Antigen presentation by B lymphocytes: how receptor signaling directs membrane trafficking

Current Opinion in Immunology

Volumn 19, Issue 1, 2007, Pages 93-98

  Vascotto, Fulvia ^a   Le Roux, Delphine ^a   Lankar, Danielle ^a   Faure André, Gabrielle ^a   Vargas, Pablo ^a   Guermonprez, Pierre ^a   Lennon Duménil, Ana Maria ^a  

^a INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; B LYMPHOCYTE RECEPTOR; CYTOSKELETON PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE ANTIGEN; VESICULAR TRANSPORT PROTEIN;

ANTIGEN FUNCTION; ANTIGEN PRESENTATION; B LYMPHOCYTE; CELL MEMBRANE TRANSPORT; CYTOSKELETON; MEMBRANE VESICLE; MICROTUBULE; MOLECULAR DYNAMICS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANTIGEN PRESENTATION; B-LYMPHOCYTES; BIOLOGICAL TRANSPORT, ACTIVE; CELL MEMBRANE; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION;

EID: 33846108819     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2006.11.011     Document Type: Review

References (51)

1. Niiro H., and Clark E.A. Regulation of B-cell fate by antigen-receptor signals. Nat Rev Immunol 2 (2002) 945-956
2. Mitchison N.A. T-cell-B-cell cooperation. Nat Rev Immunol 4 (2004) 308-312
3. Bryant P., and Ploegh H. Class II MHC peptide loading by the professionals. Curr Opin Immunol 16 (2004) 96-102
4. Lennon-Dumenil A.M., Bakker A.H., Wolf-Bryant P., Ploegh H.L., and Lagaudriere-Gesbert C. A closer look at proteolysis and MHC-class-II-restricted antigen presentation. Curr Opin Immunol 14 (2002) 15-21
5. Watts C. Antigen processing in the endocytic compartment. Curr Opin Immunol 13 (2001) 26-31
6. Nakagawa T.Y., and Rudensky A.Y. The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation. Immunol Rev 172 (1999) 121-129
7. Villadangos J.A., Bryant R.A., Deussing J., Driessen C., Lennon-Dumenil A.M., Riese R.J., Roth W., Saftig P., Shi G.P., Chapman H.A., et al. Proteases involved in MHC class II antigen presentation. Immunol Rev 172 (1999) 109-120
8. Cheng P.C., Steele C.R., Gu L., Song W., and Pierce S.K. MHC class II antigen processing in B cells: accelerated intracellular targeting of antigens. J Immunol 162 (1999) 7171-7180
9. Aluvihare V.R., Khamlichi A.A., Williams G.T., Adorini L., and Neuberger M.S. Acceleration of intracellular targeting of antigen by the B-cell antigen receptor: importance depends on the nature of the antigen-antibody interaction. EMBO J 16 (1997) 3553-3562
10. Siemasko K., Eisfelder B.J., Williamson E., Kabak S., and Clark M.R. Cutting edge: signals from the B lymphocyte antigen receptor regulate MHC class II containing late endosomes. J Immunol 160 (1998) 5203-5208
11. Drake J.R., Lewis T.A., Condon K.B., Mitchell R.N., and Webster P. Involvement of MIIC-like late endosomes in B cell receptor-mediated antigen processing in murine B cells. J Immunol 162 (1999) 1150-1155
12. Siemasko K., and Clark M.R. The control and facilitation of MHC class II antigen processing by the BCR. Curr Opin Immunol 13 (2001) 32-36
13. Lankar D., Vincent-Schneider H., Briken V., Yokozeki T., Raposo G., and Bonnerot C. Dynamics of major histocompatibility complex class II compartments during B cell receptor-mediated cell activation. J Exp Med 195 (2002) 461-472
14. Boes M., Cuvillier A., and Ploegh H. Membrane specializations and endosome maturation in dendritic cells and B cells. Trends Cell Biol 14 (2004) 175-183
15. Forquet F., Barois N., Machy P., Trucy J., Zimmermann V.S., Leserman L., and Davoust J. Presentation of antigens internalized through the B cell receptor requires newly synthesized MHC class II molecules. J Immunol 162 (1999) 3408-3416
16. Zimmermann V.S., Rovere P., Trucy J., Serre K., Machy P., Forquet F., Leserman L., and Davoust J. Engagement of B cell receptor regulates the invariant chain-dependent MHC class II presentation pathway. J Immunol 162 (1999) 2495-2502
17. Boes M., van der Wel N., Peperzak V., Kim Y.M., Peters P.J., and Ploegh H. In vivo control of endosomal architecture by class II-associated invariant chain and cathepsin S. Eur J Immunol 35 (2005) 2552-2562
18. Yokozeki T., Adler K., Lankar D., and Bonnerot C. B cell receptor-mediated Syk-independent activation of phosphatidylinositol 3-kinase, Ras, and mitogen-activated protein kinase pathways. J Immunol 171 (2003) 1328-1335
19. Mitchell R.N., Barnes K.A., Grupp S.A., Sanchez M., Misulovin Z., Nussenzweig M.C., and Abbas A.K. Intracellular targeting of antigens internalized by membrane immunoglobulin in B lymphocytes. J Exp Med 181 (1995) 1705-1714
20. Parent B.A., Wang X., and Song W. Stability of the B cell antigen receptor modulates its signaling and antigen-targeting functions. Eur J Immunol 32 (2002) 1839-1846
21. Bonnerot C., Lankar D., Hanau D., Spehner D., Davoust J., Salamero J., and Fridman W.H. Role of B cell receptor Igα and Igβ subunits in MHC class II-restricted antigen presentation. Immunity 3 (1995) 335-347
22. Li C., Siemasko K., Clark M.R., and Song W. Cooperative interaction of Igα and Igβ of the BCR regulates the kinetics and specificity of antigen targeting. Int Immunol 14 (2002) 1179-1191
23. Hou P., Araujo E., Zhao T., Zhang M., Massenburg D., Veselits M., Doyle C., Dinner A.R., and Clark M.R. B cell antigen receptor signaling and internalization are mutually exclusive events. PLoS Biol 4 (2006) e200. This work shows that BCR tyrosine phosphorylation and internalization induced upon cross-linking are two mutually exclusive events. This results from the fact that the same tyrosine motifs are required for both processes. Only a minor fraction of the BCR is phosphorylated upon stimulation, and this fraction is selectively retained on the cell surface where it plays a role as a signaling receptor complex. These results are supported by a mathematical exclusive model, which provides an explanation for the role of surface-phosphorylated BCR in enhancing signaling induced by low-avidity ligands.
24. Lankar D., Briken V., Adler K., Weiser P., Cassard S., Blank U., Viguier M., and Bonnerot C. Syk tyrosine kinase and B cell antigen receptor (BCR) immunoglobulin-alpha subunit determine BCR-mediated major histocompatibility complex class II-restricted antigen presentation. J Exp Med 188 (1998) 819-831
25. Granboulan M., Lankar D., Raposo G., Bonnerot C., and Hivroz C. Phosphoinositide 3-kinase activation by Igβ controls de novo formation of an antigen-processing compartment. J Biol Chem 278 (2003) 4331-4338
26. Raiborg C., Rusten T.E., and Stenmark H. Protein sorting into multivesicular endosomes. Curr Opin Cell Biol 15 (2003) 446-455
27. Rao N., Ghosh A.K., Ota S., Zhou P., Reddi A.L., Hakezi K., Druker B.K., Wu J., and Band H. The non-receptor tyrosine kinase Syk is a target of Cbl-mediated ubiquitylation upon B-cell receptor stimulation. EMBO J 20 (2001) 7085-7095
28. Sohn H.W., Gu H., and Pierce S.K. Cbl-b negatively regulates B cell antigen receptor signaling in mature B cells through ubiquitination of the tyrosine kinase Syk. J Exp Med 197 (2003) 1511-1524
29. Shao Y., Yang C., Elly C., and Liu Y.C. Differential regulation of the B cell receptor-mediated signaling by the E3 ubiquitin ligase Cbl. J Biol Chem 279 (2004) 43646-43653
30. Guermonprez P., England P., Bedouelle H., and Leclerc C. The rate of dissociation between antibody and antigen determines the efficiency of antibody-mediated antigen presentation to T cells. J Immunol 161 (1998) 4542-4548
31. Batista F.D., and Neuberger M.S. Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity 8 (1998) 751-759. This study demonstrates that the affinity of the BCR for its intended Ag determines the strength of signaling and Ag presentation. By analysing a broad range of different lysozyme mutants for specific BCRs, the authors establish a threshold, a ceiling and an off-rate for B-cell responses. They further show that the affinity threshold is bypassed when the Ag is oligomerized.
32. Antoniou A.N., and Watts C. Antibody modulation of antigen presentation: positive and negative effects on presentation of the tetanus toxin antigen via the murine B cell isoform of FcγRII. Eur J Immunol 32 (2002) 530-540
33. Kim Y.M., Pan J.Y., Korbel G.A., Peperzak V., Boes M., and Ploegh H.L. Monovalent ligation of the B cell receptor induces receptor activation but fails to promote antigen presentation. Proc Natl Acad Sci USA 103 (2006) 3327-3332. This study compares the ability of BCR-internalized monomers and oligomers of HEL to signal and travel in primary B lymphocytes. They demonstrate that the strength of HEL-induced signaling is less dependent on its oligomerization state than HEL trafficking and presentation, which occurs only when using polyvalent HEL.
34. Cheng P.C., Dykstra M.L., Mitchell R.N., and Pierce S.K. A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. J Exp Med 190 (1999) 1549-1560
35. Cheng P.C., Brown B.K., Song W., and Pierce S.K. Translocation of the B cell antigen receptor into lipid rafts reveals a novel step in signaling. J Immunol 166 (2001) 3693-3701
36. Stoddart A., Dykstra M.L., Brown B.K., Song W., Pierce S.K., and Brodsky F.M. Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. Immunity 17 (2002) 451-462
37. Poloso N.J., Muntasell A., and Roche P.A. MHC class II molecules traffic into lipid rafts during intracellular transport. J Immunol 173 (2004) 4539-4546
38. Gupta N., Wollscheid B., Watts J.D., Scheer B., Aebersold R., and DeFranco A.L. Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat Immunol 7 (2006) 625-633. The authors identify the adaptor protein Ezrin in a comparative proteomic analysis of lipid rafts from resting versus BCR-activated cells. They demonstrate that Ezrin inactivation permits BCR-induced coalescence of lipid rafts by transiently disconnecting the plasma membrane from the actin cortex. This finding suggests that cytoskeleton reorganization controls lipid raft dynamics during BCR signalling.
39. Hao S., and August A. Actin depolymerization transduces the strength of B-cell receptor stimulation. Mol Biol Cell 16 (2005) 2275-2284. This study describes that, upon BCR engagement, the actin network partially depolymerises in a signaling strength-dependent manner. This early event of actin reorganization allows the lipid raft coalescence at the plasma membrane, leading to enhanced BCR signaling. It is followed by a second step of polarized re-polymerization of the actin cytoskeleton.
40. Barois N., Forquet F., and Davoust J. Actin microfilaments control the MHC class II antigen presentation pathway in B cells. J Cell Sci 111 (1998) 1791-1800
41. Brown B.K., and Song W. The actin cytoskeleton is required for the trafficking of the B cell antigen receptor to the late endosomes. Traffic 2 (2001) 414-427
42. Gondre-Lewis T.A., Moquin A.E., and Drake J.R. Prolonged antigen persistence within nonterminal late endocytic compartments of antigen-specific B lymphocytes. J Immunol 166 (2001) 6657-6664
43. Carrasco Y.R., and Batista F.D. B cell recognition of membrane-bound antigen: an exquisite way of sensing ligands. Curr Opin Immunol 18 (2006) 286-291
44. Qi H., Egen J.G., Huang A.Y., and Germain R.N. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 312 (2006) 1672-1676. This article describes the visualization by two-photon microscopy of lymph node B cells that exit from high-endothelial venules to interact with Ag-loaded DCs. This finding suggests a possible role for Ag-specific interactions between B cells and DCs in promoting T cell-dependent B lymphocyte responses.
45. Carrasco Y.R., Fleire S.J., Cameron T., Dustin M.L., and Batista F.D. LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity 20 (2004) 589-599
46. Carrasco Y.R., and Batista F.D. B-cell activation by membrane-bound antigens is facilitated by the interaction of VLA-4 with VCAM-1. EMBO J 25 (2006) 889-899
47. Fleire S.J., Goldman J.P., Carrasco Y.R., Weber M., Bray D., and Batista F.D. B cell ligand discrimination through a spreading and contraction response. Science 312 (2006) 738-741. This group has previously shown that B cells can capture membrane-bound Ag through formation of an immunological synapse [51]. In this study, they show that this event is associated with a membrane spreading and contraction two-phase response. Spreading and contraction rely on BCR signaling and on the actin cytoskeleton, and allow concentration of the Ag at the membrane for efficient extraction. A mathematical model is presented to demonstrate that this process is important for extraction of membrane-bound Ag that have low affinity for the BCR.
48. Peters J.D., Furlong M.T., Asai D.J., Harrison M.L., and Geahlen R.L. Syk, activated by cross-linking the B-cell antigen receptor, localizes to the cytosol where it interacts with and phosphorylates alpha-tubulin on tyrosine. J Biol Chem 271 (1996) 4755-4762
49. Wubbolts R., Fernandez-Borja M., Jordens I., Reits E., Dusseljee S., Echeverri C., Vallee R.B., and Neefjes J. Opposing motor activities of dynein and kinesin determine retention and transport of MHC class II-containing compartments. J Cell Sci 112 (1999) 785-795
50. Nashar T.O., and Drake J.R. The pathway of antigen uptake and processing dictates MHC class II-mediated B cell survival and activation. J Immunol 174 (2005) 1306-1316. The authors compare the effect of engaging MHC class II-peptide complexes generated by BCR-mediated Ag uptake (type I complex) with those generated by fluid phase endocytosis (type II complex) on B-cell responses, as measured by their survival rate and expression of activation markers. They show that type I complexes lead to increased B-cell activation and survival, suggesting that appropriate Ag targeting is key to induce the relevant immune response.
51. Batista F.D., Iber D., and Neuberger M.S. B cells acquire antigen from target cells after synapse formation. Nature 411 (2001) 489-494