The actin cytoskeleton coordinates the signal transduction and antigen processing functions of the B cell antigen receptor

doi:10.1007/s11515-013-1272-0

Front Biol

2013, Vol. 8

Issue (5) : 475-485 https://doi.org/10.1007/s11515-013-1272-0

REVIEW

The actin cytoskeleton coordinates the signal transduction and antigen processing functions of the B cell antigen receptor

Chaohong LIU¹, Margaret K. FALLEN¹, Heather MILLER¹, Arpita UPADHYAYA², Wenxia SONG^1,3(

)

1. Department of Cell Biology & Molecular Genetics, University of Maryland, College Park, MD 20742, USA; 2. Department of Physics, University of Maryland, College Park, MD 20742, USA; 3. Division of Immunology, Children’s Hospital of Chongqing Medical University, Chongqing 400014, China

Download: PDF(242 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

The B cell antigen receptor (BCR) is the sensor on the B cell surface that surveys foreign molecules (antigen) in our bodies and activates B cells to generate antibody responses upon encountering cognate antigen. The binding of antigen to the BCR induces signaling cascades in the cytoplasm, which provides the first signal for B cell activation. Subsequently, BCRs internalize and target bound antigen to endosomes, where antigen is processed into T cell recognizable forms. T helper cells generate the second activation signal upon binding to antigen presented by B cells. The optimal activation of B cells requires both signals, thereby depending on the coordination of BCR signaling and antigen transport functions. Antigen binding to the BCR also induces rapid remodeling of the cortical actin network of B cells. While being initiated and controlled by BCR signaling, recent studies reveal that this actin remodeling is critical for both the signaling and antigen processing functions of the BCR, indicating a role for actin in coordinating these two pathways. Here we will review previous and recent studies on actin reorganization during BCR activation and BCR-mediated antigen processing, and discuss how actin remodeling translates BCR signaling into rapid antigen uptake and processing while providing positive and negative feedback to BCR signaling.

Keywords actin cytoskeleton endocytosis signal transduction receptor

Corresponding Author(s): SONG Wenxia,Email:wenxsong@umd.edu

Issue Date: 01 October 2013

Cite this article:

Chaohong LIU,Margaret K. FALLEN,Heather MILLER, et al. The actin cytoskeleton coordinates the signal transduction and antigen processing functions of the B cell antigen receptor[J]. Front Biol, 2013, 8(5): 475-485.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-013-1272-0
https://academic.hep.com.cn/fib/EN/Y2013/V8/I5/475

Fig.1 Role of the actin cytoskeleton in coordination of BCR signaling and antigen processing functions. BCR signaling triggers actin reorganization as a series of sequential events. An initial transient detachment and disassembly of the cortical actin network is induced by dephosphorylation ezrin and cofilin (A), and a subsequent polarized actin reassembly is mediated in part by Btk activated WASP (B). The actin remodeling facilitates BCR self-clustering and signaling induction in BCR microclusters. Actin-driven B cell spreading enhances BCR microclustering and signaling (A-B). The transition of actin-mediated cell spreading to contraction promotes the coalescence of BCR microclusters and the formation of the central cluster, which leads to signaling attenuation (C). B cell contraction also likely helps to gather BCR-antigen complexes into endocytosing vesicles. The continuous actin remodeling, the actin adaptor protein Apb1 that couples F-actin with dynamin, and the actin motor non-muscle myosin II (MyoII) are required for the formation and fission of BCR containing budding vesicles from the plasma membrane (D).

Tab.1 Actin regulators that are involved in BCR signaling and endocytosis

1	Ahmed S (2011). Nanoscopy of cell architecture: The actin-membrane interface. BioArchitecture , 1(1): 32–38 doi: 10.4161/bioa.1.1.14799 pmid:21866260
2	Amann K J, Pollard T D (2001). The Arp2/3 complex nucleates actin filament branches from the sides of pre-existing filaments. Nat Cell Biol , 3(3): 306–310 doi: 10.1038/35060104 pmid:11231582
3	Baba Y, Hashimoto S, Matsushita M, Watanabe D, Kishimoto T, Kurosaki T, Tsukada S (2001). BLNK mediates Syk-dependent Btk activation. Proc Natl Acad Sci USA , 98(5): 2582–2586 doi: 10.1073/pnas.051626198 pmid:11226282
4	Bachvaroff R J, Miller F, Rapaport F T (1980). Appearance of cytoskeletal components on the surface of leukemia cells and of lymphocytes transformed by mitogens and Epstein-Barr virus. Proc Natl Acad Sci USA , 77(8): 4979–4983 doi: 10.1073/pnas.77.8.4979 pmid:6254049
5	Bassing C H, Swat W, Alt F W (2002). The mechanism and regulation of chromosomal V(D)J recombination. Cell , 109(2 Suppl): S45–S55 doi: 10.1016/S0092-8674(02)00675-X pmid:11983152
6	Bernstein B W, Bamburg J R (2010). ADF/cofilin: a functional node in cell biology. Trends Cell Biol , 20(4): 187–195 doi: 10.1016/j.tcb.2010.01.001 pmid:20133134
7	Blundell M P, Bouma G, Metelo J, Worth A, Calle Y, Cowell L A, Westerberg L S, Moulding D A, Mirando S, Kinnon C, Cory G O, Jones G E, Snapper S B, Burns S O, Thrasher A J (2009). Phosphorylation of WASp is a key regulator of activity and stability in vivo. Proc Natl Acad Sci USA , 106(37): 15738–15743 doi: 10.1073/pnas.0904346106 pmid:19805221
8	Boes M, Cuvillier A, Ploegh H (2004). Membrane specializations and endosome maturation in dendritic cells and B cells. Trends Cell Biol , 14(4): 175–183 doi: 10.1016/j.tcb.2004.02.004 pmid:15066635
9	Bolland S, Pearse R N, Kurosaki T, Ravetch J V (1998). SHIP modulates immune receptor responses by regulating membrane association of Btk. Immunity , 8(4): 509–516 doi: 10.1016/S1074-7613(00)80555-5 pmid:9586640
10	Braun J, Fujiwara K, Pollard T D, Unanue E R (1978). Two distinct mechanisms for redistribution of lymphocyte surface macromolecules. I. Relationship to cytoplasmic myosin. J Cell Biol , 79(2 Pt 1): 409–418 doi: 10.1083/jcb.79.2.409 pmid:309887
11	Braun J, Hochman P S, Unanue E R (1982). Ligand-induced association of surface immunoglobulin with the detergent-insoluble cytoskeletal matrix of the B lymphocyte. J Immunol , 128(3): 1198–1204 pmid:6976988
12	Brauweiler A M, Cambier J C (2003). Fc gamma RIIB activation leads to inhibition of signalling by independently ligated receptors. Biochem Soc Trans , 31(Pt 1): 281–285 doi: 10.1042/BST0310281 pmid:12546702
13	Brezski R J, Monroe J G (2008). B-cell receptor. Adv Exp Med Biol , 640: 12–21 doi: 10.1007/978-0-387-09789-3_2 pmid:19065780
14	Brown B K, Song W (2001). The actin cytoskeleton is required for the trafficking of the B cell antigen receptor to the late endosomes. Traffic , 2(6): 414–427 doi: 10.1034/j.1600-0854.2001.002006414.x pmid:11389769
15	Carpenter C L (2004). Btk-dependent regulation of phosphoinositide synthesis. Biochem Soc Trans , 32(Pt 2): 326–329 doi: 10.1042/BST0320326 pmid:15046600
16	Carrasco Y R, Fleire S J, Cameron T, Dustin M L, Batista F D (2004). LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity , 20(5): 589–599 doi: 10.1016/S1074-7613(04)00105-0 pmid:15142527
17	Casten L A, Kaumaya P, Pierce S K (1988). Enhanced T cell responses to antigenic peptides targeted to B cell surface Ig, Ia, or class I molecules. J Exp Med , 168(1): 171–180 doi: 10.1084/jem.168.1.171 pmid:2840479
18	Collins A, Warrington A, Taylor K A, Svitkina T (2011). Structural organization of the actin cytoskeleton at sites of clathrin-mediated endocytosis. Curr Biol , 21(14): 1167–1175 doi: 10.1016/j.cub.2011.05.048 pmid:21723126
19	Cory G O, Cramer R, Blanchoin L, Ridley A J (2003). Phosphorylation of the WASP-VCA domain increases its affinity for the Arp2/3 complex and enhances actin polymerization by WASP. Mol Cell , 11(5): 1229–1239 doi: 10.1016/S1097-2765(03)00172-2 pmid:12769847
20	Cory G O, Garg R, Cramer R, Ridley A J (2002). Phosphorylation of tyrosine 291 enhances the ability of WASp to stimulate actin polymerization and filopodium formation. Wiskott-Aldrich Syndrome protein. J Biol Chem , 277(47): 45115–45121 doi: 10.1074/jbc.M203346200 pmid:12235133
21	Dal Porto J M, Gauld S B, Merrell K T, Mills D, Pugh-Bernard A E, Cambier J (2004). B cell antigen receptor signaling 101. Mol Immunol , 41(6-7): 599–613 doi: 10.1016/j.molimm.2004.04.008 pmid:15219998
22	Depoil D, Fleire S, Treanor B L, Weber M, Harwood N E, Marchbank K L, Tybulewicz V L, Batista F D (2008). CD19 is essential for B cell activation by promoting B cell receptor-antigen microcluster formation in response to membrane-bound ligand. Nat Immunol , 9(1): 63–72 doi: 10.1038/ni1547 pmid:18059271
23	Dustin M L (2008). T-cell activation through immunological synapses and kinapses. Immunol Rev , 221(1): 77–89 doi: 10.1111/j.1600-065X.2008.00589.x pmid:18275476
24	Engels N, K?nig L M, Heemann C, Lutz J, Tsubata T, Griep S, Schrader V, Wienands J (2009). Recruitment of the cytoplasmic adaptor Grb2 to surface IgG and IgE provides antigen receptor-intrinsic costimulation to class-switched B cells. Nat Immunol , 10(9): 1018–1025 doi: 10.1038/ni.1764 pmid:19668218
25	Etienne-Manneville S (2004). Cdc42—the centre of polarity. J Cell Sci , 117(Pt 8): 1291–1300 doi: 10.1242/jcs.01115 pmid:15020669
26	Fehon R G, McClatchey A I, Bretscher A (2010). Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol , 11(4): 276–287 doi: 10.1038/nrm2866 pmid:20308985
27	Fievet B T, Gautreau A, Roy C, Del Maestro L, Mangeat P, Louvard D, Arpin M (2004). Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J Cell Biol , 164(5): 653–659 doi: 10.1083/jcb.200307032 pmid:14993232
28	Finkelstein L D, Schwartzberg P L (2004). Tec kinases: shaping T-cell activation through actin. Trends Cell Biol , 14(8): 443–451 doi: 10.1016/j.tcb.2003.07.001 pmid:15308211
29	Firat-Karalar E N, Welch M D (2011). New mechanisms and functions of actin nucleation. Curr Opin Cell Biol , 23(1): 4–13 doi: 10.1016/j.ceb.2010.10.007 pmid:21093244
30	Fleire S J, Goldman J P, Carrasco Y R, Weber M, Bray D, Batista F D (2006). B cell ligand discrimination through a spreading and contraction response. Science , 312(5774): 738–741 doi: 10.1126/science.1123940 pmid:16675699
31	Freeman S A, Lei V, Dang-Lawson M, Mizuno K, Roskelley C D, Gold M R (2011). Cofilin-mediated F-actin severing is regulated by the Rap GTPase and controls the cytoskeletal dynamics that drive lymphocyte spreading and BCR microcluster formation. J Immunol , 187(11): 5887–5900 doi: 10.4049/jimmunol.1102233 pmid:22068232
32	Fujimoto M, Poe J C, Satterthwaite A B, Wahl M I, Witte O N, Tedder T F (2002). Complementary roles for CD19 and Bruton’s tyrosine kinase in B lymphocyte signal transduction. J Immunol , 168(11): 5465–5476 pmid:12023340
33	Galletta B J, Mooren O L, Cooper J A (2010). Actin dynamics and endocytosis in yeast and mammals. Curr Opin Biotechnol , 21(5): 604–610 doi: 10.1016/j.copbio.2010.06.006 pmid:20637595
34	Gonzalez S F, Degn S E, Pitcher L A, Woodruff M, Heesters B A, Carroll M C (2011). Trafficking of B cell antigen in lymph nodes. Annu Rev Immunol , 29(1): 215–233 doi: 10.1146/annurev-immunol-031210-101255 pmid:21219172
35	Gonzalez S F, Pitcher L A, Mempel T, Schuerpf F, Carroll M C (2009). B cell acquisition of antigen in vivo. Curr Opin Immunol , 21(3): 251–257 doi: 10.1016/j.coi.2009.05.013 pmid:19515546
36	Guagliardi L E, Koppelman B, Blum J S, Marks M S, Cresswell P, Brodsky F M (1990). Co-localization of molecules involved in antigen processing and presentation in an early endocytic compartment. Nature , 343(6254): 133–139 doi: 10.1038/343133a0 pmid:2404209
37	Gupta N, Wollscheid B, Watts J D, Scheer B, Aebersold R, DeFranco A L (2006). Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat Immunol , 7(6): 625–633 doi: 10.1038/ni1337 pmid:16648854
38	Harder T, Scheiffele P, Verkade P, Simons K (1998). Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol , 141(4): 929–942 doi: 10.1083/jcb.141.4.929 pmid:9585412
39	Hartwig J H, Jugloff L S, De Groot N J, Grupp S A, Jongstra-Bilen J (1995). The ligand-induced membrane IgM association with the cytoskeletal matrix of B cells is not mediated through the Ig alpha beta heterodimer. J Immunol , 155(8): 3769–3779 pmid:7561081
40	Harwood N E, Batista F D (2009). Visualizing the molecular and cellular events underlying the initiation of B-cell activation. Curr Top Microbiol Immunol , 334: 153–177 doi: 10.1007/978-3-540-93864-4_7 pmid:19521685
41	Harwood N E, Batista F D (2010). Early events in B cell activation. Annu Rev Immunol , 28(1): 185–210 doi: 10.1146/annurev-immunol-030409-101216 pmid:20192804
42	Ilani T, Vasiliver-Shamis G, Vardhana S, Bretscher A, Dustin M L (2009). T cell antigen receptor signaling and immunological synapse stability require myosin IIA. Nat Immunol , 10(5): 531–539 doi: 10.1038/ni.1723 pmid:19349987
43	Jugloff L S, Jongstra-Bilen J (1997). Cross-linking of the IgM receptor induces rapid translocation of IgM-associated Ig alpha, Lyn, and Syk tyrosine kinases to the membrane skeleton. J Immunol , 159(3): 1096–1106 pmid:9233602
44	Kumari S, Vardhana S, Cammer M, Curado S, Santos L, Sheetz M P, Dustin M L (2012). T Lymphocyte Myosin IIA is Required for Maturation of the Immunological Synapse. Front Immunol , 3: 230 doi: 10.3389/fimmu.2012.00230 pmid:22912631
45	Kurosaki T (2011). Regulation of BCR signaling. Mol Immunol , 48(11): 1287–1291 doi: 10.1016/j.molimm.2010.12.007 pmid:21195477
46	Kusumi A, Fujiwara T K, Chadda R, Xie M, Tsunoyama T A, Kalay Z, Kasai R S, Suzuki K G (2012a). Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of Singer and Nicolson’s fluid-mosaic model. Annu Rev Cell Dev Biol , 28(1): 215–250 doi: 10.1146/annurev-cellbio-100809-151736 pmid:22905956
47	Kusumi A, Fujiwara T K, Morone N, Yoshida K J, Chadda R, Xie M, Kasai R S, Suzuki K G (2012b). Membrane mechanisms for signal transduction: the coupling of the meso-scale raft domains to membrane-skeleton-induced compartments and dynamic protein complexes. Semin Cell Dev Biol , 23(2): 126–144 doi: 10.1016/j.semcdb.2012.01.018 pmid:22309841
48	Labno C M, Lewis C M, You D, Leung D W, Takesono A, Kamberos N, Seth A, Finkelstein L D, Rosen M K, Schwartzberg P L, Burkhardt J K (2003). Itk functions to control actin polymerization at the immune synapse through localized activation of Cdc42 and WASP. Curr Biol , 13(18): 1619–1624 doi: 10.1016/j.cub.2003.08.005 pmid:13678593
49	Larbolette O, Wollscheid B, Schweikert J, Nielsen P J, Wienands J (1999). SH3P7 is a cytoskeleton adapter protein and is coupled to signal transduction from lymphocyte antigen receptors. Mol Cell Biol , 19(2): 1539–1546 pmid:9891087
50	Liu C, Miller H, Hui K L, Grooman B, Bolland S, Upadhyaya A, Song W (2011). A balance of Bruton’s tyrosine kinase and SHIP activation regulates B cell receptor cluster formation by controlling actin remodeling. J Immunol , 187(1): 230–239 doi: 10.4049/jimmunol.1100157 pmid:21622861
51	Liu C, Miller H, Orlowski G, Hang H, Upadhyaya A, Song W (2012a). Actin reorganization is required for the formation of polarized B cell receptor signalosomes in response to both soluble and membrane-associated antigens. J Immunol , 188(7): 3237–3246 doi: 10.4049/jimmunol.1103065 pmid:22387556
52	Liu C, Miller H, Sharma S, Beaven A, Upadhyaya A, Song W (2012b). Analyzing actin dynamics during the activation of the B cell receptor in live B cells. Biochem Biophys Res Commun , 427(1): 202–206 doi: 10.1016/j.bbrc.2012.09.046 pmid:22995298
53	Liu W, Meckel T, Tolar P, Sohn H W, Pierce S K (2010a). Antigen affinity discrimination is an intrinsic function of the B cell receptor. J Exp Med , 207(5): 1095–1111 doi: 10.1084/jem.20092123 pmid:20404102
54	Liu W, Meckel T, Tolar P, Sohn H W, Pierce S K (2010b). Intrinsic properties of immunoglobulin IgG1 isotype-switched B cell receptors promote microclustering and the initiation of signaling. Immunity , 32(6): 778–789 doi: 10.1016/j.immuni.2010.06.006 pmid:20620943
55	Liu W, Won Sohn H, Tolar P, Meckel T, Pierce S K (2010c). Antigen-induced oligomerization of the B cell receptor is an early target of Fc gamma RIIB inhibition. J Immunol , 184(4): 1977–1989 doi: 10.4049/jimmunol.0902334 pmid:20083655
56	Malhotra S, Kovats S, Zhang W, Coggeshall K M (2009a). B cell antigen receptor endocytosis and antigen presentation to T cells require Vav and dynamin. J Biol Chem , 284(36): 24088–24097 doi: 10.1074/jbc.M109.014209 pmid:19586920
57	Malhotra S, Kovats S, Zhang W, Coggeshall K M (2009b). Vav and Rac activation in B cell antigen receptor endocytosis involves Vav recruitment to the adapter protein LAB. J Biol Chem , 284(52): 36202–36212 doi: 10.1074/jbc.M109.040089 pmid:19858206
58	Mongini P K, Blessinger C A, Highet P F, Inman J K (1992). Membrane IgM-mediated signaling of human B cells. Effect of increased ligand binding site valency on the affinity and concentration requirements for inducing diverse stages of activation. J Immunol , 148(12): 3892–3901 pmid:1376344
59	Mooren O L, Galletta B J, Cooper J A (2012). Roles for actin assembly in endocytosis. Annu Rev Biochem , 81(1): 661–686 doi: 10.1146/annurev-biochem-060910-094416 pmid:22663081
60	Natkanski E, Lee W Y, Mistry B, Casal A, Molloy J E, Tolar P (2013). B Cells Use Mechanical Energy to Discriminate Antigen Affinities. Science , 340(6140): 1587–1590 doi: 10.1126/science.1237572 pmid:23686338
61	Neisch A L, Fehon R G (2011). Ezrin, Radixin and Moesin: key regulators of membrane-cortex interactions and signaling. Curr Opin Cell Biol , 23(4): 377–382 doi: 10.1016/j.ceb.2011.04.011 pmid:21592758
62	Niiro H, Clark E A (2002). Regulation of B-cell fate by antigen-receptor signals. Nat Rev Immunol , 2(12): 945–956 doi: 10.1038/nri955 pmid:12461567
63	O’Neill S K, Getahun A, Gauld S B, Merrell K T, Tamir I, Smith M J, Dal Porto J M, Li Q Z, Cambier J C (2011). Monophosphorylation of CD79a and CD79b ITAM motifs initiates a SHIP-1 phosphatase-mediated inhibitory signaling cascade required for B cell anergy. Immunity , 35(5): 746–756 doi: 10.1016/j.immuni.2011.10.011 pmid:22078222
64	Oltz E M (2001). Regulation of antigen receptor gene assembly in lymphocytes. Immunol Res , 23(2-3): 121–133 doi: 10.1385/IR:23:2-3:121 pmid:11444378
65	Onabajo O O, Seeley M K, Kale A, Qualmann B, Kessels M, Han J, Tan T H, Song W (2008). Actin-binding protein 1 regulates B cell receptor-mediated antigen processing and presentation in response to B cell receptor activation. J Immunol , 180(10): 6685–6695 pmid:18453588
66	Padrick S B, Rosen M K (2010). Physical mechanisms of signal integration by WASP family proteins. Annu Rev Biochem , 79(1): 707–735 doi: 10.1146/annurev.biochem.77.060407.135452 pmid:20533885
67	Park J Y, Jongstra-Bilen J (1997). Interactions between membrane IgM and the cytoskeleton involve the cytoplasmic domain of the immunoglobulin receptor. Eur J Immunol , 27(11): 3001–3009 doi: 10.1002/eji.1830271137 pmid:9394830
68	Pollard T D, Cooper J A (2009). Actin, a central player in cell shape and movement. Science , 326(5957): 1208–1212 doi: 10.1126/science.1175862 pmid:19965462
69	Puré E, Tardelli L (1992). Tyrosine phosphorylation is required for ligand-induced internalization of the antigen receptor on B lymphocytes. Proc Natl Acad Sci USA , 89(1): 114–117 doi: 10.1073/pnas.89.1.114 pmid:1370346
70	Reth M (1992). Antigen receptors on B lymphocytes. Annu Rev Immunol , 10(1): 97–121 doi: 10.1146/annurev.iy.10.040192.000525 pmid:1591006
71	Ridley A J (2011). Life at the leading edge. Cell , 145(7): 1012–1022 doi: 10.1016/j.cell.2011.06.010 pmid:21703446
72	Saito K, Tolias K F, Saci A, Koon H B, Humphries L A, Scharenberg A, Rawlings D J, Kinet J P, Carpenter C L (2003). BTK regulates PtdIns-4,5-P2 synthesis: importance for calcium signaling and PI3K activity. Immunity , 19(5): 669–678 doi: 10.1016/S1074-7613(03)00297-8 pmid:14614854
73	Schreiner G F, Fujiwara K, Pollard T D, Unanue E R (1977). Redistribution of myosin accompanying capping of surface Ig. J Exp Med , 145(5): 1393–1398 doi: 10.1084/jem.145.5.1393 pmid:323408
74	Schreiner G F, Unanue E R (1977). Capping and the lymphocyte: models for membrane reorganization. J Immunol , 119(5): 1549–1551 pmid:334966
75	Sharma S, Orlowski G, Song W (2009). Btk regulates B cell receptor-mediated antigen processing and presentation by controlling actin cytoskeleton dynamics in B cells. J Immunol , 182(1): 329–339 pmid:19109164
76	Siemasko K, Clark M R (2001). The control and facilitation of MHC class II antigen processing by the BCR. Curr Opin Immunol , 13(1): 32–36 doi: 10.1016/S0952-7915(00)00178-3 pmid:11154914
77	Simons P C, Pietromonaco S F, Reczek D, Bretscher A, Elias L (1998). C-terminal threonine phosphorylation activates ERM proteins to link the cell’s cortical lipid bilayer to the cytoskeleton. Biochem Biophys Res Commun , 253(3): 561–565 doi: 10.1006/bbrc.1998.9823 pmid:9918767
78	Sohn H W, Tolar P, Jin T, Pierce S K (2006). Fluorescence resonance energy transfer in living cells reveals dynamic membrane changes in the initiation of B cell signaling. Proc Natl Acad Sci USA , 103(21): 8143–8148 doi: 10.1073/pnas.0509858103 pmid:16690746
79	Sohn H W, Tolar P, Pierce S K (2008). Membrane heterogeneities in the formation of B cell receptor-Lyn kinase microclusters and the immune synapse. J Cell Biol , 182(2): 367–379 doi: 10.1083/jcb.200802007 pmid:18644892
80	Song W, Cho H, Cheng P, Pierce S K (1995). Entry of B cell antigen receptor and antigen into class II peptide-loading compartment is independent of receptor cross-linking. J Immunol , 155(9): 4255–4263 pmid:7594583
81	Stoddart A, Dykstra M L, Brown B K, Song W, Pierce S K, Brodsky F M (2002). Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. Immunity , 17(4): 451–462 doi: 10.1016/S1074-7613(02)00416-8 pmid:12387739
82	Stoddart A, Jackson A P, Brodsky F M (2005). Plasticity of B cell receptor internalization upon conditional depletion of clathrin. Mol Biol Cell , 16(5): 2339–2348 doi: 10.1091/mbc.E05-01-0025 pmid:15716350
83	Stradal T E, Scita G (2006). Protein complexes regulating Arp2/3-mediated actin assembly. Curr Opin Cell Biol , 18(1): 4–10 doi: 10.1016/j.ceb.2005.12.003 pmid:16343889
84	Thrasher A J, Burns S O (2010). WASP: a key immunological multitasker. Nat Rev Immunol , 10(3): 182–192 doi: 10.1038/nri2724 pmid:20182458
85	Tolar P, Hanna J, Krueger P D, Pierce S K (2009a). The constant region of the membrane immunoglobulin mediates B cell-receptor clustering and signaling in response to membrane antigens. Immunity , 30(1): 44–55 doi: 10.1016/j.immuni.2008.11.007 pmid:19135393
86	Tolar P, Sohn H W, Liu W, Pierce S K (2009b). The molecular assembly and organization of signaling active B-cell receptor oligomers. Immunol Rev , 232(1): 34–41 doi: 10.1111/j.1600-065X.2009.00833.x pmid:19909354
87	Tolar P, Sohn H W, Pierce S K (2005). The initiation of antigen-induced B cell antigen receptor signaling viewed in living cells by fluorescence resonance energy transfer. Nat Immunol , 6(11): 1168–1176 doi: 10.1038/ni1262 pmid:16200067
88	Tolar P, Sohn H W, Pierce S K (2008). Viewing the antigen-induced initiation of B-cell activation in living cells. Immunol Rev , 221(1): 64–76 doi: 10.1111/j.1600-065X.2008.00583.x pmid:18275475
89	Treanor B, Depoil D, Bruckbauer A, Batista F D (2011). Dynamic cortical actin remodeling by ERM proteins controls BCR microcluster organization and integrity. J Exp Med , 208(5): 1055–1068 doi: 10.1084/jem.20101125 pmid:21482698
90	Treanor B, Depoil D, Gonzalez-Granja A, Barral P, Weber M, Dushek O, Bruckbauer A, Batista F D (2010). The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity , 32(2): 187–199 doi: 10.1016/j.immuni.2009.12.005 pmid:20171124
91	Unanue E R, Perkins W D, Karnovsky M J (1972). Ligand-induced movement of lymphocyte membrane macromolecules. I. Analysis by immunofluorescence and ultrastructural radioautography. J Exp Med , 136(4): 885–906 doi: 10.1084/jem.136.4.885 pmid:4626851
92	Van Troys M, Huyck L, Leyman S, Dhaese S, Vandekerkhove J, Ampe C (2008). Ins and outs of ADF/cofilin activity and regulation. Eur J Cell Biol , 87(8-9): 649–667 doi: 10.1016/j.ejcb.2008.04.001 pmid:18499298
93	Vascotto F, Le Roux D, Lankar D, Faure-André G, Vargas P, Guermonprez P, Lennon-Duménil A M (2007). Antigen presentation by B lymphocytes: how receptor signaling directs membrane trafficking. Curr Opin Immunol , 19(1): 93–98 doi: 10.1016/j.coi.2006.11.011 pmid:17140785
94	Vicente-Manzanares M, Ma X, Adelstein R S, Horwitz A R (2009). Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol , 10(11): 778–790 doi: 10.1038/nrm2786 pmid:19851336
95	Weber M, Treanor B, Depoil D, Shinohara H, Harwood N E, Hikida M, Kurosaki T, Batista F D (2008). Phospholipase C-gamma2 and Vav cooperate within signaling microclusters to propagate B cell spreading in response to membrane-bound antigen. J Exp Med , 205(4): 853–868 doi: 10.1084/jem.20072619 pmid:18362175
96	Yang N, Higuchi O, Ohashi K, Nagata K, Wada A, Kangawa K, Nishida E, Mizuno K (1998). Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature , 393(6687): 809–812 doi: 10.1038/31735 pmid:9655398
97	Yokoyama N, Lougheed J, Miller W T (2005). Phosphorylation of WASP by the Cdc42-associated kinase ACK1: dual hydroxyamino acid specificity in a tyrosine kinase. J Biol Chem , 280(51): 42219–42226 doi: 10.1074/jbc.M506996200 pmid:16257963
98	Yuseff M I, Reversat A, Lankar D, Diaz J, Fanget I, Pierobon P, Randrian V, Larochette N, Vascotto F, Desdouets C, Jauffred B, Bellaiche Y, Gasman S, Darchen F, Desnos C, Lennon-Duménil A M (2011). Polarized secretion of lysosomes at the B cell synapse couples antigen extraction to processing and presentation. Immunity , 35(3): 361–374 doi: 10.1016/j.immuni.2011.07.008 pmid:21820334

[1]	Kimberly D. Girling,Yu Tian Wang. Neuroprotective strategies for NMDAR-mediated excitotoxicity in Huntington’s Disease[J]. Front. Biol., 2016, 11(6): 439-458.
[2]	Fu-Ming Zhou,Li Li,Juming Yue,John A. Dani. Transcription factor Pitx3 mutant mice as a model for Parkinson’s disease[J]. Front. Biol., 2016, 11(6): 427-438.
[3]	Rachel Babij,Natalia De Marco Garcia. Neuronal activity controls the development of interneurons in the somatosensory cortex[J]. Front. Biol., 2016, 11(6): 459-470.
[4]	Kai Jiang,Jianhang Jia. Smoothened regulation in response to Hedgehog stimulation[J]. Front. Biol., 2015, 10(6): 475-486.
[5]	Anita E. Autry,Megumi Adachi,Lisa M. Monteggia. Dynamic methylation driven by neuronal activity in hippocampal neurons impacts complex behavior[J]. Front. Biol., 2015, 10(5): 439-447.
[6]	Young-Cho Kim,Stephanie L. Alberico,Eric Emmons,Nandakumar S. Narayanan. New therapeutic strategies targeting D1-type dopamine receptors for neuropsychiatric disease[J]. Front. Biol., 2015, 10(3): 230-238.
[7]	Olga KSIONDA, Andre LIMNANDER, Jeroen P. ROOSE. RasGRP Ras guanine nucleotide exchange factors in cancer[J]. Front Biol, 2013, 8(5): 508-532.
[8]	Michael S. FLEMING, Wenqin LUO. The anatomy, function, and development of mammalian Aβ low-threshold mechanoreceptors[J]. Front Biol, 2013, 8(4): 408-420.
[9]	Yonggang ZHANG, Wenhui HU. NFκB signaling regulates embryonic and adult neurogenesis[J]. Front Biol, 2012, 7(4): 277-291.
[10]	Hao LI, Xiao-Chun XU. Lost expression of thyroid hormone receptor-β1 mRNA in esophageal cancer[J]. Front Biol, 2012, 7(4): 368-373.
[11]	Xin YANG, Fengyang DENG, Katrina M. RAMONELL. Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity[J]. Front Biol, 2012, 7(2): 155-166.
[12]	Peter E. ZAGE, Andrew J. BEAN. Growth factor receptor trafficking as a potential therapeutic target in pediatric cancer[J]. Front Biol, 2012, 7(1): 1-13.
[13]	Tong LUO, Wei-Hua WU, Bo-Shiun CHEN. NMDA receptor signaling: death or survival?[J]. Front Biol, 2011, 6(6): 468-476.
[14]	Saijun MO, Shengli YANG, Zongbin CUI. New glimpses of caveolin-1 functions in embryonic development and human diseases[J]. Front Biol, 2011, 6(5): 367-376.
[15]	Xiaosong LIU, Jian ZHAO. GPCR, a rider of Alzheimer’s disease[J]. Front Biol, 2011, 6(4): 282-288.

Viewed

Full text

Abstract

Cited

Shared

Discussed