User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Synovial Tissue: Turning the Page to Precision Medicine in Arthritis.

Primary tabs

download
  • Open access
  • PDF
  • 647.31 K
Triaille, Clément [UCL] Lauwerys, Bernard [UCL]

Rheumatoid arthritis (RA) is a chronic systemic inflammatory disease targeting the joints. Current treatment strategies are based on clinical, biological and radiological features, yet still fail to reach the goal of early low disease activity in a significant number of cases. Hence, there is a need for refining current treatment algorithms, using accurate markers of response to therapy. Because RA induces histological and molecular alterations in the synovium even before apparition of clinical symptoms, synovial biopsies are a promising tool in the search of such new biomarkers. Histological and molecular characteristics of RA synovitis are heterogeneous. Variations in synovial lining layer hyperplasia, in cellular infiltration of the sublining by immune cells of myeloid and lymphoid lineages, and in molecular triggers of these features are currently categorized using well-defined pathotypes: myeloid, lymphoid, fibroid and pauci-immune. Here, we first bring the plasticity of RA synovitis under scrutiny, i.e., how variations in synovial characteristics are associated with relevant clinical features (disease duration, disease activity, effects of therapies, disease severity). Primary response to a specific drug could be, at least theoretically, related to the representation of the molecular pathway targeted by the drug in the synovium. Alternatively, absence of primary response to a specific agent could be due to disease severity, i.e., overrepresentation of all synovial molecular pathways driving disease activity overwhelming the capacity of any drug to block them. Using this theoretical frame, we will highlight how the findings of previous studies trying to link response to therapy with synovial changes provide promising perspectives on bridging the gap to personalized medicine in RA.

Document type Article de périodique (Journal article) – Synthèse de littérature
Access type Accès libre
Publication date 2019
Language Anglais
Journal information "Frontiers in medicine" - Vol. 6, p. 46 [1-12] (2019)
Peer reviewed yes
Publisher Frontiers Media S.A. ((Switzerland) Basel)
e-issn 2296-858X
Publication status Publié
Affiliations UCL - SSS/IREC/RUMA - Pôle de Pathologies rhumatismales
UCL - (SLuc) Service de rhumatologie
UCL - (SLuc) Service d'hématologie et d'oncologie pédiatrique
Keywords biologics ; precision medicine ; response to therapy ; rheumatoid arthritis ; synovial biopsies
Links
  1. Aletaha Daniel, Neogi Tuhina, Silman Alan J., Funovits Julia, Felson David T., Bingham Clifton O., Birnbaum Neal S., Burmester Gerd R., Bykerk Vivian P., Cohen Marc D., Combe Bernard, Costenbader Karen H., Dougados Maxime, Emery Paul, Ferraccioli Gianfranco, Hazes Johanna M. W., Hobbs Kathryn, Huizinga Tom W. J., Kavanaugh Arthur, Kay Jonathan, Kvien Tore K., Laing Timothy, Mease Philip, Ménard Henri A., Moreland Larry W., Naden Raymond L., Pincus Theodore, Smolen Josef S., Stanislawska-Biernat Ewa, Symmons Deborah, Tak Paul P., Upchurch Katherine S., Vencovský Jiří, Wolfe Frederick, Hawker Gillian, 2010 Rheumatoid arthritis classification criteria: An American College of Rheumatology/European League Against Rheumatism collaborative initiative, 10.1002/art.27584
  2. Aletaha, Ann Rheum Dis., 69, 1580 (2010)
  3. Visser K., Goekoop-Ruiterman Y. P. M., de Vries-Bouwstra J. K., Ronday H. K., Seys P. E. H., Kerstens P. J. S. M., Huizinga T. W. J., Dijkmans B. A. C., Allaart C. F., 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, 10.1136/ard.2009.121160
  4. Smolen Josef S, Landewé Robert, Bijlsma Johannes, Burmester Gerd, Chatzidionysiou Katerina, Dougados Maxime, Nam Jackie, Ramiro Sofia, Voshaar Marieke, van Vollenhoven Ronald, Aletaha Daniel, Aringer Martin, Boers Maarten, Buckley Chris D, Buttgereit Frank, Bykerk Vivian, Cardiel Mario, Combe Bernard, Cutolo Maurizio, van Eijk-Hustings Yvonne, Emery Paul, Finckh Axel, Gabay Cem, Gomez-Reino Juan, Gossec Laure, Gottenberg Jacques-Eric, Hazes Johanna M W, Huizinga Tom, Jani Meghna, Karateev Dmitry, Kouloumas Marios, Kvien Tore, Li Zhanguo, Mariette Xavier, McInnes Iain, Mysler Eduardo, Nash Peter, Pavelka Karel, Poór Gyula, Richez Christophe, van Riel Piet, Rubbert-Roth Andrea, Saag Kenneth, da Silva Jose, Stamm Tanja, Takeuchi Tsutomu, Westhovens René, de Wit Maarten, van der Heijde Désirée, EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2016 update, 10.1136/annrheumdis-2016-210715
  5. Nam Jackie L, Takase-Minegishi Kaoru, Ramiro Sofia, Chatzidionysiou Katerina, Smolen Josef S, van der Heijde Désirée, Bijlsma Johannes W, Burmester Gerd R, Dougados Maxime, Scholte-Voshaar Marieke, van Vollenhoven Ronald, Landewé Robert, Efficacy of biological disease-modifying antirheumatic drugs: a systematic literature review informing the 2016 update of the EULAR recommendations for the management of rheumatoid arthritis, 10.1136/annrheumdis-2016-210713
  6. Aletaha Daniel, Smolen Josef S., Diagnosis and Management of Rheumatoid Arthritis : A Review, 10.1001/jama.2018.13103
  7. Kelly S, Humby F, Filer A, Ng N, Di Cicco M, Hands R E, Rocher V, Bombardieri M, D'Agostino M A, McInnes I B, Buckley C D, Taylor P C, Pitzalis C, Ultrasound-guided synovial biopsy: a safe, well-tolerated and reliable technique for obtaining high-quality synovial tissue from both large and small joints in early arthritis patients, 10.1136/annrheumdis-2013-204603
  8. Baeten D., Van den Bosch F., Elewaut D., Stuer A., Veys E. M., De Keyser F., Needle Arthroscopy of the Knee with Synovial Biopsy Sampling: Technical Experience in 150 Patients, 10.1007/s100670050134
  9. Najm Aurélie, Orr Carl, Heymann Marie-Françoise, Bart Géraldine, Veale Douglas J., Le Goff Benoît, Success Rate and Utility of Ultrasound-guided Synovial Biopsies in Clinical Practice, 10.3899/jrheum.151441
  10. Orr Carl, Vieira-Sousa Elsa, Boyle David L., Buch Maya H., Buckley Christopher D., Cañete Juan D., Catrina Anca I., Choy Ernest H. S., Emery Paul, Fearon Ursula, Filer Andrew, Gerlag Danielle, Humby Frances, Isaacs John D., Just Søren A., Lauwerys Bernard R., Le Goff Benoit, Manzo Antonio, McGarry Trudy, McInnes Iain B., Najm Aurélie, Pitzalis Constantino, Pratt Arthur, Smith Malcolm, Tak Paul P., Tas Sander W., Thurlings Rogier, Fonseca João E., Veale Douglas J., Synovial tissue research: a state-of-the-art review, 10.1038/nrrheum.2017.115
  11. Krenn V, Morawietz L, Burmester G-R, Kinne R W, Mueller-Ladner U, Muller B, Haupl T, Synovitis score: discrimination between chronic low-grade and high-grade synovitis, 10.1111/j.1365-2559.2006.02508.x
  12. Toukap A. Nzeusseu, Galant C., Theate I., Maudoux A. L., Lories R. J. U., Houssiau F. A., Lauwerys B. R., Identification of distinct gene expression profiles in the synovium of patients with systemic lupus erythematosus, 10.1002/art.22578
  13. Baeten D, Comparative study of the synovial histology in rheumatoid arthritis, spondyloarthropathy, and osteoarthritis: influence of disease duration and activity, 10.1136/ard.59.12.945
  14. Kruithof Elli, Baeten Dominique, De Rycke Leen, Vandooren Bernard, Foell Dirk, Roth Johannes, Cañete Juan D, Boots Annemieke M, Veys Eric M, De Keyser Filip, 10.1186/ar1698
  15. Ulfgren A.-K., Interindividual and intra-articular variation of proinflammatory cytokines in patients with rheumatoid arthritis: potential implications for treatment, 10.1136/ard.59.6.439
  16. Dennis Glynn, Holweg Cécile TJ, Kummerfeld Sarah K, Choy David F, Setiadi A, Hackney Jason A, Haverty Peter M, Gilbert Houston, Lin Wei, Diehl Lauri, Fischer S, Song An, Musselman David, Klearman Micki, Gabay Cem, Kavanaugh Arthur, Endres Judith, Fox David A, Martin Flavius, Townsend Michael J, Synovial phenotypes in rheumatoid arthritis correlate with response to biologic therapeutics, 10.1186/ar4555
  17. Pitzalis Costantino, Kelly Stephen, Humby Frances, New learnings on the pathophysiology of RA from synovial biopsies : , 10.1097/bor.0b013e32835fd8eb
  18. Takemura Seisuke, Braun Andrea, Crowson Cynthia, Kurtin Paul J., Cofield Robert H., O’Fallon William M., Goronzy Jörg J., Weyand Cornelia M., Lymphoid Neogenesis in Rheumatoid Synovitis, 10.4049/jimmunol.167.2.1072
  19. van de Sande M. G. H., Thurlings R. M., Boumans M. J. H., Wijbrandts C. A., Modesti M. G., Gerlag D. M., Tak P. P., Presence of lymphocyte aggregates in the synovium of patients with early arthritis in relationship to diagnosis and outcome: is it a constant feature over time?, 10.1136/ard.2010.139287
  20. Canete J D, Celis R, Moll C, Izquierdo E, Marsal S, Sanmarti R, Palacin A, Lora D, de la Cruz J, Pablos J L, Clinical significance of synovial lymphoid neogenesis and its reversal after anti-tumour necrosis factor   therapy in rheumatoid arthritis, 10.1136/ard.2008.089284
  21. Klimiuk, J Rheumatol., 32, 1666 (2005)
  22. Thurlings Rogier M., Wijbrandts Carla A., Mebius Reina E., Cantaert Tineke, Dinant Huibert J., van der Pouw-Kraan Tineke C. T. M., Verweij Cornelis L., Baeten Dominique, Tak Paul P., Synovial lymphoid neogenesis does not define a specific clinical rheumatoid arthritis phenotype, 10.1002/art.23505
  23. Ducreux Julie, Durez Patrick, Galant Christine, Nzeusseu Toukap Adrien, Van den Eynde Benoît, Houssiau Frédéric A., Lauwerys Bernard R., Global Molecular Effects of Tocilizumab Therapy in Rheumatoid Arthritis Synovium : Molecular Effects of Tocilizumab Therapy, 10.1002/art.38202
  24. Shen-Orr Shai S, Gaujoux Renaud, Computational deconvolution: extracting cell type-specific information from heterogeneous samples, 10.1016/j.coi.2013.09.015
  25. Papalexi Efthymia, Satija Rahul, Single-cell RNA sequencing to explore immune cell heterogeneity, 10.1038/nri.2017.76
  26. Orr Carl, Najm Aurelie, Biniecka Monika, McGarry Trudy, Ng Chin-Teck, Young Francis, Fearon Ursula, Veale Douglas J., Synovial Immunophenotype and Anti-Citrullinated Peptide Antibodies in Rheumatoid Arthritis Patients : Relationship to Treatment Response and Radiologic Prognosis, 10.1002/art.40218
  27. Humby Frances, Bombardieri Michele, Manzo Antonio, Kelly Stephen, Blades Mark C, Kirkham Bruce, Spencer Jo, Pitzalis Costantino, Ectopic Lymphoid Structures Support Ongoing Production of Class-Switched Autoantibodies in Rheumatoid Synovium, 10.1371/journal.pmed.0060001
  28. Doorenspleet M E, Klarenbeek P L, de Hair M J H, van Schaik B D C, Esveldt R E E, van Kampen A H C, Gerlag D M, Musters A, Baas F, Tak P P, de Vries N, Rheumatoid arthritis synovial tissue harbours dominant B-cell and plasma-cell clones associated with autoreactivity, 10.1136/annrheumdis-2012-202861
  29. Kerkman Priscilla F, Kempers Ayla C, van der Voort Ellen I H, van Oosterhout Maikel, Huizinga Tom W J, Toes René E M, Scherer Hans U, Synovial fluid mononuclear cells provide an environment for long-term survival of antibody-secreting cells and promote the spontaneous production of anti-citrullinated protein antibodies, 10.1136/annrheumdis-2015-208554
  30. Harre Ulrike, Georgess Dan, Bang Holger, Bozec Aline, Axmann Roland, Ossipova Elena, Jakobsson Per-Johan, Baum Wolfgang, Nimmerjahn Falk, Szarka Eszter, Sarmay Gabriella, Krumbholz Grit, Neumann Elena, Toes Rene, Scherer Hans-Ulrich, Catrina Anca Irinel, Klareskog Lars, Jurdic Pierre, Schett Georg, Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin, 10.1172/jci60975
  31. Takemura Seisuke, Klimiuk Piotr A., Braun Andrea, Goronzy Jörg J., Weyand Cornelia M., T Cell Activation in Rheumatoid Synovium Is B Cell Dependent, 10.4049/jimmunol.167.8.4710
  32. Armas-González Estefanía, Díaz-Martín Ana, Domínguez-Luis María Jesús, Arce-Franco María Teresa, Herrera-García Ada, Hernández-Hernández María Vanesa, Bustabad Sagrario, Usategui Alicia, Pablos José L., Cañete Juan D., Díaz-González Federico, Differential Antigen-presenting B Cell Phenotypes from Synovial Microenvironment of Patients with Rheumatoid and Psoriatic Arthritis, 10.3899/jrheum.141577
  33. Meednu Nida, Zhang Hengwei, Owen Teresa, Sun Wen, Wang Victor, Cistrone Christopher, Rangel-Moreno Javier, Xing Lianping, Anolik Jennifer H., Production of RANKL by Memory B Cells: A Link Between B Cells and Bone Erosion in Rheumatoid Arthritis : B CELL PRODUCTION OF RANKL IN RA, 10.1002/art.39489
  34. Yeo L., Toellner K.-M., Salmon M., Filer A., Buckley C. D., Raza K., Scheel-Toellner D., Cytokine mRNA profiling identifies B cells as a major source of RANKL in rheumatoid arthritis, 10.1136/ard.2011.153312
  35. Orr Carl K., Najm Aurelie, Young Francis, McGarry Trudy, Biniecka Monika, Fearon Ursula, Veale Douglas J., The Utility and Limitations of CRP, ESR and DAS28-CRP in Appraising Disease Activity in Rheumatoid Arthritis, 10.3389/fmed.2018.00185
  36. Orange Dana E., Agius Phaedra, DiCarlo Edward F., Robine Nicolas, Geiger Heather, Szymonifka Jackie, McNamara Michael, Cummings Ryan, Andersen Kathleen M., Mirza Serene, Figgie Mark, Ivashkiv Lionel B., Pernis Alessandra B., Jiang Caroline S., Frank Mayu O., Darnell Robert B., Lingampali Nithya, Robinson William H., Gravallese Ellen, Bykerk Vivian P., Goodman Susan M., Donlin Laura T., , Identification of Three Rheumatoid Arthritis Disease Subtypes by Machine Learning Integration of Synovial Histologic Features and RNA Sequencing Data, 10.1002/art.40428
  37. Kasperkovitz Pia V., Timmer Trieneke C. G., Smeets Tom J., Verbeet Nicolette L., Tak Paul P., van baarsen Lisa G. M., Baltus Belinda, Huizinga Tom W. J., Pieterman Elsbet, Fero Mike, Firestein Gary S., van der Pouw Kraan Tineke C. T. M., Verweij Cornelis L., Fibroblast-like synoviocytes derived from patients with rheumatoid arthritis show the imprint of synovial tissue heterogeneity: Evidence of a link between an increased myofibroblast-like phenotype and high-inflammation synovitis, 10.1002/art.20811
  38. Smeets T J M, Analysis of the cell infiltrate and expression of proinflammatory cytokines and matrix metalloproteinases in arthroscopic synovial biopsies: comparison with synovial samples from patients with end stage, destructive rheumatoid arthritis, 10.1136/ard.62.7.635
  39. Lequerré Thierry, Bansard Carine, Vittecoq Olivier, Derambure Céline, Hiron Martine, Daveau Maryvonne, Tron François, Ayral Xavier, Biga Norman, Auquit-Auckbur Isabelle, Chiocchia Gilles, Le Loët Xavier, Salier Jean-Philippe, Early and long-standing rheumatoid arthritis: distinct molecular signatures identified by gene-expression profiling in synovia, 10.1186/ar2744
  40. Tsubaki Takahito, Arita Norimasa, Kawakami Takuma, Shiratsuchi Takayuki, Yamamoto Haruyasu, Takubo Nobuo, Yamada Kazuhito, Nakata Sanpei, Yamamoto Sumiki, Nose Masato, 10.1186/ar1751
  41. Lauwerys Bernard R., Hernández-Lobato Daniel, Gramme Pierre, Ducreux Julie, Dessy Adrien, Focant Isabelle, Ambroise Jérôme, Bearzatto Bertrand, Nzeusseu Toukap Adrien, Van den Eynde Benoît J., Elewaut Dirk, Gala Jean-Luc, Durez Patrick, Houssiau Frédéric A., Helleputte Thibault, Dupont Pierre, Heterogeneity of Synovial Molecular Patterns in Patients with Arthritis, 10.1371/journal.pone.0122104
  42. van Oosterhout M., Bajema I., Levarht E. W. N., Toes R. E. M., Huizinga T. W. J., van Laar J. M., Differences in synovial tissue infiltrates between anti–cyclic citrullinated peptide–positive rheumatoid arthritis and anti–cyclic citrullinated peptide–negative rheumatoid arthritis, 10.1002/art.23148
  43. van Baarsen Lisa G. M., Wijbrandts Carla A., Timmer Trieneke C. G., van der Pouw Kraan Tineke C. T. M., Tak Paul P., Verweij Cornelis L., Synovial tissue heterogeneity in rheumatoid arthritis in relation to disease activity and biomarkers in peripheral blood, 10.1002/art.27415
  44. De Groof Aurélie, Ducreux Julie, Humby Frances, Nzeusseu Toukap Adrien, Badot Valérie, Pitzalis Costantino, Houssiau Frédéric A., Durez Patrick, Lauwerys Bernard R., Higher expression of TNFα-induced genes in the synovium of patients with early rheumatoid arthritis correlates with disease activity, and predicts absence of response to first line therapy, 10.1186/s13075-016-0919-z
  45. Badot Valérie, Galant Christine, Nzeusseu Toukap Adrien, Theate Ivan, Maudoux Anne-Lise, Van den Eynde Benoît J, Durez Patrick, Houssiau Frédéric A, Lauwerys Bernard R, Gene expression profiling in the synovium identifies a predictive signature of absence of response to adalimumab therapy in rheumatoid arthritis, 10.1186/ar2678
  46. Gutierrez-Roelens I., Galant C., Theate I., Lories R. J., Durez P., Nzeusseu-Toukap A., Van den Eynde B., Houssiau F. A., Lauwerys B. R., Rituximab treatment induces the expression of genes involved in healing processes in the rheumatoid arthritis synovium, 10.1002/art.30292
  47. van, Arthritis Rheum., 63, 1507 (2011)
  48. Vos Koen, Thurlings Rogier M., Wijbrandts Carla A., van Schaardenburg Dirkjan, Gerlag Daniëlle M., Tak Paul P., Early effects of rituximab on the synovial cell infiltrate in patients with rheumatoid arthritis, 10.1002/art.22400
  49. Teng, Arthritis Rheum., 56, 3909 (2007)
  50. Kavanaugh A, Rosengren S, Lee S J, Hammaker D, Firestein G S, Kalunian K, Wei N, Boyle D L, Assessment of rituximab's immunomodulatory synovial effects (ARISE trial). 1: clinical and synovial biomarker results, 10.1136/ard.2007.074229
  51. Smeets, Arthritis Rheum., 48, 2155 (2003)
  52. BRESNIHAN BARRY, PONTIFEX ELIZA, THURLINGS ROGIER M., VINKENOOG MARJOLEIN, EL-GABALAWY HANI, FEARON URSULA, FITZGERALD OLIVER, GERLAG DANIELLE M., ROONEY TERENCE, van de SANDE MARLEEN G., VEALE DOUGLAS, VOS KOEN, TAK PAUL-PETER, Synovial Tissue Sublining CD68 Expression Is a Biomarker of Therapeutic Response in Rheumatoid Arthritis Clinical Trials: Consistency Across Centers, 10.3899/jrheum.090348
  53. Bresnihan, J Rheumatol., 34, 620 (2007)
  54. Lindberg Johan, Wijbrandts Carla A., van Baarsen Lisa G., Nader Gustavo, Klareskog Lars, Catrina Anca, Thurlings Rogier, Vervoordeldonk Margriet, Lundeberg Joakim, Tak Paul P., The Gene Expression Profile in the Synovium as a Predictor of the Clinical Response to Infliximab Treatment in Rheumatoid Arthritis, 10.1371/journal.pone.0011310
  55. Aletaha Daniel, Funovits Julia, Keystone Edward C., Smolen Josef S., Disease activity early in the course of treatment predicts response to therapy after one year in rheumatoid arthritis patients, 10.1002/art.22943
  56. Felson David T., Anderson Jennifer J., Boers Maarten, Bombardier Claire, Furst Daniel, Goldsmith Charles, Katz Linda M., Lightfoot Robert, Paulus Harold, Strand Vibeke, Tugwell Peter, Weinblatt Michael, James Williams H., Wolfe Frederick, Kieszak Stephanie, American college of rheumatology preliminary definition of improvement in rheumatoid arthritis, 10.1002/art.1780380602
  57. van, Arthritis Rheum., 39, 39 (1996)
  58. Wolbink Gerrit Jan, Vis Marijn, Lems Willem, Voskuyl Alexandre E., De Groot Els, Nurmohamed Michael T., Stapel Steven, Tak Paul P., Aarden Lucien, Dijkmans Ben, Development of antiinfliximab antibodies and relationship to clinical response in patients with rheumatoid arthritis, 10.1002/art.21671
  59. Bartelds G. M, Wijbrandts C. A, Nurmohamed M. T, Stapel S., Lems W. F, Aarden L., Dijkmans B. A C, Tak P. P., Wolbink G. J., Clinical response to adalimumab: relationship to anti-adalimumab antibodies and serum adalimumab concentrations in rheumatoid arthritis, 10.1136/ard.2006.065615
  60. Lindberg Johan, af Klint Erik, Catrina Anca, Nilsson Peter, Klareskog Lars, Ulfgren Ann-Kristin, Lundeberg Joakim, 10.1186/ar2090
  61. van der Pouw Kraan T C, Wijbrandts C A, van Baarsen L G, Rustenburg F, Baggen J M, Verweij C L, Tak P P, Responsiveness to anti-tumour necrosis factor   therapy is related to pre-treatment tissue inflammation levels in rheumatoid arthritis patients, 10.1136/ard.2007.081950
  62. Hogan Vanessa E, Holweg Cécile T J, Choy David F, Kummerfeld Sarah K, Hackney Jason A, Teng Y K Onno, Townsend Michael J, vanLaar Jacob M, Pretreatment synovial transcriptional profile is associated with early and late clinical response in rheumatoid arthritis patients treated with rituximab, 10.1136/annrheumdis-2011-201115
  63. Klaasen Ruth, Thurlings Rogier M., Wijbrandts Carla A., van Kuijk Arno W., Baeten Dominique, Gerlag Danielle M., Tak Paul P., The relationship between synovial lymphocyte aggregates and the clinical response to infliximab in rheumatoid arthritis: A prospective study, 10.1002/art.24913
  64. Gabay Cem, Emery Paul, van Vollenhoven Ronald, Dikranian Ara, Alten Rieke, Pavelka Karel, Klearman Micki, Musselman David, Agarwal Sunil, Green Jennifer, Kavanaugh Arthur, Tocilizumab monotherapy versus adalimumab monotherapy for treatment of rheumatoid arthritis (ADACTA): a randomised, double-blind, controlled phase 4 trial, 10.1016/s0140-6736(13)60250-0
  65. Badot V., Durez P., Van den Eynde B.J., Nzeusseu-Toukap A., Houssiau F.A., Lauwerys B.R., Rheumatoid arthritis synovial fibroblasts produce a soluble form of the interleukin-7 receptor in response to pro-inflammatory cytokines, 10.1111/j.1582-4934.2010.01228.x
  66. Raterman Hennie G, Vosslamber Saskia, de Ridder Sander, Nurmohamed Michael T, Lems Willem F, Boers Maarten, van de Wiel Mark, Dijkmans Ben AC, Verweij Cornelis L, Voskuyl Alexandre E, Interferon type I signature may predict non response upon rituximab in rheumatoid arthritis patients, 10.1186/ar3819
  67. Thurlings Rogier M., Boumans Marie, Tekstra Janneke, van Roon Joel A., Vos Koen, van Westing Daisy Marie, van Baarsen Lisa G., Bos Carina, Kirou Kyriakos A., Gerlag Danielle M., Crow Mary K., Bijlsma Johannes W., Verweij Cornelis L., Tak Paul P., Relationship between the type I interferon signature and the response to rituximab in rheumatoid arthritis patients : Type I IFN Signature and Response to Rituximab in RA, 10.1002/art.27702
  68. Humby Frances, Kelly Stephen, Bugatti Serena, Manzo Antonio, Filer Andrew, Mahto Arti, Fonseca Joao Eurico, Lauwerys Bernard, D’Agostino Maria-Antonietta, Naredo Esperanza, Lories Rik, Montecucco Carlomaurizio, Tak Paul Peter, Fitzgerald Oliver, Smith Malcolm D., Veale Douglas J., Choy Ernest H., Strand Vibeke, Pitzalis Costantino, Evaluation of Minimally Invasive, Ultrasound-guided Synovial Biopsy Techniques by the OMERACT Filter — Determining Validation Requirements, 10.3899/jrheum.141199
  69. van de Sande M. G. H., Gerlag D. M., Lodde B. M., van Baarsen L. G. M., Alivernini S., Codullo V., Felea I., Vieira-Sousa E., Fearon U., Reece R., Montecucco C., Veale D. J., Pitzalis C., Emery P., Klareskog L., McInnes I. B., Tak P. P., Evaluating antirheumatic treatments using synovial biopsy: a recommendation for standardisation to be used in clinical trials, 10.1136/ard.2010.139550
  70. Stephenson William, Donlin Laura T., Butler Andrew, Rozo Cristina, Bracken Bernadette, Rashidfarrokhi Ali, Goodman Susan M., Ivashkiv Lionel B., Bykerk Vivian P., Orange Dana E., Darnell Robert B., Swerdlow Harold P., Satija Rahul, Single-cell RNA-seq of rheumatoid arthritis synovial tissue using low-cost microfluidic instrumentation, 10.1038/s41467-017-02659-x
Bibliographic reference Triaille, Clément ; Lauwerys, Bernard. Synovial Tissue: Turning the Page to Precision Medicine in Arthritis.. In: Frontiers in medicine, Vol. 6, p. 46 [1-12] (2019)
Permanent URL http://hdl.handle.net/2078.1/216952