Restoring oxidant signaling suppresses proarthritogenic T cell effector functions in rheumatoid arthritis

Science Translational Medicine

Volumn 8, Issue 331, 2016, Pages

  Yang, Zhen ^a   Shen, Yi ^a   Oishi, Hisashi ^a,c   Matteson, Eric L ^b   Tian, Lu ^a   Goronzy, Jörg J ^a   Weyand, Cornelia M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PENTOSE PHOSPHATE; REACTIVE OXYGEN METABOLITE; GLUTATHIONE; OXIDIZING AGENT; SCAVENGER;

ARTICLE; CD4+ T LYMPHOCYTE; CELL LINEAGE; CLINICAL ARTICLE; CONTROLLED STUDY; EFFECTOR CELL; G2 PHASE CELL CYCLE CHECKPOINT; GLUCOSE UTILIZATION; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SYNOVITIS; TH1 CELL; TH17 CELL; UPREGULATION; CELL CYCLE CHECKPOINT; CELL DIFFERENTIATION; CELL PROLIFERATION; IMMUNOLOGY; INFLAMMATION; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; PENTOSE PHOSPHATE CYCLE; PHYSIOLOGICAL STRESS; T LYMPHOCYTE;

ARTHRITIS, RHEUMATOID; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; CELL PROLIFERATION; FREE RADICAL SCAVENGERS; GLUCOSE; GLUTATHIONE; HUMANS; INFLAMMATION; NADP; OXIDANTS; OXIDATION-REDUCTION; PENTOSE PHOSPHATE PATHWAY; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTES;

EID: 84961841635     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aad7151     Document Type: Article

References (44)

1. J. J. Goronzy, C. M. Weyand, Developments in the scientific understanding of rheumatoid arthritis. Arthritis Res. Ther. 11, 249 (2009).
2. J. J. O'Shea, A. Laurence, I. B. McInnes, Back to the future: Oral targeted therapy for RA and other autoimmune diseases. Nat. Rev. Rheumatol. 9, 173-182 (2013).
3. C. M.Weyand, Z. Yang, J. J. Goronzy, T-cell aging in rheumatoid arthritis. Curr. Opin. Rheumatol. 26, 93-100 (2014).
4. Z. Yang, H. Fujii, S. V. Mohan, J. J. Goronzy, C. M. Weyand, Phosphofructokinase deficiency impairs ATP generation, autophagy, and redox balance in rheumatoid arthritis T cells. J. Exp. Med. 210, 2119-2134 (2013).
5. V. P. Badovinac, J. S. Haring, J. T. Harty, Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8+ T cell response to infection. Immunity 26, 827-841 (2007).
6. E. L. Pearce, M. C. Poffenberger, C.-H. Chang, R. G. Jones, Fueling immunity: Insights into metabolism and lymphocyte function. Science 342, 1242454 (2013).
7. E. L. Pearce, E. J. Pearce, Metabolic pathways in immune cell activation and quiescence. Immunity 38, 633-643 (2013).
8. K. M. Holmström, T. Finkel, Cellular mechanisms and physiological consequences of redoxdependent signalling. Nat. Rev. Mol. Cell Biol. 15, 411-421 (2014).
9. S. E. Weinberg, L. A. Sena, N. S. Chandel, Mitochondria in the regulation of innate and adaptive immunity. Immunity 42, 406-417 (2015).
10. S. Dröse, U. Brandt, Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol. 748, 145-169 (2012).
11. H. Fujii, L. Shao, I. Colmegna, J. J. Goronzy, C. M. Weyand, Telomerase insufficiency in rheumatoid arthritis. Proc. Natl. Acad. Sci. U.S.A. 106, 4360-4365 (2009).
12. G. Le Friec, D. Sheppard, P. Whiteman, C. M. Karsten, S. A.-T. Shamoun, A. Laing, L. Bugeon, M. J. Dallman, T. Melchionna, C. Chillakuri, R. A. Smith, C. Drouet, L. Couzi, V. Fremeaux-Bacchi, J. Köhl, S. N. Waddington, J. M.McDonnell, A. Baker, P. A. Handford, S. M. Lea, C. Kemper, The CD46-Jagged1 interaction is critical for human TH1 immunity. Nat. Immunol. 13, 1213-1221 (2012).
13. C. S. Wilcox, Effects of tempol and redox-cycling nitroxides in models of oxidative stress. Pharmacol. Ther. 126, 119-145 (2010).
14. T. T. Paull, Mechanisms of ATM activation. Annu. Rev. Biochem., 84, 711-738 (2015).
15. Z. Guo, S. Kozlov, M. F. Lavin, M. D. Person, T. T. Paull, ATM activation by oxidative stress. Science 330, 517-521 (2010).
16. R. R. Nazarewicz, A. Bikineyeva, S. I. Dikalov, Rapid and specific measurements of superoxide using fluorescence spectroscopy. J. Biomol. Screen. 18, 498-503 (2013).
17. L. Shao, J. J. Goronzy, C. M. Weyand, DNA-dependent protein kinase catalytic subunit mediates T-cell loss in rheumatoid arthritis. EMBO Mol. Med. 2, 415-427 (2010).
18. D. M. Lee, H. P. Kiener, S. K. Agarwal, E. H. Noss, G. F. M. Watts, O. Chisaka, M. Takeichi, M. B. Brenner, Cadherin-11 in synovial lining formation and pathology in arthritis. Science 315, 1006-1010 (2007).
19. Z. Yang, E. L. Matteson, J. J. Goronzy, C. M. Weyand, T-cell metabolism in autoimmune disease. Arthritis Res. Ther. 17, 29 (2015).
20. N. J. MacIver, R. D. Michalek, J. C. Rathmell, Metabolic regulation of T lymphocytes. Annu. Rev. Immunol. 31, 259-283 (2013).
21. S. Devadas, L. Zaritskaya, S. G. Rhee, L. Oberley, M. S. Williams, Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: Selective regulation of mitogen-activated protein kinase activation and Fas ligand expression. J. Exp. Med. 195, 59-70 (2002).
22. P. Gergely Jr., C. Grossman, B. Niland, F. Puskas, H. Neupane, F. Allam, K. Banki, P. E. Phillips, A. Perl, Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus. Arthritis Rheum. 46, 175-190 (2002).
23. Z.-W. Lai, R. Hanczko, E. Bonilla, T. N. Caza, B. Clair, A. Bartos, G. Miklossy, J. Jimah, E. Doherty, H. Tily, L. Francis, R. Garcia, M. Dawood, J. Yu, I. Ramos, I. Coman, S. V. Faraone, P. E. Phillips, A. Perl, N-acetylcysteine reduces disease activity by blocking mammalian target of rapamycin in T cells from systemic lupus erythematosus patients: A randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 64, 2937-2946 (2012).
24. M. Hultqvist, P. Olofsson, J. Holmberg, B. T. Bäckström, J. Tordsson, R. Holmdahl, Enhanced autoimmunity, arthritis, and encephalomyelitis in mice with a reduced oxidative burst due to a mutation in the Ncf1 gene. Proc. Natl. Acad. Sci. U.S.A. 101, 12646-12651 (2004).
25. R. Holmdahl, O. Sareila, A. Pizzolla, S. Winter, C. Hagert, N. Jaakkola, T. Kelkka, L. M. Olsson, K. Wing, L. Bäckdahl, Hydrogen peroxide as an immunological transmitter regulating autoreactive T cells. Antioxid. Redox Signal. 18, 1463-1474 (2013).
26. K. A. Gelderman, M. Hultqvist, A. Pizzolla, M. Zhao, K. S. Nandakumar, R. Mattsson, R. Holmdahl, Macrophages suppress T cell responses and arthritis development in mice by producing reactive oxygen species. J. Clin. Invest. 117, 3020-3028 (2007).
27. K. Lee, H. Y. Won, M. A. Bae, J.-H. Hong, E. S. Hwang, Spontaneous and aging-dependent development of arthritis in NADPH oxidase 2 deficiency through altered differentiation of CD11b+ and Th/Treg cells. Proc. Natl. Acad. Sci. U.S.A. 108, 9548-9553 (2011).
28. V. A. Gerriets, R. J. Kishton, A. G. Nichols, A. N. Macintyre, M. Inoue, O. Ilkayeva, P. S. Winter, X. Liu, B. Priyadharshini, M. E. Slawinska, L. Haeberli, C. Huck, L. A. Turka, K. C. Wood, L. P. Hale, P. A. Smith, M. A. Schneider, N. J. MacIver, J. W. Locasale, C. B. Newgard, M. L. Shinohara, J. C. Rathmell, Metabolic programming and PDHK1 control CD4+ T cell subsets and inflammation. J. Clin. Invest. 125, 194-207 (2015).
29. E. M. Kang, B. E. Marciano, S. DeRavin, K. A. Zarember, S. M. Holland, H. L. Malech, Chronic granulomatous disease: Overview and hematopoietic stem cell transplantation. J. Allergy Clin. Immunol. 127, 1319-1326 (2011).
30. L. Shao, H. Fujii, I. Colmegna, H. Oishi, J. J. Goronzy, C. M. Weyand, Deficiency of the DNA repair enzyme ATM in rheumatoid arthritis. J. Exp. Med. 206, 1435-1449 (2009).
31. A. R. Exley, S. Buckenham, E. Hodges, R. Hallam, P. Byrd, J. Last, C. Trinder, S. Harris, N. Screaton, A. P. Williams, A. M. Taylor, J. M. Shneerson, Premature ageing of the immune system underlies immunodeficiency in ataxia telangiectasia. Clin. Immunol. 140, 26-36 (2011).
32. A. D. D'Souza, I. A. Parish, D. S. Krause, S. M. Kaech, G. S. Shadel, Reducing mitochondrial ROS improves disease-related pathology in a mouse model of ataxia-telangiectasia. Mol. Ther. 21, 42-48 (2013).
33. A. Elson, Y. Wang, C. J. Daugherty, C. C. Morton, F. Zhou, J. Campos-Torres, P. Leder, Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 93, 13084-13089 (1996).
34. T. Isoda, M. Takagi, J. Piao, S. Nakagama, M. Sato, K. Masuda, T. Ikawa, M. Azuma, T. Morio, H. Kawamoto, S. Mizutani, Process for immune defect and chromosomal translocation during early thymocyte development lacking ATM. Blood 120, 789-799 (2012).
35. A. M. Westbrook, R. H. Schiestl, Atm-deficient mice exhibit increased sensitivity to dextran sulfate sodium-induced colitis characterized by elevated DNA damage and persistent immune activation. Cancer Res. 70, 1875-1884 (2010).
36. A. D. D'Souza, I. A. Parish, S. E. McKay, S. M. Kaech, G. S. Shadel, Aberrant CD8+ T-cell responses and memory differentiation upon viral infection of an ataxia-telangiectasia mouse model driven by hyper-activated Akt and mTORC1 signaling. Am. J. Pathol. 178, 2740-2751 (2011).
37. K. N. Pollizzi, J. D. Powell, Integrating canonical and metabolic signalling programmes in the regulation of T cell responses. Nat. Rev. Immunol. 14, 435-446 (2014).
38. J. Blagih, F. Coulombe, E. E. Vincent, F. Dupuy, G. Galicia-Vázquez, E. Yurchenko, T. C. Raissi, G. J. van der Windt, B. Viollet, E. L. Pearce, J. Pelletier, C. A. Piccirillo, C. M. Krawczyk, M. Divangahi, R. G. Jones, The energy sensor AMPK regulates T cell metabolic adaptation and effector responses in vivo. Immunity 42, 41-54 (2015).
39. J. D. Powell, E. B. Heikamp, K. N. Pollizzi, A. T. Waickman, A modified model of T-cell differentiation based on mTOR activity and metabolism. Cold Spring Harb. Symp. Quant. Biol. 78, 125-130 (2013).
40. J. M. Jamison, J. Gilloteaux, H. S. Taper, J. L. Summers, Evaluation of the in vitro and in vivo antitumor activities of vitamin C and K-3 combinations against human prostate cancer. J. Nutr. 131, 158S-160S (2001).
41. G. M. Delgoffe, K. N. Pollizzi, A. T. Waickman, E. Heikamp, D. J. Meyers, M. R. Horton, B. Xiao, P. F. Worley, J. D. Powell, The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat. Immunol. 12, 295-303 (2011).
42. G. Li, M. Yu, W.-W. Lee, M. Tsang, E. Krishnan, C. M. Weyand, J. J. Goronzy, Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat. Med. 18, 1518-1524 (2012).
43. T. M. Seyler, Y. W. Park, S. Takemura, R. J. Bram, P. J. Kurtin, J. J. Goronzy, C. M. Weyand, BLyS and APRIL in rheumatoid arthritis. J. Clin. Invest. 115, 3083-3092 (2005).
44. S. Takemura, P. A. Klimiuk, A. Braun, J. J. Goronzy, C. M. Weyand, T cell activation in rheumatoid synovium is B cell dependent. J. Immunol. 167, 4710-4718 (2001).