Biological Clock Perspective in Rheumatoid Arthritis.
Biological clock
Immune system
Neuroendocrine system
Rheumatoid arthritis
Journal
Inflammation
ISSN: 1573-2576
Titre abrégé: Inflammation
Pays: United States
ID NLM: 7600105
Informations de publication
Date de publication:
10 Aug 2024
10 Aug 2024
Historique:
received:
17
02
2024
accepted:
01
08
2024
revised:
13
06
2024
medline:
10
8
2024
pubmed:
10
8
2024
entrez:
10
8
2024
Statut:
aheadofprint
Résumé
Rheumatoid arthritis (RA) is a chronic autoimmune disease characterized by systemic polyarticular pain, and its main pathological features include inflammatory cell infiltration, synovial fibroblast proliferation, and cartilage erosion. Immune cells, synovial cells and neuroendocrine factors play pivotal roles in the pathophysiological mechanism underlying rheumatoid arthritis. Biological clock genes regulate immune cell functions, which is linked to rhythmic changes in arthritis pathology. Additionally, the interaction between biological clock genes and neuroendocrine factors is also involved in rhythmic changes in rheumatoid arthritis. This review provides an overview of the contributions of circadian rhythm genes to RA pathology, including their interaction with the immune system and their involvement in regulating the secretion and function of neuroendocrine factors. A molecular understanding of the role of the circadian rhythm in RA may offer insights for effective disease management.
Identifiants
pubmed: 39126449
doi: 10.1007/s10753-024-02120-4
pii: 10.1007/s10753-024-02120-4
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
ID : 82102533
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Conigliaro, P., A. D’Antonio, S. Pinto, et al. 2020. Autoimmune thyroid disorders and rheumatoid arthritis: A bidirectional interplay. Autoimmunity Reviews 19 (6): 102529.
pubmed: 32234405
doi: 10.1016/j.autrev.2020.102529
Aletaha, D., and J.S. Smolen. 2018. Diagnosis and Management of Rheumatoid Arthritis: A Review. JAMA 320: 1360–1372.
pubmed: 30285183
doi: 10.1001/jama.2018.13103
Smolen, J.S., D. Aletaha, and I.B. McInnes. 2016. Rheumatoid arthritis. Lancet 388: 2023–2038.
pubmed: 27156434
doi: 10.1016/S0140-6736(16)30173-8
Guo, Q., Y. Wang, D. Xu, J. Nossent, N.J. Pavlos, and J. Xu. 2018. Rheumatoid arthritis: Pathological mechanisms and modern pharmacologic therapies. Bone Res 6: 15.
pubmed: 29736302
pmcid: 5920070
doi: 10.1038/s41413-018-0016-9
Deane, K.D., M.K. Demoruelle, L.B. Kelmenson, K.A. Kuhn, J.M. Norris, and V.M. Holers. 2017. Genetic and environmental risk factors for rheumatoid arthritis. Best Practice & Research Clinical Rheumatology 31 (1): 3–18.
doi: 10.1016/j.berh.2017.08.003
Van der Woude, D., J.J. Houwing-Duistermaat, R.E. Toes, et al. 2009. Quantitative heritability of anti-citrullinated protein antibody-positive and anti-citrullinated protein antibody-negative rheumatoid arthritis. Arthritis and Rheumatism 60 (4): 916–923.
pubmed: 19333951
doi: 10.1002/art.24385
Messemaker, T.C., T.W. Huizinga, and F. Kurreeman. 2015. Immunogenetics of rheumatoid arthritis: Understanding functional implications. Journal of Autoimmunity 64: 74–81.
pubmed: 26215034
doi: 10.1016/j.jaut.2015.07.007
Pivovarova-Ramich, O., H.G. Zimmermann, and F. Paul. 2023. Multiple sclerosis and circadian rhythms: Can diet act as a treatment? Acta Psychologica 237 (4): e13939.
Downton, P., J.O. Early, and J.E. Gibbs. 2020. Circadian rhythms in adaptive immunity. Immunology 161 (4): 268–277.
pubmed: 31837013
Angelousi, A., N. Nasiri-Ansari, E. Spilioti, et al. 2018. Altered expression of circadian clock genes in polyglandular autoimmune syndrome type III. Endocrine 59 (1): 109–119.
pubmed: 28884339
doi: 10.1007/s12020-017-1407-1
Early, J.O., D. Menon, C.A. Wyse, et al. 2018. Circadian clock protein BMAL1 regulates IL-1β in macrophages via NRF2. Proc Natl Acad Sci U S A 115 (36): E8460–E8468.
pubmed: 30127006
pmcid: 6130388
doi: 10.1073/pnas.1800431115
Wu, Y., B. Tao, T. Zhang, Y. Fan, and R. Mao. 2019. Pan-Cancer Analysis Reveals Disrupted Circadian Clock Associates With T Cell Exhaustion. Frontiers in Immunology 10: 2451.
pubmed: 31708917
pmcid: 6821711
doi: 10.3389/fimmu.2019.02451
Gray, K.J., and J.E. Gibbs. 2022. Adaptive immunity, chronic inflammation and the clock. Semin Immunopathol 44 (2): 209–224.
pubmed: 35233691
pmcid: 8901482
doi: 10.1007/s00281-022-00919-7
Ye, H., H. Weng, Y. Xu, et al. 2022. Efectiveness and safety of aerobic exercise for rheumatoid arthritis: A systematic review and meta-analysis of randomized controlled trials. BMC Sports Science, Medicine and Rehabilitation 14 (1): 17.
pubmed: 35123568
pmcid: 8818158
doi: 10.1186/s13102-022-00408-2
Aletaha, D., T. Neogi, A.J. Silman, et al. 2010. Rheumatoid arthritis classifcation criteria: An American College of Rheumatology/European League Against Rheumatism collaborative initiative. Annals of the Rheumatic Diseases 69: 1580–1588.
pubmed: 20699241
doi: 10.1136/ard.2010.138461
Arvidson, N.G., B. Gudbjörnsson, L. Elfman, A.C. Rydén, T.H. Tötterman, and R. Hällgren. 1994. Circadian rhythm of serum interleukin-6 in rheumatoid arthritis. Annals of the Rheumatic Diseases 53 (8): 521–524.
pubmed: 7944637
pmcid: 1005392
doi: 10.1136/ard.53.8.521
Perry, M.G., J.R. Kirwan, D.S. Jessop, and L.P. Hunt. 2009. Overnight variations in cortisol, interleukin 6, tumour necrosis factor alpha and other cytokines in people with rheumatoid arthritis. Annals of the Rheumatic Diseases 68 (1): 63–68.
pubmed: 18375536
doi: 10.1136/ard.2007.086561
Sulli, A., G.J. Maestroni, B. Villaggio, E. Hertens, C. Craviotto, C. Pizzorni, M. Briata, B. Seriolo, and M. Cutolo. 2002. Melatonin serum levels in rheumatoid arthritis. Annals. New York Academy of Sciences 966: 276–283.
doi: 10.1111/j.1749-6632.2002.tb04227.x
Butler, T., J.R. Maidstone, K.M. Rutter, T.J. McLaughlin, W.D. Ray, and E.J. Gibbs. 2023. The Associations of Chronotype and Shift Work With Rheumatoid Arthritis. Journal of Biological Rhythms 38 (5): 510–518.
pubmed: 37382359
pmcid: 10475206
doi: 10.1177/07487304231179595
Puttonen, S., T. Oksanen, J. Vahtera, J. Pentti, M. Virtanen, P. Salo, and M. Kivimaki. 2010. Is shift work a risk factor for rheumatoid arthritis? The Finnish Public Sector study. Annals of the Rheumatic Diseases 69: 779–780.
pubmed: 20237124
doi: 10.1136/ard.2008.099184
Gibbs, J.E., and D.W. Ray. 2013. The role of the circadian clock in rheumatoid arthritis. Arthritis Research & Therapy 15 (1): 205.
doi: 10.1186/ar4146
Ralph, M.R., R.G. Foster, F.C. Davis, and M. Menaker. 1990. Transplanted suprachiasmatic nucleus determines circadian period. Science 247: 975–978.
pubmed: 2305266
doi: 10.1126/science.2305266
Paul, J.R., J.A. Davis, L.K. Goode, et al. 2020. Circadian regulation of membrane physiology in neural oscillators throughout the brain. European Journal of Neuroscience 51: 109–138.
pubmed: 30633846
doi: 10.1111/ejn.14343
Meredith, A.L., S.W. Wiler, B.H. Miller, et al. 2006. BK calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nature Neuroscience 9: 1041–1049.
pubmed: 16845385
pmcid: 2909323
doi: 10.1038/nn1740
Bass, J., and M.A. Lazar. 2016. Circadian time signatures of fitness and disease. Science 354: 994–999.
pubmed: 27885004
doi: 10.1126/science.aah4965
Cermakian, N., and P. Sassone-Corsi. 2000. Multilevel regulation of the circadian clock. Nature Reviews Molecular Cell Biology 1 (1): 59–67.
pubmed: 11413490
doi: 10.1038/35036078
Gamble, K.L., R. Berry, S.J. Frank, et al. 2014. Circadian clock control of endocrine factors. Nature Reviews. Endocrinology 10 (8): 466–475.
pubmed: 24863387
pmcid: 4304769
doi: 10.1038/nrendo.2014.78
Kizaki, T., S. Sato, K. Shirato, et al. 2015. Effect of circadian rhythm on clinical and pathophysiological conditions and inflammation. Critical Reviews in Immunology 35 (4): 261–275.
pubmed: 26757391
doi: 10.1615/CritRevImmunol.2015014925
Albrecht, U. 2012. Timing to perfection: The biology of central and peripheral circadian clocks. Neuron 74 (2): 246–260.
pubmed: 22542179
doi: 10.1016/j.neuron.2012.04.006
Olkkonen, J., V.P. Kouri, E. Kuusela, et al. 2017. DEC2 blocks the effect of the ARNTL2/ NPAS2 dimer on the expression of PER3 and DBP. Journal of Circadian Rhythms 15: 6.
pubmed: 30210560
pmcid: 5624067
doi: 10.5334/jcr.149
King, D.P., Y. Zhao, A.M. Sangoram, et al. 1997. Positional cloning of the mouse circadian clock gene. Cell 89: 641–653.
pubmed: 9160755
pmcid: 3815553
doi: 10.1016/S0092-8674(00)80245-7
Patke, A., M.W. Young, and S. Axelrod. 2020. Molecular mechanisms and physiological importance of circadian rhythms. Nature Reviews Molecular Cell Biology 21: 67–84.
pubmed: 31768006
doi: 10.1038/s41580-019-0179-2
Koike, N., S.-H. Yoo, H.-C. Huang, et al. 2012. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338: 349–354.
pubmed: 22936566
pmcid: 3694775
doi: 10.1126/science.1226339
Place, D.E., and T.D. Kanneganti. 2020. The innate immune system and cell death in autoinflammatory and autoimmune disease. Current Opinion in Immunology 67: 95–105.
pubmed: 33242752
doi: 10.1016/j.coi.2020.10.013
Szekanecz, Z., I.B. McInnes, G. Schett, S. Szamosi, S. Benkő, and G. Szűcs. 2021. Autoinflammation and autoimmunity across rheumatic and musculoskeletal diseases. Nature Reviews Rheumatology 17 (10): 585–595.
pubmed: 34341562
doi: 10.1038/s41584-021-00652-9
Scherer, H.U., T. Häupl, and G.R. Burmester. 2020. The etiology of rheumatoid arthritis. Journal of Autoimmunity 110: 102400.
pubmed: 31980337
doi: 10.1016/j.jaut.2019.102400
Hemmer, B., M. Kerschensteiner, and T. Korn. 2015. Role of the innate and adaptive immune responses in the course of multiple sclerosis. Lancet Neurology 14 (4): 406–419.
pubmed: 25792099
doi: 10.1016/S1474-4422(14)70305-9
Kucuksezer, U.C., E. Aktas Cetin, F. Esen, et al. 2021. The Role of Natural Killer Cells in Autoimmune Diseases. Frontiers in Immunology 12: 622306.
pubmed: 33717125
pmcid: 7947192
doi: 10.3389/fimmu.2021.622306
Toubi, E., and Z. Vadasz. 2019. Innate immune-responses and their role in driving autoimmunity. Autoimmunity Reviews 18 (3): 306–311.
pubmed: 30639645
doi: 10.1016/j.autrev.2018.10.005
Litman, G.W., and M.D. Cooper. 2007. Why study the evolution of immunity? Nature Immunology 8 (6): 547–548.
pubmed: 17514203
pmcid: 3684968
doi: 10.1038/ni0607-547
Janeway, C.A., Jr., and R. Medzhitov. 2002. Innate immune recognition. Annual Review of Immunology 20: 197–216.
pubmed: 11861602
doi: 10.1146/annurev.immunol.20.083001.084359
Hand, L.E., T.W. Hopwood, S.H. Dickson, et al. 2016. The circadian clock regulates inflammatory arthritis. The FASEB Journal 30 (11): 3759–3770.
pubmed: 27488122
pmcid: 5067252
doi: 10.1096/fj.201600353R
Pham, L., L. Baiocchi, L. Kennedy, et al. 2021. The interplay between mast cells, pineal gland, and circadian rhythm: Links between histamine, melatonin, and inflammatory mediators. Journal of Pineal Research 70 (2): e12699.
pubmed: 33020940
doi: 10.1111/jpi.12699
Christ, P., A.S. Sowa, O. Froy, and A. Lorentz. 2018. The Circadian Clock Drives Mast Cell Functions in Allergic Reactions. Frontiers in Immunology 9: 7.
doi: 10.3389/fimmu.2018.01526
Martínez de Toda, I., C. Vida, E. Díaz-Del Cerro, and M. De la Fuente. 2021. The Immunity Clock. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 76 (11): 1939–1945.
pubmed: 33979432
doi: 10.1093/gerona/glab136
Arjona, A., and D.K. Sarkar. 2006. Evidence supporting a circadian control of natural killer cell function. Brain, Behavior, and Immunity 20 (5): 469–476.
pubmed: 16309885
doi: 10.1016/j.bbi.2005.10.002
Gibbs, J.E., J. Blaikley, S. Beesley, et al. 2012. The nuclear receptor REV-ERBα mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proceedings of the National Academy of Sciences U S A 109 (2): 582–587.
doi: 10.1073/pnas.1106750109
Keller, M., J. Mazuch, U. Abraham, et al. 2009. A circadian clock in macrophages controls inflammatory immune responses. Proceedings of the National Academy of Sciences U S A 106 (50): 21407–21412.
doi: 10.1073/pnas.0906361106
Cao, Q., X. Zhao, J. Bai, et al. 2017. Circadian clock cryptochrome proteins regulate autoimmunity. Proceedings of the National Academy of Sciences U S A 114 (47): 12548–12553.
doi: 10.1073/pnas.1619119114
Hirose, M., A. Leliavski, L.V.M. de Assis, et al. 2024. Chronic Inflammation Disrupts Circadian Rhythms in Splenic CD4+ and CD8+ T Cells in Mice. Cells 13 (2): 151.
pubmed: 38247842
pmcid: 10814081
doi: 10.3390/cells13020151
Constantinides, M.G., B.D. McDonald, P.A. Verhoef, and A. Bendelac. 2014. A committed precursor to innate lymphoid cells. Nature 508 (7496): 397–401.
pubmed: 24509713
pmcid: 4003507
doi: 10.1038/nature13047
Lim, A.I., Y. Li, S. Lopez-Lastra, et al. 2017. Systemic Human ILC Precursors Provide a Substrate for Tissue ILC Differentiation. Cell 168 (6): 1086-1100.e10.
pubmed: 28283063
doi: 10.1016/j.cell.2017.02.021
Yamin, R., O. Berhani, H. Peleg, et al. 2019. High percentages and activity of synovial fluid NK cells present in patients with advanced stage active Rheumatoid Arthritis. Science and Reports 9 (1): 1351.
doi: 10.1038/s41598-018-37448-z
Arjona, A., N. Boyadjieva, and D.K. Sarkar. 2004. Circadian rhythms of granzyme B, perforin, IFN-gamma and NK cell cytolytic activity in the spleen: Effects of chronic ethanol. The Journal of Immunology 172 (5): 2811–2817.
pubmed: 14978081
doi: 10.4049/jimmunol.172.5.2811
Arjona, A., and D.K. Sarkar. 2005. Circadian oscillations of clock genes, cytolytic factors, and cytokines in rat NK cells. The Journal of Immunology 174 (12): 7618–7624.
pubmed: 15944262
doi: 10.4049/jimmunol.174.12.7618
Logan, R.W., O. Wynne, D. Levitt, D. Price, and D.K. Sarkar. 2013. Altered circadian expression of cytokines and cytolytic factors in splenic natural killer cells of Per1(-/-) mutant mice. Journal of Interferon and Cytokine Research 33 (3): 108–114.
pubmed: 23402528
pmcid: 3595954
doi: 10.1089/jir.2012.0092
Adrover, J.M., C. Del Fresno, G. Crainiciuc, et al. 2019. A Neutrophil Timer Coordinates Immune Defense and Vascular Protection. Immunity 50 (2): 390-402.e10.
pubmed: 30709741
doi: 10.1016/j.immuni.2019.01.002
Aroca-Crevillén, A., J.M. Adrover, and A. Hidalgo. 2020. Circadian Features of Neutrophil Biology. Frontiers in Immunology 11: 576.
pubmed: 32346378
pmcid: 7169427
doi: 10.3389/fimmu.2020.00576
Haimovich, B., J. Calvano, A.D. Haimovich, et al. 2010. In vivo endotoxin synchronizes and suppresses clock gene expression in human peripheral blood leukocytes. Critical Care Medicine 38 (3): 751–758.
pubmed: 20081528
doi: 10.1097/CCM.0b013e3181cd131c
Casanova-Acebes, M., C. Pitaval, L.A. Weiss, et al. 2013. Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell 153 (5): 1025–1035.
pubmed: 23706740
pmcid: 4128329
doi: 10.1016/j.cell.2013.04.040
Zhang, D., G. Chen, D. Manwani, et al. 2015. Neutrophil ageing is regulated by the microbiome. Nature 525 (7570): 528–532.
pubmed: 26374999
pmcid: 4712631
doi: 10.1038/nature15367
Sennels, H.P., H.L. Jørgensen, A.L. Hansen, et al. 2011. Diurnal variation of hematology parameters in healthy young males: The Bispebjerg study of diurnal variations. Scandinavian Journal of Clinical and Laboratory Investigation 71 (7): 532–541.
pubmed: 21988588
doi: 10.3109/00365513.2011.602422
Gibbs, J., L. Ince, L. Matthews, et al. 2014. An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nature Medicine 20 (8): 919–926.
pubmed: 25064128
pmcid: 4268501
doi: 10.1038/nm.3599
Wijbrandts, C.A., C.E. Vergunst, J.J. Haringman, et al. 2007. Absence of changes in the number of synovial sublining macrophages after ineffective treatment for rheumatoid arthritis: Implications for use of synovial sublining macrophages as a biomarker. Arthritis and Rheumatism 56 (11): 3869–3871.
pubmed: 17968928
doi: 10.1002/art.22964
Huang, Q.Q., R. Doyle, S.Y. Chen, et al. 2021. Critical role of synovial tissue-resident macrophage niche in joint homeostasis and suppression of chronic inflammation. Science Advances 7 (2): eabd0515.
pubmed: 33523968
pmcid: 7787490
doi: 10.1126/sciadv.abd0515
Alivernini, S., L. MacDonald, A. Elmesmari, et al. 2020. Distinct synovial tissue macrophage subsets regulate inflammation and remission in rheumatoid arthritis. Nature Medicine 26 (8): 1295–1306.
pubmed: 32601335
doi: 10.1038/s41591-020-0939-8
Chen, S., K.K. Fuller, J.C. Dunlap, and J.J. Loros. 2020. A Pro- and Anti-inflammatory Axis Modulates the Macrophage Circadian Clock. Frontiers in Immunology 11: 867.
pubmed: 32477351
pmcid: 7240016
doi: 10.3389/fimmu.2020.00867
Hong, H., Y.M. Cheung, X. Cao, Y. Wu, C. Li, and X.Y. Tian. 2021. REV-ERBα agonist SR9009 suppresses IL-1β production in macrophages through BMAL1-dependent inhibition of inflammasome. Biochemical Pharmacology 192: 114701.
pubmed: 34324866
doi: 10.1016/j.bcp.2021.114701
Croft, A.P., J. Campos, K. Jansen, et al. 2019. Distinct fibroblast subsets drive inflammation and damage in arthritis. Nature 570 (7760): 246–251.
pubmed: 31142839
pmcid: 6690841
doi: 10.1038/s41586-019-1263-7
Haringman, J.J., D.M. Gerlag, A.H. Zwinderman, et al. 2005. Synovial tissue macrophages: A sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Annals of the Rheumatic Diseases 64 (6): 834–838.
pubmed: 15576415
doi: 10.1136/ard.2004.029751
Degboé, Y., B. Rauwel, M. Baron, et al. 2019. Polarization of Rheumatoid Macrophages by TNF Targeting Through an IL-10/STAT3 Mechanism. Frontiers in Immunology 10: 3.
pubmed: 30713533
pmcid: 6345709
doi: 10.3389/fimmu.2019.00003
Prendergast, C.T., A. Patakas, S. Al-Khabouri, et al. 2018. Visualising the interaction of CD4 T cells and DCs in the evolution of inflammatory arthritis. Annals of the Rheumatic Diseases 77 (4): 579–588.
pubmed: 29358281
doi: 10.1136/annrheumdis-2017-212279
Wehr, P., H. Purvis, S.C. Law, and R. Thomas. 2019. Dendritic cells, T cells and their interaction in rheumatoid arthritis. Clinical and Experimental Immunology 196 (1): 12–27.
pubmed: 30589082
pmcid: 6422662
doi: 10.1111/cei.13256
Hu, X.X., Y.J. Wu, J. Zhang, and W. Wei. 2019. T-cells interact with B cells, dendritic cells, and fibroblast-like synoviocytes as hub-like key cells in rheumatoid arthritis. International Immunopharmacology 70: 428–434.
pubmed: 30856393
doi: 10.1016/j.intimp.2019.03.008
Suwa, Y., Y. Nagafuchi, S. Yamada, and K. Fujio. 2023. The role of dendritic cells and their immunometabolism in rheumatoid arthritis. Frontiers in Immunology 14: 1161148.
pubmed: 37251399
pmcid: 10213288
doi: 10.3389/fimmu.2023.1161148
Nobis, C.C., G. Dubeau Laramée, L. Kervezee, D. Maurice De Sousa, N. Labrecque, and N. Cermakian. 2019. The circadian clock of CD8 T cells modulates their early response to vaccination and the rhythmicity of related signaling pathways. Proc Natl Acad Sci U S A 116 (40): 20077–20086.
pubmed: 31527231
pmcid: 6778233
doi: 10.1073/pnas.1905080116
Holtkamp, S.J., L.M. Ince, C. Barnoud, et al. 2021. Circadian clocks guide dendritic cells into skin lymphatics. Nature Immunology 22 (11): 1375–1381.
pubmed: 34663979
pmcid: 8553624
doi: 10.1038/s41590-021-01040-x
Lee, D.S.W., O.L. Rojas, and J.L. Gommerman. 2021. B cell depletion therapies in autoimmune disease: Advances and mechanistic insights. Nature Reviews. Drug Discovery 20 (3): 179–199.
pubmed: 33324003
doi: 10.1038/s41573-020-00092-2
Dang, V.D., A.L. Stefanski, A.C. Lino, and T. Dörner. 2022. B- and Plasma Cell Subsets in Autoimmune Diseases: Translational Perspectives. Journal of Investigative Dermatology 142 (3 Pt B): 811–822.
pubmed: 34955289
doi: 10.1016/j.jid.2021.05.038
Barnas, J.L., R.J. Looney, and J.H. Anolik. 2019. B cell targeted therapies in autoimmune disease. Current Opinion in Immunology 61: 92–99.
pubmed: 31733607
pmcid: 6982404
doi: 10.1016/j.coi.2019.09.004
Li, J., M. Zhao, W. Luo, J. Huang, B. Zhao, and Z. Zhou. 2023. B cell metabolism in autoimmune diseases: Signaling pathways and interventions. Frontiers in Immunology 14: 1232820.
pubmed: 37680644
pmcid: 10481957
doi: 10.3389/fimmu.2023.1232820
Haselmayer, P., M. Camps, L. Liu-Bujalski, et al. 2019. Efficacy and Pharmacodynamic Modeling of the BTK Inhibitor Evobrutinib in Autoimmune Disease Models. The Journal of Immunology 202 (10): 2888–2906.
pubmed: 30988116
pmcid: 6500888
doi: 10.4049/jimmunol.1800583
Nakken, B., L.A. Munthe, Y.T. Konttinen, et al. 2011. B-cells and their targeting in rheumatoid arthritis–current concepts and future perspectives. Autoimmunity Reviews 11 (1): 28–34.
pubmed: 21777703
doi: 10.1016/j.autrev.2011.06.010
Ia, K., A. Saxena, K.S. Nandakumar, et al. 2015. B-cell epitope spreading and inflammation in a mouse model of arthritis is associated with a deficiency in reactive oxygen species production. European Journal of Immunology 45 (8): 2243–2251.
doi: 10.1002/eji.201545518
Humby, F., M. Lewis, N. Ramamoorthi, et al. 2019. Synovial cellular and molecular signatures stratify clinical response to csDMARD therapy and predict radiographic progression in early rheumatoid arthritis patients. Annals of the Rheumatic Diseases 78 (6): 761–772.
pubmed: 30878974
doi: 10.1136/annrheumdis-2018-214539
Kavanaugh, A., S. Rosengren, S.J. Lee, et al. 2008. Assessment of rituximab’s immunomodulatory synovial effects (ARISE trial). 1: clinical and synovial biomarker results. Annals of the Rheumatic Diseases 67 (3): 402–408.
pubmed: 17644541
doi: 10.1136/ard.2007.074229
Silver, A.C., A. Arjona, M.E. Hughes, M.N. Nitabach, and E. Fikrig. 2012. Circadian expression of clock genes in mouse macrophages, dendritic cells, and B cells. Brain, Behavior, and Immunity 26 (3): 407–413.
pubmed: 22019350
doi: 10.1016/j.bbi.2011.10.001
Hemmers, S., and A.Y. Rudensky. 2015. The Cell-Intrinsic Circadian Clock Is Dispensable for Lymphocyte Differentiation and Function. Cell Reports 11 (9): 1339–1349.
pubmed: 26004187
doi: 10.1016/j.celrep.2015.04.058
Liu, J.L., C.Y. Wang, T.Y. Cheng, et al. 2021. Circadian Clock Disruption Suppresses PDL1+ Intraepithelial B Cells in Experimental Colitis and Colitis-Associated Colorectal Cancer. Cell Mol Gastroenterol Hepatolx 12 (1): 251–276.
doi: 10.1016/j.jcmgh.2021.02.008
Levine, A.G., A. Mendoza, S. Hemmers, et al. 2017. Stability and function of regulatory T cells expressing the transcription factor T-bet. Nature 546 (7658): 421–425.
pubmed: 28607488
pmcid: 5482236
doi: 10.1038/nature22360
Sawant, D.V., H. Yano, M. Chikina, et al. 2019. Adaptive plasticity of IL-10+ and IL-35+ Treg cells cooperatively promotes tumor T cell exhaustion. Nature Immunology 20 (6): 724–735.
pubmed: 30936494
pmcid: 6531353
doi: 10.1038/s41590-019-0346-9
Almeida, A.R., B. Rocha, A.A. Freitas, and C. Tanchot. 2005. Homeostasis of T cell numbers: From thymus production to peripheral compartmentalization and the indexation of regulatory T cells. Seminars in Immunology 17 (3): 239–249.
pubmed: 15826829
doi: 10.1016/j.smim.2005.02.002
Maggi, E., L. Cosmi, F. Liotta, P. Romagnani, S. Romagnani, and F. Annunziato. 2005. Thymic regulatory T cells. Autoimmunity Reviews 4 (8): 579–586.
pubmed: 16214099
doi: 10.1016/j.autrev.2005.04.010
Minaduola, M., A. Aili, Y. Bao, Z. Peng, Q. Ge, and R. Jin. 2022. The circadian clock sets a spatial-temporal window for recent thymic emigrants. Immunology and Cell Biology 100 (9): 731–741.
pubmed: 36030488
doi: 10.1111/imcb.12582
Lang, V., S. Ferencik, B. Ananthasubramaniam, A. Kramer, and B. Maier. 2021. Susceptibility rhythm to bacterial endotoxin in myeloid clock-knockout mice. eLife 10: e62469.
pubmed: 34661529
pmcid: 8598165
doi: 10.7554/eLife.62469
Sutton, C.E., C.M. Finlay, M. Raverdeau, et al. 2017. Loss of the molecular clock in myeloid cells exacerbates T cell-mediated CNS autoimmune disease. Nature Communications 8 (1): 1923.
pubmed: 29234010
pmcid: 5727202
doi: 10.1038/s41467-017-02111-0
Druzd, D., O. Matveeva, L. Ince, et al. 2017. Lymphocyte Circadian Clocks Control Lymph Node Trafficking and Adaptive Immune Responses. Immunity 46 (1): 120–132.
pubmed: 28087238
pmcid: 5263259
doi: 10.1016/j.immuni.2016.12.011
Hand, L.E., K.J. Gray, S.H. Dickson, et al. 2020. Regulatory T cells confer a circadian signature on inflammatory arthritis. Nature Communications 11 (1): 1658.
pubmed: 32245954
pmcid: 7125185
doi: 10.1038/s41467-020-15525-0
Yang, J., M.S. Sundrud, J. Skepner, and T. Yamagata. 2014. Targeting Th17 cells in autoimmune diseases. Trends in Pharmacological Sciences 35 (10): 493–500.
pubmed: 25131183
doi: 10.1016/j.tips.2014.07.006
Hall, J.A., M. Pokrovskii, L. Kroehling, et al. 2022. Transcription factor RORα enforces stability of the Th17 cell effector program by binding to a Rorc cis-regulatory element. Immunity 55 (11): 2027-2043.e9.
pubmed: 36243007
pmcid: 9757081
doi: 10.1016/j.immuni.2022.09.013
Kumar, R., A.L. Theiss, and K. Venuprasad. 2021. RORγt protein modifications and IL-17-mediated inflammation. Trends in Immunology 42 (11): 1037–1050.
pubmed: 34635393
pmcid: 8556362
doi: 10.1016/j.it.2021.09.005
Chang, C., C.S. Loo, X. Zhao, et al. 2019. The nuclear receptor REV-ERBα modulates Th17 cell-mediated autoimmune disease. Proc Natl Acad Sci U S A 116 (37): 18528–18536.
pubmed: 31455731
pmcid: 6744854
doi: 10.1073/pnas.1907563116
Amir, M., S. Chaudhari, R. Wang, et al. 2018. REV-ERBα Regulates TH17 Cell Development and Autoimmunity. Cell Reports 25 (13): 3733-3749.e8.
pubmed: 30590045
doi: 10.1016/j.celrep.2018.11.101
Bartok, B., and G.S. Firestein. 2010. Fibroblast-like synoviocytes: Key effector cells in rheumatoid arthritis. Immunological Reviews 233 (1): 233–255.
pubmed: 20193003
pmcid: 2913689
doi: 10.1111/j.0105-2896.2009.00859.x
Falconer, J., A.N. Murphy, S.P. Young, et al. 2018. Review: Synovial Cell Metabolism and Chronic Inflammation in Rheumatoid Arthritis. Arthritis & Rhematology 70 (7): 984–999.
doi: 10.1002/art.40504
Chijimatsu, R., and T. Saito. 2019. Mechanisms of synovial joint and articular cartilage development. Cellular and Molecular Life Sciences 76 (20): 3939–3952.
pubmed: 31201464
pmcid: 11105481
doi: 10.1007/s00018-019-03191-5
Tu, J., W. Hong, P. Zhang, X. Wang, H. Körner, and W. Wei. 2018. Ontology and Function of Fibroblast-Like and Macrophage-Like Synoviocytes: How Do They Talk to Each Other and Can They Be Targeted for Rheumatoid Arthritis Therapy? Frontiers in Immunology 9: 1467.
pubmed: 29997624
pmcid: 6028561
doi: 10.3389/fimmu.2018.01467
Feng, L.J., T.C. Jiang, C.Y. Zhou, et al. 2014. Activated macrophage-like synoviocytes are resistant to endoplasmic reticulum stress-induced apoptosis in antigen-induced arthritis. Inflammation Research 63 (5): 335–346.
pubmed: 24468888
doi: 10.1007/s00011-013-0705-1
Yoshida, K., A. Nakai, K. Kaneshiro, et al. 2018. TNF-α induces expression of the circadian clock gene Bmal1 via dual calcium-dependent pathways in rheumatoid synovial cells. Biochemical and Biophysical Research Communications 495 (2): 1675–1680.
pubmed: 29217191
doi: 10.1016/j.bbrc.2017.12.015
Haas, S., and R.H. Straub. 2012. Disruption of rhythms of molecular clocks in primary synovial fibroblasts of patients with osteoarthritis and rheumatoid arthritis, role of IL-1β/TNF. Arthritis Research & Therapy 14 (3): R122.
doi: 10.1186/ar3852
Hand, L.E., S.H. Dickson, A.J. Freemont, D.W. Ray, and J.E. Gibbs. 2019. The circadian regulator Bmal1 in joint mesenchymal cells regulates both joint development and inflammatory arthritis. Arthritis Research & Therapy 21 (1): 5.
doi: 10.1186/s13075-018-1770-1
Yoshida, K., A. Hashiramoto, T. Okano, et al. 2013. TNF-α modulates expression of the circadian clock gene Per2 in rheumatoid synovial cells. Scandinavian Journal of Rheumatology 42 (4): 276–280.
pubmed: 23496259
doi: 10.3109/03009742.2013.765031
Hashiramoto, A., T. Yamane, K. Tsumiyama, et al. 2010. Mammalian clock gene Cryptochrome regulates arthritis via proinflammatory cytokine TNF-alpha. The Journal of Immunology 184 (3): 1560–1565.
pubmed: 20042581
doi: 10.4049/jimmunol.0903284
Obst, R. 2015. The Timing of T Cell Priming and Cycling. Frontiers in Immunology 6: 563.
pubmed: 26594213
pmcid: 4633513
doi: 10.3389/fimmu.2015.00563
Wood, P.A., J. Du-Quiton, S. You, and W.J. Hrushesky. 2006. Circadian clock coordinates cancer cell cycle progression, thymidylate synthase, and 5-fluorouracil therapeutic index. Molecular Cancer Therapeutics 5 (8): 2023–2033.
pubmed: 16928823
doi: 10.1158/1535-7163.MCT-06-0177
Suzuki, K., K. Yoshida, T. Ueha, et al. 2018. Methotrexate upregulates circadian transcriptional factors PAR bZIP to induce apoptosis on rheumatoid arthritis synovial fibroblasts. Arthritis Research & Therapy 20 (1): 55.
doi: 10.1186/s13075-018-1552-9
Hafezi, S., and M. Rahmani. 2021. Targeting BCL-2 in Cancer: Advances, Challenges, and Perspectives. Cancers (Basel) 13 (6): 1292.
pubmed: 33799470
doi: 10.3390/cancers13061292
Okamoto, K., A. Zaanan, H. Kawakami, S. Huang, and F.A. Sinicrope. 2015. Reversal of Mutant KRAS-Mediated Apoptosis Resistance by Concurrent Noxa/Bik Induction and Bcl-2/Bcl-xL Antagonism in Colon Cancer Cells. Molecular Cancer Research 13 (4): 659–669.
pubmed: 25548100
doi: 10.1158/1541-7786.MCR-14-0476
Boers, M., L. Hartman, D. Opris-Belinski, et al. 2022. Low dose, add-on prednisolone in patients with rheumatoid arthritis aged 65+: The pragmatic randomised, double-blind placebo-controlled GLORIA trial. Annals of the Rheumatic Diseases 81 (7): 925–936.
pubmed: 35641125
doi: 10.1136/annrheumdis-2021-221957
De Bosscher, K., I.M. Beck, L. Dejager, et al. 2014. Selective modulation of the glucocorticoid receptor can distinguish between transrepression of NF-κB and AP-1. Cellular and Molecular Life Sciences 71 (1): 143–163.
pubmed: 23784308
doi: 10.1007/s00018-013-1367-4
Olejniczak, I., H. Oster, and D.W. Ray. 2014. Glucocorticoid circadian rhythms in immune function. Semin Immunopathol 44 (2): 153–163.
doi: 10.1007/s00281-021-00889-2
Shimba, A., and K. Ikuta. 2020. Control of immunity by glucocorticoids in health and disease. Semin Immunopathol 42 (6): 669–680.
pubmed: 33219395
doi: 10.1007/s00281-020-00827-8
Taves, M.D., and J.D. Ashwell. 2021. Glucocorticoids in T cell development, differentiation and function. Nature Reviews Immunology 21 (4): 233–243.
pubmed: 33149283
doi: 10.1038/s41577-020-00464-0
Kokkinopoulou, I., A. Diakoumi, and P. Moutsatsou. 2021. Glucocorticoid Receptor Signaling in Diabetes. International Journal of Molecular Sciences 22 (20): 11173.
pubmed: 34681832
pmcid: 8537243
doi: 10.3390/ijms222011173
Waeber, G., T. Calandra, C. Bonny, and R. Bucala. 1999. A role for the endocrine and pro-inflammatory mediator MIF in the control of insulin secretion during stress. Diabetes/Metabolism Research and Reviews 15 (1): 47–54.
pubmed: 10398546
doi: 10.1002/(SICI)1520-7560(199901/02)15:1<47::AID-DMRR9>3.0.CO;2-J
Cheifetz, P.N. 1971. The daily rhythm of the secretion of corticotrophin and corticosterone in rats and mice. Journal of Endocrinology 49 (3): xi–xii.
pubmed: 4326300
Irvine, C.H., and S.L. Alexander. 1994. Factors affecting the circadian rhythm in plasma cortisol concentrations in the horse. Domestic Animal Endocrinology 11 (2): 227–238.
pubmed: 8045104
doi: 10.1016/0739-7240(94)90030-2
Minnetti, M., V. Hasenmajer, R. Pofi, et al. 2020. Fixing the broken clock in adrenal disorders: Focus on glucocorticoids and chronotherapy. Journal of Endocrinology 246 (2): R13–R31.
pubmed: 32380472
doi: 10.1530/JOE-20-0066
Nader, N., G.P. Chrousos, and T. Kino. 2010. Interactions of the circadian CLOCK system and the HPA axis. Trends in Endocrinology and Metabolism 21 (5): 277–286.
pubmed: 20106676
doi: 10.1016/j.tem.2009.12.011
Buttgereit, F., G. Doering, A. Schaeffler, et al. 2008. Efficacy of modified-release versus standard prednisone to reduce duration of morning stiffness of the joints in rheumatoid arthritis (CAPRA-1): A double-blind, randomised controlled trial. Lancet 371 (9608): 205–214.
pubmed: 18207016
doi: 10.1016/S0140-6736(08)60132-4
Buttgereit, F., G. Doering, A. Schaeffler, et al. 2010. Targeting pathophysiological rhythms: Prednisone chronotherapy shows sustained efficacy in rheumatoid arthritis. Annals of the Rheumatic Diseases 69 (7): 1275–1280.
pubmed: 20542963
doi: 10.1136/ard.2009.126888
De Silva, M., A. Binder, and B.L. Hazleman. 1984. The timing of prednisolone dosage and its effect on morning stiffness in rheumatoid arthritis. Annals of the Rheumatic Diseases 43 (6): 790–793.
pubmed: 6395813
pmcid: 1001537
doi: 10.1136/ard.43.6.790
Deandrade, J.R., J.N. McCormick, and A.G. Hill. 1964. SMALL DOSES OF PREDNISOLONE IN THE MANAGEMENT OF RHEUMATOID ARTHRITIS. Annals of the Rheumatic Diseases 23 (2): 158–162.
pubmed: 14130037
doi: 10.1136/ard.23.2.158
Arvidson, N.G., B. Gudbjörnsson, A. Larsson, and R. Hällgren. 1997. The timing of glucocorticoid administration in rheumatoid arthritis. Annals of the Rheumatic Diseases 56 (1): 27–31.
pubmed: 9059137
pmcid: 1752253
doi: 10.1136/ard.56.1.27
Spiga, F., J.J. Walker, J.R. Terry, and S.L. Lightman. 1999. HPA axis-rhythms. Comprehensive Physiology 4 (3): 1273–1298.
Son, Y.L., T. Ubuka, M. Narihiro, et al. 2014. Molecular basis for the activation of gonadotropin-inhibitory hormone gene transcription by corticosterone. Endocrinology 155 (5): 1817–1826.
pubmed: 24552400
doi: 10.1210/en.2013-2076
Kennedy, C.L.M., S.D. Carter, K.R. Mifsud, and J.M.H.M. Reul. 2014. Unexpected effects of metyrapone on corticosteroid receptor interaction with the genome and subsequent gene transcription in the hippocampus of male rats. Journal of Neuroendocrinology 32 (2): e12820.
doi: 10.1111/jne.12820
Han, D.H., Y.J. Lee, K. Kim, C.J. Kim, and S. Cho. 2014. Modulation of glucocorticoid receptor induction properties by core circadian clock proteins. Molecular and Cellular Endocrinology 383 (1–2): 170–180.
pubmed: 24378737
doi: 10.1016/j.mce.2013.12.013
Okabe, T., R. Chavan, S.S. Fonseca Costa, A. Brenna, J.A. Ripperger, and U. Albrecht. 2016. REV-ERBα influences the stability and nuclear localization of the glucocorticoid receptor. Journal of Cell Science 129 (21): 4143–4154.
pubmed: 27686098
pmcid: 5117207
doi: 10.1242/jcs.190959
Murayama, Y., N. Yahagi, Y. Takeuchi, et al. 2019. Glucocorticoid receptor suppresses gene expression of Rev-erbα (Nr1d1) through interaction with the CLOCK complex. FEBS Letters 593 (4): 423–432.
pubmed: 30659595
doi: 10.1002/1873-3468.13328
Quattrocelli, M., M. Wintzinger, K. Miz, et al. 2022. Muscle mitochondrial remodeling by intermittent glucocorticoid drugs requires an intact circadian clock and muscle PGC1α. Science Advances 8 (7): eabm1189.
pubmed: 35179955
pmcid: 8856622
doi: 10.1126/sciadv.abm1189
Bering, T., H. Hertz, and M.F. Rath. 2022. Rhythmic Release of Corticosterone Induces Circadian Clock Gene Expression in the Cerebellum. Neuroendocrinology 110 (7–8): 604–615.
Lamia, K.A., S.J. Papp, R.T. Yu, et al. 2011. Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 480 (7378): 552–556.
pubmed: 22170608
pmcid: 3245818
doi: 10.1038/nature10700
Claustrat, B., J. Brun, and G. Chazot. 2005. The basic physiology and pathophysiology of melatonin. Sleep Medicine Reviews 9 (1): 11–24.
pubmed: 15649735
doi: 10.1016/j.smrv.2004.08.001
Pevet, P., and E. Challet. 2011. Melatonin: Both master clock output and internal time-giver in the circadian clocks network. Journal of Physiology - Paris 105 (4–6): 170–182.
pubmed: 21914478
doi: 10.1016/j.jphysparis.2011.07.001
Hansson, I., R. Holmdahl, and R. Mattsson. 1990. Constant darkness enhances autoimmunity to type II collagen and exaggerates development of collagen-induced arthritis in DBA/1 mice. Journal of Neuroimmunology 27 (1): 79–84.
pubmed: 2318959
doi: 10.1016/0165-5728(90)90139-E
Hansson, I., R. Holmdahl, and R. Mattsson. 1992. The pineal hormone melatonin exaggerates development of collagen-induced arthritis in mice. Journal of Neuroimmunology 39 (1–2): 23–30.
pubmed: 1619037
doi: 10.1016/0165-5728(92)90171-G
Bang, J., H.W. Chang, H.R. Jung, et al. 2012. Melatonin attenuates clock gene cryptochrome1, which may aggravate mouse anti-type II collagen antibody-induced arthritis. Rheumatology International 32 (2): 379–385.
pubmed: 21113809
doi: 10.1007/s00296-010-1641-9
Shigeyoshi, Y., K. Taguchi, S. Yamamoto, et al. 1997. Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 91 (7): 1043–1053.
pubmed: 9428526
doi: 10.1016/S0092-8674(00)80494-8
Huang, C.C., C.H. Chiou, S.C. Liu, et al. 2019. Melatonin attenuates TNF-α and IL-1β expression in synovial fibroblasts and diminishes cartilage degradation: Implications for the treatment of rheumatoid arthritis. Journal of Pineal Research 66 (3): e12560.
pubmed: 30648758
doi: 10.1111/jpi.12560
Jiménez-Caliani, A.J., S. Jiménez-Jorge, P. Molinero, et al. 2005. Dual effect of melatonin as proinflammatory and antioxidant in collagen-induced arthritis in rats. Journal of Pineal Research 38 (2): 93–99.
pubmed: 15683463
doi: 10.1111/j.1600-079X.2004.00175.x
Garcia-Mauriño, S., M.G. Gonzalez-Haba, J.R. Calvo, R. Goberna, and J.M. Guerrero. 1998. Involvement of nuclear binding sites for melatonin in the regulation of IL-2 and IL-6 production by human blood mononuclear cells. Journal of Neuroimmunology 92 (1–2): 76–84.
pubmed: 9916882
doi: 10.1016/S0165-5728(98)00179-9
Barrett, P., M. Morris, W.S. Choi, A. Ross, and P.J. Morgan. 1999. Melatonin receptors and signal transduction mechanisms. Biological Signals and Receptors 8 (1–2): 6–14.
pubmed: 10085457
doi: 10.1159/000014563
Carlberg, C., and I. Wiesenberg. 1995. The orphan receptor family RZR/ROR, melatonin and 5-lipoxygenase: An unexpected relationship. Journal of Pineal Research 18 (4): 171–178.
pubmed: 8531047
doi: 10.1111/j.1600-079X.1995.tb00157.x
Ma, H., J. Kang, W. Fan, H. He, and F. Huang. 2021. ROR: Nuclear Receptor for Melatonin or Not? Molecules 26 (9): 2693.
pubmed: 34064466
pmcid: 8124216
doi: 10.3390/molecules26092693
Jahanban-Esfahlan, R., S. Mehrzadi, R.J. Reiter, et al. 2018. Melatonin in regulation of inflammatory pathways in rheumatoid arthritis and osteoarthritis: Involvement of circadian clock genes. British Journal of Pharmacology 175 (16): 3230–3238.
pubmed: 28585236
doi: 10.1111/bph.13898