Current understanding of the pathophysiology of systemic juvenile idiopathic arthritis (sJIA) and target-directed therapeutic approaches

Clinical Immunology

Volumn 159, Issue 1, 2015, Pages 72-83

  Bruck, Normi ^a   Schnabel, Anja ^a   Hedrich, Christian M ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Cytokine; Inflammation; Pathophysiology; Still's disease; Systemic JIA; Treatment

Indexed keywords

ADALIMUMAB; C REACTIVE PROTEIN; CANAKINUMAB; CORTICOSTEROID; CRYOPYRIN; DISEASE MODIFYING ANTIRHEUMATIC DRUG; ETANERCEPT; INTERFERON REGULATORY FACTOR 5; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; METHOTREXATE; PROTEIN S 100; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; RILONACEPT; TOCILIZUMAB; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR INHIBITOR; ANTIRHEUMATIC AGENT; CYTOKINE; GLUCOCORTICOID; HYBRID PROTEIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR ALPHA;

ANEMIA; ARTHRITIS; AUTOLOGOUS HEMATOPOIETIC STEM CELL TRANSPLANTATION; CORTICOSTEROID THERAPY; CYTOKINE RESPONSE; DISEASE COURSE; DNA POLYMORPHISM; FEVER; GENE MUTATION; GENERALIZED LYMPHADENOPATHY; GENETIC ASSOCIATION; HEMOPHAGOCYTIC SYNDROME; HUMAN; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MACROPHAGE ACTIVATION SYNDROME; MACROPHAGE MIGRATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REVIEW; SPLENOMEGALY; SYNOVIAL FLUID; SYSTEMIC JUVENILE IDIOPATHIC ARTHRITIS; TREATMENT RESPONSE; ANTAGONISTS AND INHIBITORS; ARTHRITIS, JUVENILE; GENETICS; IMMUNOLOGY;

ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIRHEUMATIC AGENTS; ARTHRITIS, JUVENILE; CYTOKINES; GLUCOCORTICOIDS; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; MACROPHAGE ACTIVATION SYNDROME; RECOMBINANT FUSION PROTEINS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84929591196     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2015.04.018     Document Type: Review

References (85)

1. Hedrich C.M., Bruck N., Fiebig B., Gahr M. Anakinra: a safe and effective first-line treatment in systemic onset juvenile idiopathic arthritis (SoJIA). Rheumatol. Int. 2012, 32(11):3525-3530.
2. Petty R.E., Southwood T.R., Manners P., et al. International League of Associations for Rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J. Rheumatol. 2004, 31(2):390-392.
3. Still G.F. On a form of chronic joint disease in children. Med.-Chir. Trans. 1897, 80:47-60. (9).
4. Correll C.K., Binstadt B.A. Advances in the pathogenesis and treatment of systemic juvenile idiopathic arthritis. Pediatr. Res. 2014, 75(1-2):176-183.
5. Martini A. Systemic juvenile idiopathic arthritis. Autoimmun. Rev. 2012, 12(1):56-59.
6. Mellins E.D., Macaubas C., Grom A.A. Pathogenesis of systemic juvenile idiopathic arthritis: some answers, more questions. Nat. Rev. Rheumatol. 2011, 7(7):416-426.
7. Behrens E.M., Beukelman T., Gallo L., et al. Evaluation of the presentation of systemic onset juvenile rheumatoid arthritis: data from the Pennsylvania Systemic Onset Juvenile Arthritis Registry (PASOJAR). J. Rheumatol. 2008, 35(2):343-348.
8. Brydges S., Kastner D.L. The systemic autoinflammatory diseases: inborn errors of the innate immune system. Curr. Top. Microbiol. Immunol. 2006, 305:127-160.
9. Hedrich C.M., Tsokos G.C. Bridging the gap between autoinflammation and autoimmunity. Clin. Immunol. 2013, 147(3):151-154.
10. Park H., Bourla A.B., Kastner D.L., Colbert R.A., Siegel R.M. Lighting the fires within: the cell biology of autoinflammatory diseases. Nat. Rev. Immunol. 2012, 12(8):570-580.
11. Oen K., Malleson P.N., Cabral D.A., Rosenberg A.M., Petty R.E., Cheang M. Disease course and outcome of juvenile rheumatoid arthritis in a multicenter cohort. J. Rheumatol. 2002, 29(9):1989-1999.
12. Schneider R., Lang B.A., Reilly B.J., et al. Prognostic indicators of joint destruction in systemic-onset juvenile rheumatoid arthritis. J. Pediatr. 1992, 120(2 Pt 1):200-205.
13. Singh-Grewal D., Schneider R., Bayer N., Feldman B.M. Predictors of disease course and remission in systemic juvenile idiopathic arthritis: significance of early clinical and laboratory features. Arthritis Rheum. 2006, 54(5):1595-1601.
14. Pascual V., Allantaz F., Arce E., Punaro M., Banchereau J. Role of interleukin-1 (IL-1) in the pathogenesis of systemic onset juvenile idiopathic arthritis and clinical response to IL-1 blockade. J. Exp. Med. 2005, 201(9):1479-1486.
15. Fall N., Barnes M., Thornton S., et al. Gene expression profiling of peripheral blood from patients with untreated new-onset systemic juvenile idiopathic arthritis reveals molecular heterogeneity that may predict macrophage activation syndrome. Arthritis Rheum. 2007, 56(11):3793-3804.
16. Ogilvie E.M., Khan A., Hubank M., Kellam P., Woo P. Specific gene expression profiles in systemic juvenile idiopathic arthritis. Arthritis Rheum. 2007, 56(6):1954-1965.
17. Nigrovic P.A., Mannion M., Prince F.H., et al. Anakinra as first-line disease-modifying therapy in systemic juvenile idiopathic arthritis: report of forty-six patients from an international multicenter series. Arthritis Rheum. 2011, 63(2):545-555.
18. Vastert S.J., de Jager W., Noordman B.J., et al. Effectiveness of first-line treatment with recombinant interleukin-1 receptor antagonist in steroid-naive patients with new-onset systemic juvenile idiopathic arthritis: results of a prospective cohort study. Arthritis Rheumatol. 2014, 66(4):1034-1043.
19. Verbsky J.W., White A.J. Effective use of the recombinant interleukin 1 receptor antagonist anakinra in therapy resistant systemic onset juvenile rheumatoid arthritis. J. Rheumatol. 2004, 31(10):2071-2075.
20. de Jager W., Hoppenreijs E.P., Wulffraat N.M., Wedderburn L.R., Kuis W., Prakken B.J. Blood and synovial fluid cytokine signatures in patients with juvenile idiopathic arthritis: a cross-sectional study. Ann. Rheum. Dis. 2007, 66(5):589-598.
21. de Jager W., Vastert S.J., Beekman J.M., et al. Defective phosphorylation of interleukin-18 receptor beta causes impaired natural killer cell function in systemic-onset juvenile idiopathic arthritis. Arthritis Rheum. 2009, 60(9):2782-2793.
22. Barker B.R., Taxman D.J., Ting J.P. Cross-regulation between the IL-1beta/IL-18 processing inflammasome and other inflammatory cytokines. Curr. Opin. Immunol. 2011, 23(5):591-597.
23. Hedrich C.M., Bruck N., Paul D., Hahn G., Gahr M., Rosen-Wolff A. "Mutation negative" familial cold autoinflammatory syndrome (FCAS) in an 8-year-old boy: clinical course and functional studies. Rheumatol. Int. 2012, 32(9):2629-2636.
24. Hedrich C.M., Fiebig B., Sallmann S., et al. Good response to IL-1beta blockade by anakinra in a 23-year-old CINCA/NOMID patient without mutations in the CIAS1 gene. Cytokine profiles and functional studies. Scand. J. Rheumatol. 2008, 37(5):385-389.
25. Day T.G., Ramanan A.V., Hinks A., et al. Autoinflammatory genes and susceptibility to psoriatic juvenile idiopathic arthritis. Arthritis Rheum. 2008, 58(7):2142-2146.
26. Cazzola M., Ponchio L., de Benedetti F., et al. Defective iron supply for erythropoiesis and adequate endogenous erythropoietin production in the anemia associated with systemic-onset juvenile chronic arthritis. Blood 1996, 87(11):4824-4830.
27. de Benedetti F., Massa M., Robbioni P., Ravelli A., Burgio G.R., Martini A. Correlation of serum interleukin-6 levels with joint involvement and thrombocytosis in systemic juvenile rheumatoid arthritis. Arthritis Rheum. 1991, 34(9):1158-1163.
28. De Benedetti F., Meazza C., Oliveri M., et al. Effect of IL-6 on IGF binding protein-3: a study in IL-6 transgenic mice and in patients with systemic juvenile idiopathic arthritis. Endocrinology 2001, 142(11):4818-4826.
29. Pignatti P., Vivarelli M., Meazza C., Rizzolo M.G., Martini A., De Benedetti F. Abnormal regulation of interleukin 6 in systemic juvenile idiopathic arthritis. J. Rheumatol. 2001, 28(7):1670-1676.
30. De Benedetti F., Brunner H., Ruperto N., et al. Catch-up growth during tocilizumab therapy for systemic juvenile idiopathic arthritis: results from a phase iii trial. Arthritis Rheumatol. 2015, 67(3):840-848.
31. Jin J., Samuvel D.J., Zhang X., et al. Coactivation of TLR4 and TLR2/6 coordinates an additive augmentation on IL-6 gene transcription via p38MAPK pathway in U937 mononuclear cells. Mol. Immunol. 2011, 49(3):423-432.
32. Kessel C., Holzinger D., Foell D. Phagocyte-derived S100 proteins in autoinflammation: putative role in pathogenesis and usefulness as biomarkers. Clin. Immunol. 2013, 147(3):229-241.
33. Foell D., Frosch M., Sorg C., Roth J. Phagocyte-specific calcium-binding S100 proteins as clinical laboratory markers of inflammation. Clin. Chim. Acta 2004, 344(1-2):37-51.
34. Kallinich T., Wittkowski H., Keitzer R., Roth J., Foell D. Neutrophil-derived S100A12 as novel biomarker of inflammation in familial Mediterranean fever. Ann. Rheum. Dis. 2010, 69(4):677-682.
35. Wittkowski H., Frosch M., Wulffraat N., et al. S100A12 is a novel molecular marker differentiating systemic-onset juvenile idiopathic arthritis from other causes of fever of unknown origin. Arthritis Rheum. 2008, 58(12):3924-3931.
36. Luksch H., Romanowski M.J., Chara O., et al. Naturally occurring genetic variants of human caspase-1 differ considerably in structure and the ability to activate interleukin-1beta. Hum. Mutat. 2013, 34(1):122-131.
37. Stock C.J., Ogilvie E.M., Samuel J.M., Fife M., Lewis C.M., Woo P. Comprehensive association study of genetic variants in the IL-1 gene family in systemic juvenile idiopathic arthritis. Genes Immun. 2008, 9(4):349-357.
38. Fishman D., Faulds G., Jeffery R., et al. The effect of novel polymorphisms in the interleukin-6 (IL-6) gene on IL-6 transcription and plasma IL-6 levels, and an association with systemic-onset juvenile chronic arthritis. J. Clin. Invest. 1998, 102(7):1369-1376.
39. Ogilvie E.M., Fife M.S., Thompson S.D., et al. The -174G allele of the interleukin-6 gene confers susceptibility to systemic arthritis in children: a multicenter study using simplex and multiplex juvenile idiopathic arthritis families. Arthritis Rheum. 2003, 48(11):3202-3206.
40. Donn R.P., Shelley E., Ollier W.E., Thomson W., British Paediatric Rheumatology Study G. A novel 5'-flanking region polymorphism of macrophage migration inhibitory factor is associated with systemic-onset juvenile idiopathic arthritis. Arthritis Rheum. 2001, 44(8):1782-1785.
41. De Benedetti F., Meazza C., Vivarelli M., et al. Functional and prognostic relevance of the -173 polymorphism of the macrophage migration inhibitory factor gene in systemic-onset juvenile idiopathic arthritis. Arthritis Rheum. 2003, 48(5):1398-1407.
42. Meazza C., Travaglino P., Pignatti P., et al. Macrophage migration inhibitory factor in patients with juvenile idiopathic arthritis. Arthritis Rheum. 2002, 46(1):232-237.
43. Hedrich C.M., Bream J.H. Cell type-specific regulation of IL-10 expression in inflammation and disease. Immunol. Res. 2010, 47(1-3):185-206.
44. Hofmann S.R., Rosen-Wolff A., Tsokos G.C., Hedrich C.M. Biological properties and regulation of IL-10 related cytokines and their contribution to autoimmune disease and tissue injury. Clin. Immunol. 2012, 143(2):116-127.
45. Hofmann S.R., Schwarz T., Moller J.C., et al. Chronic non-bacterial osteomyelitis is associated with impaired Sp1 signaling, reduced IL10 promoter phosphorylation, and reduced myeloid IL-10 expression. Clin. Immunol. 2011, 141(3):317-327.
46. Fife M.S., Gutierrez A., Ogilvie E.M., et al. Novel IL10 gene family associations with systemic juvenile idiopathic arthritis. Arthritis Res. Ther. 2006, 8(5):R148.
47. Moller J.C., Paul D., Ganser G., et al. IL10 promoter polymorphisms are associated with systemic onset juvenile idiopathic arthritis (SoJIA). Clin. Exp. Rheumatol. 2010, 28(6):912-918.
48. van den Ham H.J., de Jager W., Bijlsma J.W., Prakken B.J., de Boer R.J. Differential cytokine profiles in juvenile idiopathic arthritis subtypes revealed by cluster analysis. Rheumatology 2009, 48(8):899-905.
49. Hedrich C.M., Hahn G., Girschick H.J., Morbach H. A clinical and pathomechanistic profile of chronic nonbacterial osteomyelitis/chronic recurrent multifocal osteomyelitis and challenges facing the field. Expert. Rev. Clin. Immunol. 2013, 9(9):845-854.
50. Hedrich C.M., Hofmann S.R., Pablik J., Morbach H., Girschick H.J. Autoinflammatory bone disorders with special focus on chronic recurrent multifocal osteomyelitis (CRMO). Pediatr. Rheumatol. Online J. 2013, 11(1):47.
51. Hofmann S.R., Roesen-Wolff A., Hahn G., Hedrich C.M. Update: cytokine dysregulation in chronic nonbacterial osteomyelitis (CNO). Int. J. Rheumatol. 2012, 2012:310206.
52. Morbach H., Hedrich C.M., Beer M., Girschick H.J. Autoinflammatory bone disorders. Clin. Immunol. 2013, 147(3):185-196.
53. Wakil S.M., Monies D.M., Abouelhoda M., et al. Association of a mutation in LACC1 with a monogenic form of systemic juvenile idiopathic arthritis. Arthritis Rheumatol. 2015, 67(1):288-295.
54. Lisova Z.A., Lisov A.V., Leontievsky A.A. Two laccase isoforms of the basidiomycete Cerrena unicolor VKMF-3196. Induction, isolation and properties. J. Basic Microbiol. 2010, 50(1):72-82.
55. Sales-Marques C., Salomao H., Fava V.M., et al. NOD2 and CCDC122-LACC1 genes are associated with leprosy susceptibility in Brazilians. Hum. Genet. 2014, 133(12):1525-1532.
56. Grant A.V., Alter A., Huong N.T., et al. Crohn's disease susceptibility genes are associated with leprosy in the Vietnamese population. J. Infect. Dis. 2012, 206(11):1763-1767.
57. Hadchouel M., Prieur A.M., Griscelli C. Acute hemorrhagic, hepatic, and neurologic manifestations in juvenile rheumatoid arthritis: possible relationship to drugs or infection. J. Pediatr. 1985, 106(4):561-566.
58. Behrens E.M., Beukelman T., Paessler M., Cron R.Q. Occult macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis. J. Rheumatol. 2007, 34(5):1133-1138.
59. Sawhney S., Woo P., Murray K.J. Macrophage activation syndrome: a potentially fatal complication of rheumatic disorders. Arch. Dis. Child. 2001, 85(5):421-426.
60. Donn R., Ellison S., Lamb R., Day T., Baildam E., Ramanan A.V. Genetic loci contributing to hemophagocytic lymphohistiocytosis do not confer susceptibility to systemic-onset juvenile idiopathic arthritis. Arthritis Rheum. 2008, 58(3):869-874.
61. Zhang K., Biroschak J., Glass D.N., et al. Macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis is associated with MUNC13-4 polymorphisms. Arthritis Rheum. 2008, 58(9):2892-2896.
62. Vastert S.J., van Wijk R., D'Urbano L.E., et al. Mutations in the perforin gene can be linked to macrophage activation syndrome in patients with systemic onset juvenile idiopathic arthritis. Rheumatology 2010, 49(3):441-449.
63. Yanagimachi M., Goto H., Miyamae T., et al. Association of IRF5 polymorphisms with susceptibility to hemophagocytic lymphohistiocytosis in children. J. Clin. Immunol. 2011, 31(6):946-951.
64. Yanagimachi M., Naruto T., Miyamae T., et al. Association of IRF5 polymorphisms with susceptibility to macrophage activation syndrome in patients with juvenile idiopathic arthritis. J. Rheumatol. 2011, 38(4):769-774.
65. Beukelman T. Treatment advances in systemic juvenile idiopathic arthritis. F1000Prime Rep. 2014, 6:21.
66. Garcia-Carrasco M., Fuentes-Alexandro S., Escarcega R.O., Rojas-Rodriguez J., Escobar L.E. Efficacy of thalidomide in systemic onset juvenile rheumatoid arthritis. Joint Bone Spine 2007, 74(5):500-503.
67. Quartier P. Current treatments for juvenile idiopathic arthritis. Joint Bone Spine 2010, 77(6):511-516.
68. Brinkman D.M., Jol-van der Zijde C.M., ten Dam M.M., et al. Resetting the adaptive immune system after autologous stem cell transplantation: lessons from responses to vaccines. J. Clin. Immunol. 2007, 27(6):647-658.
69. Brinkman D.M., de Kleer I.M., ten Cate R., et al. Autologous stem cell transplantation in children with severe progressive systemic or polyarticular juvenile idiopathic arthritis: long-term follow-up of a prospective clinical trial. Arthritis Rheum. 2007, 56(7):2410-2421.
70. Russo R.A., Katsicas M.M. Clinical remission in patients with systemic juvenile idiopathic arthritis treated with anti-tumor necrosis factor agents. J. Rheumatol. 2009, 36(5):1078-1082.
71. De Benedetti F., Brunner H.I., Ruperto N., et al. Randomized trial of tocilizumab in systemic juvenile idiopathic arthritis. N. Engl. J. Med. 2012, 367(25):2385-2395.
72. Ruperto N., Brunner H.I., Quartier P., et al. Two randomized trials of canakinumab in systemic juvenile idiopathic arthritis. N. Engl. J. Med. 2012, 367(25):2396-2406.
73. Boraschi D., Tagliabue A. The interleukin-1 receptor family. Semin. Immunol. 2013, 25(6):394-407.
74. Goldbach-Mansky R., Dailey N.J., Canna S.W., et al. Neonatal-onset multisystem inflammatory disease responsive to interleukin-1beta inhibition. N. Engl. J. Med. 2006, 355(6):581-592.
75. Quartier P., Allantaz F., Cimaz R., et al. A multicentre, randomised, double-blind, placebo-controlled trial with the interleukin-1 receptor antagonist anakinra in patients with systemic-onset juvenile idiopathic arthritis (ANAJIS trial). Ann. Rheum. Dis. 2011, 70(5):747-754.
76. Ruperto N., Quartier P., Wulffraat N., et al. A phase II, multicenter, open-label study evaluating dosing and preliminary safety and efficacy of canakinumab in systemic juvenile idiopathic arthritis with active systemic features. Arthritis Rheum. 2012, 64(2):557-567.
77. Goldbach-Mansky R., Shroff S.D., Wilson M., et al. A pilot study to evaluate the safety and efficacy of the long-acting interleukin-1 inhibitor rilonacept (interleukin-1 Trap) in patients with familial cold autoinflammatory syndrome. Arthritis Rheum. 2008, 58(8):2432-2442.
78. Hashkes P.J., Spalding S.J., Giannini E.H., et al. Rilonacept for colchicine-resistant or -intolerant familial Mediterranean fever: a randomized trial. Ann. Intern. Med. 2012, 157(8):533-541.
79. Hoffman H.M., Throne M.L., Amar N.J., et al. Efficacy and safety of rilonacept (interleukin-1 Trap) in patients with cryopyrin-associated periodic syndromes: results from two sequential placebo-controlled studies. Arthritis Rheum. 2008, 58(8):2443-2452.
80. Petryna O., Cush J.J., Efthimiou P. IL-1 Trap rilonacept in refractory adult onset Still's disease. Ann. Rheum. Dis. 2012, 71(12):2056-2057.
81. Yokota S., Miyamae T., Imagawa T., et al. Therapeutic efficacy of humanized recombinant anti-interleukin-6 receptor antibody in children with systemic-onset juvenile idiopathic arthritis. Arthritis Rheum. 2005, 52(3):818-825.
82. Yokota S., Miyamae T., Imagawa T., Katakura S., Kurosawa R., Mori M. Clinical study of tocilizumab in children with systemic-onset juvenile idiopathic arthritis. Clin. Rev. Allergy Immunol. 2005, 28(3):231-238.
83. DeWitt E.M., Kimura Y., Beukelman T., et al. Consensus treatment plans for new-onset systemic juvenile idiopathic arthritis. Arthritis Care Res. 2012, 64(7):1001-1010.
84. Kimura Y., DeWitt E.M., Beukelman T., et al. Adding canakinumab to the Childhood Arthritis and Rheumatology Research Alliance consensus treatment plans for systemic juvenile idiopathic arthritis: comment on the article by DeWitt et al. Arthritis Care Res. 2014, 66(9):1430-1431.
85. Nigrovic P.A. Review: is there a window of opportunity for treatment of systemic juvenile idiopathic arthritis?. Arthritis Rheumatol. 2014, 66(6):1405-1413.