Reduced levels of CCL2 and CXCL10 in systemic lupus erythematosus patients under treatment with prednisone, mycophenolate mofetil, or hydroxychloroquine, except in a high STAT1 subset

Arthritis Research and Therapy

Volumn 16, Issue 1, 2014, Pages

  Dominguez Gutierrez, Paul R ^a   Ceribelli, Angela ^a,c,d   Satoh, Minoru ^b   Sobel, Eric S ^b   Reeves, Westley H ^b   Chan, Edward K L ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^c HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; BIOLOGICAL MARKER; CCL2 PROTEIN, HUMAN; CXCL10 PROTEIN, HUMAN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HYDROXYCHLOROQUINE; MONOCYTE CHEMOTACTIC PROTEIN 1; MYCOPHENOLATE MOFETIL; MYCOPHENOLIC ACID; PREDNISONE; STAT1 PROTEIN; STAT1 PROTEIN, HUMAN;

ANALOGS AND DERIVATIVES; BLOOD; HUMAN; LUPUS ERYTHEMATOSUS, SYSTEMIC; REAL TIME POLYMERASE CHAIN REACTION;

ANTI-INFLAMMATORY AGENTS; BIOLOGICAL MARKERS; CHEMOKINE CCL2; CHEMOKINE CXCL10; HUMANS; HYDROXYCHLOROQUINE; LUPUS ERYTHEMATOSUS, SYSTEMIC; MYCOPHENOLIC ACID; PREDNISONE; REAL-TIME POLYMERASE CHAIN REACTION; STAT1 TRANSCRIPTION FACTOR;

EID: 84892708134     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4451     Document Type: Article

References (55)

1. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, Shark KB, Grande WJ, Hughes KM, Kapur V, Gregersen PK, Behrens TW. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA 2003, 100:2610-2615. 10.1073/pnas.0337679100, 151388, 12604793.
2. Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, Pascual V. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med 2003, 197:711-723. 10.1084/jem.20021553, 2193846, 12642603.
3. Crow MK. Interferon pathway activation in systemic lupus erythematosus. Curr Rheumatol Rep 2005, 7:463-468. 10.1007/s11926-005-0053-4, 16303107.
4. Preble OT, Black RJ, Friedman RM, Klippel JH, Vilcek J. Systemic lupus erythematosus: presence in human serum of an unusual acid-labile leukocyte interferon. Science 1982, 216:429-431. 10.1126/science.6176024, 6176024.
5. Karonitsch T, Feierl E, Steiner CW, Dalwigk K, Korb A, Binder N, Rapp A, Steiner G, Scheinecker C, Smolen J, Aringer M. Activation of the interferon-gamma signaling pathway in systemic lupus erythematosus peripheral blood mononuclear cells. Arthritis Rheum 2009, 60:1463-1471. 10.1002/art.24449, 19404947.
6. Bauer JW, Baechler EC, Petri M, Batliwalla FM, Crawford D, Ortmann WA, Espe KJ, Li W, Patel DD, Gregersen PK, Behrens TW. Elevated serum levels of interferon-regulated chemokines are biomarkers for active human systemic lupus erythematosus. PLoS Med 2006, 3:e491. 10.1371/journal.pmed.0030491, 1702557, 17177599.
7. Bauer JW, Petri M, Batliwalla FM, Koeuth T, Wilson J, Slattery C, Panoskaltsis-Mortari A, Gregersen PK, Behrens TW, Baechler EC. Interferon-regulated chemokines as biomarkers of systemic lupus erythematosus disease activity: a validation study. Arthritis Rheum 2009, 60:3098-3107. 10.1002/art.24803, 2842939, 19790071.
8. Xia M, Sui Z. Recent developments in CCR2 antagonists. Expert Opin Ther Pat 2009, 19:295-303. 10.1517/13543770902755129, 19441905.
9. Loetscher M, Loetscher P, Brass N, Meese E, Moser B. Lymphocyte-specific chemokine receptor CXCR3: regulation, chemokine binding and gene localization. Eur J Immunol 1998, 28:3696-3705. 10.1002/(SICI)1521-4141(199811)28:11<3696::AID-IMMU3696>3.0.CO;2-W, 9842912.
10. Weng Y, Siciliano SJ, Waldburger KE, Sirotina-Meisher A, Staruch MJ, Daugherty BL, Gould SL, Springer MS, DeMartino JA. Binding and functional properties of recombinant and endogenous CXCR3 chemokine receptors. J Biol Chem 1998, 273:18288-18291. 10.1074/jbc.273.29.18288, 9660793.
11. Han C, Fu J, Liu Z, Huang H, Luo L, Yin Z. Dipyrithione inhibits IFN-gamma-induced JAK/STAT1 signaling pathway activation and IP-10/CXCL10 expression in RAW264.7 cells. Inflamm Res 2010, 59:809-816. 10.1007/s00011-010-0192-6, 20372968.
12. Ceribelli A, Satoh M, Chan EKL. MicroRNAs and autoimmunity. Curr Opin Immunol 2012, 24:686-691. 10.1016/j.coi.2012.07.011, 3508200, 22902047.
13. Ceribelli A, Yao B, Dominguez-Gutierrez PR, Nahid MA, Satoh M, Chan EKL. MicroRNAs in systemic rheumatic diseases. Arthritis Res Ther 2011, 13:229. 10.1186/ar3377, 3239341, 21787439.
14. Tang Y, Luo X, Cui H, Ni X, Yuan M, Guo Y, Huang X, Zhou H, de Vries N, Tak PP, Chen S, Shen N. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum 2009, 60:1065-1075. 10.1002/art.24436, 19333922.
15. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 2006, 103:12481-12486. 10.1073/pnas.0605298103, 1567904, 16885212.
16. Nahid MA, Rivera M, Lucas A, Chan EK, Kesavalu L. Polymicrobial infection with periodontal pathogens specifically enhances microRNA miR-146a in ApoE-/- mice during experimental periodontal disease. Infect Immun 2011, 79:1597-1605. 10.1128/IAI.01062-10, 3067556, 21263019.
17. Nahid MA, Pauley KM, Satoh M, Chan EKL. miR-146a is critical for endotoxin-induced tolerance: implication in innate immunity. J Biol Chem 2009, 284:34590-34599. 10.1074/jbc.M109.056317, 2787321, 19840932.
18. Chan EKL, Ceribelli A, Satoh M. MicroRNA-146a in autoimmunity and innate immune responses. Ann Rheum Dis 2013, 72:ii90-ii95.
19. Pauley KM, Stewart CM, Gauna AE, Dupre LC, Kuklani R, Chan AL, Pauley BA, Reeves WH, Chan EK, Cha S. Altered miR-146a expression in Sjogren's syndrome and its functional role in innate immunity. Eur J Immunol 2011, 41:2029-2039. 10.1002/eji.201040757, 3760391, 21469088.
20. Sonkoly E, Stahle M, Pivarcsi A. MicroRNAs: novel regulators in skin inflammation. Clin Exp Dermatol 2008, 33:312-315. 10.1111/j.1365-2230.2008.02804.x, 18419608.
21. Sonkoly E, Wei T, Janson PC, Saaf A, Lundeberg L, Tengvall-Linder M, Norstedt G, Alenius H, Homey B, Scheynius A, Stahle M, Pivarcsi A. MicroRNAs: novel regulators involved in the pathogenesis of psoriasis?. PLoS One 2007, 2:e610. 10.1371/journal.pone.0000610, 1905940, 17622355.
22. Nakasa T, Miyaki S, Okubo A, Hashimoto M, Nishida K, Ochi M, Asahara H. Expression of microRNA-146 in rheumatoid arthritis synovial tissue. Arthritis Rheum 2008, 58:1284-1292. 10.1002/art.23429, 2749927, 18438844.
23. Pauley KM, Satoh M, Chan AL, Bubb MR, Reeves WH, Chan EK. Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res Ther 2008, 10:R101. 10.1186/ar2493, 2575615, 18759964.
24. Stanczyk J, Pedrioli DM, Brentano F, Sanchez-Pernaute O, Kolling C, Gay RE, Detmar M, Gay S, Kyburz D. Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum 2008, 58:1001-1009. 10.1002/art.23386, 18383392.
25. Dominguez-Gutierrez PR, Ceribelli A, Satoh M, Sobel ES, Reeves WH, Chan EKL. Elevated STAT1 correlates with increased CCL2 and CXCL10 levels in peripheral blood of patients with systemic lupus erythematosus. Arthritis Res Ther 2014, 16:R20. 10.1186/ar4448, 24451065.
26. Guiducci C, Gong M, Xu Z, Gill M, Chaussabel D, Meeker T, Chan JH, Wright T, Punaro M, Bolland S, Soumelis V, Banchereau J, Coffman RL, Pascual V, Barrat FJ. TLR recognition of self nucleic acids hampers glucocorticoid activity in lupus. Nature 2010, 465:937-941. 10.1038/nature09102, 2964153, 20559388.
27. Bhattacharyya S, Zhao Y, Kay TW, Muglia LJ. Glucocorticoids target suppressor of cytokine signaling 1 (SOCS1) and type 1 interferons to regulate Toll-like receptor-induced STAT1 activation. Proc Natl Acad Sci USA 2011, 108:9554-9559. 10.1073/pnas.1017296108, 3111275, 21606371.
28. Aittomaki S, Pesu M, Groner B, Janne OA, Palvimo JJ, Silvennoinen O. Cooperation among Stat1, glucocorticoid receptor, and PU.1 in transcriptional activation of the high-affinity Fc gamma receptor I in monocytes. J Immunol 2000, 164:5689-5697.
29. Dall'era M, Chakravarty EF. Treatment of mild, moderate, and severe lupus erythematosus: focus on new therapies. Curr Rheumatol Rep 2011, 13:308-316. 10.1007/s11926-011-0186-6, 21584692.
30. Chaturvedi A, Pierce SK. How location governs toll-like receptor signaling. Traffic 2009, 10:621-628. 10.1111/j.1600-0854.2009.00899.x, 2741634, 19302269.
31. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol 2003, 21:335-376. 10.1146/annurev.immunol.21.120601.141126, 12524386.
32. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982, 25:1271-1277. 10.1002/art.1780251101, 7138600.
33. Nahid MA, Yao B, Dominguez-Gutierrez PR, Kesavalu L, Satoh M, Chan EKL. Regulation of TLR2-mediated tolerance and cross-tolerance through IRAK4 modulation by miR-132 and miR-212. J Immunol 2013, 190:1250-1263. 10.4049/jimmunol.1103060, 3552145, 23264652.
34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
35. Herbst R, Liu Z, Jallal B, Yao Y. Biomarkers for systemic lupus erythematosus. Int J Rheum Dis 2012, 15:433-444. 10.1111/j.1756-185X.2012.01764.x, 23083033.
36. Hanley JA, Negassa A, Edwardes MD, Forrester JE. Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol 2003, 157:364-375. 10.1093/aje/kwf215, 12578807.
37. Crow MK, Kirou KA, Wohlgemuth J. Microarray analysis of interferon-regulated genes in SLE. Autoimmunity 2003, 36:481-490. 10.1080/08916930310001625952, 14984025.
38. Kirou KA, Lee C, George S, Louca K, Papagiannis IG, Peterson MG, Ly N, Woodward RN, Fry KE, Lau AY, Prentice JG, Wohlgemuth JG, Crow MK. Coordinate overexpression of interferon-alpha-induced genes in systemic lupus erythematosus. Arthritis Rheum 2004, 50:3958-3967. 10.1002/art.20798, 15593221.
39. Nikpour M, Dempsey AA, Urowitz MB, Gladman DD, Barnes DA. Association of a gene expression profile from whole blood with disease activity in systemic lupus erythaematosus. Ann Rheum Dis 2008, 67:1069-1075. 10.1136/ard.2007.074765, 18063674.
40. Qing X, Putterman C. Gene expression profiling in the study of the pathogenesis of systemic lupus erythematosus. Autoimmun Rev 2004, 3:505-509. 10.1016/j.autrev.2004.07.001, 15546798.
41. Rhen T, Cidlowski JA. Antiinflammatory action of glucocorticoids-new mechanisms for old drugs. N Engl J Med 2005, 353:1711-1723. 10.1056/NEJMra050541, 16236742.
42. Hu X, Li WP, Meng C, Ivashkiv LB. Inhibition of IFN-gamma signaling by glucocorticoids. J Immunol 2003, 170:4833-4839.
43. Fulkerson PC, Zimmermann N, Hassman LM, Finkelman FD, Rothenberg ME. Pulmonary chemokine expression is coordinately regulated by STAT1, STAT6, and IFN-gamma. J Immunol 2004, 173:7565-7574.
44. Kok SH, Hong CY, Kuo MY, Wang CC, Hou KL, Lin YT, Galson DL, Lin SK. Oncostatin M-induced CCL2 transcription in osteoblastic cells is mediated by multiple levels of STAT-1 and STAT-3 signaling: an implication for the pathogenesis of arthritis. Arthritis Rheum 2009, 60:1451-1462. 10.1002/art.24452, 19404962.
45. Valente AJ, Xie JF, Abramova MA, Wenzel UO, Abboud HE, Graves DT. A complex element regulates IFN-gamma-stimulated monocyte chemoattractant protein-1 gene transcription. J Immunol 1998, 161:3719-3728.
46. Ansari AW, Schmidt RE, Heiken H. Prednisolone mediated suppression of HIV-1 viral load strongly correlates with C-C chemokine CCL2: in vivo and in vitro findings. Clin Immunol 2007, 125:1-4. 10.1016/j.clim.2007.07.003, 17707134.
47. Matsuo H, Tamura M, Kabashima N, Serino R, Tokunaga M, Shibata T, Matsumoto M, Aijima M, Oikawa S, Anai H, Nakashima Y. Prednisolone inhibits hyperosmolarity-induced expression of MCP-1 via NF-kappaB in peritoneal mesothelial cells. Kidney Int 2006, 69:736-746. 10.1038/sj.ki.5000131, 16518329.
48. de Kruif MD, Lemaire LC, Giebelen IA, Groot AP, Pater JM, van den Pangaart PS, Elliott PJ, van der Poll T. Effects of prednisolone on the systemic release of mediators of cell-mediated cytotoxicity during human endotoxemia. Shock 2008, 29:458-461.
49. Khodarev NN, Roizman B, Weichselbaum RR. Molecular pathways: interferon/stat1 pathway: role in the tumor resistance to genotoxic stress and aggressive growth. Clin Cancer Res 2012, 18:3015-3021. 10.1158/1078-0432.CCR-11-3225, 22615451.
50. Khodarev NN, Beckett M, Labay E, Darga T, Roizman B, Weichselbaum RR. STAT1 is overexpressed in tumors selected for radioresistance and confers protection from radiation in transduced sensitive cells. Proc Natl Acad Sci USA 2004, 101:1714-1719. 10.1073/pnas.0308102100, 341831, 14755057.
51. Khodarev NN, Minn AJ, Efimova EV, Darga TE, Labay E, Beckett M, Mauceri HJ, Roizman B, Weichselbaum RR. Signal transducer and activator of transcription 1 regulates both cytotoxic and prosurvival functions in tumor cells. Cancer Res 2007, 67:9214-9220. 10.1158/0008-5472.CAN-07-1019, 17909027.
52. Kita K, Sugaya S, Zhai L, Wu YP, Wano C, Chigira S, Nomura J, Takahashi S, Ichinose M, Suzuki N. Involvement of LEU13 in interferon-induced refractoriness of human RSa cells to cell killing by X rays. Radiat Res 2003, 160:302-308. 10.1667/RR3039, 12926988.
53. Rickardson L, Fryknas M, Dhar S, Lovborg H, Gullbo J, Rydaker M, Nygren P, Gustafsson MG, Larsson R, Isaksson A. Identification of molecular mechanisms for cellular drug resistance by combining drug activity and gene expression profiles. Br J Cancer 2005, 93:483-492. 10.1038/sj.bjc.6602699, 2361589, 16012520.
54. Roberts D, Schick J, Conway S, Biade S, Laub PB, Stevenson JP, Hamilton TC, O'Dwyer PJ, Johnson SW. Identification of genes associated with platinum drug sensitivity and resistance in human ovarian cancer cells. Br J Cancer 2005, 92:1149-1158. 10.1038/sj.bjc.6602447, 2361951, 15726096.
55. de Prati AC, Ciampa AR, Cavalieri E, Zaffini R, Darra E, Menegazzi M, Suzuki H, Mariotto S. STAT1 as a new molecular target of anti-inflammatory treatment. Curr Med Chem 2005, 12:1819-1828. 10.2174/0929867054546645, 16101503.