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Systemic Lupus Erythematosus


(A study of belimumab in subjects with systemic lupus erythematosus [BLISS] 52 and BLISS 76) resulted in the approval of this biologic in the US and Europe. The approval of belimumab represents a significant advancement in the treatment of SLE and suggests that the development of biological agents capable of regulating the activity of specific B-cell subsets, via inhibition of soluble factors and/or neutralisation of cell–cell interactions, may provide clinical benefit to


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2. Nurieva RI, Chung Y, Hwang D, et al., Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages, Immunity, 2008;29:138–49.


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6. Yoshinaga SK, Whoriskey JS, Khare SD, et al., T-cell co-stimulation through B7RP-1 and ICOS, Nature, 1999;402:827–32.


7. Hutloff A, Dittrich AM, Beier KC, et al., ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28, Nature, 1999;397:263–6.


8. Bauquet AT, Jin H, Paterson AM, et al., The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells, Nat Immunol, 2009;10:167–75.


9. Wassink L, Vieira PL, Smits HH, et al., ICOS expression by activated human Th cells is enhanced by IL-12 and IL-23: increased ICOS expression enhances the effector function of both Th1 and Th2 cells, J Immunol, 2004;173:1779–86.


10. Chtanova T, Tangye SG, Newton R, et al., T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells, J Immunol, 2004;173:68–78.


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13. Glasmacher E, Hoefig KP, Vogel KU, et al., Roquin binds inducible costimulator mRNA and effectors of mRNA decay to induce microRNA-independent post-transcriptional repression, Nat Immunol, 2010;11:725–33.


14. Simpson N, Gatenby PA, Wilson A, et al., Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus, Arthritis Rheum, 2010;62:234–44.


15. Watanabe M, Takagi Y, Kotani M, et al., Down-regulation of ICOS ligand by interaction with ICOS functions as a regulatory mechanism for immune responses, J Immunol, 2008;180:5222–34.


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SLE patients. In the light of the cellular and molecular mechanisms of TFH cells involved in the regulation of GC B-cell responses, additional therapies targeting the ICOS–ICOSL pathway are warranted. By blocking the ICOS signalling pathway, these types of therapies may promise an alternative opportunity to reduce disease activity in patients with SLE. Phase I clinical studies with AMG-557 and MEDI-570 are already under way.45,46


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17. Schmitt N, Morita R, Bourdery L, et al., Human dendritic cells induce the differentiation of interleukin-21-producing T follicular helper-like cells through interleukin-12, Immunity, 2009;31:158–69.


18. Ma CS, Suryani S, Avery DT, et al., Early commitment of naive human CD4(+) T cells to the T follicular helper (T(FH)) cell lineage is induced by IL-12, Immunol Cell Biol, 2009;87:590–600.


19. Crotty S, Follicular helper CD4 T cells (TFH), Annu Rev Immunol, 2011;29:621–63.


20. Choi YS, Kageyama R, Eto D, et al., ICOS Receptor Instructs T Follicular Helper Cell versus Effector Cell Differentiation via Induction of the Transcriptional Repressor Bcl6, Immunity, 2011;34:932–46.


21. Cyster JG, Ansel KM, Reif K, et al., Follicular stromal cells and lymphocyte homing to follicles, Immunol Rev, 2000;176:181–93.


22. Lee SK, Rigby RJ, Zotos D, et al., B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells, J Exp Med, 2011;208:1377–88.


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25. Odegard JM, Marks BR, DiPlacido LD, et al., ICOS-dependent extrafollicular helper T cells elicit IgG production via IL-21 in systemic autoimmunity, J Exp Med, 2008;205:2873–86.


26. Poholek AC, Hansen K, Hernandez SG, et al., In vivo regulation of Bcl6 and T follicular helper cell development, J Immunol, 2010;185:313–26.


27. Rasheed AU, Rahn HP, Sallusto F, et al., Follicular B helper T cell activity is confined to CXCR5(hi)ICOS(hi) CD4 T cells and is independent of CD57 expression, Eur J Immunol, 2006;36:1892–1903.


28. Barone F, Bombardieri M, Rosado MM, et al., CXCL13, CCL21, and CXCL12 expression in salivary glands of patients with Sjogren's syndrome and MALT lymphoma: association with reactive and malignant areas of lymphoid organization, J Immunol, 2008;180:5130–40.


29. Ezzat M, El-Gammasy T, Shaheen K, Shokr E, Elevated production of serum B-cell-attracting chemokine-1 (BCA-1/CXCL13) is correlated with childhood-onset lupus disease activity, severity, and renal involvement, Lupus, 2011;20:845–54.


30. Wong CK, Wong PT, Tam LS, et al., Elevated production of B cell chemokine CXCL13 is correlated with systemic lupus erythematosus disease activity, J Clin Immunol, 2010;30:45–52.


31. Lee HT, Shiao YM, Wu TH, et al., Serum BLC/CXCL13 concentrations and renal expression of CXCL13/CXCR5 in patients with systemic lupus erythematosus and lupus nephritis, J Rheumatol, 2010;37:45–52.


32. Manzo A, Vitolo B, Humby F, et al., Mature antigen- experienced T helper cells synthesize and secrete the B cell chemoattractant CXCL13 in the inflammatory environment of the rheumatoid joint, Arthritis Rheum, 2008;58:3377–87.


33. McAdam AJ, Greenwald RJ, Levin MA, et al., ICOS is critical for CD40-mediated antibody class switching, Nature, 2001;409:102–5.


34. Tafuri A, Shahinian A, Bladt F, et al., ICOS is essential for effective T-helper-cell responses, Nature, 2001;409:105–9.


35. Yong PF, Salzer U, Grimbacher B, The role of costimulation in antibody deficiencies: ICOS and common variable immunodeficiency, Immunol Rev, 2009;229:101–13.


36. Kawamoto M, Harigai M, Hara M, et al., Expression and function of inducible co-stimulator in patients with systemic lupus erythematosus: possible involvement in excessive interferon-gamma and anti-double-stranded DNA antibody production, Arthritis Res Ther, 2006;8:R62.


37. Hu YL, Metz DP, Chung J, et al., B7RP-1 blockade ameliorates autoimmunity through regulation of follicular helper T cells, J Immunol, 2009;182:1421–8.


38. Rottman JB, Smith T, Tonra JR, et al., The costimulatory molecule ICOS plays an important role in the immunopathogenesis of EAE, Nat Immunol, 2001;2:605–11.


39. Tajima N, Tezuka K, Tanaka M, et al., Critical role of activation-inducible lymphocyte immunomediatory molecule/inducible costimulator in the effector function of human T cells: a comparative in vitro study of effects of its blockade and CD28 blockade in human beings and monkeys, Hum Immunol, 2008;69:399–408.


40. Carlesso G, et al., manuscript in preparation. 41. Dorner T, Kaufmann J, Wegener WA, et al., Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus, Arthritis Res Ther, 2006;8:R74.


42. Wallace D, Kalunian K, Petri M, et al., Epratuzumab demonstrates clinically meaningful improvements in patients with moderate to severe systemic lupus erythematosus (SLE): results from EMBLEM, a phase IIb study, Ann Rheum Dis, 2010;69(Suppl. 3):558.


43. Navarra SV, Guzman RM, Gallacher AE, et al., Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial, Lancet, 2011;377:721–31.


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45. Amgen A, Randomized, Double-blind, Placebo-controlled, Ascending, Multiple Dose Study to Evaluate the Safety, Tolerability, Pharmacokinetics and Pharmacodynamics of AMG 557 in Subjects With Systemic Lupus Erythematosus. Available at: http://clinicaltrials.gov/ct2/show/NCT00774943 (accessed 24 October 2011).


46. MedImmune, A Phase 1, Double-Blind, Randomized, Single Ascending Dose Study of the Safety and Tolerability of MEDI-570 in Systemic Lupus Erythematosus. Available at: http://clinicaltrials.gov/ct2/show/NCT01127321 (accessed 24 October 2011).


47. Liu SM, Xavier R, Good KL, et al., Immune cell transcriptome datasets reveal novel leukocyte subset-specific genes and genes associated with allergic processes, J Allergy Clin Immunol, 2006;118:496–503.


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