Identification of proteoglycans as the APRIL-specific binding partners

Journal of Experimental Medicine

Volumn 201, Issue 9, 2005, Pages 1375-1383

  Ingold, Karine ^a   Zumsteg, Adrian ^a,d   Tardivel, Aubry ^a   Huard, Bertrand ^b   Steiner, Quynh Giao ^a   Cachero, Teresa G ^c   Qiang, Fang ^c   Gorelik, Leonid ^c   Kalled, Susan L ^c   Acha Orbea, Hans ^a   Rennert, Paul D ^c   Tschopp, Jürg ^a   Schneider, Pascal ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c BIOGEN   (United States)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

APRIL PROTEIN; B CELL MATURATION ANTIGEN; B LYMPHOCYTE RECEPTOR; GLYCOSAMINOGLYCAN POLYSULFATE; GLYPICAN; HEPARIN; PROTEOGLYCAN; SYNDECAN; SYNDECAN 1; TRANSMEMBRANE ACTIVATOR AND CALCIUM SIGNAL MODULATING CYCLOPHILIN LIGAND INTERACTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL PROLIFERATION; CELL SURVIVAL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; LIGAND BINDING; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; OLIGOMERIZATION; PLASMA CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; RECEPTOR AFFINITY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; B-CELL ACTIVATING FACTOR; B-CELL ACTIVATION FACTOR RECEPTOR; B-CELL MATURATION ANTIGEN; B-LYMPHOCYTES; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; FLOW CYTOMETRY; HEPARIN; HUMANS; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MICE; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PLASMA CELLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEOGLYCANS; RECEPTORS, TUMOR NECROSIS FACTOR; TRANSFECTION; TRANSMEMBRANE ACTIVATOR AND CAML INTERACTOR PROTEIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 20844432040     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20042309     Document Type: Article

References (51)

1. Mackay, F., P. Schneider, P. Rennert, and J. Browning. 2003. BAFF AND APRIL: a tutorial on B cell survival. Annu. Rev. Immunol. 21:231-264.
2. Patel, D.R., H.J. Wallweber, J. Yin, S.K. Shriver, S.A. Marsters, N.C. Gordon, M.A. Starovasnik, and R.F. Kelley. 2004. Engineering an APRIL-specific B cell maturation antigen. J. Biol. Chem. 279:16727-16735.
3. Rennert, P., P. Schneider, T.G. Cachero, J. Thompson, L. Trabach, S. Hertig, N. Holler, F. Qian, C. Mullen, K. Strauch, et al. 2000. A soluble form of BCMA, a receptor for the TNF family member APRIL, inhibits tumor cell growth. J. Exp. Med. 192:1677-1684.
4. Seshasayee, D., P. Valdez, M. Yan, V.M. Dixit, D. Tumas, and I.S. Grewal. 2003. Loss of TACI causes fatal lymphoproliferation and autoimmunity, establishing TACI as an inhibitory BLyS receptor. Immunity. 18:279-288.
5. O'Connor, B.P., V.S. Raman, L.D. Erickson, W.J. Cook, L.K. Weaver, C. Ahonen, L.L. Lin, G.T. Mantchev, R.J. Bram, and R.J. Noelle. 2004. BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 199:91-98.
6. Litinskiy, M.B., B. Nardelli, D.M. Hilbert, B. He, A. Schaffer, P. Casali, and A. Cerutti. 2002. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3:822-829.
7. Castigli, E., S. Scott, F. Dedeoglu, P. Bryce, H. Jabara, A.K. Bhan, E. Mizoguchi, and R.S. Geha. 2004. Impaired IgA class switching in APRIL-deficient mice. Proc. Natl. Acad. Sci. USA. 101:3903-3908.
8. Hahne, M., T. Kataoka, M. Schroter, K. Hofmann, M. Irmler, J.L. Bodmer, P. Schneider, T. Bornand, N. Holler, L.E. French, et al. 1998. APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J. Exp. Med. 188:1185-1190.
9. Deshayes, F., G. Lapree, A. Portier, Y. Richard, P. Pencalet, D. Mahieu-Caputo, P. Horellou, and A. Tsapis. 2004. Abnormal production of the TNF-homologue APRIL increases the proliferation of human malignant glioblastoma cell lines via a specific receptor. Oncogene. 23:3005-3012.
10. Hymowitz, S.G., D.R. Patel, H.J. Wallweber, S. Runyon, M. Yan, J. Yin, S.K. Shriver, N.C. Gordon, B. Pan, N.J. Skelton, R.F. Kelley, and M.A. Starovasnik. 2004. Structures of APRIL-receptor complexes: Like BCMA, TACI employs only a single cysteine-rich domain for high-affinity ligand binding. J. Biol. Chem. 280:7218-7227.
11. Roditi, I., H. Schwarz, T.W. Pearson, R.P. Beecroft, M.K. Liu, J.P. Richardson, H.J. Buhring, J. Pleiss, R. Bulow, and R.O. Williams. 1989. Procyclin gene expression and loss of the variant surface glycoprotein during differentiation of Trypanosoma brucei. J. Cell Biol. 108:737-746.
12. Thompson, J.S., S.A. Bixler, F. Qian, K. Vora, M.L. Scott, T.G. Cachero, C. Hession, P. Schneider, I.D. Sizing, C. Mullen, et al. 2001. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science. 293:2108-2111.
13. Yan, M., S.A. Marsters, I.S. Grewal, H. Wang, A. Ashkenazi, and V.M. Dixit. 2000. Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nat. Immunol. 1:37-41.
14. Gras, M.P., Y. Laabi, G. Linares-Cruz, M.O. Blondel, J.P. Rigaut, J.C. Brouet, G. Leca, R. Haguenauer-Tsapis, and A. Tsapis. 1995. BC-MAp: an integral membrane protein in the Golgi apparatus of human mature B lymphocytes. Int. Immunol. 7:1093-1106.
15. Ardavin, C., P. Martin, I. Ferrero, I. Azcoitia, F. Anjuere, H. Diggelmann, F. Luthi, S. Luther, and H. Acha-Orbea. 1999. B cell response after MMTV infection: extrafollicular plasmablasts represent the main infected population and can transmit viral infection. J. Immunol. 162:2538-2545.
16. Yu, G., T. Boone, J. Delaney, N. Hawkins, M. Kelley, M. Ramakrishnan, S. McCabe, W.R. Qiu, M. Kornuc, X.Z. Xia, et al. 2000. APRIL and TALL-I and receptors BCMA and TACI: system for regulating humoral immunity. Nat. Immunol. 1:252-256.
17. Holler, N., A. Tardivel, M. Kovacsovics-Bankowski, S. Hertig, O. Gaide, F. Martinon, A. Tinel, D. Deperthes, S. Calderara, T. Schulthess, et al. 2003. Two adjacent trimeric Fas ligands are required for Fas signaling and formation of a death inducing signaling complex. Mol. Cell. Biol. 23:1428-1440.
18. Ng, L.G., A.P. Sutherland, R. Newton, F. Qian, T.G. Cachera, M.L. Scott, J.S. Thompson, J. Wheway, T. Chtanova, J. Groom, et al. 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.
19. Shulga-Morskaya, S., M. Dobles, M.E. Walsh, L.G. Ng, F. MacKay, S.P. Rao, S.L. Railed, and M.L. Scott. 2004. B cell-activating factor belonging to the TNF family acts through separate receptors to support B cell survival and T cell-independent antibody formation. J. Immunol. 173:2331-2341.
20. Jacob, J., R. Kassir, and G. Kelsoe. 1991. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J. Exp. Med. 173:1165-1175.
21. Wu, Y., D. Bressette, J.A. Carrell, T. Kaufman, P. Feng, K. Taylor, Y. Gan, Y.H. Cho, A.D. Garcia, E. Gollatz, et al. 2000. Tumor necrosis factor (TNF) receptor superfamily member TACI is a high affinity receptor for TNF family members APRIL and BLyS. J. Biol. Chem. 275:35478-35485.
22. Xia, X.Z., J. Treanor, G. Senaldi, S.D. Khare, T. Boone, M. Kelley, L.E. Theill, A. Colombero, I. Solovyev, F. Lee, et al. 2000. TACI is a TRAF-interacting receptor for TALL-1, a tumor necrosis factor family member involved in B cell regulation. J. Exp. Med. 192:137-143.
23. Xu, S., and K.P. Lam. 2001. B-cell maturation protein, which binds the tumor necrosis factor family members BAFF and APRIL, is dispensable for humoral immune responses. Mol. Cell. Biol. 21:4067-4074.
24. Yan, M., J.R. Brady, B. Chan, W.P. Lee, B. Hsu, S. Harless, M. Cancro, I.S. Grewal, and V.M. Dixit. 2001. Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency. Curr. Biol. 11:1547-1552.
25. Robeva, A.S., Y. Yan-Neale, P. Burfeind, D.L. Bodian, G.W. Chirn, F. Kolbinger, M. Labow, and R.D. Vallon. 2003. Rapid expression cloning of receptors using epitope-tagged ligands and high-speed cell sorting. Cytometry. 51:59-67.
26. Gross, J.A., J. Johnston, S. Mudri, R. Enselman, S.R. Dillon, K. Madden, W. Xu, J. Parrish-Novak, D. Foster, C. Lofton-Day, et al. 2000. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature. 404:995-999.
27. Lortat-Jacob, H., A. Grosdidier, and A. Imberty. 2002. Structural diversity of heparan sulfate binding domains in chemokines. Proc. Natl. Acad. Sci. USA. 99:1229-1234.
28. Wallweber, H.J., D.M. Compaan, M.A. Starovasnik, and S.G. Hymowitz. 2004. The crystal structure of a proliferation-inducing ligand, APRIL. J. Mol. Biol. 343:283-290.
29. Schneider, P., N. Holler, J.L. Bodmer, M. Hahne, K. Frei, A. Fontana, and J. Tschopp. 1998. Conversion of membrane-bound Fas(CD95) ligand to its soluble form is associated with downregulation of its proapoptotic activity and loss of liver toxicity. J. Exp. Med. 187:1205-1213.
30. Lopez-Fraga, M., R. Fernandez, J.P. Albar, and M. Hahne. 2001. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO Rep. 2:945-951.
31. Dementiev, A., M. Petitou, J.M. Herbert, and P.G. Gettins. 2004. The ternary complex of antithrombin-anhydrothrombin-heparin reveals the basis of inhibitor specificity. Nat Struct Mol Biol. 11:863-867.
32. Li, W., D.J. Johnson, C.T. Esmon, and J.A. Huntington. 2004. Structure of the antithrombin-thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol. 11:857-862.
33. Pellegrini, L., D.F. Burke, F. von Delft, B. Mulloy, and T.L. Blundell. 2000. Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature. 407:1029-1034.
34. Schlessinger, J., A.N. Plotnikov, O.A. Ibrahimi, A.V. Eliseenkova, B.K. Yeh, A. Yayon, R.J. Linhardt, and M. Mohammadi. 2000. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell. 6:743-750.
35. Sasisekharan, R., Z. Shriver, G. Venkataraman, and U. Narayanasami. 2002. Roles of heparan-sulphate glycosaminoglycans in cancer. Nat. Rev. Cancer. 2:521-528.
36. Pradet-Balade, B., J.P. Medema, M. Lopez-Fraga, J.C. Lozano, G.M. Kolfschoten, A. Picard, A.C. Martinez, J.A. Garcia-Sanz, and M. Hahne. 2002. An endogenous hybrid mRNA encodes TWE-PRIL, a functional cell surface TWEAK-APRIL fusion protein. EMBO J. 21:5711-5720.
37. Lau, E.K., C.D. Paavola, Z. Johnson, J.P. Gaudry, E. Geretti, F. Borlat, A.J. Kungl, A.E. Proudfoot, and T.M. Handel. 2004. Identification of the glycosaminoglycan binding site of the CC chemokine, MCP-1: implications for structure and function in vivo. J. Biol. Chem. 279:22294-22305.
38. Novak, A.J., J.R. Darce, B.K. Arendt, B. Harder, K. Henderson, W. Kindsvogel, J.A. Gross, P.R. Greipp, and D.F. Jelinek. 2004. Expression of BCMA, TACI, and BAFF-R in multiple myeloma: a mechanism for growth and survival. Blood. 103:689-694.
39. Kern, C., J.F. Cornuel, C. Billard, R. Tang, D. Rouillard, V. Stenou, T. Defrance, F. Ajchenbaum-Cymbalista, P.Y. Simonin, S. Feldblum, and J.P. Kolb. 2004. Involvement of BAFF and APRIL in the resistance to apoptosis of B-CLL through an autocrine pathway. Blood. 103:679-688.
40. He, B., A. Chadburn, E. Jou, E.J. Schattner, D.M. Knowles, and A. Cerutti. 2004. Lymphoma B cells evade apoptosis through the TNF family members BAFF/BLyS and APRIL. J. Immunol. 172:3268-3279.
41. Moreaux, J., E. Legouffe, E. Jourdan, P. Quittet, T. Reme, C. Lugagne, P. Moine, J.F. Rossi, B. Klein, and K. Tarte. 2004. BAFF and APRIL protect myeloma cells from apoptosis induced by interleukin 6 deprivation and dexamethasone. Blood. 103:3148-3157.
42. Planelles, L., C.E. Carvalho-Pinto, G. Hardenberg, S. Smaniotto, W. Savino, R. Gomez-Caro, M. Alvarez-Mon, J. de Jong, E. Eldering, A.C. Martinez, et al. 2004. APRIL promotes B-1 cell-associated neoplasm. Cancer Cell. 6:399-408.
43. Sanderson, R.D., and M. Borset. 2002. Syndecan-1 in B lymphoid malignancies. Ann. Hematol. 81:125-135.
44. Timar, J., K. Lapis, J. Dudas, A. Sebestyen, L. Kopper, and I. Kovalszky. 2002. Proteoglycans and tumor progression: Janus-faced molecules with contradictory functions in cancer. Semin. Cancer Biol. 12:173-186.
45. Ponta, H., L. Sherman, and P.A. Herrlich. 2003. CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 4:33-45.
46. Van Driel, M., U. Gunthert, A.C. van Kessel, P. Joling, R. Stauder, H.M. Lokhorst, and A.C. Bloem. 2002. CD44 variant isoforms are involved in plasma cell adhesion to bone marrow stromal cells. Leukemia. 16:135-143.
47. Vincent, T., and N. Mechti. 2004. IL-6 regulates CD44 cell surface expression on human myeloma cells. Leukemia. 18:967-975.
48. Couchman, J.R. 2003. Syndecans: proteoglycan regulators of cell-surface microdomains? Nat. Rev. Mol. Cell Biol. 4:926-937.
49. Holler, N., T. Kataoka, J.L. Bodmer, P. Romero, J. Romero, D. Deperthes, J. Engel, J. Tschopp, and P. Schneider. 2000. Development of improved soluble inhibitors of FasL and CD40L based on oligomerized receptors. J. Immunol. Methods. 237:159-173.
50. Pelletier, M., J.S. Thompson, F. Qian, S.A. Bixler, D. Gong, T. Cachero, K. Gilbride, E. Day, M. Zafari, C. Benjamin, et al. 2003. Comparison of soluble decoy IgG fusion proteins of BAFF-R and BCMA as antagonists for BAFF. J. Biol. Chem. 278:33127-33133.
51. Lalor, P.A., G.J. Nossal, R.D. Sanderson, and M.G. McHeyzer-Williams. 1992. Functional and molecular characterization of single, (4-hydroxy-3- nitrophenyl)acetyl (NP)-specific, IgG1 + B cells from antibody-secreting and memory B cell pathways in the C57BL/6 immune response to NP. Eur. J. Immunol. 22:3001-3011.