased risk of cardiovascular diseases due to inflammatory responses and the risk of infection from immunosuppressive treatment. Due to the diversity of symptoms and treatment-resistant diseases, SLE management remains a challenging issue. Nevertheless, the use of next-generation therapeutics with stem cell and gene therapy may bring better outcomes to SLE treatment in the future. This review highlights the autoimmune responses as well as potential therapeutic interventions for SLE particularly focusing on the recent therapeutic advancements and challenges.

Keywords: Lupus, autoantibodies, cytokine, immunosuppressants, pathogenesis, rheumatoid arthritis.

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[1]
Heimovski, F.E.; Simioni, J.A.; Skare, T.L. Systemic lupus erythematosus and Raynaud’s phenomenon. An. Bras. Dermatol., 2015, 90(6), 837-840.
[http://dx.doi.org/10.1590/abd1806-4841.20153881] [PMID: 26734864]
[2]
Giles, B.M.; Boackle, S.A. Linking complement and anti-dsDNA antibodies in the pathogenesis of systemic lupus erythematosus. Immunol. Res., 2013, 55(1-3), 10-21.
[http://dx.doi.org/10.1007/s12026-012-8345-z] [PMID: 22941560]
[3]
Narayanan, K.B.; Park, H.H. Toll/interleukin-1 receptor (TIR) domain-mediated cellular signaling pathways. Apoptosis, 2015, 20(2), 196-209.
[http://dx.doi.org/10.1007/s10495-014-1073-1] [PMID: 25563856]
[4]
Nelson, P.; Rylance, P.; Roden, D.; Trela, M.; Tugnet, N. Viruses as potential pathogenic agents in systemic lupus erythematosus. Lupus, 2014, 23(6), 596-605.
[http://dx.doi.org/10.1177/0961203314531637] [PMID: 24763543]
[5]
Mountz, J.D.; Hsu, H.C.; Ballesteros-Tato, A. Dysregulation of T follicular helper cells in lupus. J. Immunol., 2019, 202(6), 1649-1658.
[http://dx.doi.org/10.4049/jimmunol.1801150] [PMID: 30833421]
[6]
Gupta, S.; Kaplan, M.J. Bite of the wolf: Innate immune responses propagate autoimmunity in lupus. J. Clin. Invest., 2021, 131(3), e144918.
[http://dx.doi.org/10.1172/JCI144918] [PMID: 33529160]
[7]
Choi, M.Y.; Costenbader, K.H. Understanding the concept of pre-clinical autoimmunity: Prediction and prevention of systemic lupus erythematosus: Identifying risk factors and developing strategies against disease development. Front. Immunol., 2022, 13, 890522.
[http://dx.doi.org/10.3389/fimmu.2022.890522] [PMID: 35720390]
[8]
Pinna, S.; Pasella, S.; Deiana, M.; Baralla, A.; Mannu, A.; Masala, A.G.E.; Pileri, P.V.; Deiana, N.; Scognamillo, F.; Pala, C.; Zinellu, A.; Carru, C.; Deiana, L. Proteomic analysis of human plasma and peripheral blood mononuclear cells in Systemic Lupus Erythematosus patients. J. Immunol. Methods, 2017, 446, 37-46.
[http://dx.doi.org/10.1016/j.jim.2017.03.019] [PMID: 28390925]
[9]
Ciccacci, C; Latini, A; Perricone, C; Conigliaro, P; Colafrancesco, S; Ceccarelli, F; Priori, R; Conti, F; Perricone, R; Novelli, G TNFAIP3 gene polymorphisms in three common autoimmune diseases: Systemic lupus erythematosus, rheumatoid arthritis, and primary Sjogren Syndrome-Association with disease susceptibility and clinical phenotypes in Italian patients. J. Immunol. Res., 2019, 2019, 6728694.
[10]
Weinhold, B. Epigenetics: The science of change. Environ. Health Perspect., 2006, 114(3), A160-A167.
[http://dx.doi.org/10.1289/ehp.114-a160]
[11]
Farivar, S.; Shaabanpour Aghamaleki, F. Effects of major epigenetic factors on systemic lupus erythematosus. Iran. Biomed. J., 2018, 22(5), 294-302.
[http://dx.doi.org/10.29252/ibj.22.5.294] [PMID: 29803202]
[12]
Absher, D.M.; Li, X.; Waite, L.L.; Gibson, A.; Roberts, K.; Edberg, J.; Chatham, W.W.; Kimberly, R.P. Genome-wide DNA methylation analysis of systemic lupus erythematosus reveals persistent hypomethylation of interferon genes and compositional changes to CD4+ T-cell populations. PLoS Genet., 2013, 9(8), e1003678.
[http://dx.doi.org/10.1371/journal.pgen.1003678] [PMID: 23950730]
[13]
Skopelja-Gardner, S.; Tai, J.; Sun, X.; Tanaka, L.; Kuchenbecker, J.A.; Snyder, J.M.; Kubes, P.; Mustelin, T.; Elkon, K.B. Acute skin exposure to ultraviolet light triggers neutrophil-mediated kidney inflammation. Proc. Natl. Acad. Sci., 2021, 118(3), e2019097118.
[http://dx.doi.org/10.1073/pnas.2019097118] [PMID: 33397815]
[14]
Menke, J.; Hsu, M.Y.; Byrne, K.T.; Lucas, J.A.; Rabacal, W.A.; Croker, B.P.; Zong, X.H.; Stanley, E.R.; Kelley, V.R. Sunlight triggers cutaneous lupus through a CSF-1-dependent mechanism in MRL-Fas(lpr) mice. J. Immunol., 2008, 181(10), 7367-7379.
[http://dx.doi.org/10.4049/jimmunol.181.10.7367] [PMID: 18981160]
[15]
Greiling, T.M.; Dehner, C.; Chen, X.; Hughes, K.; Iñiguez, A.J.; Boccitto, M.; Ruiz, D.Z.; Renfroe, S.C.; Vieira, S.M.; Ruff, W.E.; Sim, S.; Kriegel, C.; Glanternik, J.; Chen, X.; Girardi, M.; Degnan, P.; Costenbader, K.H.; Goodman, A.L.; Wolin, S.L.; Kriegel, M.A. Commensal orthologs of the human autoantigen Ro60 as triggers of autoimmunity in lupus. Sci. Transl. Med., 2018, 10(434), eaan2306.
[http://dx.doi.org/10.1126/scitranslmed.aan2306] [PMID: 29593104]
[16]
Ruff, W.E.; Kriegel, M.A. Autoimmune host–microbiota interactions at barrier sites and beyond. Trends Mol. Med., 2015, 21(4), 233-244.
[http://dx.doi.org/10.1016/j.molmed.2015.02.006] [PMID: 25771098]
[17]
Manfredo Vieira, S.; Hiltensperger, M.; Kumar, V.; Zegarra-Ruiz, D.; Dehner, C.; Khan, N.; Costa, F.R.C.; Tiniakou, E.; Greiling, T.; Ruff, W.; Barbieri, A.; Kriegel, C.; Mehta, S.S.; Knight, J.R.; Jain, D.; Goodman, A.L.; Kriegel, M.A. Translocation of a gut pathobiont drives autoimmunity in mice and humans. Science, 2018, 359(6380), 1156-1161.
[http://dx.doi.org/10.1126/science.aar7201] [PMID: 29590047]
[18]
Turer, E.E.; Tavares, R.M.; Mortier, E.; Hitotsumatsu, O.; Advincula, R.; Lee, B.; Shifrin, N.; Malynn, B.A.; Ma, A. Homeostatic MyD88-dependent signals cause lethal inflamMation in the absence of A20. J. Exp. Med., 2008, 205(2), 451-464.
[http://dx.doi.org/10.1084/jem.20071108] [PMID: 18268035]
[19]
Zegarra-Ruiz, DF; El Beidaq, A; Iñiguez, AJ; Di Ricco, ML; Vieira, SM; Ruff, WE; Mubiru, D; Fine, RL; Sterpka, J; Greiling, TM A diet-sensitive commensal Lactobacillus strain mediates TLR7-dependent systemic autoimmunity. Cell Host Microbe, 2019, 25(1), 113-127.
[http://dx.doi.org/10.1016/j.chom.2018.11.009] [PMID: 30581114]
[20]
Coit, P.; Sawalha, A.H. The human microbiome in rheumatic autoimmune diseases: A comprehensive review. Clin. Immunol., 2016, 170, 70-79.
[http://dx.doi.org/10.1016/j.clim.2016.07.026] [PMID: 27493014]
[21]
Larsen, M.; Sauce, D.; Deback, C.; Arnaud, L.; Mathian, A.; Miyara, M.; Boutolleau, D.; Parizot, C.; Dorgham, K.; Papagno, L.; Appay, V.; Amoura, Z.; Gorochov, G. Exhausted cytotoxic control of Epstein-Barr virus in human lupus. PLoS Pathog., 2011, 7(10), e1002328.
[http://dx.doi.org/10.1371/journal.ppat.1002328] [PMID: 22028659]
[22]
Iwakiri, D.; Zhou, L.; Samanta, M.; Matsumoto, M.; Ebihara, T.; Seya, T.; Imai, S.; Fujieda, M.; Kawa, K.; Takada, K. Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from toll-like receptor 3. J. Exp. Med., 2009, 206(10), 2091-2099.
[http://dx.doi.org/10.1084/jem.20081761] [PMID: 19720839]
[23]
Yadav, P.; Tran, H.; Ebegbe, R.; Gottlieb, P.; Wei, H.; Lewis, R.H.; Mumbey-Wafula, A.; Kaplan, A.; Kholdarova, E.; Spatz, L. Antibodies elicited in response to EBNA-1 may cross-react with dsDNA. PLoS One, 2011, 6(1), e14488.
[http://dx.doi.org/10.1371/journal.pone.0014488] [PMID: 21245919]
[24]
Deng, C.; Lu, Q.; Zhang, Z.; Rao, T.; Attwood, J.; Yung, R.; Richardson, B. Hydralazine may induce autoimmunity by inhibiting extracellular signal-regulated kinase pathway signaling. Arthritis Rheum., 2003, 48(3), 746-756.
[http://dx.doi.org/10.1002/art.10833] [PMID: 12632429]
[25]
Kaul, A.; Gordon, C.; Crow, M.K.; Touma, Z.; Urowitz, M.B.; van Vollenhoven, R.; Ruiz-Irastorza, G.; Hughes, G. Systemic lupus erythematosus. Nat. Rev. Dis. Primers, 2016, 2(1), 16039.
[http://dx.doi.org/10.1038/nrdp.2016.39] [PMID: 27306639]
[26]
Bertsias, G.; Cervera, R. Boumpas, DT Systemic lupus erythematosus: Pathogenesis and clinical features. In: EULAR textbook on rheumatic diseases; Bijlsma; J. BMJ Group: London, 2012; pp. 476-505.
[27]
Odhams, C.A.; Roberts, A.L.; Vester, S.K.; Duarte, C.S.T.; Beales, C.T.; Clarke, A.J.; Lindinger, S.; Daffern, S.J.; Zito, A.; Chen, L.; Jones, L.L.; Boteva, L.; Morris, D.L.; Small, K.S.; Fernando, M.M.A.; Cunninghame Graham, D.S.; Vyse, T.J. Interferon inducible X-linked gene CXorf21 may contribute to sexual dimorphism in Systemic Lupus Erythematosus. Nat. Commun., 2019, 10(1), 2164.
[http://dx.doi.org/10.1038/s41467-019-10106-2] [PMID: 31092820]
[28]
Soni, C.; Wong, E.B.; Domeier, P.P.; Khan, T.N.; Satoh, T.; Akira, S.; Rahman, Z.S.M. B cell-intrinsic TLR7 signaling is essential for the development of spontaneous germinal centers. J. Immunol., 2014, 193(9), 4400-4414.
[http://dx.doi.org/10.4049/jimmunol.1401720] [PMID: 25252960]
[29]
Kassi, E; Moutsatsou, P Estrogen receptor signaling and its relationship to cytokines in systemic lupus erythematosus. J. Biomed. Biotechnol., 2010, 2010, 317452.
[http://dx.doi.org/10.1155/2010/317452]
[30]
Moulton, V.R.; Tsokos, G.C. Why do women get lupus? Clin. Immunol., 2012, 144(1), 53-56.
[http://dx.doi.org/10.1016/j.clim.2012.04.003] [PMID: 22659035]
[31]
Liang, Y.; Tsoi, L.C.; Xing, X.; Beamer, M.A.; Swindell, W.R.; Sarkar, M.K.; Berthier, C.C.; Stuart, P.E.; Harms, P.W.; Nair, R.P.; Elder, J.T.; Voorhees, J.J.; Kahlenberg, J.M.; Gudjonsson, J.E. A gene network regulated by the transcription factor VGLL3 as a promoter of sex-biased autoimmune diseases. Nat. Immunol., 2017, 18(2), 152-160.
[http://dx.doi.org/10.1038/ni.3643] [PMID: 27992404]
[32]
Dragin, N.; Nancy, P.; Villegas, J.; Roussin, R.; Le Panse, R.; Berrih-Aknin, S. Balance between estrogens and proinflammatory cytokines regulates chemokine production involved in thymic germinal center formation. Sci. Rep., 2017, 7(1), 7970.
[http://dx.doi.org/10.1038/s41598-017-08631-5] [PMID: 28801669]
[33]
Manni, M.; Gupta, S.; Ricker, E.; Chinenov, Y.; Park, S.H.; Shi, M.; Pannellini, T.; Jessberger, R.; Ivashkiv, L.B.; Pernis, A.B. Regulation of age-associated B cells by IRF5 in systemic autoimmunity. Nat. Immunol., 2018, 19(4), 407-419.
[http://dx.doi.org/10.1038/s41590-018-0056-8] [PMID: 29483597]
[34]
Sanchez-Guerrero, J.; Karlson, E.W.; Liang, M.H.; Hunter, D.J.; Speizer, F.E.; Colditz, G.A. Past use of oral contraceptives and the risk of developing systemic lupus erythematosus. Arthritis Rheum., 1997, 40(5), 804-808.
[http://dx.doi.org/10.1002/art.1780400505] [PMID: 9153539]
[35]
Sánchez-Guerrero, J.; Uribe, A.G.; Jiménez-Santana, L.; Mestanza-Peralta, M.; Lara-Reyes, P.; Seuc, A.H.; Cravioto, M.C. A trial of contraceptive methods in women with systemic lupus erythematosus. N. Engl. J. Med., 2005, 353(24), 2539-2549.
[http://dx.doi.org/10.1056/NEJMoa050817] [PMID: 16354890]
[36]
Thomas, R.; Jawad, A.S. Systemic lupus erythematosus: Rarer in men than women but more severe. Trends Urol. Men’s Health, 2022, 13(5), 11-14.
[http://dx.doi.org/10.1002/tre.876]
[37]
Scofield, R.H.; Bruner, G.R.; Namjou, B.; Kimberly, R.P.; Ramsey-Goldman, R.; Petri, M.; Reveille, J.D.; Alarcón, G.S.; Vilá, L.M.; Reid, J.; Harris, B.; Li, S.; Kelly, J.A.; Harley, J.B. Klinefelter’s syndrome (47,XXY) in male systemic lupus erythematosus patients: Support for the notion of a gene-dose effect from the X chromosome. Arthritis Rheum., 2008, 58(8), 2511-2517.
[http://dx.doi.org/10.1002/art.23701] [PMID: 18668569]
[38]
Kamitaki, N.; Sekar, A.; Handsaker, R.E.; de Rivera, H.; Tooley, K.; Morris, D.L.; Taylor, K.E.; Whelan, C.W.; Tombleson, P.; Loohuis, L.M.O.; Boehnke, M.; Kimberly, R.P.; Kaufman, K.M.; Harley, J.B.; Langefeld, C.D.; Seidman, C.E.; Pato, M.T.; Pato, C.N.; Ophoff, R.A.; Graham, R.R.; Criswell, L.A.; Vyse, T.J.; McCarroll, S.A. Complement genes contribute sex-biased vulnerability in diverse disorders. Nature, 2020, 582(7813), 577-581.
[http://dx.doi.org/10.1038/s41586-020-2277-x] [PMID: 32499649]
[39]
Liu, Z.; Davidson, A. Taming lupus—a new understanding of pathogenesis is leading to clinical advances. Nat. Med., 2012, 18(6), 871-882.
[http://dx.doi.org/10.1038/nm.2752] [PMID: 22674006]
[40]
Scharer, C.D.; Blalock, E.L.; Mi, T.; Barwick, B.G.; Jenks, S.A.; Deguchi, T.; Cashman, K.S.; Neary, B.E.; Patterson, D.G.; Hicks, S.L.; Khosroshahi, A.; Eun-Hyung Lee, F.; Wei, C.; Sanz, I.; Boss, J.M. Epigenetic programming underpins B cell dysfunction in human SLE. Nat. Immunol., 2019, 20(8), 1071-1082.
[http://dx.doi.org/10.1038/s41590-019-0419-9] [PMID: 31263277]
[41]
Zumaquero, E.; Stone, S.L.; Scharer, C.D.; Jenks, S.A.; Nellore, A.; Mousseau, B.; Rosal-Vela, A.; Botta, D.; Bradley, J.E.; Wojciechowski, W.; Ptacek, T.; Danila, M.I.; Edberg, J.C.; Bridges, S.L., Jr; Kimberly, R.P.; Chatham, W.W.; Schoeb, T.R.; Rosenberg, A.F.; Boss, J.M.; Sanz, I.; Lund, F.E. IFNγ induces epigenetic programming of human T-bethi B cells and promotes TLR7/8 and IL-21 induced differentiation. eLife, 2019, 8, e41641.
[http://dx.doi.org/10.7554/eLife.41641] [PMID: 31090539]
[42]
Hamilton, J.A.; Wu, Q.; Yang, P.; Luo, B.; Liu, S.; Li, J.; L Mattheyses, A.; Sanz, I.; Chatham, W.W.; Hsu, H-C.; Mountz, J.D. Cutting edge: Intracellular IFN-β and distinct type I IFN expression patterns in circulating systemic lupus erythematosus B cells. J. Immunol., 2018, 201(8), 2203-2208.
[http://dx.doi.org/10.4049/jimmunol.1800791] [PMID: 30201809]
[43]
Charles, N.; Hardwick, D.; Daugas, E.; Illei, G.G.; Rivera, J. Basophils and the T helper 2 environment can promote the development of lupus nephritis. Nat. Med., 2010, 16(6), 701-707.
[http://dx.doi.org/10.1038/nm.2159] [PMID: 20512127]
[44]
Henault, J.; Riggs, J.M.; Karnell, J.L.; Liarski, V.M.; Li, J.; Shirinian, L.; Xu, L.; Casey, K.A.; Smith, M.A.; Khatry, D.B.; Izhak, L.; Clarke, L.; Herbst, R.; Ettinger, R.; Petri, M.; Clark, M.R.; Mustelin, T.; Kolbeck, R.; Sanjuan, M.A. Self-reactive IgE exacerbates interferon responses associated with autoimmunity. Nat. Immunol., 2016, 17(2), 196-203.
[http://dx.doi.org/10.1038/ni.3326] [PMID: 26692173]
[45]
Zhu, J.; Liu, X.; Xie, C.; Yan, M.; Yu, Y.; Sobel, E.S.; Wakeland, E.K.; Mohan, C. T cell hyperactivity in lupus as a consequence of hyperstimulatory antigen-presenting cells. J. Clin. Invest., 2005, 115(7), 1869-1878.
[http://dx.doi.org/10.1172/JCI23049] [PMID: 15951839]
[46]
Mohan, C.; Adams, S.; Stanik, V.; Datta, S.K. Nucleosome: A major immunogen for pathogenic autoantibody-inducing T cells of lupus. J. Exp. Med., 1993, 177(5), 1367-1381.
[http://dx.doi.org/10.1084/jem.177.5.1367] [PMID: 8478612]
[47]
Kim, S.J.; Lee, K.; Diamond, B. Follicular helper T cells in systemic lupus erythematosus. Front. Immunol., 2018, 9, 1793.
[http://dx.doi.org/10.3389/fimmu.2018.01793] [PMID: 30123218]
[48]
Faliti, C.E.; Gualtierotti, R.; Rottoli, E.; Gerosa, M.; Perruzza, L.; Romagnani, A.; Pellegrini, G.; De Ponte Conti, B.; Rossi, R.L.; Idzko, M.; Mazza, E.M.C.; Bicciato, S.; Traggiai, E.; Meroni, P.L.; Grassi, F. P2X7 receptor restrains pathogenic Tfh cell generation in systemic lupus erythematosus. J. Exp. Med., 2019, 216(2), 317-336.
[http://dx.doi.org/10.1084/jem.20171976] [PMID: 30655308]
[49]
Garcia-Romo, GS; Caielli, S; Vega, B; Connolly, J; Allantaz, F; Xu, Z; Punaro, M; Baisch, J; Guiducci, C; Coffman, RL Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med., 2011, 3(73), 73ra20.
[http://dx.doi.org/10.1126/scitranslmed.3001201]
[50]
Frangou, E.; Chrysanthopoulou, A.; Mitsios, A.; Kambas, K.; Arelaki, S.; Angelidou, I.; Arampatzioglou, A.; Gakiopoulou, H.; Bertsias, G.K.; Verginis, P.; Ritis, K.; Boumpas, D.T. REDD1/autophagy pathway promotes thromboinflammation and fibrosis in human systemic lupus erythematosus (SLE) through NETs decorated with tissue factor (TF) and interleukin-17A (IL-17A). Ann. Rheum. Dis., 2019, 78(2), 238-248.
[http://dx.doi.org/10.1136/annrheumdis-2018-213181] [PMID: 30563869]
[51]
Puga, I.; Cols, M.; Barra, C.M.; He, B.; Cassis, L.; Gentile, M.; Comerma, L.; Chorny, A.; Shan, M.; Xu, W. Erratum: B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen (Nature Immunology (2012) 13 (170-180)). Nat. Immunol., 2014, 15, 205.
[http://dx.doi.org/10.1038/ni0214-205a]
[52]
Caielli, S.; Veiga, D.T.; Balasubramanian, P.; Athale, S.; Domic, B.; Murat, E.; Banchereau, R.; Xu, Z.; Chandra, M.; Chung, C.H.; Walters, L.; Baisch, J.; Wright, T.; Punaro, M.; Nassi, L.; Stewart, K.; Fuller, J.; Ucar, D.; Ueno, H.; Zhou, J.; Banchereau, J.; Pascual, V.A. CD4+ T cell population expanded in lupus blood provides B cell help through interleukin-10 and succinate. Nat. Med., 2019, 25(1), 75-81.
[http://dx.doi.org/10.1038/s41591-018-0254-9] [PMID: 30478422]
[53]
Georgiev, M.; Agle, L.M.A.; Chu, J.L.; Elkon, K.B.; Ashany, D. Mature dendritic cells readily break tolerance in normal mice but do not lead to disease expression. Arthritis Rheum., 2005, 52(1), 225-238.
[http://dx.doi.org/10.1002/art.20759] [PMID: 15641101]
[54]
Pathak, S.; Mohan, C. Cellular and molecular pathogenesis of systemic lupus erythematosus: Lessons from animal models. Arthritis Res. Ther., 2011, 13(5), 241.
[http://dx.doi.org/10.1186/ar3465] [PMID: 21989039]
[55]
Chen, M.; Wang, Y.H.; Wang, Y.; Huang, L.; Sandoval, H.; Liu, Y.J.; Wang, J. Dendritic cell apoptosis in the maintenance of immune tolerance. Science, 2006, 311(5764), 1160-1164.
[http://dx.doi.org/10.1126/science.1122545] [PMID: 16497935]
[56]
Katsuyama, E; Suarez-Fueyo, A; Bradley, SJ; Mizui, M; Marin, AV; Mulki, L; Krishfield, S; Malavasi, F; Yoon, J; Sui, SJH The CD38/NAD/SIRTUIN1/EZH2 axis mitigates cytotoxic CD8 T cell function and identifies patients with SLE prone to infections. Cell Reports, 2020, 30, 112-123.e4.
[57]
Mizui, M.; Koga, T.; Lieberman, L.A.; Beltran, J.; Yoshida, N.; Johnson, M.C.; Tisch, R.; Tsokos, G.C. IL-2 protects lupus-prone mice from multiple end-organ damage by limiting CD4-CD8- IL-17-producing T cells. J. Immunol., 2014, 193(5), 2168-2177.
[http://dx.doi.org/10.4049/jimmunol.1400977] [PMID: 25063876]
[58]
Tanaka, S.; Ise, W.; Inoue, T.; Ito, A.; Ono, C.; Shima, Y.; Sakakibara, S.; Nakayama, M.; Fujii, K.; Miura, I.; Sharif, J.; Koseki, H.; Koni, P.A.; Raman, I.; Li, Q.Z.; Kubo, M.; Fujiki, K.; Nakato, R.; Shirahige, K.; Araki, H.; Miura, F.; Ito, T.; Kawakami, E.; Baba, Y.; Kurosaki, T. Tet2 and Tet3 in B cells are required to repress CD86 and prevent autoimmunity. Nat. Immunol., 2020, 21(8), 950-961.
[http://dx.doi.org/10.1038/s41590-020-0700-y] [PMID: 32572241]
[59]
Comte, D.; Karampetsou, M.P.; Kis-Toth, K.; Yoshida, N.; Bradley, S.J.; Kyttaris, V.C.; Tsokos, G.C. Brief report: CD4+ T Cells from patients with systemic lupus erythematosus respond poorly to exogenous interleukin‐2. Arthritis Rheumatol., 2017, 69(4), 808-813.
[http://dx.doi.org/10.1002/art.40014] [PMID: 27992687]
[60]
Sharabi, A.; Tsokos, G.C. T cell metabolism: New insights in systemic lupus erythematosus pathogenesis and therapy. Nat. Rev. Rheumatol., 2020, 16(2), 100-112.
[http://dx.doi.org/10.1038/s41584-019-0356-x] [PMID: 31949287]
[61]
Maeda, K.; Otomo, K.; Yoshida, N.; Abu-Asab, M.S.; Ichinose, K.; Nishino, T.; Kono, M.; Ferretti, A.; Bhargava, R.; Maruyama, S.; Bickerton, S.; Fahmy, T.M.; Tsokos, M.G.; Tsokos, G.C. CaMK4 compromises podocyte function in autoimmune and nonautoimmune kidney disease. J. Clin. Invest., 2018, 128(8), 3445-3459.
[http://dx.doi.org/10.1172/JCI99507] [PMID: 29985166]
[62]
Winchester, R.; Wiesendanger, M.; Zhang, H.Z.; Steshenko, V.; Peterson, K.; Geraldino-Pardilla, L.; Ruiz-Vazquez, E.; D’Agati, V. Immunologic characteristics of intrarenal T cells: Trafficking of expanded CD8+ T cell β-chain clonotypes in progressive lupus nephritis. Arthritis Rheum., 2012, 64(5), 1589-1600.
[http://dx.doi.org/10.1002/art.33488] [PMID: 22130908]
[63]
Barrat, F.J.; Meeker, T.; Gregorio, J.; Chan, J.H.; Uematsu, S.; Akira, S.; Chang, B.; Duramad, O.; Coffman, R.L. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med., 2005, 202(8), 1131-1139.
[http://dx.doi.org/10.1084/jem.20050914] [PMID: 16230478]
[64]
Jacquemin, C.; Augusto, J.F.; Scherlinger, M.; Gensous, N.; Forcade, E.; Douchet, I.; Levionnois, E.; Richez, C.; Lazaro, E.; Duffau, P.; Truchetet, M.E.; Seneschal, J.; Couzi, L.; Pellegrin, J.L.; Viallard, J.F.; Schaeverbeke, T.; Pascual, V.; Contin-Bordes, C.; Blanco, P. OX40L/OX40 axis impairs follicular and natural Treg function in human SLE. JCI Insight, 2018, 3(24), e122167.
[http://dx.doi.org/10.1172/jci.insight.122167] [PMID: 30568041]
[65]
Furie, R.; Werth, V.P.; Merola, J.F.; Stevenson, L.; Reynolds, T.L.; Naik, H.; Wang, W.; Christmann, R.; Gardet, A.; Pellerin, A.; Hamann, S.; Auluck, P.; Barbey, C.; Gulati, P.; Rabah, D.; Franchimont, N. Monoclonal antibody targeting BDCA2 ameliorates skin lesions in systemic lupus erythematosus. J. Clin. Invest., 2019, 129(3), 1359-1371.
[http://dx.doi.org/10.1172/JCI124466] [PMID: 30645203]
[66]
Joo, H.; Coquery, C.; Xue, Y.; Gayet, I.; Dillon, S.R.; Punaro, M.; Zurawski, G.; Banchereau, J.; Pascual, V.; Oh, S. Serum from patients with SLE instructs monocytes to promote IgG and IgA plasmablast differentiation. J. Exp. Med., 2012, 209(7), 1335-1348.
[http://dx.doi.org/10.1084/jem.20111644] [PMID: 22689824]
[67]
Dema, B.; Charles, N. Advances in mechanisms of systemic lupus erythematosus. Discov. Med., 2014, 17(95), 247-255.
[PMID: 24882716]
[68]
Gatto, M.; Zen, M.; Ghirardello, A.; Bettio, S.; Bassi, N.; Iaccarino, L.; Punzi, L.; Doria, A. Emerging and critical issues in the pathogenesis of lupus. Autoimmun. Rev., 2013, 12(4), 523-536.
[http://dx.doi.org/10.1016/j.autrev.2012.09.003] [PMID: 23000207]
[69]
Wikenheiser, D.J.; Stumhofer, J.S. ICOS co-stimulation: Friend or foe? Front. Immunol., 2016, 7, 304.
[http://dx.doi.org/10.3389/fimmu.2016.00304] [PMID: 27559335]
[70]
Matta, B.; Song, S.; Li, D.; Barnes, B.J. Interferon regulatory factor signaling in autoimmune disease. Cytokine, 2017, 98, 15-26.
[http://dx.doi.org/10.1016/j.cyto.2017.02.006] [PMID: 28283223]
[71]
Hao, Y.; O’Neill, P.; Naradikian, M.S.; Scholz, J.L.; Cancro, M.P. A B-cell subset uniquely responsive to innate stimuli accumulates in aged mice. Blood, 2011, 118(5), 1294-1304.
[http://dx.doi.org/10.1182/blood-2011-01-330530] [PMID: 21562046]
[72]
Rubtsov, A.V.; Rubtsova, K.; Fischer, A.; Meehan, R.T.; Gillis, J.Z.; Kappler, J.W.; Marrack, P. Toll-like receptor 7 (TLR7)–driven accumulation of a novel CD11c+ B-cell population is important for the development of autoimmunity. Blood, 2011, 118(5), 1305-1315.
[http://dx.doi.org/10.1182/blood-2011-01-331462] [PMID: 21543762]
[73]
Sachinidis, A.; Xanthopoulos, K.; Garyfallos, A. Age-associated B cells (ABCs) in the prognosis, diagnosis and therapy of Systemic Lupus Erythematosus (SLE). Mediterr. J. Rheumatol., 2020, 31(3), 311-318.
[http://dx.doi.org/10.31138/mjr.31.3.311] [PMID: 33163863]
[74]
Båve, U.; Magnusson, M.; Eloranta, M.L.; Perers, A.; Alm, G.V.; Rönnblom, L. Fc gamma RIIa is expressed on natural IFN-alpha-producing cells (plasmacytoid dendritic cells) and is required for the IFN-alpha production induced by apoptotic cells combined with lupus IgG. J. Immunol., 2003, 171(6), 3296-3302.
[http://dx.doi.org/10.4049/jimmunol.171.6.3296] [PMID: 12960360]
[75]
Sakaguchi, S. Naturally a rising cd4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol., 2004, 22(1), 531-562.
[http://dx.doi.org/10.1146/annurev.immunol.21.120601.141122] [PMID: 15032588]
[76]
Thurman, J.M.; Yapa, R. Complement therapeutics in autoimmune disease. Front. Immunol., 2019, 10, 672.
[http://dx.doi.org/10.3389/fimmu.2019.00672] [PMID: 31001274]
[77]
Crispín, J.C.; Oukka, M.; Bayliss, G.; Cohen, R.A.; Van Beek, C.A.; Stillman, I.E.; Kyttaris, V.C.; Juang, Y.T.; Tsokos, G.C. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J. Immunol., 2008, 181(12), 8761-8766.
[http://dx.doi.org/10.4049/jimmunol.181.12.8761] [PMID: 19050297]
[78]
Davidson, A.; Aranow, C.; Mackay, M. Lupus nephritis: Challenges and progress. Curr. Opin. Rheumatol., 2019, 31(6), 682-688.
[http://dx.doi.org/10.1097/BOR.0000000000000642] [PMID: 31389814]
[79]
Liarski, VM; Kaverina, N; Chang, A; Brandt, D; Yanez, D; Talasnik, L; Carlesso, G; Herbst, R; Utset, TO; Labno, C Cell distance mapping identifies functional T follicular helper cells in inflamed human renal tissue. Sci. Trans. Med., 2014, 6, 230ra46-230ra46.
[http://dx.doi.org/10.1126/scitranslmed.3008146]
[80]
Der, E.; Suryawanshi, H.; Morozov, P.; Kustagi, M.; Goilav, B.; Ranabothu, S.; Izmirly, P.; Clancy, R.; Belmont, H.M.; Koenigsberg, M.; Mokrzycki, M.; Rominieki, H.; Graham, J.A.; Rocca, J.P.; Bornkamp, N.; Jordan, N.; Schulte, E.; Wu, M.; Pullman, J.; Slowikowski, K.; Raychaudhuri, S.; Guthridge, J.; James, J.; Buyon, J.; Tuschl, T.; Putterman, C. Tubular cell and keratinocyte single-cell transcriptomics applied to lupus nephritis reveal type I IFN and fibrosis relevant pathways. Nat. Immunol., 2019, 20(7), 915-927.
[http://dx.doi.org/10.1038/s41590-019-0386-1] [PMID: 31110316]
[81]
Yung, S.; Yap, D.Y.H.; Chan, T.M. A review of advances in the understanding of lupus nephritis pathogenesis as a basis for emerging therapies. F1000 Res., 2020, 9, 905.
[http://dx.doi.org/10.12688/f1000research.22438.1] [PMID: 32789005]
[82]
Thurman, J.M. Complement and the kidney: An overview. Adv. Chronic Kidney Dis., 2020, 27(2), 86-94.
[http://dx.doi.org/10.1053/j.ackd.2019.10.003] [PMID: 32553250]
[83]
Jarrett, P.; Werth, V.P. A review of cutaneous lupus erythematosus: Improving outcomes with a multidisciplinary approach. J. Multidiscip. Healthc., 2019, 12, 419-428.
[http://dx.doi.org/10.2147/JMDH.S179623] [PMID: 31213824]
[84]
Ramirez-Ortiz, Z.G.; Pendergraft, W.F., III; Prasad, A.; Byrne, M.H.; Iram, T.; Blanchette, C.J.; Luster, A.D.; Hacohen, N.; Khoury, J.E.; Means, T.K. The scavenger receptor SCARF1 mediates the clearance of apoptotic cells and prevents autoimmunity. Nat. Immunol., 2013, 14(9), 917-926.
[http://dx.doi.org/10.1038/ni.2670] [PMID: 23892722]
[85]
Pieterse, E.; Rother, N.; Garsen, M.; Hofstra, J.M.; Satchell, S.C.; Hoffmann, M.; Loeven, M.A.; Knaapen, H.K.; van der Heijden, O.W.H.; Berden, J.H.M.; Hilbrands, L.B.; van der Vlag, J. Neutrophil extracellular traps drive endothelial-to-mesenchymal transition. Arterioscler. Thromb. Vasc. Biol., 2017, 37(7), 1371-1379.
[http://dx.doi.org/10.1161/ATVBAHA.117.309002] [PMID: 28495931]
[86]
Martens, H.A.; Zuurman, M.W.; de Lange, A.H.M.; Nolte, I.M.; van der Steege, G.; Navis, G.J.; Kallenberg, C.G.M.; Seelen, M.A.; Bijl, M. Analysis of C1q polymorphisms suggests association with systemic lupus erythematosus, serum C1q and CH50 levels and disease severity. Ann. Rheum. Dis., 2009, 68(5), 715-720.
[http://dx.doi.org/10.1136/ard.2007.085688] [PMID: 18504288]
[87]
Oh, S.H.; Roh, H.J.; Kwon, J.E.; Lee, S.H.; Kim, J.Y.; Choi, H.J.; Lim, B.J. Expression of interleukin-17 is correlated with interferon-α expression in cutaneous lesions of lupus erythematosus. Clin. Exp. Dermatol., 2011, 36(5), 512-520.
[http://dx.doi.org/10.1111/j.1365-2230.2010.03996.x] [PMID: 21631571]
[88]
Mande, P.; Zirak, B.; Ko, W.C.; Taravati, K.; Bride, K.L.; Brodeur, T.Y.; Deng, A.; Dresser, K.; Jiang, Z.; Ettinger, R.; Fitzgerald, K.A.; Rosenblum, M.D.; Harris, J.E.; Marshak-Rothstein, A. Fas ligand promotes an inducible TLR-dependent model of cutaneous lupus–like inflammation. J. Clin. Invest., 2018, 128(7), 2966-2978.
[http://dx.doi.org/10.1172/JCI98219] [PMID: 29889098]
[89]
Järvinen, T.M.; Hellquist, A.; Koskenmies, S.; Einarsdottir, E.; Koskinen, L.L.E.; Jeskanen, L.; Berglind, L.; Panelius, J.; Hasan, T.; Ranki, A.; Kere, J.; Saarialho-Kere, U. Tyrosine kinase 2 and interferon regulatory factor 5 polymorphisms are associated with discoid and subacute cutaneous lupus erythematosus. Exp. Dermatol., 2010, 19(2), 123-131.
[http://dx.doi.org/10.1111/j.1600-0625.2009.00982.x] [PMID: 19758313]
[90]
Laurinaviciene, R.; Sandholdt, L.H.; Bygum, A. Drug-induced cutaneous lupus erythematosus: 88 new cases. Eur. J. Dermatol., 2017, 27(1), 28-33.
[http://dx.doi.org/10.1684/ejd.2016.2912] [PMID: 27799135]
[91]
Kuhn, A.; Aberer, E. Bata-Csörgő, Z.; Caproni, M.; Dreher, A.; Frances, C.; Gläser, R.; Klötgen, H.W.; Landmann, A.; Marinovic, B.; Nyberg, F.; Olteanu, R.; Ranki, A.; Szepietowski, J.C.; Volc-Platzer, B. S2k guideline for treatment of cutaneous lupus erythematosus - guided by the European Dermatology Forum (EDF) in cooperation with the European Academy of Dermatology and Venereology (EADV). J. Eur. Acad. Dermatol. Venereol., 2017, 31(3), 389-404.
[http://dx.doi.org/10.1111/jdv.14053] [PMID: 27859683]
[92]
Narayanan, K.B.; Ali, M.; Barclay, B.J.; Cheng, Q.S.; D’Abronzo, L.; Dornetshuber-Fleiss, R.; Ghosh, P.M.; Gonzalez Guzman, M.J.; Lee, T.J.; Leung, P.S.; Li, L.; Luanpitpong, S.; Ratovitski, E.; Rojanasakul, Y.; Romano, M.F.; Romano, S.; Sinha, R.K.; Yedjou, C.; Al-Mulla, F.; Al-Temaimi, R.; Amedei, A.; Brown, D.G.; Ryan, E.P.; Colacci, A.M.; Hamid, R.A.; Mondello, C.; Raju, J.; Salem, H.K.; Woodrick, J.; Scovassi, A.I.; Singh, N.; Vaccari, M.; Roy, R.; Forte, S.; Memeo, L.; Kim, S.Y.; Bisson, W.H.; Lowe, L.; Park, H.H. Disruptive environmental chemicals and cellular mechanisms that confer resistance to cell death. Carcinogenesis, 2015, 36(Suppl. 1), S89-S110.
[http://dx.doi.org/10.1093/carcin/bgv032] [PMID: 26106145]
[93]
Zeller, C.; Appenzeller, S. Cardiovascular disease in systemic lupus erythematosus: The role of traditional and lupus related risk factors. Curr. Cardiol. Rev., 2008, 4(2), 116-122.
[http://dx.doi.org/10.2174/157340308784245775] [PMID: 19936286]
[94]
Shi, G.P. Immunomodulation of vascular diseases: Atherosclerosis and autoimmunity. Eur. J. Vasc. Endovasc. Surg., 2010, 39(4), 485-494.
[http://dx.doi.org/10.1016/j.ejvs.2010.01.028] [PMID: 20188603]
[95]
Salmon, J.E.; Roman, M.J. Accelerated atherosclerosis in systemic lupus erythematosus: Implications for patient management. Curr. Opin. Rheumatol., 2001, 13(5), 341-344.
[http://dx.doi.org/10.1097/00002281-200109000-00001] [PMID: 11604586]
[96]
Badui, E.; Garcia-Rubi, D.; Robles, E.; Jimenez, J.; Juan, L.; Deleze, M.; Diaz, A.; Mintz, G. Cardiovascular manifestations in systemic lupus erythematosus. Prospective study of 100 patients. Angiology, 1985, 36(7), 431-441.
[http://dx.doi.org/10.1177/000331978503600705] [PMID: 4025948]
[97]
Gazarian, M.; Feldman, B.M.; Benson, L.N.; Gilday, D.L.; Laxer, R.M.; Silverman, E.D. Assessment of myocardial perfusion and function in childhood systemic lupus erythematosus. J. Pediatr., 1998, 132(1), 109-116.
[http://dx.doi.org/10.1016/S0022-3476(98)70494-9] [PMID: 9470010]
[98]
Hosenpud, J.D.; Montanaro, A.; Hart, M.V.; Haines, J.E.; Specht, H.D.; Bennett, R.M.; Kloster, F.E. Myocardial perfusion abnormalities in asymptomatic patients with systemic lupus erythematosus. Am. J. Med., 1984, 77(2), 286-292.
[http://dx.doi.org/10.1016/0002-9343(84)90704-6] [PMID: 6465176]
[99]
Jacobsen, S.; Petersen, J.; Ullman, S.; Junker, P.; Voss, A.; Rasmussen, J.M.; Tarp, U.; Poulsen, L.H.; van Overeem Hansen, G.; Skaarup, B.; Hansen, T.M.; Pødenphant, J.; Halberg, P. Mortality and causes of death of 513 Danish patients with systemic lupus erythematosus. Scand. J. Rheumatol., 1999, 28(2), 75-80.
[http://dx.doi.org/10.1080/030097499442522] [PMID: 10229135]
[100]
Svenungsson, E.; Jensen-Urstad, K.; Heimbürger, M.; Silveira, A.; Hamsten, A.; de Faire, U.; Witztum, J.L.; Frostegård, J. Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation, 2001, 104(16), 1887-1893.
[http://dx.doi.org/10.1161/hc4101.097518] [PMID: 11602489]
[101]
Carlucci, P.M.; Purmalek, M.M.; Dey, A.K.; Temesgen-Oyelakin, Y.; Sakhardande, S.; Joshi, A.A.; Lerman, J.B.; Fike, A.; Davis, M.; Chung, J.H.; Playford, M.P.; Naqi, M.; Mistry, P.; Gutierrez-Cruz, G.; Dell’Orso, S.; Naz, F.; Salahuddin, T.; Natarajan, B.; Manna, Z.; Tsai, W.L.; Gupta, S.; Grayson, P.; Teague, H.; Chen, M.Y.; Sun, H.W.; Hasni, S.; Mehta, N.N.; Kaplan, M.J. Neutrophil subsets and their gene signature associate with vascular inflammation and coronary atherosclerosis in lupus. JCI Insight, 2018, 3(8), e99276.
[http://dx.doi.org/10.1172/jci.insight.99276] [PMID: 29669944]
[102]
Knight, J.S.; Luo, W.; O’Dell, A.A.; Yalavarthi, S.; Zhao, W.; Subramanian, V.; Guo, C.; Grenn, R.C.; Thompson, P.R.; Eitzman, D.T.; Kaplan, M.J. Peptidylarginine deiminase inhibition reduces vascular damage and modulates innate immune responses in murine models of atherosclerosis. Circ. Res., 2014, 114(6), 947-956.
[http://dx.doi.org/10.1161/CIRCRESAHA.114.303312] [PMID: 24425713]
[103]
Liu, Y.; Kaplan, M.J. Cardiovascular disease in systemic lupus erythematosus: An update. Curr. Opin. Rheumatol., 2018, 30(5), 441-448.
[http://dx.doi.org/10.1097/BOR.0000000000000528] [PMID: 29870498]
[104]
Buie, J.J.; Renaud, L.L.; Muise-Helmericks, R.; Oates, J.C. IFN-α negatively regulates the expression of endothelial nitric oxide synthase and nitric oxide production: Implications for systemic lupus erythematosus. J. Immunol., 2017, 199(6), 1979-1988.
[http://dx.doi.org/10.4049/jimmunol.1600108] [PMID: 28779021]
[105]
Ryu, H.; Chung, Y. Dyslipidemia promotes germinal center reactions via IL-27. BMB Rep., 2018, 51(8), 371-372.
[http://dx.doi.org/10.5483/BMBRep.2018.51.8.171] [PMID: 30037367]
[106]
Tsokos, G.C. Autoimmunity and organ damage in systemic lupus erythematosus. Nat. Immunol., 2020, 21(6), 605-614.
[http://dx.doi.org/10.1038/s41590-020-0677-6] [PMID: 32367037]
[107]
Duffau, P; Seneschal, J; Nicco, C; Richez, C; Lazaro, E; Douchet, I; Bordes, C; Viallard, J-F; Goulvestre, C; Pellegrin, J-L Platelet CD154 potentiates interferon-α secretion by plasmacytoid dendritic cells in systemic lupus erythematosus. Sci. Trans. Med., 2010, 2, 47ra63-47ra63.
[http://dx.doi.org/10.1126/scitranslmed.3001001]
[108]
Hammad, S.M.; Harden, O.C.; Wilson, D.A.; Twal, W.O.; Nietert, P.J.; Oates, J.C. Plasma sphingolipid profile associated with subclinical atherosclerosis and clinical disease markers of systemic lupus erythematosus: Potential predictive value. Front. Immunol., 2021, 12, 694318.
[http://dx.doi.org/10.3389/fimmu.2021.694318] [PMID: 34367153]
[109]
Hanly, J.G.; Urowitz, M.B.; Sanchez-Guerrero, J.; Bae, S.C.; Gordon, C.; Wallace, D.J.; Isenberg, D.; Alarcón, G.S.; Clarke, A.; Bernatsky, S.; Merrill, J.T.; Petri, M.; Dooley, M.A.; Gladman, D.; Fortin, P.R.; Steinsson, K.; Bruce, I.; Manzi, S.; Khamashta, M.; Zoma, A.; Aranow, C.; Ginzler, E.; Van Vollenhoven, R.; Font, J.; Sturfelt, G.; Nived, O.; Ramsey-Goldman, R.; Kalunian, K.; Douglas, J.; Thompson, K.; Farewell, V. Neuropsychiatric events at the time of diagnosis of systemic lupus erythematosus: An international inception cohort study. Arthritis Rheum., 2007, 56(1), 265-273.
[http://dx.doi.org/10.1002/art.22305] [PMID: 17195230]
[110]
Weckerle, C.E.; Niewold, T.B. The unexplained female predominance of systemic lupus erythematosus: Clues from genetic and cytokine studies. Clin. Rev. Allergy Immunol., 2011, 40(1), 42-49.
[http://dx.doi.org/10.1007/s12016-009-8192-4] [PMID: 20063186]
[111]
Hanly, J.G. Neuropsychiatric lupus. Curr. Rheumatol. Rep., 2001, 3(3), 205-212.
[http://dx.doi.org/10.1007/s11926-001-0020-7] [PMID: 11352789]
[112]
Muscal, E.; Brey, R.L. Neurologic manifestations of systemic lupus erythematosus in children and adults. Neurol. Clin., 2010, 28(1), 61-73.
[http://dx.doi.org/10.1016/j.ncl.2009.09.004] [PMID: 19932376]
[113]
Sakic, B.; Kolb, B.; Whishaw, I.Q.; Gorny, G.; Szechtman, H.; Denburg, J.A. Immunosuppression prevents neuronal atrophy in lupus-prone mice. J. Neuroimmunol., 2000, 111(1-2), 93-101.
[http://dx.doi.org/10.1016/S0165-5728(00)00364-7] [PMID: 11063826]
[114]
Sakic, B.; Kirkham, D.L.; Ballok, D.A.; Mwanjewe, J.; Fearon, I.M.; Macri, J.; Yu, G.; Sidor, M.M.; Denburg, J.A.; Szechtman, H.; Lau, J.; Ball, A.K.; Doering, L.C. Proliferating brain cells are a target of neurotoxic CSF in systemic autoimmune disease. J. Neuroimmunol., 2005, 169(1-2), 68-85.
[http://dx.doi.org/10.1016/j.jneuroim.2005.08.010] [PMID: 16198428]
[115]
Pröbstel, A.K.; Thanei, M.; Erni, B.; Lecourt, A.C.; Branco, L.; André, R.; Roux-Lombard, P.; Koenig, K.F.; Huynh-Do, U.; Ribi, C.; Chizzolini, C.; Kappos, L.; Trendelenburg, M.; Derfuss, T. Association of antibodies against myelin and neuronal antigens with neuroinflammation in systemic lupus erythematosus. Rheumatology, 2019, 58(5), 908-913.
[http://dx.doi.org/10.1093/rheumatology/key282] [PMID: 30265368]
[116]
Schwartz, N.; Stock, A.D.; Putterman, C. Neuropsychiatric lupus: New mechanistic insights and future treatment directions. Nat. Rev. Rheumatol., 2019, 15(3), 137-152.
[http://dx.doi.org/10.1038/s41584-018-0156-8] [PMID: 30659245]
[117]
Goldschen, L.; Ellrodt, J.; Amonoo, H.L.; Feldman, C.H.; Case, S.M.; Koenen, K.C.; Kubzansky, L.D.; Costenbader, K.H. The link between post-traumatic stress disorder and systemic lupus erythematosus. Brain Behav. Immun., 2022, 108, 292-301.
[PMID: 36535611]
[118]
Pan, L.; Lu, M.P.; Wang, J.H.; Xu, M.; Yang, S.R. Immunological pathogenesis and treatment of systemic lupus erythematosus. World J. Pediatr., 2020, 16(1), 19-30.
[http://dx.doi.org/10.1007/s12519-019-00229-3] [PMID: 30796732]
[119]
Amissah-Arthur, M.B.; Gordon, C. Contemporary treatment of systemic lupus erythematosus: An update for clinicians. Ther. Adv. Chronic Dis., 2010, 1(4), 163-175.
[http://dx.doi.org/10.1177/2040622310380100] [PMID: 23251736]
[120]
Sawalha, A.H.; Kovats, S. Dehydroepiandrosterone in systemic lupus erythematosus. Curr. Rheumatol. Rep., 2008, 10(4), 286-291.
[http://dx.doi.org/10.1007/s11926-008-0046-1] [PMID: 18662508]
[121]
Marder, W.; Somers, E.C.; Kaplan, M.J.; Anderson, M.R.; Lewis, E.E.; McCune, W.J. Effects of Prasterone (dehydroepiandrosterone) on markers of cardiovascular risk and bone turnover in premenopausal women with systemic lupus erythematosus: A pilot study. Lupus, 2010, 19(10), 1229-1236.
[http://dx.doi.org/10.1177/0961203310371156] [PMID: 20530522]
[122]
Li, Y; Palmisano, M; Sun, DA-O; Zhou, S Pharmacokinetic disposition difference between cyclosporine and voclosporin drives their distinct efficacy and safety profiles in clinical studies. Clin. Pharmacol., 2020, 12, 83-96.
[http://dx.doi.org/10.2147/CPAA.S255789]
[123]
Heo, Y.A. Voclosporin: First approval. Drugs, 2021, 81(5), 605-610.
[http://dx.doi.org/10.1007/s40265-021-01488-z] [PMID: 33788181]
[124]
Rovin, B.H.; Teng, Y.K.O.; Ginzler, E.M.; Arriens, C.; Caster, D.J.; Romero-Diaz, J.; Gibson, K.; Kaplan, J.; Lisk, L.; Navarra, S.; Parikh, S.V.; Randhawa, S.; Solomons, N.; Huizinga, R.B. Efficacy and safety of voclosporin versus placebo for lupus nephritis (AURORA 1): A double-blind, randomised, multicentre, placebo-controlled, phase 3 trial. Lancet, 2021, 397(10289), 2070-2080.
[http://dx.doi.org/10.1016/S0140-6736(21)00578-X] [PMID: 33971155]
[125]
Moroni, G.; Ponticelli, C. AURORA 1 reports efficacy of voclosporin in lupus nephritis. Nat. Rev. Nephrol., 2021, 17(10), 637-638.
[http://dx.doi.org/10.1038/s41581-021-00460-0] [PMID: 34211153]
[126]
Tanaka, Y.; Luo, Y.; O’Shea, J.J.; Nakayamada, S. Janus kinase-targeting therapies in rheumatology: A mechanisms-based approach. Nat. Rev. Rheumatol., 2022, 18(3), 133-145.
[http://dx.doi.org/10.1038/s41584-021-00726-8] [PMID: 34987201]
[127]
Bonnardeaux, E.; Dutz, JP Oral tofacitinib citrate for recalcitrant cutaneous lupus. JAAD Case Rep., 2021, 20, 61-64.
[128]
Yan, Q.; Chen, W.; Song, H.; Long, X.; Zhang, Z.; Tang, X.; Chen, H.; Lin, H.; Sun, L. Tofacitinib ameliorates lupus through suppression of t Cell Activation mediasted by TGF-Beta type I receptor. Front. Immunol., 2021, 12, 675542.
[http://dx.doi.org/10.3389/fimmu.2021.675542] [PMID: 34394075]
[129]
Hasni, S.A.; Gupta, S.; Davis, M.; Poncio, E.; Temesgen-Oyelakin, Y.; Carlucci, P.M.; Wang, X.; Naqi, M.; Playford, M.P.; Goel, R.R.; Li, X.; Biehl, A.J.; Ochoa-Navas, I.; Manna, Z.; Shi, Y.; Thomas, D.; Chen, J.; Biancotto, A.; Apps, R.; Cheung, F.; Kotliarov, Y.; Babyak, A.L.; Zhou, H.; Shi, R.; Stagliano, K.; Tsai, W.L.; Vian, L.; Gazaniga, N.; Giudice, V.; Lu, S.; Brooks, S.R.; MacKay, M.; Gregersen, P.; Mehta, N.N.; Remaley, A.T.; Diamond, B.; O’Shea, J.J.; Gadina, M.; Kaplan, M.J. Phase 1 double-blind randomized safety trial of the Janus kinase inhibitor tofacitinib in systemic lupus erythematosus. Nat. Commun., 2021, 12(1), 3391.
[http://dx.doi.org/10.1038/s41467-021-23361-z] [PMID: 34099646]
[130]
Bjorklund, C.C.; Kang, J.; Amatangelo, M.; Polonskaia, A.; Katz, M.; Chiu, H.; Couto, S.; Wang, M.; Ren, Y.; Ortiz, M.; Towfic, F.; Flynt, J.E.; Pierceall, W.; Thakurta, A. Iberdomide (CC-220) is a potent cereblon E3 ligase modulator with antitumor and immunostimulatory activities in lenalidomide- and pomalidomideresistant multiple myeloma cells with dysregulated CRBN. Leukemia, 2020, 34(4), 1197-1201.
[http://dx.doi.org/10.1038/s41375-019-0620-8] [PMID: 31719682]
[131]
Merrill, J.T.; Werth, V.P.; Furie, R.; van Vollenhoven, R.; Dörner, T.; Petronijevic, M.; Velasco, J.; Majdan, M.; Irazoque-Palazuelos, F.; Weiswasser, M.; Korish, S.; Ye, Y.; Gaudy, A.; Schafer, P.H.; Liu, Z.; Agafonova, N.; Delev, N. Phase 2 trial of iberdomide in systemic lupus erythematosus. N. Engl. J. Med., 2022, 386(11), 1034-1045.
[http://dx.doi.org/10.1056/NEJMoa2106535] [PMID: 35294813]
[132]
Schafer, P.H.; Ye, Y.; Wu, L.; Kosek, J.; Ringheim, G.; Yang, Z.; Liu, L.; Thomas, M.; Palmisano, M.; Chopra, R. Cereblon modulator iberdomide induces degradation of the transcription factors Ikaros and Aiolos: Immunomodulation in healthy volunteers and relevance to systemic lupus erythematosus. Ann. Rheum. Dis., 2018, 77(10), 1516-1523.
[http://dx.doi.org/10.1136/annrheumdis-2017-212916] [PMID: 29945920]
[133]
Dörner, T.; Shock, A.; Goldenberg, D.M.; Lipsky, P.E. The mechanistic impact of CD22 engagement with epratuzumab on B cell function: Implications for the treatment of systemic lupus erythematosus. Autoimmun. Rev., 2015, 14(12), 1079-1086.
[http://dx.doi.org/10.1016/j.autrev.2015.07.013] [PMID: 26212727]
[134]
Dörner, T.; Kaufmann, J.; Wegener, W.A.; Teoh, N.; Goldenberg, D.M.; Burmester, G.R. Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus. Arthritis Res. Ther., 2006, 8(3), R74.
[http://dx.doi.org/10.1186/ar1942] [PMID: 16630358]
[135]
Dubey, A.K.; Handu, S.S.; Dubey, S.; Sharma, P.; Sharma, K.K.; Ahmed, Q.M. Belimumab: First targeted biological treatment for systemic lupus erythematosus. J. Pharmacol. Pharmacother., 2011, 2(4), 317-319.
[http://dx.doi.org/10.4103/0976-500X.85930] [PMID: 22025872]
[136]
Halpern, W.G.; Lappin, P.; Zanardi, T.; Cai, W.; Corcoran, M.; Zhong, J.; Baker, K.P. Chronic administration of belimumab, a BLyS antagonist, decreases tissue and peripheral blood B-lymphocyte populations in cynomolgus monkeys: Pharmacokinetic, pharmacodynamic, and toxicologic effects. Toxicol. Sci., 2006, 91(2), 586-599.
[http://dx.doi.org/10.1093/toxsci/kfj148] [PMID: 16517838]
[137]
Baker, K.P.; Edwards, B.M.; Main, S.H.; Choi, G.H.; Wager, R.E.; Halpern, W.G.; Lappin, P.B.; Riccobene, T.; Abramian, D.; Sekut, L.; Sturm, B.; Poortman, C.; Minter, R.R.; Dobson, C.L.; Williams, E.; Carmen, S.; Smith, R.; Roschke, V.; Hilbert, D.M.; Vaughan, T.J.; Albert, V.R. Generation and characterization of LymphoStat-B, a human monoclonal antibody that antagonizes the bioactivities of B lymphocyte stimulator. Arthritis Rheum., 2003, 48(11), 3253-3265.
[http://dx.doi.org/10.1002/art.11299] [PMID: 14613291]
[138]
Pierpont, T.M.; Limper, C.B.; Richards, K.L. Past, present, and future of rituximab-the world’s first oncology monoclonal antibody therapy. Front. Oncol., 2018, 8, 163.
[http://dx.doi.org/10.3389/fonc.2018.00163] [PMID: 29915719]
[139]
Maloney, D.G.; Smith, B.; Rose, A. Rituximab: Mechanism of action and resistance. Semin. Oncol., 2002, 29(1), 2-9.
[http://dx.doi.org/10.1053/sonc.2002.30156]
[140]
Jordan, N.; Lutalo, P.M.K.; D’Cruz, D.P. Novel therapeutic agents in clinical development for systemic lupus erythematosus. BMC Med., 2013, 11(1), 120.
[http://dx.doi.org/10.1186/1741-7015-11-120] [PMID: 23642011]
[141]
Stohl, W. Therapeutic targeting of the BAFF/APRIL axis in systemic lupus erythematosus. Expert Opin. Ther. Targets, 2014, 18(4), 473-489.
[http://dx.doi.org/10.1517/14728222.2014.888415] [PMID: 24521424]
[142]
Deeks, E.D. Anifrolumab: Fist apprroval. Drugs, 2021, 81(15), 1795-1802.
[http://dx.doi.org/10.1007/s40265-021-01604-z] [PMID: 34554438]
[143]
Tanaka, Y.; Tummala, R. Anifrolumab, a monoclonal antibody to the type I interferon receptor subunit 1, for the treatment of systemic lupus erythematosus: An overview from clinical trials. Mod. Rheumatol., 2021, 31(1), 1-12.
[http://dx.doi.org/10.1080/14397595.2020.1812201] [PMID: 32814461]
[144]
Fairfax, K.; Mackay, I.R.; Mackay, F. BAFF/BLyS inhibitors: A new prospect for treatment of systemic lupus erythematosus. IUBMB Life, 2012, 64(7), 595-602.
[http://dx.doi.org/10.1002/iub.1046] [PMID: 22641424]
[145]
Tran, N.L.; Schneider, P.; Santiago-Raber, M.L. TACI-dependent APRIL signaling maintains autoreactive B cells in a mouse model of systemic lupus erythematosus. Eur. J. Immunol., 2017, 47(4), 713-723.
[http://dx.doi.org/10.1002/eji.201646630] [PMID: 28267197]
[146]
Garcia-Carmona, Y.; Ting, A.T.; Radigan, L.; Athuluri Divakar, S.K.; Chavez, J.; Meffre, E.; Cerutti, A.; Cunningham-Rundles, C. TACI isoforms regulate ligand binding and receptor function. Front. Immunol., 2018, 9, 2125.
[http://dx.doi.org/10.3389/fimmu.2018.02125] [PMID: 30333819]
[147]
Wu, Y.; Bressette, D.; Carrell, J.A.; Kaufman, T.; Feng, P.; Taylor, K.; Gan, Y.; Cho, Y.H.; Garcia, A.D.; Gollatz, E.; Dimke, D.; LaFleur, D.; Migone, T.S.; Nardelli, B.; Wei, P.; Ruben, S.M.; Ullrich, S.J.; Olsen, H.S.; Kanakaraj, P.; Moore, P.A.; Baker, K.P. Tumor necrosis factor (TNF) receptor superfamily member TACI is a high affinity receptor for TNF family members APRIL and BLyS. J. Biol. Chem., 2000, 275(45), 35478-35485.
[http://dx.doi.org/10.1074/jbc.M005224200] [PMID: 10956646]
[148]
Rönnblom, L.; Elkon, K.B. Cytokines as therapeutic targets in SLE. Nat. Rev. Rheumatol., 2010, 6(6), 339-347.
[http://dx.doi.org/10.1038/nrrheum.2010.64] [PMID: 20440285]
[149]
Dörner, T.; Kinnman, N.; Tak, P.P. Targeting B cells in immunemediated inflammatory disease: A comprehensive review of mechanisms of action and identification of biomarkers. Pharmacol. Ther., 2010, 125(3), 464-475.
[http://dx.doi.org/10.1016/j.pharmthera.2010.01.001] [PMID: 20097226]
[150]
Linsley, P.S.; Wallace, P.M.; Johnson, J.; Gibson, M.G.; Greene, J.L.; Ledbetter, J.A.; Singh, C.; Tepper, M.A. Immunosuppression in vivo by a soluble form of the CTLA-4 T cell activation molecule. Science, 1992, 257(5071), 792-795.
[http://dx.doi.org/10.1126/science.1496399] [PMID: 1496399]
[151]
Liu, P.C.; Ssu, C.T.; Tsao, Y.P.; Liou, T.L.; Tsai, C.Y.; Chou, C.T.; Chen, M.H.; Leu, C.M. Cytotoxic T lymphocyte-associated antigen-4-Ig (CTLA-4-Ig) suppresses Staphylococcus aureus-induced CD80, CD86, and pro-inflammatory cytokine expression in human B cells. Arthritis Res. Ther., 2020, 22(1), 64.
[http://dx.doi.org/10.1186/s13075-020-2138-x] [PMID: 32228715]
[152]
Moreland, L.W.; Alten, R.; Van Den Bosch, F.; Appelboom, T.; Leon, M.; Emery, P.; Cohen, S.; Luggen, M.; Shergy, W.; Nuamah, I.; Becker, J.C. Costimulatory blockade in patients with rheumatoid arthritis: A pilot, dose-finding, double-blind, placebo-controlled clinical trial evaluating CTLA-4Ig and LEA29Y eighty-five days after the first infusion. Arthritis Rheum., 2002, 46(6), 1470-1479.
[http://dx.doi.org/10.1002/art.10294] [PMID: 12115176]
[153]
Boumpas, D.T.; Furie, R.; Manzi, S.; Illei, G.G.; Wallace, D.J.; Balow, J.E.; Vaishnaw, A.; Group, B.L.N.T. A short course of BG9588 (anti-CD40 ligand antibody) improves serologic activity and decreases hematuria in patients with proliferative lupus glomerulonephritis. Arthritis Rheum., 2003, 48(3), 719-727.
[http://dx.doi.org/10.1002/art.10856] [PMID: 12632425]
[154]
Henn, V.; Slupsky, J.R.; Gräfe, M.; Anagnostopoulos, I.; Förster, R.; Müller-Berghaus, G.; Kroczek, R.A. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature, 1998, 391(6667), 591-594.
[http://dx.doi.org/10.1038/35393] [PMID: 9468137]
[155]
Daikh, D.I.; Wofsy, D. Cutting edge: Reversal of murine lupus nephritis with CTLA4Ig and cyclophosphamide. J. Immunol., 2001, 166(5), 2913-2916.
[http://dx.doi.org/10.4049/jimmunol.166.5.2913] [PMID: 11207238]
[156]
Aringer, M.; Steiner, G.; Graninger, W.B.; Höfler, E.; Steiner, C.W.; Smolen, J.S. Effects of short-term infliximab therapy on autoantibodies in systemic lupus erythematosus. Arthritis Rheum., 2007, 56(1), 274-279.
[http://dx.doi.org/10.1002/art.22327] [PMID: 17195231]
[157]
Matsumura, R.; Umemiya, K.; Sugiyama, T.; Sueishi, M.; Umibe, T.; Ichikawa, K.; Yoshimura, M. Anti-tumor necrosis factor therapy in patients with difficult-to-treat lupus nephritis: A prospective series of nine patients. Clin. Exp. Rheumatol., 2009, 27(3), 416-421.
[PMID: 19604433]
[158]
Obermoser, G.; Pascual, V. The interferon-α signature of systemic lupus erythematosus. Lupus, 2010, 19(9), 1012-1019.
[http://dx.doi.org/10.1177/0961203310371161] [PMID: 20693194]
[159]
Yao, Y.; Richman, L.; Higgs, B.W.; Morehouse, C.A.; de los Reyes, M.; Brohawn, P.; Zhang, J.; White, B.; Coyle, A.J.; Kiener, P.A.; Jallal, B. Neutralization of interferon-α/β-inducible genes and downstream effect in a phase I trial of an anti-interferon-α monoclonal antibody in systemic lupus erythematosus. Arthritis Rheum., 2009, 60(6), 1785-1796.
[http://dx.doi.org/10.1002/art.24557] [PMID: 19479852]
[160]
Khamashta, M.; Merrill, J.T.; Werth, V.P.; Furie, R.; Kalunian, K.; Illei, G.G.; Drappa, J.; Wang, L.; Greth, W. Sifalimumab, an anti-interferon-α monoclonal antibody, in moderate to severe systemic lupus erythematosus: A randomised, double-blind, placebo-controlled study. Ann. Rheum. Dis., 2016, 75(11), 1909-1916.
[http://dx.doi.org/10.1136/annrheumdis-2015-208562] [PMID: 27009916]
[161]
Choy, E.H.; De Benedetti, F.; Takeuchi, T.; Hashizume, M.; John, M.R.; Kishimoto, T. Translating IL-6 biology into effective treatments. Nat. Rev. Rheumatol., 2020, 16(6), 335-345.
[http://dx.doi.org/10.1038/s41584-020-0419-z] [PMID: 32327746]
[162]
Liang, B.; Gardner, D.B.; Griswold, D.E.; Bugelski, P.J.; Song, X.Y.R. Anti-interleukin-6 monoclonal antibody inhibits autoimmune responses in a murine model of systemic lupus erythematosus. Immunology, 2006, 119(3), 296-305.
[http://dx.doi.org/10.1111/j.1365-2567.2006.02433.x] [PMID: 17067309]
[163]
Abani, O.; Abbas, A.; Abbas, F.; Abbas, M.; Abbasi, S.; Abbass, H.; Abbott, A.; Abdallah, N.; Abdelaziz, A.; Abdelfattah, M. Tocilizumab in patients admitted to hospital with COVID-19 (RECOVERY): A randomised, controlled, open-label, platform trial. Lancet, 2021, 397(10285), 1637-1645.
[http://dx.doi.org/10.1016/S0140-6736(21)00676-0] [PMID: 33933206]
[164]
Wang, X.; Wong, K.; Ouyang, W.; Rutz, S. Targeting IL-10 family cytokines for the treatment of human diseases. Cold Spring Harb. Perspect. Biol., 2019, 11(2), a028548.
[http://dx.doi.org/10.1101/cshperspect.a028548] [PMID: 29038121]
[165]
Corinti, S.; Albanesi, C.; la Sala, A.; Pastore, S.; Girolomoni, G. Regulatory activity of autocrine IL-10 on dendritic cell functions. J. Immunol., 2001, 166(7), 4312-4318.
[http://dx.doi.org/10.4049/jimmunol.166.7.4312] [PMID: 11254683]
[166]
Aletaha, D.; Landewe, R.; Karonitsch, T.; Bathon, J.; Boers, M.; Bombardier, C.; Bombardieri, S.; Choi, H.; Combe, B.; Dougados, M.; Emery, P.; Gomez-Reino, J.; Keystone, E.; Koch, G.; Kvien, T.K.; Martin-Mola, E.; Matucci-Cerinic, M.; Michaud, K.; O’dell, J.; Paulus, H.; Pincus, T.; Richards, P.; Simon, L.; Siegel, J.; Smolen, J.S.; Sokka, T.; Strand, V.; Tugwell, P.; van der Heijde, D.; van Riel, P.; Vlad, S.; van Vollenhoven, R.; Ward, M.; Weinblatt, M.; Wells, G.; White, B.; Wolfe, F.; Zhang, B.; Zink, A.; Felson, D. Reporting disease activity in clinical trials of patients with rheumatoid arthritis: EULAR/ACR collaborative recommendations. Arthritis Rheum., 2008, 59(10), 1371-1377.
[http://dx.doi.org/10.1002/art.24123] [PMID: 18821648]
[167]
Fedorak, R.N.; Gangl, A.; Elson, C.O.; Rutgeerts, P.; Schreiber, S.; Wild, G.; Hanauer, S.B.; Kilian, A.; Cohard, M.; LeBeaut, A.; Feagan, B. Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn’s disease. Gastroenterology, 2000, 119(6), 1473-1482.
[http://dx.doi.org/10.1053/gast.2000.20229] [PMID: 11113068]
[168]
Llorente, L.; Zou, W.; Levy, Y.; Richaud-Patin, Y.; Wijdenes, J.; Alcocer-Varela, J.; Morel-Fourrier, B.; Brouet, J.C.; Alarcon-Segovia, D.; Galanaud, P.; Emilie, D. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J. Exp. Med., 1995, 181(3), 839-844.
[http://dx.doi.org/10.1084/jem.181.3.839] [PMID: 7869046]
[169]
Sordé, L.; Spindeldreher, S.; Palmer, E.; Karle, A. Massive immune response against IVIg interferes with response against other antigens in mice: A new mode of action? PLoS One, 2017, 12(10), e0186046.
[http://dx.doi.org/10.1371/journal.pone.0186046] [PMID: 29023507]
[170]
Zandman-Goddard, G.; Blank, M.; Shoenfeld, Y. Intravenous immunoglobulins in systemic lupus erythematosus: From the bench to the bedside. Lupus, 2009, 18(10), 884-888.
[http://dx.doi.org/10.1177/0961203309106921] [PMID: 19671787]
[171]
Sthoeger, Z.M.; Dayan, M.; Tcherniack, A.; Green, L.; Toledo, S.; Segal, R.; Elkayam, O.; Mozes, E. Modulation of autoreactive responses of peripheral blood lymphocytes of patients with systemic lupus erythematosus by peptides based on human and murine anti-DNA autoantibodies. Clin. Exp. Immunol., 2003, 131(2), 385-392.
[http://dx.doi.org/10.1046/j.1365-2249.2003.02058.x] [PMID: 12562403]
[172]
Sthoeger, Z.M.; Sharabi, A.; Molad, Y.; Asher, I.; Zinger, H.; Dayan, M.; Mozes, E. Treatment of lupus patients with a tolerogenic peptide, hCDR1 (Edratide): Immunomodulation of gene expression. J. Autoimmun., 2009, 33(1), 77-82.
[http://dx.doi.org/10.1016/j.jaut.2009.03.009] [PMID: 19346102]
[173]
Blank, M.; Shoenfeld, Y. The story of the 16/6 idiotype and systemic lupus erythematosus. Isr. Med. Assoc. J., 2008, 10(1), 37-39.
[PMID: 18300569]
[174]
Sharabi, A.; Zinger, H.; Zborowsky, M.; Sthoeger, Z.M.; Mozes, E. A peptide based on the complementarity-determining region 1 of an autoantibody ameliorates lupus by up-regulating CD4 + CD25 + cells and TGF-β. Proc. Natl. Acad. Sci., 2006, 103(23), 8810-8815.
[http://dx.doi.org/10.1073/pnas.0603201103] [PMID: 16735466]
[175]
Parameswaran, R.; David, H.B.; Sharabi, A.; Zinger, H.; Mozes, E. B-cell activating factor (BAFF) plays a role in the mechanism of action of a tolerogenic peptide that ameliorates lupus. Clin. Immunol., 2009, 131(2), 223-232.
[http://dx.doi.org/10.1016/j.clim.2008.12.009] [PMID: 19188092]
[176]
Mauermann, N.; Sthoeger, Z.; Zinger, H.; Mozes, E. Amelioration of lupus manifestations by a peptide based on the complementarity determining region 1 of an autoantibody in severe combined immunodeficient (SCID) mice engrafted with peripheral blood lymphocytes of systemic lupus erythematosus (SLE) patients. Clin. Exp. Immunol., 2004, 137(3), 513-520.
[http://dx.doi.org/10.1111/j.1365-2249.2004.02559.x] [PMID: 15320900]
[177]
Mosca, M.; Baldini, C.; Bombardieri, S. LJP-394 (abetimus sodium) in the treatment of systemic lupus erythematosus. Expert Opin. Pharmacother., 2007, 8(6), 873-879.
[http://dx.doi.org/10.1517/14656566.8.6.873] [PMID: 17425481]
[178]
Talotta, R.; Atzeni, F.; Laska, M.J. Therapeutic peptides for the treatment of systemic lupus erythematosus: A place in therapy. Expert Opin. Investig. Drugs, 2020, 29(8), 845-867.
[http://dx.doi.org/10.1080/13543784.2020.1777983] [PMID: 32500750]
[179]
Ogura, S; Karasawa, K; Ono, W; Ito, A; Seki, M; Yamaguchi, Y; Kamizawa, M; Tosaka, M; Ushio, Y; Sugiura, N Successful treatment with belimumab in a patient with refractory systemic lupus erythematosus after initiation of hemodialysis: Considering the synergistic effect of belimumab and immunological burn-out phenomenon in end stage renal disease patients on hemodialysis. Blood Purif., 2020, 51(2), 182-188.
[180]
Stummvoll, G.H. Immunoadsorption (IAS) for systemic lupus erythematosus. Lupus, 2011, 20(2), 115-119.
[http://dx.doi.org/10.1177/0961203310389487] [PMID: 21303827]
[181]
Choi, M.; Hahn, J.; Malspeis, S.; Stevens, E.; Karlson, E.; Sparks, J.; Yoshida, K.; Kubzansky, L.; Costenbader, K. A combination of healthy lifestyle behaviors reduce risk of incident systemic lupus erythematosus in the nurses’ health studies. Arthritis Rheumatol., 2020, 72(S10)
[182]
Obrișcă, B.; Sorohan, B.; Tuță, L.; Ismail, G. Advances in lupus nephritis pathogenesis: From bench to bedside. Int. J. Mol. Sci., 2021, 22(7), 3766.
[http://dx.doi.org/10.3390/ijms22073766] [PMID: 33916456]
[183]
Wise, L.M.; Stohl, W. Belimumab and rituximab in systemic lupus erythematosus: A tale of two B cell-targeting agents. Front. Med., 2020, 7, 303.
[http://dx.doi.org/10.3389/fmed.2020.00303] [PMID: 32695790]
[184]
Hamawy, M.M. Molecular actions of calcineurin inhibitors. Drug News Perspect., 2003, 16(5), 277-282.
[http://dx.doi.org/10.1358/dnp.2003.16.5.829315] [PMID: 12942158]
[185]
Costedoat-Chalumeau, N.; Dunogué, B.; Morel, N.; Le Guern, V.; Guettrot-Imbert, G. Hydroxychloroquine: A multifaceted treatment in lupus. Presse Med., 2014, 43(6), e167-e180.
[http://dx.doi.org/10.1016/j.lpm.2014.03.007] [PMID: 24855048]
[186]
Decker, J.L.; Klippel, J.H.; Plotz, P.H.; Steinberg, A.D. Cyclophosphamide or azathioprine in lupus glomerulonephritis. A controlled trial: Results at 28 months. Ann. Intern. Med., 1975, 83(5), 606-615.
[http://dx.doi.org/10.7326/0003-4819-83-5-606] [PMID: 1106278]

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