CIN85 drives B cell responses by linking BCR signals to the canonical NF-κB pathway

Journal of Experimental Medicine

Volumn 208, Issue 7, 2011, Pages 1447-1457

  Kometani, Kohei ^a   Yamada, Takayuki ^a,b   Sasaki, Yoshiteru ^c   Yokosuka, Tadashi ^a   Saito, Takashi ^a   Rajewsky, Klaus ^c   Ishiai, Masamichi ^b   Hikida, Masaki ^a,b   Kurosaki, Tomohiro ^a,b,d  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

^c CENTER FOR BLOOD RESEARCH   (United States)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; B LYMPHOCYTE RECEPTOR; CBL PROTEIN; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVATION; GENE DELETION; IMMUNE RESPONSE; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE;

ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; BASE SEQUENCE; CELL PROLIFERATION; CELL SURVIVAL; DNA PRIMERS; I-KAPPA B KINASE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOPLASM PROTEINS; NERVE TISSUE PROTEINS; NF-KAPPA B; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 79960355211     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20102665     Document Type: Article

References (51)

1. Anderson, S.M., M.M. Tomayko, A. Ahuja, A.M. Haberman, and M.J. Shlomchik. 2007. New markers for murine memory B cells that define mutated and unmutated subsets. J. Exp. Med. 204:2103-2114.
2. Baba, Y., K. Nishida, Y. Fujii, T. Hirano, M. Hikida, and T. Kurosaki. 2008. Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat. Immunol. 9:81-88.
3. Bezsonova, I., M.C. Bruce, S. Wiesner, H. Lin, D. Rotin, and J.D. Forman-Kay. 2008. Interactions between the three CIN85 SH3 domains and ubiquitin: implications for CIN85 ubiquitination. Biochemistry. 47:8937-8949.
4. Bléry, M., L. Tze, L.A. Miosge, J.E. Jun, and C.C. Goodnow. 2006. Essential role of membrane cholesterol in accelerated BCR internalization and uncoupling from NF-(B in B cell clonal anergy. J. Exp. Med. 203:1773-1783.
5. Buchman, V.L., C. Luke, E.B. Borthwick, I. Gout, and N. Ninkina. 2002. Organization of the mouse Ruk locus and expression of isoforms in mouse tissues. Gene. 295:13-17.
6. Cinamon, G., M.A. Zachariah, O.M. Lam, F.W. Foss Jr., and J.G. Cyster. 2008. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 9:54-62.
7. Dikic, I. 2002. CIN85/CMS family of adaptor molecules. FEBS Lett. 529:110-115.
8. Dikic, I., and S. Giordano. 2003. Negative receptor signalling. Curr. Opin. Cell Biol. 15:128-135.
9. Dustin, M.L., M.W. Olszowy, A.D. Holdorf, J. Li, S. Bromley, N. Desai, P. Widder, F. Rosenberger, P.A. van der Merwe, P.M. Allen, and A.S. Shaw. 1998. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell. 94:667-677.
10. Fu, C., C.W. Turck, T. Kurosaki, and A.C. Chan. 1998. BLNK: a central linker protein in B cell activation. Immunity. 9:93-103.
11. Goitsuka, R., Y. Fujimura, H. Mamada, A. Umeda, T. Morimura, K. Uetsuka, K. Doi, S. Tsuji, and D. Kitamura. 1998. BASH, a novel signaling molecule preferentially expressed in B cells of the bursa of Fabricius. J. Immunol. 161:5804-5808.
12. Gout, I., G. Middleton, J. Adu, N.N. Ninkina, L.B. Drobot, V. Filonenko, G. Matsuka, A.M. Davies, M. Waterfield, and V.L. Buchman. 2000. Negative regulation of PI 3-kinase by Ruk, a novel adaptor protein. EMBO J. 19:4015-4025.
13. Guinamard, R., M. Okigaki, J. Schlessinger, and J.V. Ravetch. 2000. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immunol. 1:31-36.
14. Hardy, R.R., and K. Hayakawa. 2001. B cell development pathways. Annu. Rev. Immunol. 19:595-621.
15. Hayakawa, K., M. Asano, S.A. Shinton, M. Gui, D. Allman, C.L. Stewart, J. Silver, and R.R. Hardy. 1999. Positive selection of natural autoreactive B cells. Science. 285:113-116.
16. Hobeika, E., S. Thiemann, B. Storch, H. Jumaa, P.J. Nielsen, R. Pelanda, and M. Reth. 2006. Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA. 103:13789-13794.
17. Hutchings, N.J., N. Clarkson, R. Chalkley, A.N. Barclay, and M.H. Brown. 2003. Linking the T cell surface protein CD2 to the actin-capping protein CAPZ via CMS and CIN85. J. Biol. Chem. 278:22396-22403.
18. Itano, A.A., S.J. McSorley, R.L. Reinhardt, B.D. Ehst, E. Ingulli, A.Y. Rudensky, and M.K. Jenkins. 2003. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity. 19:47-57.
19. Joazeiro, C.A., S.S. Wing, H. Huang, J.D. Leverson, T. Hunter, and Y.C. Liu. 1999. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science. 286:309-312.
20. Jun, J.E., and C.C. Goodnow. 2003. Scaffolding of antigen receptors for immunogenic versus tolerogenic signaling. Nat. Immunol. 4:1057-1064.
21. Kanayama, A., R.B. Seth, L. Sun, C.K. Ea, M. Hong, A. Shaito, Y.H. Chiu, L. Deng, and Z.J. Chen. 2004. TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell. 15:535-548.
22. Kitaura, Y., I.K. Jang, Y. Wang, Y.C. Han, T. Inazu, E.J. Cadera, M. Schlissel, R.R. Hardy, and H. Gu. 2007. Control of the B cell-intrinsic tolerance programs by ubiquitin ligases Cbl and Cbl-b. Immunity. 26:567-578.
23. Köntgen, F., G. Süss, C. Stewart, M. Steinmetz, and H. Bluethmann. 1993. Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int. Immunol. 5:957-964.
24. Lam, K.P., R. Kühn, and K. Rajewsky. 1997. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell. 90:1073-1083.
25. Legrand-Poels, S., G. Kustermans, F. Bex, E. Kremmer, T.A. Kufer, and J. Piette. 2007. Modulation of Nod2-dependent NF-kappaB signaling by the actin cytoskeleton. J. Cell Sci. 120:1299-1310.
26. Molfetta, R., F. Belleudi, G. Peruzzi, S. Morrone, L. Leone, I. Dikic, M. Piccoli, L. Frati, M.R. Torrisi, A. Santoni, and R. Paolini. 2005. CIN85 regulates the ligand-dependent endocytosis of the IgE receptor: a new molecular mechanism to dampen mast cell function. J. Immunol. 175:4208-4216.
27. Monroe, J.G. 2006. ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat. Rev. Immunol. 6:283-294.
28. Navarro, M.N., G. Nusspaumer, P. Fuentes, S. González-García, J. Alcain, and M.L. Toribio. 2007. Identification of CMS as a cytosolic adaptor of the human pTalpha chain involved in pre-TCR function. Blood. 110:4331-4340.
29. Oh-hora, M., S. Johmura, A. Hashimoto, M. Hikida, and T. Kurosaki. 2003. Requirement for Ras guanine nucleotide releasing protein 3 in coupling phospholipase C-γ2 to Ras in B cell receptor signaling. J. Exp. Med. 198:1841-1851.
30. Pape, K.A., D.M. Catron, A.A. Itano, and M.K. Jenkins. 2007. The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity. 26:491-502.
31. Peruzzi, G., R. Molfetta, F. Gasparrini, L. Vian, S. Morrone, M. Piccoli, L. Frati, A. Santoni, and R. Paolini. 2007. The adaptor molecule CIN85 regulates Syk tyrosine kinase level by activating the ubiquitin-proteasome degradation pathway. J. Immunol. 179:2089-2096.
32. Petrelli, A., G.F. Gilestro, S. Lanzardo, P.M. Comoglio, N. Migone, and S. Giordano. 2002. The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature. 416:187-190.
33. Rickert, R.C., K. Rajewsky, and J. Roes. 1995. Impairment of T-celldependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature. 376:352-355.
34. Saijo, K., I. Mecklenbräuker, A. Santana, M. Leitger, C. Schmedt, and A. Tarakhovsky. 2002. Protein kinase C (controls nuclear factor (B activation in B cells through selective regulation of the I(B kinase α. J. Exp. Med. 195:1647-1652.
35. Sasaki, Y., E. Derudder, E. Hobeika, R. Pelanda, M. Reth, K. Rajewsky, and M. Schmidt-Supprian. 2006. Canonical NF-kappaB activity, dispensable for B cell development, replaces BAFF-receptor signals and promotes B cell proliferation upon activation. Immunity. 24:729-739.
36. Schiemann, B., J.L. Gommerman, K. Vora, T.G. Cachero, S. Shulga-Morskaya, M. Dobles, E. Frew, and M.L. Scott. 2001. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science. 293:2111-2114.
37. Shih, T.A., E. Meffre, M. Roederer, and M.C. Nussenzweig. 2002. Role of BCR affinity in T cell dependent antibody responses in vivo. Nat. Immunol. 3:570-575.
38. Shimokawa, N., K. Haglund, S.M. Hölter, C. Grabbe, V. Kirkin, N. Koibuchi, C. Schultz, J. Rozman, D. Hoeller, C.H. Qiu, et al. 2010. CIN85 regulates dopamine receptor endocytosis and governs behaviour in mice. EMBO J. 29:2421-2432.
39. Shinohara, H., and T. Kurosaki. 2009. Comprehending the complex connection between PKCbeta, TAK1, and IKK in BCR signaling. Immunol. Rev. 232:300-318.
40. Shinohara, H., S. Maeda, H. Watarai, and T. Kurosaki. 2007. I(B kinase (-induced phosphorylation of CARMA1 contributes to CARMA1- Bcl10-MALT1 complex formation in B cells. J. Exp. Med. 204:3285-3293.
41. Soubeyran, P., K. Kowanetz, I. Szymkiewicz, W.Y. Langdon, and I. Dikic. 2002. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature. 416:183-187.
42. Su, T.T., B. Guo, Y. Kawakami, K. Sommer, K. Chae, L.A. Humphries, R.M. Kato, S. Kang, L. Patrone, R. Wall, et al. 2002. PKC-beta controls I kappa B kinase lipid raft recruitment and activation in response to BCR signaling. Nat. Immunol. 3:780-786.
43. Sun, L., L. Deng, C.K. Ea, Z.P. Xia, and Z.J. Chen. 2004. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell. 14:289-301.
44. Swanson, C.L., T.J. Wilson, P. Strauch, M. Colonna, R. Pelanda, and R.M. Torres. 2010. Type I IFN enhances follicular B cell contribution to the T cell-independent antibody response. J. Exp. Med. 207:1485-1500.
45. Szymkiewicz, I., K. Kowanetz, P. Soubeyran, A. Dinarina, S. Lipkowitz, and I. Dikic. 2002. CIN85 participates in Cbl-b-mediated down-regulation of receptor tyrosine kinases. J. Biol. Chem. 277:39666-39672.
46. Take, H., S. Watanabe, K. Takeda, Z.X. Yu, N. Iwata, and S. Kajigaya. 2000. Cloning and characterization of a novel adaptor protein, CIN85, that interacts with c-Cbl. Biochem. Biophys. Res. Commun. 268:321-328.
47. Wang, D., R. Matsumoto, Y. You, T. Che, X.Y. Lin, S.L. Gaffen, and X. Lin. 2004. CD3/CD28 costimulation-induced NF-kappaB activation is mediated by recruitment of protein kinase C-theta, Bcl10, and IkappaB kinase beta to the immunological synapse through CARMA1. Mol. Cell. Biol. 24:164-171.
48. Watanabe, S., H. Take, K. Takeda, Z.X. Yu, N. Iwata, and S. Kajigaya. 2000. Characterization of the CIN85 adaptor protein and identification of components involved in CIN85 complexes. Biochem. Biophys. Res. Commun. 278:167-174.
49. Wen, L., J. Brill-Dashoff, S.A. Shinton, M. Asano, R.R. Hardy, and K. Hayakawa. 2005. Evidence of marginal-zone B cell-positive selection in spleen. Immunity. 23:297-308.
50. Wienands, J., J. Schweikert, B. Wollscheid, H. Jumaa, P.J. Nielsen, and M. Reth. 1998. SLP-65: a new signaling component in B lymphocytes which requires expression of the antigen receptor for phosphorylation. J. Exp. Med. 188:791-795.
51. Yamada, T., T. Kurosaki, and M. Hikida. 2008. Essential roles of mgcRac-GAP in multilineage differentiation and survival of murine hematopoietic cells. Biochem. Biophys. Res. Commun. 372:941-946.