Immune response profiling in early rheumatoid arthritis: Discovery of a novel interaction of treatment response with viral immunity

Arthritis Research and Therapy

Volumn 15, Issue 6, 2013, Pages

  Davis III, John M ^a   Knutson, Keith L ^b   Strausbauch, Michael A ^a   Green, Abigail B ^c   Crowson, Cynthia S ^c   Therneau, Terry M ^c   Matteson, Eric L ^a,c   Gabriel, Sherine E ^a,c  

^a MAYO CLINIC   (United States)

^b Vaccine and Gene Therapy Institute of Florida   (United States)

^c Mayo Clinic College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; HYDROXYCHLOROQUINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; METHOTREXATE; PREDNISONE; ANTIRHEUMATIC AGENT;

ADULT; AGE; ARTICLE; BLOOD CELL; BODY MASS; COHORT ANALYSIS; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DAS28; DISEASE ACTIVITY; DISEASE DURATION; EPSTEIN BARR VIRUS; FEMALE; FOLLOW UP; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNE RESPONSE; MAJOR CLINICAL STUDY; MALE; OBSERVATIONAL STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PROSPECTIVE STUDY; RHEUMATOID ARTHRITIS; RHEUMATOLOGY; SEX; T LYMPHOCYTE; TREATMENT OUTCOME; TREATMENT RESPONSE; UPREGULATION; VIRUS IMMUNITY; CELLULAR IMMUNITY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; EPSTEIN BARR VIRUS INFECTION; IMMUNOLOGY; MIDDLE AGED; PRINCIPAL COMPONENT ANALYSIS; VIROLOGY;

ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; EPSTEIN-BARR VIRUS INFECTIONS; FEMALE; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNITY, CELLULAR; MALE; MIDDLE AGED; PRINCIPAL COMPONENT ANALYSIS; T-LYMPHOCYTES; TREATMENT OUTCOME;

EID: 84888102914     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4389     Document Type: Article

References (43)

1. Smolen JS, Aletaha D, Bijlsma JW, Breedveld FC, Boumpas D, Burmester G, Combe B, Cutolo M, de Wit M, Dougados M, Emery P, Gibofsky A, Gomez-Reino JJ, Haraoui B, Kalden J, EC K, Kvien TK, McInnes I, Martin-Mola E, Montecucco C, Schoels M, van der Heijde D, et al. Treating rheumatoid arthritis to target: recommendations of an international task force. Ann Rheum Dis 2010, 69(4):631-637. 10.1136/ard.2009.123919, 3015099, 20215140.
2. Goekoop-Ruiterman YP, de Vries-Bouwstra JK, Allaart CF, van Zeben D, Kerstens PJ, Hazes JM, Zwinderman AH, Peeters AJ, de Jonge-Bok JM, Mallee C, de Beus WM, de Sonnaville PB, Ewals JA, Breedveld FC, Dijkmans BA, et al. Comparison of treatment strategies in early rheumatoid arthritis: a randomized trial. Ann Intern Med 2007, 146(6):406-415. 10.7326/0003-4819-146-6-200703200-00005, 17371885.
3. van Vollenhoven RF, Ernestam S, Geborek P, Petersson IF, Coster L, Waltbrand E, Zickert A, Theander J, Thorner A, Hellstrom H, Teleman A, Dackhammar C, Akre F, Forslind K, Ljung L, Oding R, Chatzidionysiou A, Wornert M, Bratt J, et al. Addition of infliximab compared with addition of sulfasalazine and hydroxychloroquine to methotrexate in patients with early rheumatoid arthritis (Swefot trial): 1-year results of a randomised trial. Lancet 2009, 374(9688):459-466. 10.1016/S0140-6736(09)60944-2, 19665644.
4. Verstappen SM, Jacobs JW, van der Veen MJ, Heurkens AH, Schenk Y, ter Borg EJ, Blaauw AA, Bijlsma JW. Intensive treatment with methotrexate in early rheumatoid arthritis: aiming for remission. Computer Assisted Management in Early Rheumatoid Arthritis (CAMERA, an open-label strategy trial). Ann Rheum Dis 2007, 66:1443-1449. 10.1136/ard.2007.071092, 2111604, 17519278.
5. Radovits BJ, Fransen J, Al Shamma S, Eijsbouts AM, van Riel PL, Laan RF. Excess mortality emerges after 10 years in an inception cohort of early rheumatoid arthritis. Arthritis Care Res (Hoboken) 2010, 62:362-370. 10.1002/acr.20105, 20391482.
6. Avina-Zubieta JA, Thomas J, Sadatsafavi M, Lehman AJ, Lacaille D. Risk of incident cardiovascular events in patients with rheumatoid arthritis: a meta-analysis of observational studies. Ann Rheum Dis 2012, 71:1524-1529. 10.1136/annrheumdis-2011-200726, 22425941.
7. Leeb BF, Andel I, Sautner J, Nothnagl T, Rintelen B. The DAS28 in rheumatoid arthritis and fibromyalgia patients. Rheumatology (Oxford) 2004, 43:1504-1507. 10.1093/rheumatology/keh322, 15252215.
8. Brown AK, Quinn MA, Karim Z, Conaghan PG, Peterfy CG, Hensor E, Wakefield RJ, O'Connor PJ, Emery P. Presence of significant synovitis in rheumatoid arthritis patients with disease-modifying antirheumatic drug-induced clinical remission: evidence from an imaging study may explain structural progression. Arthritis Rheum 2006, 54:3761-3773. 10.1002/art.22190, 17133543.
9. Szkudlarek M, Klarlund M, Narvestad E, Court-Payen M, Strandberg C, Jensen KE, Thomsen HS, Ostergaard M. Ultrasonography of the metacarpophalangeal and proximal interphalangeal joints in rheumatoid arthritis: a comparison with magnetic resonance imaging, conventional radiography and clinical examination. Arthritis Res Ther 2006, 8:R52. 10.1186/ar1904, 1526591, 16519793.
10. Davis JM, Knutson KL, Strausbauch MA, Crowson CS, Therneau TM, Wettstein PJ, Matteson EL, Gabriel SE. Analysis of complex biomarkers for human immune-mediated disorders based on cytokine responsiveness of peripheral blood cells. J Immunol 2010, 184:7297-7304. 10.4049/jimmunol.0904180, 2882518, 20495063.
11. Hueber W, Tomooka BH, Batliwalla F, Li W, Monach PA, Tibshirani RJ, Van Vollenhoven RF, Lampa J, Saito K, Tanaka Y, Genovese MC, Klareskog L, Gregersen PK, Robinson WH, et al. Blood autoantibody and cytokine profiles predict response to anti-tumor necrosis factor therapy in rheumatoid arthritis. Arthritis Res Ther 2009, 11(3):R76. 10.1186/ar2706, 2714123, 19460157.
12. Hueber W, Tomooka BH, Zhao X, Kidd BA, Drijfhout JW, Fries JF, van Venrooij WJ, Metzger AL, Genovese MC, Robinson WH. Proteomic analysis of secreted proteins in early rheumatoid arthritis: anti-citrulline autoreactivity is associated with up regulation of proinflammatory cytokines. Ann Rheum Dis 2007, 66:712-719. 10.1136/ard.2006.054924, 1954670, 16901957.
13. Churchman SM, Geiler J, Parmar R, Horner EA, Church LD, Emery P, Buch MH, McDermott MF, Ponchel F. Multiplexing immunoassays for cytokine detection in the serum of patients with rheumatoid arthritis: lack of sensitivity and interference by rheumatoid factor. Clin Exp Rheumatol 2012, 30:534-542.
14. Todd DJ, Knowlton N, Amato M, Frank MB, Schur PH, Izmailova ES, Roubenoff R, Shadick NA, Weinblatt ME, Centola M, Lee DM, et al. Erroneous augmentation of multiplex assay measurements in patients with rheumatoid arthritis due to heterophilic binding by serum rheumatoid factor. Arthritis Rheum 2011, 63(4):894-903. 10.1002/art.30213, 21305505.
15. Davis JM, Knutson KL, Strausbauch MA, Crowson CS, Therneau TM, Wettstein PJ, Roger VL, Matteson EL, Gabriel SE. A signature of aberrant immune responsiveness identifies myocardial dysfunction in rheumatoid arthritis. Arthritis Rheum 2011, 63:1497-1506. 3106129, 21384332.
16. Davis JM, Knutson KL, Skinner JA, Strausbauch MA, Crowson CS, Therneau TM, Wettstein PJ, Matteson EL, Gabriel SE. A profile of immune response to herpesvirus is associated with radiographic damage in rheumatoid arthritis. Arthritis Res Ther 2012, 14:R24. 10.1186/ar3706, 3392817, 22293286.
17. Aletaha D, Breedveld FC, Smolen JS. The need for new classification criteria for rheumatoid arthritis. Arthritis Rheum 2005, 52:3333-3336. 10.1002/art.21410, 16255014.
18. van der Helm-van Mil AH, Detert J, le Cessie S, Filer A, Bastian H, Burmester GR, Huizinga TW, Raza K. Validation of a prediction rule for disease outcome in patients with recent-onset undifferentiated arthritis: moving toward individualized treatment decision-making. Arthritis Rheum 2008, 58:2241-2247. 10.1002/art.23681, 18668546.
19. van der Helm-van Mil AH, le Cessie S, van Dongen H, Breedveld FC, Toes RE, Huizinga TW. A prediction rule for disease outcome in patients with recent-onset undifferentiated arthritis: how to guide individual treatment decisions. Arthritis Rheum 2007, 56:433-440. 10.1002/art.22380, 17265478.
20. Fries JF, Spitz P, Kraines RG, Holman HR. Measurement of patient outcome in arthritis. Arthritis Rheum 1980, 23:137-145. 10.1002/art.1780230202, 7362664.
21. Fries JF, Spitz PW, Young DY. The dimensions of health outcomes: the health assessment questionnaire, disability and pain scales. J Rheumatol 1982, 9:789-793.
22. Wells G, Becker JC, Teng J, Dougados M, Schiff M, Smolen J, Aletaha D, van Riel PL. Validation of the 28-joint Disease Activity Score (DAS28) and European League Against Rheumatism response criteria based on C-reactive protein against disease progression in patients with rheumatoid arthritis, and comparison with the DAS28 based on erythrocyte sedimentation rate. Ann Rheum Dis 2009, 68:954-960. 10.1136/ard.2007.084459, 2674547, 18490431.
23. Prevoo ML, Hof MAV, Kuper HH, van Leeuwen MA, van de Putte LB, van Riel PL. Modified disease activity scores that include twenty-eight-joint counts. Development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis Rheum 1995, 38:44-48. 10.1002/art.1780380107, 7818570.
24. Drouin J, Haraoui B. Predictors of clinical response and radiographic progression in patients with rheumatoid arthritis treated with methotrexate monotherapy. J Rheumatol 2010, 37:1405-1410. 10.3899/jrheum.090838, 20436076.
25. Visser K, Goekoop-Ruiterman YP, de Vries-Bouwstra JK, Ronday HK, Seys PE, Kerstens PJ, Huizinga TW, Dijkmans BA, Allaart CF. A matrix risk model for the prediction of rapid radiographic progression in patients with rheumatoid arthritis receiving different dynamic treatment strategies: post hoc analyses from the BeSt study. Ann Rheum Dis 2010, 69:1333-1337. 10.1136/ard.2009.121160, 20498212.
26. Vastesaeger N, Xu S, Aletaha D, St Clair EW, Smolen JS. A pilot risk model for the prediction of rapid radiographic progression in rheumatoid arthritis. Rheumatology (Oxford) 2009, 48:1114-1121. 10.1093/rheumatology/kep155, 19589891.
27. Saevarsdottir S, Wallin H, Seddighzadeh M, Ernestam S, Geborek P, Petersson IF, Bratt J, van Vollenhoven RF. Predictors of response to methotrexate in early DMARD naive rheumatoid arthritis: results from the initial open-label phase of the SWEFOT trial. Ann Rheum Dis 2011, 70:469-475. 10.1136/ard.2010.139212, 21149498.
28. Isaacs JD, Ferraccioli G. The need for personalised medicine for rheumatoid arthritis. Ann Rheum Dis 2011, 70:4-7. 10.1136/ard.2010.135376, 21068091.
29. Emery P, Dorner T. Optimising treatment in rheumatoid arthritis: a review of potential biological markers of response. Ann Rheum Dis 2011, 70:2063-2070. 10.1136/ard.2010.148015, 22039166.
30. Berg L, Lampa J, Rogberg S, van Vollenhoven R, Klareskog L. Increased peripheral T cell reactivity to microbial antigens and collagen type II in rheumatoid arthritis after treatment with soluble TNF alpha receptors. Ann Rheum Dis 2001, 60:133-139. 10.1136/ard.60.2.133, 1753474, 11156546.
31. Kawashima M, Miossec P. mRNA quantification of T-bet, GATA-3, IFN-gamma, and IL-4 shows a defective Th1 immune response in the peripheral blood from rheumatoid arthritis patients: link with disease activity. J Clin Immunol 2005, 25:209-214. 10.1007/s10875-005-4092-4, 15981085.
32. Kitas GD, Salmon M, Farr M, Gaston JS, Bacon PA. Deficient interleukin 2 production in rheumatoid arthritis: association with active disease and systemic complications. Clin Exp Immunol 1988, 73:242-249. 1541612, 2972426.
33. Pierer M, Rothe K, Quandt D, Schulz A, Rossol M, Scholz R, Baerwald C, Wagner U. Anti-cytomegalovirus seropositivity in rheumatoid arthritis is associated with more severe joint destruction and more frequent joint surgery. Arthritis Rheum 2012, 64:1740-1749. 10.1002/art.34346, 22183424.
34. Kawashima M, Miossec P. Effect of treatment of rheumatoid arthritis with infliximab on IFN gamma, IL4, T-bet, and GATA-3 expression: link with improvement of systemic inflammation and disease activity. Ann Rheum Dis 2005, 64:415-418. 1755397, 15286007.
35. Abreu JR, Grabiec AM, Krausz S, Spijker R, Burakowski T, Maslinski W, Eldering E, Tak PP, Reedquist KA. The presumed hyporesponsive behavior of rheumatoid arthritis T lymphocytes can be attributed to spontaneous ex vivo apoptosis rather than defects in T cell receptor signaling. J Immunol 2009, 183:621-630. 10.4049/jimmunol.0803278, 19525395.
36. Dolhain RJ, van der Heiden AN, ter Haar NT, Breedveld FC, Miltenburg AM. Shift toward T lymphocytes with a T helper 1 cytokine-secretion profile in the joints of patients with rheumatoid arthritis. Arthritis Rheum 1996, 39:1961-1969. 10.1002/art.1780391204, 8961900.
37. Thewissen M, Somers V, Hellings N, Fraussen J, Damoiseaux J, Stinissen P. CD4 + CD28null T cells in autoimmune disease: pathogenic features and decreased susceptibility to immunoregulation. J Immunol 2007, 179:6514-6523.
38. van Bergen J, Kooy-Winkelaar EM, van Dongen H, van Gaalen FA, Thompson A, Huizinga TW, Feltkamp MC, Toes RE, Koning F. Functional killer Ig-like receptors on human memory CD4+ T cells specific for cytomegalovirus. J Immunol 2009, 182:4175-4182. 10.4049/jimmunol.0800455, 19299715.
39. Fasth AE, Snir O, Johansson AA, Nordmark B, Rahbar A, Af Klint E, Bjorkstrom NK, Ulfgren AK, van Vollenhoven RF, Malmstrom V, Trollmo C, et al. Skewed distribution of proinflammatory CD4 + CD28null T cells in rheumatoid arthritis. Arthritis Res Ther 2007, 9(5):R87. 10.1186/ar2286, 2212553, 17825098.
40. Gerli R, Schillaci G, Giordano A, Bocci EB, Bistoni O, Vaudo G, Marchesi S, Pirro M, Ragni F, Shoenfeld Y, Mannarino E, et al. CD4 + CD28- T lymphocytes contribute to early atherosclerotic damage in rheumatoid arthritis patients. Circulation 2004, 109(22):2744-2748. 10.1161/01.CIR.0000131450.66017.B3, 15159291.
41. Martens PB, Goronzy JJ, Schaid D, Weyand CM. Expansion of unusual CD4+ T cells in severe rheumatoid arthritis. Arthritis Rheum 1997, 40:1106-1114. 10.1002/art.1780400615, 9182921.
42. Rossol M, Schubert K, Meusch U, Schulz A, Biedermann B, Grosche J, Pierer M, Scholz R, Baerwald C, Thiel A, et al. Tumor necrosis factor receptor type I expression of CD4+ T cells in rheumatoid arthritis enables them to follow tumor necrosis factor gradients into the rheumatoid Synovium. Arthritis Rheum 2013, 65:1468-1476. 10.1002/art.37927, 23494522.
43. Lachmann R, Bajwa M, Vita S, Smith H, Cheek E, Akbar A, Kern F. Polyfunctional T cells accumulate in large human cytomegalovirus-specific T cell responses. J Virol 2012, 86(2):1001-1009. 10.1128/JVI.00873-11, 3255847, 22072753.