Fol. Biol. 2009, 55, 166-176

https://doi.org/10.14712/fb2009055050166

BAFF from Bone Marrow-Derived Mesenchymal Stromal Cells of Rheumatoid Arthritis Patients Improves Their B-Cell Viability-Supporting Properties

Tomáš Dallos1,2, M. Krivošíková2,3, M. Chorązy-Massalska2, E. Warnawin2, E. Záňová2,4, W. Rudnicka2, A. Radzikowska2, W. Maśliński2

12nd Department of Paediatrics, Medical Faculty, Comenius University, Bratislava, Slovak Republic
2Department of Pathophysiology and Immunology, Institute of Rheumatology, Warsaw, Poland
3Institute of Immunology, Medical Faculty, Comenius University, Bratislava, Slovak Republic
4National Institute of Rheumatic Diseases, Piešťany, Slovak Republic

Received January 2008
Accepted May 2009

References

1. Arnett, F. C., Edworthy, S. M., Bloch, D. A., McShane, D. J., Fries, J. F., Cooper, N. S., Healey, L. A., Kaplan, S. R., Liang, M .H., Luthra, H. S., Medsger, T. A., Mitchell, D. M., Neustadt, D. H., Pinals, R. S., Schaller, J. G., Sharp, J. T., Wilder, R. L., Hunder, G. G. (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 31, 315-324. <https://doi.org/10.1002/art.1780310302>
2. Benvenuto, F., Ferrari, S., Gerdoni, E., Gualandi, F., Frassoni, F., Pistoia, V., Mancardi, G., Uccelli, A. (2007) Human mesenchymal stem cells promote survival of T cells in a quiescent state. Stem Cells 25, 1753-1760. <https://doi.org/10.1634/stemcells.2007-0068>
3. Braun, A., Takemura, S., Vallejo, A. N., Goronzy, J. J., Weyand, C. M. (2004) Lymphotoxin β-mediated stimulation of synoviocytes in rheumatoid arthritis. Arthritis Rheum. 50, 2140-2150. <https://doi.org/10.1002/art.20356>
4. Cheema, G. S., Roschke, V., Hilbert, D. M., Stohl, W. (2001) Elevated serum B-lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum. 44, 1313-1319. <https://doi.org/10.1002/1529-0131(200106)44:6<1313::AID-ART223>3.0.CO;2-S>
5. Chung, N. G., Jeong, D. C., Park, S. J., Choi, B. O., Cho, B., Kim, H. K., Chun, C. S., Won, J. H., Han, C. W. (2004) Cotransplantation of marrow stromal cells may prevent lethal graft-versus-host disease in major histocompatibility complex mismatched murine hematopoietic stem cell transplantation. Int. J. Hematol. 80, 370-376. <https://doi.org/10.1532/IJH97.A30409>
6. De Vita, S., Zaja, F., Sacco, S., De Candia, A., Fanin, R., Ferraccioli, G. (2002) Efficacy of selective B cell blockade in the treatment of rheumatoid arthritis: evidence for a pathogenetic role of B cells. Arthritis Rheum. 46, 2029-2033. <https://doi.org/10.1002/art.10467>
7. Djouad, F., Plence, P., Bony, C., Tropel, P., Apparailly, F., Sany, J., Noel, D., Jorgensen, C. (2003) Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102, 3837-3844. <https://doi.org/10.1182/blood-2003-04-1193>
8. Do, R. K., Hatada, E., Lee, H., Tourigny, M. R., Hilbert, D., Chen-Kiang, S. (2000) Attenuation of apoptosis underlies B-lymphocyte stimulator enhancement of humoral immune response. J. Exp. Med. 192, 953-964. <https://doi.org/10.1084/jem.192.7.953>
9. Edwards, J. C., Szczepanski, L., Szechinski, J., FilipowiczSosnowska, A., Emery, P., Close, D. R., Stevens, R. M., Shaw, T. (2004) Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350, 2572-2581. <https://doi.org/10.1056/NEJMoa032534>
10. Friedenstein, A. J., Chailakhyan, R. K., Latsinik, N. V., Panasyuk, A. F., Keiliss-Borok, I. V. (1974) Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17, 331-340. <https://doi.org/10.1097/00007890-197404000-00001>
11. Gorelik, L., Gilbride, K., Dobles, M., Kalled, S. L., Zandman, D., Scott, M. L. (2003) Normal B cell homeostasis requires B cell activation factor production by radiation-resistant cells. J. Exp. Med. 198, 937-945. <https://doi.org/10.1084/jem.20030789>
12. Gross, J. A., Dillon, S. R., Mudri, S., Johnston, J., Littau, A., Roque, R., Rixon, M., Schou, O., Foley, K. P., Haugen, H., McMillen, S., Waggie, K., Schreckhise, R. W., Shoemaker, K., Vu, T., Moore, M., Grossman, A., Clegg, C. H. (2001) TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease impaired B cell maturation in mice lacking BLyS. Immunity 15, 289-302. <https://doi.org/10.1016/S1074-7613(01)00183-2>
13. Hill, J. A., Southwood, S., Sette, A., Jevnikar, A. M., Bell, D. A., Cairns, E. (2003) Cutting edge: the conversion of arginine to citrulline allows for a high-affinity peptide interaction with the rheumatoid arthritis-associated HLA-DRB1*0401 MHC class II molecule. J. Immunol. 171, 538-541. <https://doi.org/10.4049/jimmunol.171.2.538>
14. Hsu, B. L., Harless, S. M., Lindsley, R. C., Hilbert, D. M., Cancro, M. P. (2002) Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators. J. Immunol. 168, 5993-5996. <https://doi.org/10.4049/jimmunol.168.12.5993>
15. Jimenez-Boj, E., Redlich, K., Turk, B., Hanslik-Schnabel, B., Wanivenhaus, A., Chott, A., Smolen, J. S., Schett, G. (2005) Interaction between synovial inflammatory tissue and bone marrow in rheumatoid arthritis. J. Immunol. 175, 2579-2588. <https://doi.org/10.4049/jimmunol.175.4.2579>
16. Khare, S. D., Sarosi, I., Xia, X. Z., Miner, K., Solovyev, I., Hawkins, N., Kelley, M., Chang, D., Van, G., Ross, L., Delaney, J., Wang, L., Lacey, D., Boyle, W. J., Hsu, H. (2000) Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc. Natl. Acad. Sci. USA 97, 3370-3375. <https://doi.org/10.1073/pnas.97.7.3370>
17. Klyushnenkova, E., Mosca, J. D., Zernetkina, V., Majumdar, M. K., Beggs, K. J., Simonetti, D. W., Deans, R. J., McIntosh, K. R. (2005) T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J. Biomed. Sci. 12, 47-57. <https://doi.org/10.1007/s11373-004-8183-7>
18. Krampera, M., Glennie, S., Dyson, J., Scott, D., Laylor, R., Simpson, E., Dazzi, F. (2003) Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101, 3722-3729. <https://doi.org/10.1182/blood-2002-07-2104>
19. Le Blanc, K., Rasmusson, I., Sundberg, B., Gotherstrom, C., Hassan, M., Uzunel, M., Ringden, O. (2004) Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363, 1439-1441. <https://doi.org/10.1016/S0140-6736(04)16104-7>
20. Lesley, R., Xu, Y., Kalled, S. L., Hess, D. M., Schwab, S. R., Shu, H. B., Cyster, J. G. (2004) Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20, 441-453. <https://doi.org/10.1016/S1074-7613(04)00079-2>
21. Levine, M. H., Haberman, A. M., Sant’Angelo, D. B., Hannum, L. G., Cancro, M. P., Janeway, C. A. Jr., Shlomchik, M. J. (2000) A B-cell receptor-specific selection step governs immature to mature B cell differentiation. Proc. Natl. Acad. Sci. USA 97, 2743-2748. <https://doi.org/10.1073/pnas.050552997>
22. Loder, F., Mutschler, B., Ray, R. J., Paige, C. J., Sideras, P., Torres, R., Lamers, M. C., Carsetti, R. (1999) B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190, 75-89. <https://doi.org/10.1084/jem.190.1.75>
23. Maccario, R., Podesta, M., Moretta, A., Cometa, A., Comoli, P., Montagna, D., Daudt, L., Ibatici, A., Piaggio, G., Pozzi, S., Frassoni, F., Locatelli, F. (2005) Interaction of human mesenchymal stem cells with cells involved in alloantigenspecific immune response favours the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica 90, 516-525.
24. Mackay, F., Woodcock, S. A., Lawton, P., Ambrose, C., Baetscher, M., Schneider, P., Tschopp, J., Browning, J. L. (1999) Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 190, 1697-1710. <https://doi.org/10.1084/jem.190.11.1697>
25. MacLennan, I. C., Gulbranson-Judge, A., Toellner, K. M., Casamayor-Palleja, M., Chan, E., Sze, D. M., Luther, S. A., Orbea, H. A. (1997) The changing preference of T and B cells for partners as T-dependent antibody responses develop. Immunol. Rev. 156, 53-66. <https://doi.org/10.1111/j.1600-065X.1997.tb00958.x>
26. Marinova-Mutafchieva, L., Williams, R. O., Funa. K., Maini. R. N., Zvaifler, N. J. (2002) Inflammation is preceded by tumor necrosis factor-dependent infiltration of mesenchymal cells in experimental arthritis. Arthritis Rheum. 46, 507-513. <https://doi.org/10.1002/art.10126>
27. McQueen, F. M., Benton, N., Perry, D., Crabbe, J., Robinson, E., Yeoman, S., McLean, L, Stewart, N. (2003) Bone edema scored on magnetic resonance imaging scans of the dominant carpus at presentation predicts radiographic joint damage of the hands and feet six years later in patients with rheumatoid arthritis. Arthritis Rheum. 48, 1814-1827. <https://doi.org/10.1002/art.11162>
28. McQueen, F. M., Ostendorf, B. (2006) What is MRI bone oedema in rheumatoid arthritis and why does it matter? Arthritis Res. Ther. 8, 222. <https://doi.org/10.1186/ar2075>
29. Moreaux, J., Cremer, F. W., Reme, T., Raab, M., Mahtouk, K., Kaukel, P., Pantesco, V., De Vos, J., Jourdan, E., Jauch, A., Legouffe, E., Moos, M., Fiol, G., Goldschmidt, H., Rossi, J. F., Hose, D., Klein, B. (2005) The level of TACI gene expression in myeloma cells is associated with a signature of microenvironment dependence versus a plasmablastic signature. Blood 106, 1021-1030. <https://doi.org/10.1182/blood-2004-11-4512>
30. 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. (2004) 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. 173, 807-817. <https://doi.org/10.4049/jimmunol.173.2.807>
31. Ng, L. G., Mackay, C. R., Mackay, F. (2005) The BAFF/ APRIL system: life beyond B-lymphocytes. Mol. Immunol. 42, 763-772. <https://doi.org/10.1016/j.molimm.2004.06.041>
32. 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. (2004) BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 199, 91-98. <https://doi.org/10.1084/jem.20031330>
33. Ohata, J., Zvaifler, N. J., Nishio, M., Boyle, D. L., Kalled, S. L., Carson, D. A., Kipps, T. J. (2005) Fibroblast-like synoviocytes of mesenchymal origin express functional B cell-activating factor of the TNF family in response to proinflammatory cytokines. J. Immunol. 174, 864-870. <https://doi.org/10.4049/jimmunol.174.2.864>
34. Ostergaard, M., Peterfy, C., Conaghan, P., McQueen, F., Bird, P., Ejbjerg, B., Shnier, R., O‘Connor, P., Klarlund, M., Emery, P., Genant, H., Lassere, M., Edmonds, J. (2003) OMERACT Rheumatoid Arthritis Magnetic Resonance Imaging Studies. Core set of MRI acquisitions, joint pathology definitions, and the OMERACT RA-MRI scoring system. J. Rheumatol. 30, 1385-1388.
35. Pavelka, K., Rovenský, J., Szilasiová, A., Rovenská, E., Buc, M., Rybár, I., Kopecký, S. (2003) Rheumatoid arthritis. In: Clinical Rheumatology. eds. Pavelka, K., Rovenský, J. pp 181-214, Galén. Praha (in Czech)
36. Pers, J. O., Daridon, C., Devauchelle, V., Jousse, S., Saraux, A., Jamin, C., Youinou, P. (2005) BAFF overexpression is associated with autoantibody production in autoimmune diseases. Ann. N. Y. Acad. Sci. 1050, 34-39. <https://doi.org/10.1196/annals.1313.004>
37. Sasaki, Y., Casola, S., Kutok, J. L., Rajewsky, K., SchmidtSupprian, M. (2004) TNF family member B cell-activating factor (BAFF) receptor-dependent and -independent roles for BAFF in B cell physiology. J. Immunol. 173, 2245-2252. <https://doi.org/10.4049/jimmunol.173.4.2245>
38. Schiemann, B., Gommerman, J. L., Vora, K., Cachero, T. G., Shulga-Morskaya, S., Dobles, M., Frew, E., Scott, M. L. (2001) An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293, 2111-2114. <https://doi.org/10.1126/science.1061964>
39. Schneider, P., MacKay, F., Steiner, V., Hofmann, K., Bodmer, J. L., Holler, N., Ambrose, C., Lawton, P., Bixler, S., AchaOrbea, H., Valmori, D., Romero, P., Werner-Favre, C., Zubler, R. H., Browning, J. L., Tschopp, J. (1999) BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J. Exp. Med. 189, 1747-1756. <https://doi.org/10.1084/jem.189.11.1747>
40. Svensson, L., Jirholt, J., Holmdahl, R., Jansson, L. (1998) B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin. Exp. Immunol. 111, 521-526. <https://doi.org/10.1046/j.1365-2249.1998.00529.x>
41. Tabera, S., Pérez-Simón, J. A., Díez-Campelo M, SánchezAbarca, L. I., Blanco, B., López, A., Benito, A., Ocio, E., Sánchez-Guijo, F. M., Cañizo, C., San Miguel J. F (2008) The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes. Haematologica 93, 1301-1309. <https://doi.org/10.3324/haematol.12857>
42. Tai, Y. T., Li, X. F., Breitkreutz, I., Song, W., Neri, P., Catley, L., Podar, K., Hideshima, T., Chauhan, D., Raje, N., Schlossman, R., Richardson, P., Munshi, N. C., Anderson, K. C. (2006) Role of B-cell-activating factor in adhesion and growth of human multiple myeloma cells in the bone marrow microenvironment. Cancer Res. 66, 6675-6682. <https://doi.org/10.1158/0008-5472.CAN-06-0190>
43. Takemura, S., Klimiuk, P A., Braun, A., Goronzy, J. J., Weyand, C. M. (2001) T cell activation in rheumatoid synovium is B cell dependent. J. Immunol. 167, 4710-4718. <https://doi.org/10.4049/jimmunol.167.8.4710>
44. Tang, J., Nuccie, B. L., Ritterman, I., Liesveld, J. L., Abboud, C. N., Ryan, D. H. (1997) TGF-β down-regulates stromal IL-7 secretion and inhibits proliferation of human B cell precursors. J. Immunol. 159, 117-125. <https://doi.org/10.4049/jimmunol.159.1.117>
45. Traggiai, E., Volpi, S., Schena, F., Gattorno, M., Ferlito, F., Moretta, L., Martini, A. (2008) Bone marrow-derived mesenchymal stem cells induce both polyclonal expansion and differentiation of B cells isolated from healthy donors and systemic lupus erythematosus patients. Stem Cells 26, 562-569. <https://doi.org/10.1634/stemcells.2007-0528>
46. Warnawin, E., Burakowski, T., Gajewski, M., Radzikowska, A., Kornatka, A., Michalak, C., Małdyk, P., Maśliński, S., Maśliński, W. (2005) Preservation of chondrogenic potential of mesenchymal stem cells isolated from osteoarthritic patients during proliferation in response to platelet-derived growth factor (PDGF). Centr. Eur. J. Immunol. 30, 26-31.
47. Xin, Y., Wang, Y. M., Zhang, H., Li, J, Wang, W, Wei, Y. J., Hu, S. S. (2009) Aging adversely impacts biological properties of human bone marrow-derived mesenchymal stem cells: implications for tissue engineering heart valve construction. Artif. Organs. <https://doi.org/10.1111/j.1525-1594.2009.00824.x>
48. Yan, M., Marsters, S. A., Grewal, I. S., Wang, H., Ashkenazi, A., Dixit, V. M. (2000) Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nat. Immunol. 1, 37-41. <https://doi.org/10.1038/76889>
49. Zappia, E., Casazza, S., Pedemonte, E., Benvenuto, F., Bonanni, I., Gerdoni, E., Giunti, D., Ceravolo, A., Cazzanti, F., Frassoni, F., Mancardi, G., Uccelli, A. (2005) Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106, 1755-1761. <https://doi.org/10.1182/blood-2005-04-1496>
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