BAFF overexpression increases lymphocytic infiltration in Sjögren's target tissue, but only inefficiently promotes ectopic B-cell differentiation

Clinical Immunology

Volumn 169, Issue , 2016, Pages 69-79

  Ding, Jian ^a   Zhang, Wei ^a   Haskett, Scott ^a   Pellerin, Alex ^a   Xu, Shanqin ^a   Petersen, Britta ^a   Jandreski, Luke ^a   Hamann, Stefan ^a   Reynolds, Taylor L ^a   Zheng, Timothy S ^a   Mingueneau, Michael ^a  

^a BIOGEN   (United States)

Author keywords

Autoimmunity; B cells; BAFF; Ectopic germinal center; Sj gren's syndrome

Indexed keywords

APC PROTEIN; B CELL ACTIVATING FACTOR; CD3 ANTIGEN; CD38 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR9; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR; TNFSF13B PROTEIN, MOUSE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GERMINAL CENTER; GLAND TISSUE; HYDRODYNAMICS BASED TRANSFECTION; LYMPHOCYTIC INFILTRATION; MALE; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SJOEGREN SYNDROME; SYSTEMATIC REVIEW; TARGET ORGAN; ANIMAL; AUTOIMMUNITY; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; DNA MICROARRAY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LACRIMAL APPARATUS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PROCEDURES; XEROPHTHALMIA; XEROSTOMIA;

ANIMALS; AUTOIMMUNITY; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GERMINAL CENTER; IMMUNOHISTOCHEMISTRY; LACRIMAL APPARATUS; MALE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED NOD; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SJOGREN'S SYNDROME; XEROPHTHALMIA; XEROSTOMIA;

EID: 84979031446     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2016.06.007     Document Type: Article

References (58)

1. [1] Qin, B., Wang, J., Yang, Z., Yang, M., Ma, N., Huang, F., et al. Epidemiology of primary Sjogren's syndrome: a systematic review and meta-analysis. Ann. Rheum. Dis. 74 (2014), 1983–1989.
2. [2] Fisher, B.A., Brown, R.M., Bowman, S.J., Barone, F., A review of salivary gland histopathology in primary Sjogren's syndrome with a focus on its potential as a clinical trials biomarker. Ann. Rheum. Dis. 74 (2015), 1645–1650.
3. [3] Szyszko, E.A., Brokstad, K.A., Oijordsbakken, G., Jonsson, M.V., Jonsson, R., Skarstein, K., Salivary glands of primary Sjogren's syndrome patients express factors vital for plasma cell survival. Arthritis Res. Ther., 13, 2011, R2.
4. [4] Mingueneau, M., Boudaoud, S., Haskett, S., Reynolds, T.L., Nocturne, G., Norton, E., et al. Cytometry by time-of-flight immunophenotyping identifies a blood Sjogren's signature correlating with disease activity and glandular inflammation. J. Allergy Clin. Immunol. 137 (2016), 1809–1821.
5. [5] Risselada, A.P., Looije, M.F., Kruize, A.A., Bijlsma, J.W., van Roon, J.A., The role of ectopic germinal centers in the immunopathology of primary Sjogren's syndrome: a systematic review. Semin. Arthritis Rheum. 42 (2013), 368–376.
6. [6] Stott, D.I., Hiepe, F., Hummel, M., Steinhauser, G., Berek, C., Antigen-driven clonal proliferation of B cells within the target tissue of an autoimmune disease. The salivary glands of patients with Sjogren's syndrome. J. Clin. Invest. 102 (1998), 938–946.
7. [7] Theander, E., Vasaitis, L., Baecklund, E., Nordmark, G., Warfvinge, G., Liedholm, R., et al. Lymphoid organisation in labial salivary gland biopsies is a possible predictor for the development of malignant lymphoma in primary Sjogren's syndrome. Ann. Rheum. Dis. 70 (2011), 1363–1368.
8. [8] Zuckerman, N.S., Hazanov, H., Barak, M., Edelman, H., Hess, S., Shcolnik, H., et al. Somatic hypermutation and antigen-driven selection of B cells are altered in autoimmune diseases. J. Autoimmun. 35 (2010), 325–335.
9. [9] Kaschner, S., Hansen, A., Jacobi, A., Reiter, K., Monson, N.L., Odendahl, M., et al. Immunoglobulin Vlambda light chain gene usage in patients with Sjogren's syndrome. Arthritis Rheum. 44 (2001), 2620–2632.
10. [10] Vinuesa, C.G., Sanz, I., Cook, M.C., Dysregulation of germinal centres in autoimmune disease. Nat. Rev. Immunol. 9 (2009), 845–857.
11. [11] Allen, C.D., Ansel, K.M., Low, C., Lesley, R., Tamamura, H., Fujii, N., et al. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol. 5 (2004), 943–952.
12. [12] Kramer, J.M., Klimatcheva, E., Rothstein, T.L., CXCL13 is elevated in Sjogren's syndrome in mice and humans and is implicated in disease pathogenesis. J. Leukoc. Biol. 94 (2013), 1079–1089.
13. [13] Lied, G.A., Berstad, A., Functional and clinical aspects of the B-cell-activating factor (BAFF): a narrative review. Scand. J. Immunol. 73 (2011), 1–7.
14. [14] Mackay, F., Schneider, P., Cracking the BAFF code. Nat. Rev. Immunol. 9 (2009), 491–502.
15. [15] Goenka, R., Scholz, J.L., Sindhava, V.J., Cancro, M.P., New roles for the BLyS/BAFF family in antigen-experienced B cell niches. Cytokine Growth Factor Rev. 25 (2014), 107–113.
16. [16] Thien, M., Phan, T.G., Gardam, S., Amesbury, M., Basten, A., Mackay, F., et al. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 20 (2004), 785–798.
17. [17] Daridon, C., Devauchelle, V., Hutin, P., Le Berre, R., Martins-Carvalho, C., Bendaoud, B., et al. Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjogren's syndrome. Arthritis Rheum. 56 (2007), 1134–1144.
18. [18] Mariette, X., Roux, S., Zhang, J., Bengoufa, D., Lavie, F., Zhou, T., et al. The level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjogren's syndrome. Ann. Rheum. Dis. 62 (2003), 168–171.
19. [19] Jonsson, M.V., Szodoray, P., Jellestad, S., Jonsson, R., Skarstein, K., Association between circulating levels of the novel TNF family members APRIL and BAFF and lymphoid organization in primary Sjogren's syndrome. J. Clin. Immunol. 25 (2005), 189–201.
20. [20] Mumcu, G., Bicakcigil, M., Yilmaz, N., Ozay, H., Karacayli, U., Cimilli, H., et al. Salivary and serum B-cell activating factor (BAFF) levels after hydroxychloroquine treatment in primary Sjogren's syndrome. Oral Health Prev. Dent. 11 (2013), 229–234.
21. [21] Szodoray, P., Alex, P., Jonsson, M.V., Knowlton, N., Dozmorov, I., Nakken, B., et al. Distinct profiles of Sjogren's syndrome patients with ectopic salivary gland germinal centers revealed by serum cytokines and BAFF. Clin. Immunol. 117 (2005), 168–176.
22. [22] Sharma, A., Kiripolsky, J., Klimatcheva, E., Howell, A., Fereidouni, F., Levenson, R., et al. Early BAFF receptor blockade mitigates murine Sjogren's syndrome: concomitant targeting of CXCL13 and the BAFF receptor prevents salivary hypofunction. Clin. Immunol. 164 (2016), 85–94.
23. [23] Khare, S.D., Sarosi, I., Xia, X.Z., McCabe, S., Miner, K., Solovyev, I., et al. Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 3370–3375.
24. [24] Gross, J.A., Johnston, J., Mudri, S., Enselman, R., Dillon, S.R., Madden, K., et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404 (2000), 995–999.
25. [25] Mackay, F., Woodcock, S.A., Lawton, P., Ambrose, C., Baetscher, M., Schneider, P., et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 190 (1999), 1697–1710.
26. [26] Groom, J., Kalled, S.L., Cutler, A.H., Olson, C., Woodcock, S.A., Schneider, P., et al. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. J. Clin. Invest. 109 (2002), 59–68.
27. [27] Szodoray, P., Jonsson, R., The BAFF/APRIL system in systemic autoimmune diseases with a special emphasis on Sjogren's syndrome. Scand. J. Immunol. 62 (2005), 421–428.
28. [28] Thompson, N., Isenberg, D.A., Jury, E.C., Ciurtin, C., Exploring BAFF: its expression, receptors and contribution to the immunopathogenesis of Sjogren's syndrome. Rheumatology, 2016.
29. [29] Kroese, F.G., Abdulahad, W.H., Haacke, E., Bos, N.A., Vissink, A., Bootsma, H., B-cell hyperactivity in primary Sjogren's syndrome. Expert. Rev. Clin. Immunol. 10 (2014), 483–499.
30. [30] Groom, J.R., Fletcher, C.A., Walters, S.N., Grey, S.T., Watt, S.V., Sweet, M.J., et al. BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J. Exp. Med. 204 (2007), 1959–1971.
31. [31] Fletcher, C.A., Sutherland, A.P., Groom, J.R., Batten, M.L., Ng, L.G., Gommerman, J., et al. Development of nephritis but not sialadenitis in autoimmune-prone BAFF transgenic mice lacking marginal zone B cells. Eur. J. Immunol. 36 (2006), 2504–2514.
32. [32] Liu, F., Song, Y., Liu, D., Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 6 (1999), 1258–1266.
33. [33] Allaire, N.E., Bushnell, S.E., Bienkowska, J., Brock, G., Carulli, J., Optimization of a high-throughput whole blood expression profiling methodology and its application to assess the pharmacodynamics of interferon (IFN) beta-1a or polyethylene glycol-conjugated IFN beta-1a in healthy clinical trial subjects. BMC Res. Notes, 6, 2013, 8.
34. [34] Fava, R.A., Kennedy, S.M., Wood, S.G., Bolstad, A.I., Bienkowska, J., Papandile, A., et al. Lymphotoxin-beta receptor blockade reduces CXCL13 in lacrimal glands and improves corneal integrity in the NOD model of Sjogren's syndrome. Arthritis Res. Ther., 13, 2011, R182.
35. [35] Gatumu, M.K., Skarstein, K., Papandile, A., Browning, J.L., Fava, R.A., Bolstad, A.I., Blockade of lymphotoxin-beta receptor signaling reduces aspects of Sjogren's syndrome in salivary glands of non-obese diabetic mice. Arthritis Res. Ther., 11, 2009, R24.
36. + T Cell Subsets in the Target Tissue of Sjögren's Syndrome and Their Differential Regulation by the Lymphotoxin/LIGHT Signaling Axis. Manuscript in Revision. 2016.
37. + T cells in BAFF-transgenic mice suppress T cell effector responses. J. Immunol. 182 (2009), 793–801.
38. [38] Stohl, W., Metyas, S., Tan, S.M., Cheema, G.S., Oamar, B., Xu, D., et al. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum. 48 (2003), 3475–3486.
39. [39] Cheema, G.S., Roschke, V., Hilbert, D.M., Stohl, W., Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum. 44 (2001), 1313–1319.
40. [40] Bosello, S., Youinou, P., Daridon, C., Tolusso, B., Bendaoud, B., Pietrapertosa, D., et al. Concentrations of BAFF correlate with autoantibody levels, clinical disease activity, and response to treatment in early rheumatoid arthritis. J. Rheumatol. 35 (2008), 1256–1264.
41. [41] Delaleu, N., Nguyen, C.Q., Peck, A.B., Jonsson, R., Sjogren's syndrome: studying the disease in mice. Arthritis Res. Ther., 13, 2011, 217.
42. [42] Shen, L., Suresh, L., Li, H., Zhang, C., Kumar, V., Pankewycz, O., et al. IL-14 alpha, the nexus for primary Sjogren's disease in mice and humans. Clin. Immunol. 130 (2009), 304–312.
43. [43] Husain-Krautter, S., Kramer, J.M., Li, W., Guo, B., Rothstein, T.L., The osteopontin transgenic mouse is a new model for Sjogren's syndrome. Clin. Immunol. 157 (2015), 30–42.
44. [44] Zhang, Y., Li, J., Zhang, Y.M., Zhang, X.M., Tao, J., Effect of TACI signaling on humoral immunity and autoimmune diseases. J. Immunol. Res., 2015, 2015, 247426.
45. [45] Jacobs, H.M., Thouvenel, C.D., Leach, S., Arkatkar, T., Metzler, G., Scharping, N.E., et al. Cutting edge: BAFF promotes autoantibody production via TACI-dependent activation of transitional B cells. J. Immunol. 196 (2016), 3525–3531.
46. [46] Figgett, W.A., Deliyanti, D., Fairfax, K.A., Quah, P.S., Wilkinson-Berka, J.L., Mackay, F., Deleting the BAFF receptor TACI protects against systemic lupus erythematosus without extensive reduction of B cell numbers. J. Autoimmun. 61 (2015), 9–16.
47. [47] De Vita, S., Quartuccio, L., Seror, R., Salvin, S., Ravaud, P., Fabris, M., et al. Efficacy and safety of belimumab given for 12 months in primary Sjogren's syndrome: the BELISS open-label phase II study. Rheumatology 54 (2015), 2249–2256.
48. [48] Mariette, X., Seror, R., Quartuccio, L., Baron, G., Salvin, S., Fabris, M., et al. Efficacy and safety of belimumab in primary Sjogren's syndrome: results of the BELISS open-label phase II study. Ann. Rheum. Dis. 74 (2015), 526–531.
49. [49] Bossen, C., Schneider, P., BAFF, APRIL and their receptors: structure, function and signaling. Semin. Immunol. 18 (2006), 263–275.
50. [50] Varfolomeev, E., Kischkel, F., Martin, F., Seshasayee, D., Wang, H., Lawrence, D., et al. APRIL-deficient mice have normal immune system development. Mol. Cell. Biol. 24 (2004), 997–1006.
51. [51] Schiemann, B., Gommerman, J.L., Vora, K., Cachero, T.G., Shulga-Morskaya, S., Dobles, M., et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293 (2001), 2111–2114.
52. [52] Castigli, E., Scott, S., Dedeoglu, F., Bryce, P., Jabara, H., Bhan, A.K., et al. Impaired IgA class switching in APRIL-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 3903–3908.
53. [53] Huard, B., Tran, N.L., Benkhoucha, M., Manzin-Lorenzi, C., Santiago-Raber, M.L., Selective APRIL blockade delays systemic lupus erythematosus in mouse. PLoS One, 7, 2012, e31837.
54. [54] Jacob, C.O., Guo, S., Jacob, N., Pawar, R.D., Putterman, C., Quinn, W.J. 3rd, et al. Dispensability of APRIL to the development of systemic lupus erythematosus in NZM 2328 mice. Arthritis Rheum. 64 (2012), 1610–1619.
55. [55] Rahman, Z.S., Rao, S.P., Kalled, S.L., Manser, T., Normal induction but attenuated progression of germinal center responses in BAFF and BAFF-R signaling-deficient mice. J. Exp. Med. 198 (2003), 1157–1169.
56. [56] Vora, K.A., Wang, L.C., Rao, S.P., Liu, Z.Y., Majeau, G.R., Cutler, A.H., et al. Cutting edge: germinal centers formed in the absence of B cell-activating factor belonging to the TNF family exhibit impaired maturation and function. J. Immunol. 171 (2003), 547–551.
57. [57] Yan, M., Marsters, S.A., Grewal, I.S., Wang, H., Ashkenazi, A., Dixit, V.M., Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nat. Immunol. 1 (2000), 37–41.
58. [58] Vosters, J.L., Roescher, N., Illei, G.G., Chiorini, J.A., Tak, P.P., TACI-Fc gene therapy improves autoimmune sialadenitis but not salivary gland function in non-obese diabetic mice. Oral Dis. 18 (2012), 365–374.