Syk inhibition with fostamatinib leads to transitional B lymphocyte depletion

Clinical Immunology

Volumn 142, Issue 3, 2012, Pages 237-242

  Barr, Paul M ^a   Wei, Chungwen ^b   Roger, James ^b   Schaefer Cutillo, Julia ^a   Kelly, Jennifer L ^a   Rosenberg, Alexander F ^b   Jung, John ^b   Sanz, Iñaki ^b   Friedberg, Jonathan W ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

B cell antigen receptor; Fostamatinib; Signaling therapies; Transitional b cells

Indexed keywords

CD19 ANTIBODY; FOSTAMATINIB; INTERLEUKIN 10; PROTEIN KINASE SYK;

ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; BLOOD SAMPLING; CD19+ B LYMPHOCYTE; CLINICAL ARTICLE; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG TARGETING; FLOW CYTOMETRY; FOLLICULAR LYMPHOMA; HUMAN; INTRACELLULAR SIGNALING; LARGE CELL LYMPHOMA; LYMPHOCYTE DEPLETION; LYMPHOCYTE SUBPOPULATION; MALIGNANT NEOPLASTIC DISEASE; MANTLE CELL LYMPHOMA; PERIPHERAL BLOOD MONONUCLEAR CELL; PRE B LYMPHOCYTE; PRIORITY JOURNAL;

CELL DIFFERENTIATION; HUMANS; INTERLEUKIN-10; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; OXAZINES; PRECURSOR CELLS, B-LYMPHOID; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PYRIDINES;

EID: 84857368975     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2011.12.012     Document Type: Article

References (35)

1. Weinblatt M.E., Kavanaugh A., Genovese M.C., Musser T.K., Grossbard E.B., Magilavy D.B. An oral spleen tyrosine kinase (Syk) inhibitor for rheumatoid arthritis. N. Engl. J. Med. 2010, 363:1303-1312.
2. Friedberg J.W., Sharman J., Sweetenham J., Johnston P.B., Vose J.M., Lacasce A., Schaefer-Cutillo J., De Vos S., Sinha R., Leonard J.P., Cripe L.D., Gregory S.A., Sterba M.P., Lowe A.M., Levy R., Shipp M.A. Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia. Blood 2010, 115:2578-2585.
3. Podolanczuk A., Lazarus A.H., Crow A.R., Grossbard E., Bussel J.B. Of mice and men: an open-label pilot study for treatment of immune thrombocytopenic purpura by an inhibitor of Syk. Blood 2009, 113:3154-3160.
4. Su T.T., Rawlings D.J. Transitional B lymphocyte subsets operate as distinct checkpoints in murine splenic B cell development. J. Immunol. 2002, 168:2101-2110.
5. Petro J.B., Gerstein R.M., Lowe J., Carter R.S., Shinners N., Khan W.N. Transitional type 1 and 2 B lymphocyte subsets are differentially responsive to antigen receptor signaling. J. Biol. Chem. 2002, 277:48009-48019.
6. Loder F., Mutschler B., Ray R.J., Paige C.J., Sideras P., Torres R., Lamers M.C., Carsetti R. 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. 1999, 190:75-89.
7. Turner M., Gulbranson-Judge A., Quinn M.E., Walters A.E., MacLennan I.C., Tybulewicz V.L. Syk tyrosine kinase is required for the positive selection of immature B cells into the recirculating B cell pool. J. Exp. Med. 1997, 186:2013-2021.
8. Turner M., Mee P.J., Costello P.S., Williams O., Price A.A., Duddy L.P., Furlong M.T., Geahlen R.L., Tybulewicz V.L. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 1995, 378:298-302.
9. Blair P.A., Norena L.Y., Flores-Borja F., Rawlings D.J., Isenberg D.A., Ehrenstein M.R., Mauri C. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010, 32:129-140.
10. Iwata Y., Matsushita T., Horikawa M., DiLillo D.J., Yanaba K., Venturi G.M., Szabolcs P.M., Bernstein S.H., Magro C.M., Williams A.D., Hall R.P., St Clair E.W., Tedder T.F. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011, 117:530-541.
11. Duddy M., Niino M., Adatia F., Hebert S., Freedman M., Atkins H., Kim H.J., Bar-Or A. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. 2007, 178:6092-6099.
12. Kis L.L., Takahara M., Nagy N., Klein G., Klein E. IL-10 can induce the expression of EBV-encoded latent membrane protein-1 (LMP-1) in the absence of EBNA-2 in B lymphocytes and in Burkitt lymphoma- and NK lymphoma-derived cell lines. Blood 2006, 107:2928-2935.
13. Visser H.P., Tewis M., Willemze R., Kluin-Nelemans J.C. Mantle cell lymphoma proliferates upon IL-10 in the CD40 system. Leukemia 2000, 14:1483-1489.
14. Cortes J., Kurzrock R. Interleukin-10 in non-Hodgkin's lymphoma. Leuk. Lymphoma 1997, 26:251-259.
15. Hatton O., Phillips L.K., Vaysberg M., Hurwich J., Krams S.M., Martinez O.M. Syk activation of PI3K/Akt prevent HtrA2-dependent loss of XIAP to promote survival of Epstein-Barr virus (EBV)+ B cell lymphomas. J. Biol. Chem. 2011, 286:37368-37378.
16. Palanichamy A., Barnard J., Zheng B., Owen T., Quach T., Wei C., Looney R.J., Sanz I., Anolik J.H. Novel human transitional B cell populations revealed by B cell depletion therapy. J. Immunol. 2009, 182:5982-5993.
17. Pani G., Siminovitch K.A., Paige C.J. The motheaten mutation rescues B cell signaling and development in CD45-deficient mice. J. Exp. Med. 1997, 186:581-588.
18. Xu S., Tan J.E., Wong E.P., Manickam A., Ponniah S., Lam K.P. B cell development and activation defects resulting in xid-like immunodeficiency in BLNK/SLP-65-deficient mice. Int. Immunol. 2000, 12:397-404.
19. Wang D., Feng J., Wen R., Marine J.C., Sangster M.Y., Parganas E., Hoffmeyer A., Jackson C.W., Cleveland J.L., Murray P.J., Ihle J.N. Phospholipase Cgamma2 is essential in the functions of B cell and several Fc receptors. Immunity 2000, 13:25-35.
20. Yamazaki T., Takeda K., Gotoh K., Takeshima H., Akira S., Kurosaki T. Essential immunoregulatory role for BCAP in B cell development and function. J. Exp. Med. 2002, 195:535-545.
21. Macallan D.C., Wallace D.L., Zhang Y., Ghattas H., Asquith B., de Lara C., Worth A., Panayiotakopoulos G., Griffin G.E., Tough D.F., Beverley P.C. B-cell kinetics in humans: rapid turnover of peripheral blood memory cells. Blood 2005, 105:3633-3640.
22. Lee E.H., Hellerstein M., Wu H., Sanz I. Differences in proliferation rates of human B cell subsets by in vivo labeling of young healthy subjects. Arthritis Rheum. 2007, 56:S517.
23. Zhu Y., Herlaar E., Masuda E.S., Burleson G.R., Nelson A.J., Grossbard E.B., Clemens G.R. Immunotoxicity assessment for the novel Spleen tyrosine kinase inhibitor R406. Toxicol. Appl. Pharmacol. 2007, 221:268-277.
24. Bahjat F.R., Pine P.R., Reitsma A., Cassafer G., Baluom M., Grillo S., Chang B., Zhao F.F., Payan D.G., Grossbard E.B., Daikh D.I. An orally bioavailable spleen tyrosine kinase inhibitor delays disease progression and prolongs survival in murine lupus. Arthritis Rheum. 2008, 58:1433-1444.
25. Colonna L., Catalano G., Chew C., D'Agati V., Thomas J.W., Wong F.S., Schmitz J., Masuda E.S., Reizis B., Tarakhovsky A., Clynes R. Therapeutic targeting of Syk in autoimmune diabetes. J. Immunol. 2010, 185:1532-1543.
26. Suljagic M., Longo P.G., Bennardo S., Perlas E., Leone G., Laurenti L., Efremov D.G. The Syk inhibitor fostamatinib disodium (R788) inhibits tumor growth in the Emu- TCL1 transgenic mouse model of CLL by blocking antigen-dependent B-cell receptor signaling. Blood 2010, 116:4894-4905.
27. Miller J.P., Stadanlick J.E., Cancro M.P. Space, selection, and surveillance: setting boundaries with BLyS. J. Immunol. 2006, 176:6405-6410.
28. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
29. Samuels J., Ng Y.S., Coupillaud C., Paget D., Meffre E. Impaired early B cell tolerance in patients with rheumatoid arthritis. J. Exp. Med. 2005, 201:1659-1667.
30. Yurasov S., Wardemann H., Hammersen J., Tsuiji M., Meffre E., Pascual V., Nussenzweig M.C. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 2005, 201:703-711.
31. Llorente L., Zou W., Levy Y., Richaud-Patin Y., Wijdenes J., Alcocer-Varela J., Morel-Fourrier B., Brouet J.C., Alarcon-Segovia D., Galanaud P. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J. Exp. Med. 1995, 181:839-844.
32. Blay J.Y., Burdin N., Rousset F., Lenoir G., Biron P., Philip T., Banchereau J., Favrot M.C. Serum interleukin-10 in non-Hodgkin's lymphoma: a prognostic factor. Blood 1993, 82:2169-2174.
33. Zent C.S., LaPlant B.R., Johnston P.B., Call T.G., Habermann T.M., Micallef I.N., Witzig T.E. The treatment of recurrent/refractory chronic lymphocytic leukemia/small lymphocytic lymphoma (CLL) with everolimus results in clinical responses and mobilization of CLL cells into the circulation. Cancer 2010, 116:2201-2207.
34. Furman R.R., Byrd J.C., Brown J.R., Coutre S.E., Benson D.M., Wagner-Johnston N.D., Flinn I.W., Kahl B.S., Spurgeon S.E., Lannutti B., Giese N.A., Webb H.K., Ulrich R.G., Peterman S., Holes L.M., Yu A.S. CAL-101, an isoform-selective inhibitor of phosphatidylinositol 3-kinase P110{delta}, demonstrates clinical activity and pharmacodynamic effects in patients with relapsed or refractory chronic lymphocytic leukemia. ASH Annual Meeting Abstracts 2010, 116:55.
35. Burger J.A., O'Brien S., Fowler N., Advani R., Sharman J.P., Furman R.R., Izumi R., Buggy J., Loury D., Hamdy A., Byrd J.C., Blum K.A. The Bruton's tyrosine kinase inhibitor, PCI-32765, is well tolerated and demonstrates promising clinical activity in chronic lymphocytic leukemia (CLL) and small lymphocytic lymphoma (SLL): an update on ongoing phase 1 studies. ASH Annual Meeting Abstracts 2010, 116:57.