Targeting the BLyS-APRIL signaling pathway in SLE

Clinical Immunology

Volumn 148, Issue 3, 2013, Pages 322-327

  La Cava, Antonio ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

APRIL; BLyS BAFF; Systemic lupus erythematosus (SLE)

Indexed keywords

ANTIMALARIAL AGENT; APRIL PROTEIN; B CELL ACTIVATING FACTOR; BELIMUMAB; CORTICOSTEROID; IMMUNOSUPPRESSIVE AGENT;

CELL MATURATION; CORTICOSTEROID THERAPY; DISEASE ACTIVITY SCORE; DRUG MECHANISM; DRUG SAFETY; HUMAN; INHIBITION KINETICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; TREATMENT OUTCOME;

APRIL; BLYS/BAFF; SYSTEMIC LUPUS ERYTHEMATOSUS (SLE);

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; B-CELL ACTIVATING FACTOR; CLINICAL TRIALS, PHASE III AS TOPIC; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 13;

EID: 84881093916     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2012.11.010     Document Type: Review

References (42)

1. Batten M., Groom J., Cachero T.G., Qian F., Schneider P., Tschopp J., Browning J.L., Mackay F. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 2000, 192:1453-1466.
2. Gross J.A., Johnston J., Mudri S., Enselman R., Dillon S.R., Madden K., Xu W., Parrish-Novak J., Foster D., Lofton-Day C., Moore M., Littau A., Grossman A., Haugen H., Foley K., Blumberg H., Harrison K., Kindsvogel W., Clegg C.H. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 2000, 404:995-999.
3. Do R.K., Hatada E., Lee H., Tourigny M.R., Hilbert D., Chen-Kiang S. Attenuation of apoptosis underlies B lymphocyte stimulator enhancement of humoral immune response. J. Exp. Med. 2000, 192:953-964.
4. Scapini P., Bazzoni F., Cassatella M.A. Regulation of B-cell-activating factor (BAFF)/B lymphocyte stimulator (BLyS) expression in human neutrophils. Immunol. Lett. 2008, 116:1-6.
5. Liu Y., Hong X., Kappler J., Jiang L., Zhang R., Xu L., Pan C.H., Martin W.E., Murphy R.C., Shu H.B., Dai S., Zhang G. Ligand-receptor binding revealed by the TNF family member TALL-1. Nature 2003, 423:49-56.
6. Mackay F., Schneider P. Cracking the BAFF code. Nat. Rev. Immunol. 2009, 9:491-502.
7. Dillon S.R., Gross J.A., Ansell S.M., Novak A.J. An APRIL to remember: novel TNF ligands as therapeutic targets. Nat. Rev. Drug Discov. 2006, 5:235-246.
8. Dillon S.R., Harder B., Lewis K.B., Moore M.D., Liu H., Bukowski T.R., Hamacher N.B., Lantry M.M., Maurer M., Krejsa C.M., Ellsworth J.L., Pederson S., Elkon K.B., Wener M.H., Dall'Era M., Gross J.A. B-lymphocyte stimulator/a proliferation-inducing ligand heterotrimers are elevated in the sera of patients with autoimmune disease and are neutralized by atacicept and B-cell maturation antigen-immunoglobulin. Arthritis Res. Ther. 2010, 12:R48.
9. Ettinger R., Sims G.P., Robbins R., Withers D., Fischer R.T., Grammer A.C., Kuchen S., Lipsky P.E. IL-21 and BAFF/BLyS synergize in stimulating plasma cell differentiation from a unique population of human splenic memory B cells. J. Immunol. 2007, 178:2872-2882.
10. Thompson J.S., Bixler S.A., Qian F., Vora K., Scott M.L., Cachero T.G., Hession C., Schneider P., Sizing I.D., Mullen C., Strauch K., Zafari M., Benjamin C.D., Tschopp J., Browning J.L., Ambrose C. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 2001, 293:2108-2111.
11. Schneider P., Takatsuka H., Wilson A., Mackay F., Tardivel A., Lens S., Cachero T.G., Finke D., Beermann F., Tschopp J. Maturation of marginal zone and follicular B cells requires B cell activating factor of the tumor necrosis factor family and is independent of B cell maturation antigen. J. Exp. Med. 2001, 194:1691-1697.
12. von Bulow G.U., van Deursen J.M., Bram R.J. Regulation of the T independent humoral response by TACI. Immunity 2001, 14:573-582.
13. Hsu B.L., Harless S.M., Lindsley R.C., Hilbert D.M., Cancro M.P. Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators. J. Immunol. 2002, 168:5993-5996.
14. O'Connor B.P., Raman V.S., Erickson L.D., Cook W.J., Weaver L.K., Ahonen C., Lin L.L., Mantchev G.T., Bram R.J., Noelle R.J. BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 2004, 199:91-98.
15. Avery D.T., Kalled S.L., Ellyard J.I., Ambrose C., Bixler S.A., Thien M., Brink R., Mackay F., Hodgkin P.D., Tangye S.G. BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J. Clin. Invest. 2003, 112:286-297.
16. Harless Smith S., Cancro M.P. Integrating B cell homeostasis and selection with BLyS. Arch. Immunol. Ther. Exp. (Warsz.) 2003, 51:209-218.
17. Castigli E., Wilson S.A., Scott S., Dedeoglu F., Xu S., Lam K.P., Bram R.J., Jabara H., Geha R.S. TACI and BAFF-R mediate isotype switching in B cells. J. Exp. Med. 2005, 201:35-39.
18. Alexaki V.I., Pelekanou V., Notas G., Venihaki M., Kampa M., Dessirier V., Sabour-Alaoui S., Stathopoulos E.N., Tsapis A., Castanas E. B-cell maturation antigen (BCMA) activation exerts specific proinflammatory effects in normal human keratinocytes and is preferentially expressed in inflammatory skin pathologies. Endocrinology 2012, 153:739-749.
19. Notas G., Alexaki V.I., Kampa M., Pelekanou V., Charalampopoulos I., Sabour-Alaoui S., Pediaditakis I., Dessirier V., Gravanis A., S tathopoulos E.N., Tsapis A., Castanas E. APRIL binding to BCMA activates a JNK2-FOXO3-GADD45 pathway and induces a G2/M cell growth arrest in liver cells. J. Immunol. 2012, 189:4748-4758.
20. Sanz I., Lee F.E. B cells as therapeutic targets in SLE. Nat. Rev. Rheumatol. 2010, 6:326-337.
21. Mackay F., Woodcock S.A., Lawton P., Ambrose C., Baetscher M., Schneider P., Tschopp J., Browning J.L. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 1999, 190:1697-1710.
22. Cancro M.P., D'Cruz D.P., Khamashta M.A. The role of B lymphocyte stimulator (BLyS) in systemic lupus erythematosus. J. Clin. Invest. 2009, 119:1066-1073.
23. Kayagaki N., Yan M., Seshasayee D., et al. BAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-κB. Immunity 2002, 17:515-524.
24. Thompson J.S., Schneider P., Kalled S.L., Wang L., Lefevre E.A., Cachero T.G., MacKay F., Bixler S.A., Zafari M., Liu Z.Y., Woodcock S.A., Qian F., Batten M., Madry C., Richard Y., Benjamin C.D., Browning J.L., Tsapis A., Tschopp J., Ambrose C. BAFF binds to the tumor necrosis factor receptor-like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population. J. Exp. Med. 2000, 192:129-135.
25. Kahn P., Ramanujam M., Bethunaickan R., Huang W., Tao H., Madaio M.P., Factor S.M., Davidson A. Prevention of murine antiphospholipid syndrome by BAFF blockade. Arthritis Rheum. 2008, 58:2824-2834.
26. Becker-Merok A., Nikolaisen C., Nossent H.C. B-lymphocyte activating factor in systemic lupus erythematosus and rheumatoid arthritis in relation to autoantibody levels, disease measures and time. Lupus 2006, 15:570-576.
27. Stohl W., Metyas S., Tan S., Cheema G.S., Oamar B., Xu D., R oschke V., Wu Y., Baker K.P., Hilbert D.M. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum. 2003, 48:3475-3486.
28. Zhang J., Roschke V., Baker K.P., Wang Z., Alarcón G.S., Fessler B.J., Bastian H., Kimberly R.P., Zhou T. Cutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosus. J. Immunol. 2001, 166:6-10.
29. Furie R., Stohl W., Ginzler E.M., Becker M., Mishra N., Chatham W., Merrill J.T., Weinstein A., McCune W.J., Zhong J., Cai W., Freimuth W. Biologic activity and safety of belimumab, a neutralizing anti- B-lymphocyte stimulator (BLyS) monoclonal antibody: a phase I trial in patients with systemic lupus erythematosus. Arthritis Res. Ther. 2008, 10:R109. Belimumab Study Group.
30. Wallace D.J., Stohl W., Furie R.A., Lisse J.R., McKay J.D., Merrill J.T., Petri M.A., Ginzler E.M., Chatham W.W., McCune W.J., Fernandez V., Chevrier M.R., Zhong Z.J., Freimuth W.W. A phase II, randomized, double-blind, placebo-controlled, dose-ranging study of belimumab in patients with active systemic lupus erythematosus. Arthritis Rheum. 2009, 61:1168-1178.
31. Croker J.A., Kimberly R.P. SLE: challenges and candidates in human disease. Trends Immunol. 2005, 26:580-586.
32. Furie R.A., Petri M.A., Wallace D.J., Ginzler E.M., Merrill J.T., Stohl W., Chatham W.W., Strand V., Weinstein A., Chevrier M.R., Zhong Z.J., Freimuth W.W. Novel evidence-based systemic lupus erythematosus responder index. Arthritis Rheum. 2009, 61:1143-1151.
33. Stohl W., Hiepe F., Thomas M., Scheinberg M.A., Clarke A.E., Aranow C., Jimenez R. Belimumab, a BLys-specific inhibitor, significantly reduced autoantibodies, normalized low complement, and reduced selected B-cell populations in patients with seropositive systemic lupus erythematosus (SLE): the phase 3 BLISS studies. Arthritis Rheum. 2010, 62. (Suppl.).
34. Chatham W., Stohl W., Merrill J.T., Gruhn W., Aranow C., Burnette M., Pogue B., McCune W., Petrone D., Zhong J., Migone T., Freimuth W. Changes in circulating B-cell subtype counts, autoantibody levels and immunoglobulins that associate with therapeutic responsiveness in SLE to BLys protein antagonism by belimumab. Ann. Rheum. Dis. 2007, 66(Suppl. 11):459. LBSL02 Study Group.
35. Darce J.R., Arendt B.K., Wu X., Jelinek D.F. Regulated expression of BAFF-binding receptors during human B cell differentiation. J. Immunol. 2007, 179:7276-7286.
36. Stohl W., Hiepe F., Latinis K.M., Thomas M., Scheinberg M.A., Clarke A., Aranow C., Wellborne F.R., Abud-Mendoza C., Hough D.R., Pineda L., Migone T.S., Zhong Z.J., Freimuth W.W., Chatham W.W., BLISS-52 Study Group, BLISS-76 Study Group Belimumab reduces autoantibodies, normalizes low complement, and reduces select B-cell populations in patients with systemic lupus erythematosus. Arthritis Rheum. 2012, 64:2328-2337.
37. Chatham W.W., Wallace D.J., Stohl W., Latinis K.M., Manzi S., McCune W.J., Tegzová D., McKay J.D., Avila-Armengol H.E., Utset T.O., Zhong Z.J., Hough D.R., Freimuth W.W., Migone T.S. Effect of belimumab on vaccine antigen antibodies to influenza, pneumococcal, and tetanus vaccines in patients with systemic lupus erythematosus in the BLISS-76 trial. J. Rheumatol. 2012, 39:1632-1640. on behalf of the BLISS-76 Study Group.
38. Ng L.G., Sutherland A.P., Newton R., Qian F., Cachero T.G., Scott M.L., Thompson J.S., Wheway J., Chtanova T., Groom J., Sutton I.J., Xin C., Tangye S.G., Kalled S.L., Mackay F., Mackay C.R. B cell-activating factor belonging to the TNF family (BAFF)-R is the principal BAFF receptor facilitating BAFF costimulation of circulating T and B cells. J. Immunol. 2004, 173:807-817.
39. Huard B., Schneider P., Mauri D., Tschopp J., French L.E. T cell costimulation by the TNF ligand BAFF. J. Immunol. 2001, 167:6225-6231.
40. Fillatreau S., Sweenie C.H., McGeachy M.J., Gray D., Anderton S.M. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 2002, 3:944-950.
41. Groom J.R., Fletcher C.A., Walters S.N., Grey S.T., Watt S.V., Sweet M.J., Smyth M.J., Mackay C.R., Mackay F. BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J. Exp. Med. 2007, 204:1959-1971.
42. Dooley M.A., Houssiau F., Aranow C., D'Cruz D.P., Askanase, Anca D., Roth D., Zhong Z.J. Effect of belimumab treatment on renal outcomes: results from phase 3 belimumab clinical trials in patients with systemic lupus erythematosus [abstract]. Arthritis Rheum. 2011, 63(Suppl. 10):2472.