Synovial phenotypes in rheumatoid arthritis correlate with response to biologic therapeutics

Arthritis Research and Therapy

Volumn 16, Issue 2, 2014, Pages

  Dennis Jr, Glynn ^a   Holweg, Cécile T J ^a   Kummerfeld, Sarah K ^a   Choy, David F ^a   Setiadi, A F ^a   Hackney, Jason A ^a   Haverty, Peter M ^a   Gilbert, Houston ^a   Lin, Wei Y ^a   Diehl, Lauri ^a   Fischer, S ^a   Song, An ^a   Musselman, David ^a   Klearman, Micki ^a   Gabay, Cem ^b   Kavanaugh, Arthur ^c   Endres, Judith ^d   Fox, David A ^d   Martin, Flavius ^a,e   Townsend, Michael J ^a  

^a GENENTECH INC   (United States)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; BIOLOGICAL MARKER; BIOLOGICAL PRODUCT; BONE MORPHOGENETIC PROTEIN 6; CD14 ANTIGEN; CD19 ANTIGEN; CD20 ANTIGEN; CD38 ANTIGEN; CXCL13 CHEMOKINE; DISEASE MODIFYING ANTIRHEUMATIC DRUG; ETANERCEPT; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 9; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLIXIMAB; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; NONSTEROID ANTIINFLAMMATORY AGENT; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; RITUXIMAB; TOCILIZUMAB; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; X BOX BINDING PROTEIN 1; ANTIRHEUMATIC AGENT; MONOCLONAL ANTIBODY; TRANSCRIPTOME;

AREA UNDER THE CURVE; ARTICLE; CELL HETEROGENEITY; CELL TRANSPORT; COHORT ANALYSIS; CORRELATION ANALYSIS; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; HUMAN; MAJOR CLINICAL STUDY; MESENCHYME CELL; MONOTHERAPY; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PHAGOCYTOSIS; PHASE 4 CLINICAL TRIAL (TOPIC); PHENOTYPE; PROTEIN DEGRADATION; RECEIVER OPERATING CHARACTERISTIC; RHEUMATOID ARTHRITIS; RNA METABOLISM; RNA PROCESSING; SYNOVIUM; TREATMENT RESPONSE; ADULT; AGED; ARTHRITIS, RHEUMATOID; CLASSIFICATION; CLINICAL TRIAL; DNA MICROARRAY; FEMALE; GENETICS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; PHASE 4 CLINICAL TRIAL;

ADALIMUMAB; ADULT; AGED; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; BIOLOGICAL PRODUCTS; BIOMARKERS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; SYNOVIAL MEMBRANE; TRANSCRIPTOME;

EID: 84897146058     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4555     Document Type: Article

References (48)

1. Goronzy JJ, Weyand CM. Rheumatoid arthritis. Immunol Rev 2005, 204:55-73. 10.1111/j.0105-2896.2005.00245.x, 15790350.
2. Lee DM, Weinblatt ME. Rheumatoid arthritis. Lancet 2001, 358:903-911. 10.1016/S0140-6736(01)06075-5, 11567728.
3. Tak PP, Bresnihan B. The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis. Arthritis Rheum 2000, 43:2619-2633. 10.1002/1529-0131(200012)43:12<2619::AID-ANR1>3.0.CO;2-V, 11145019.
4. Lindstrom TM, Robinson WH. Biomarkers for rheumatoid arthritis: making it personal. Scand J Clin Lab Invest Suppl 2010, 242:79-84. 3417774, 20515283.
5. Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet 2010, 376:1094-1108. 10.1016/S0140-6736(10)60826-4, 20870100.
6. Weyand CM, Goronzy JJ. Ectopic germinal center formation in rheumatoid synovitis. Ann NY Acad Sci 2003, 987:140-149. 10.1111/j.1749-6632.2003.tb06042.x, 12727633.
7. Chan AC, Behrens TW. Personalizing medicine for autoimmune and inflammatory diseases. Nat Immunol 2013, 14:106-109. 10.1038/ni.2473, 23334822.
8. van der Pouw Kraan TC, van Gaalen FA, Huizinga TW, Pieterman E, Breedveld FC, Verweij CL. Discovery of distinctive gene expression profiles in rheumatoid synovium using cDNA microarray technology: evidence for the existence of multiple pathways of tissue destruction and repair. Genes Immun 2003, 4:187-196. 10.1038/sj.gene.6363975, 12700593.
9. van der Pouw Kraan TC, van Gaalen FA, Kasperkovitz PV, Verbeet NL, Smeets TJ, Kraan MC, Fero M, Tak PP, Huizinga TW, Pieterman E, Breedveld FC, Alizadeh AA, Verweij CL. Rheumatoid arthritis is a heterogeneous disease: evidence for differences in the activation of the STAT-1 pathway between rheumatoid tissues. Arthritis Rheum 2003, 48:2132-2145. 10.1002/art.11096, 12905466.
10. van Baarsen LG, Bos CL, van der Pouw Kraan TC, Verweij CL. Transcription profiling of rheumatic diseases. Arthritis Res Ther 2009, 11:207. 10.1186/ar2557, 2688218, 19232067.
11. Timmer TC, Baltus B, Vondenhoff M, Huizinga TW, Tak PP, Verweij CL, Mebius RE, van der Pouw Kraan TC. Inflammation and ectopic lymphoid structures in rheumatoid arthritis synovial tissues dissected by genomics technology: identification of the interleukin-7 signaling pathway in tissues with lymphoid neogenesis. Arthritis Rheum 2007, 56:2492-2502. 10.1002/art.22748, 17665400.
12. van der Pouw Kraan TC, Wijbrandts CA, van Baarsen LG, Rustenburg F, Baggen JM, Verweij CL, Tak PP. Responsiveness to anti-tumour necrosis factor alpha therapy is related to pre-treatment tissue inflammation levels in rheumatoid arthritis patients. Ann Rheum Dis 2008, 67:563-566.
13. Wijbrandts CA, Dijkgraaf MG, Kraan MC, Vinkenoog M, Smeets TJ, Dinant H, Vos K, Lems WF, Wolbink GJ, Sijpkens D, Dijkmans BA, Tak PP. The clinical response to infliximab in rheumatoid arthritis is in part dependent on pretreatment tumour necrosis factor alpha expression in the synovium. Ann Rheum Dis 2008, 67:1139-1144. 10.1136/ard.2007.080440, 2564801, 18055470.
14. Badot V, Galant C, Nzeusseu Toukap A, Theate I, Maudoux AL, Van den Eynde BJ, Durez P, Houssiau FA, Lauwerys BR. Gene expression profiling in the synovium identifies a predictive signature of absence of response to adalimumab therapy in rheumatoid arthritis. Arthritis Res Ther 2009, 11:R57. 10.1186/ar2678, 2688209, 19389237.
15. Lindberg J, Wijbrandts CA, van Baarsen LG, Nader G, Klareskog L, Catrina A, Thurlings R, Vervoordeldonk M, Lundeberg J, Tak PP. The gene expression profile in the synovium as a predictor of the clinical response to infliximab treatment in rheumatoid arthritis. PLoS One 2010, 5:e11310. 10.1371/journal.pone.0011310, 2892481, 20593016.
16. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, Medsger TA, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder GG. The American rheumatism association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988, 31:315-324. 10.1002/art.1780310302, 3358796.
17. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Muertter RN, Holko M, Ayanbule O, Yefanov A, Soboleva A. NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic Acids Res 2011, 39:D1005-D1010. 10.1093/nar/gkq1184, 3013736, 21097893.
18. Edgar R, Domrachev M, Lash AE. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207, 99122, 11752295.
19. R Development Core Team R: a language and environment for statistical computing. R Foundation for Statistical Computing 2011, Vienna, Austria: R Foundation for Statistical Computing, http://cran.r-project.org. ISBN 3-900051-07-0, R Development Core Team.
20. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
21. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193. 10.1093/bioinformatics/19.2.185, 12538238.
22. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264. 10.1093/biostatistics/4.2.249, 12925520.
23. Hackstadt AJ, Hess AM. Filtering for increased power for microarray data analysis. BMC Bioinformatics 2009, 10:11. 10.1186/1471-2105-10-11, 2661050, 19133141.
24. Bourgon R, Gentleman R, Huber W. Independent filtering increases detection power for high-throughput experiments. Proc Natl Acad Sci USA 2010, 107:9546-9551. 10.1073/pnas.0914005107, 2906865, 20460310.
25. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol 2003, 4:3.
26. Oron AP, Jiang Z, Gentleman R. Gene set enrichment analysis using linear models and diagnostics. Bioinformatics 2008, 24:2586-2591. 10.1093/bioinformatics/btn465, 2579710, 18790795.
27. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005, 102:15545-15550. 10.1073/pnas.0506580102, 1239896, 16199517.
28. Abbas AR, Baldwin D, Ma Y, Ouyang W, Gurney A, Martin F, Fong S, van Lookeren CM, Godowski P, Williams PM, Chan AC, Clark HF. Immune response in silico (IRIS): immune-specific genes identified from a compendium of microarray expression data. Genes Immun 2005, 6:319-331. 10.1038/sj.gene.6364173, 15789058.
29. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 1990, 9:811-818. 10.1002/sim.4780090710, 2218183.
30. Gabay C, Emery P, van Vollenhoven R, Dikranian A, Alten R, Pavelka K, Klearman M, Musselman D, Agarwal S, Green J, Kavanaugh A. Tocilizumab monotherapy versus adalimumab monotherapy for treatment of rheumatoid arthritis (ADACTA): a randomised, double-blind, controlled phase 4 trial. Lancet 2013, 381:1541-1550. 10.1016/S0140-6736(13)60250-0, 23515142.
31. Lazar AA, Cole BF, Bonetti M, Gelber RD. Evaluation of treatment-effect heterogeneity using biomarkers measured on a continuous scale: subpopulation treatment effect pattern plot. J. Clin Oncol 2010, 28:4539-4544. 10.1200/JCO.2009.27.9182, 2988642, 20837942.
32. Kishimoto T. Interleukin-6: from basic science to medicine-40 years in immunology. Annu Rev Immunol 2005, 23:1-21. 10.1146/annurev.immunol.23.021704.115806, 15771564.
33. Weyand CM, Kang YM, Kurtin PJ, Goronzy JJ. The power of the third dimension: tissue architecture and autoimmunity in rheumatoid arthritis. Curr Opin Rheumatol 2003, 15:259-266. 10.1097/00002281-200305000-00013, 12707579.
34. van Baarsen LG, Wijbrandts CA, Timmer TC, van der Pouw Kraan TC, Tak PP, Verweij CL. Synovial tissue heterogeneity in rheumatoid arthritis in relation to disease activity and biomarkers in peripheral blood. Arthritis Rheum 2010, 62:1602-1607.
35. van Oosterhout M, Bajema I, Levarht EW, Toes RE, Huizinga TW, van Laar JM. Differences in synovial tissue infiltrates between anti-cyclic citrullinated peptide-positive rheumatoid arthritis and anti-cyclic citrullinated peptide-negative rheumatoid arthritis. Arthritis Rheum 2008, 58:53-60. 10.1002/art.23148, 18163491.
36. Hogan VE, Holweg CT, Choy DF, Kummerfeld SK, Hackney JA, Teng YK, Townsend MJ, van Laar JM. Pretreatment synovial transcriptional profile is associated with early and late clinical response in rheumatoid arthritis patients treated with rituximab. Ann Rheum Dis 1888-1894, 2012:71.
37. 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. Blood autoantibody and cytokine profiles predict response to anti-tumor necrosis factor therapy in rheumatoid arthritis. Arthritis Res Ther 2009, 11:R76. 10.1186/ar2706, 2714123, 19460157.
38. Lal P, Su Z, Holweg CT, Silverman GJ, Schwartzman S, Kelman A, Read S, Spaniolo G, Monroe JG, Behrens TW, Townsend MJ. Inflammation and autoantibody markers identify rheumatoid arthritis patients with enhanced clinical benefit following rituximab treatment. Arthritis Rheum 2011, 63:3681-3691. 10.1002/art.30596, 22127691.
39. Klaasen R, Thurlings RM, Wijbrandts CA, van Kuijk AW, Baeten D, Gerlag DM, Tak PP. The relationship between synovial lymphocyte aggregates and the clinical response to infliximab in rheumatoid arthritis: a prospective study. Arthritis Rheum 2009, 60:3217-3224. 10.1002/art.24913, 19877042.
40. Canete JD, Celis R, Moll C, Izquierdo E, Marsal S, Sanmarti R, Palacin A, Lora D, de la Cruz J, Pablos JL. Clinical significance of synovial lymphoid neogenesis and its reversal after anti-tumour necrosis factor alpha therapy in rheumatoid arthritis. Ann Rheum Dis 2009, 68:751-756. 10.1136/ard.2008.089284, 18495732.
41. Krenn V, Schedel J, Doring A, Huppertz HI, Gohlke F, Tony HP, Vollmers HP, Muller-Hermelink HK. Endothelial cells are the major source of sICAM-1 in rheumatoid synovial tissue. Rheumatol Int 1997, 17:17-27. 10.1007/PL00006846, 9194210.
42. Witkowska AM, Borawska MH. Soluble intercellular adhesion molecule-1 (sICAM-1): an overview. Eur Cytokine Netw 2004, 15:91-98.
43. Corsiero E, Bombardieri M, Manzo A, Bugatti S, Uguccioni M, Pitzalis C. Role of lymphoid chemokines in the development of functional ectopic lymphoid structures in rheumatic autoimmune diseases. Immunol Lett 2012, 145:62-67. 10.1016/j.imlet.2012.04.013, 22698185.
44. Rosengren S, Wei N, Kalunian KC, Kavanaugh A, Boyle DL. CXCL13: a novel biomarker of B-cell return following rituximab treatment and synovitis in patients with rheumatoid arthritis. Rheumatol (Oxford) 2011, 50:603-610.
45. Meeuwisse CM, van der Linden MP, Rullmann TA, Allaart CF, Nelissen R, Huizinga TW, Garritsen A, Toes RE, van Schaik R, van der Helm-van Mil AH. Identification of CXCL13 as a marker for rheumatoid arthritis outcome using an in silico model of the rheumatic joint. Arthritis Rheum 2011, 63:1265-1273. 10.1002/art.30273, 21305530.
46. Choy E. Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatol (Oxford) 2012, 51:v3-v11.
47. Chen G, Goeddel DV. TNF-R1 signaling: a beautiful pathway. Science 2002, 296:1634-1635. 10.1126/science.1071924, 12040173.
48. Emery P, Keystone E, Tony HP, Cantagrel A, van Vollenhoven R, Sanchez A, Alecock E, Lee J, Kremer J. IL-6 receptor inhibition with tocilizumab improves treatment outcomes in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor biologicals: results from a 24-week multicentre randomised placebo-controlled trial. Ann Rheum Dis 2008, 67:1516-1523. 10.1136/ard.2008.092932, 3811149, 18625622.