CoChat
Sign Up
Cited by 70T-cell and B-cell ImmunologyCellular Mechanics and InteractionsNF-κB Signaling Pathways

The Coordination Between B Cell Receptor Signaling and the Actin Cytoskeleton During B Cell Activation

Open access
Li, Jingwen, Yin, Wei, Jing, Yukai, Kang, Danqing, Yang, Lu, Cheng, Jiali, Yu, Ze, Peng, Zican +5 more·2019·Frontiers in Immunology
DOI 10.3389/fimmu.2018.03096PMC PMC6333714
Open this paper in CoChat — free accountOpen PDF

Abstract

B-cell activation plays a crucial part in the immune system and is initiated via interaction between the B cell receptor (BCR) and specific antigens. In recent years with the help of modern imaging techniques, it was found that the cortical actin cytoskeleton changes dramatically during B-cell activation. In this review, we discuss how actin-cytoskeleton reorganization regulates BCR signaling in different stages of B-cell activation, specifically when stimulated by antigens, and also how this reorganization is mediated by BCR signaling molecules. Abnormal BCR signaling is associated with the progression of lymphoma and immunological diseases including autoimmune disorders, and recent studies have proved that impaired actin cytoskeleton can devastate the normal activation of B cells. Therefore, to figure out the coordination between the actin cytoskeleton and BCR signaling may reveal an underlying mechanism of B-cell activation, which has potential for new treatments for B-cell associated diseases.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fimmu.2018.03096

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • During B cell development and BCR editing, defective actin polymerization at immune synapses results in weaker signals, allowing for survival of autoreactive B cells with inherently stronger signals.

    “During B cell development and BCR editing, defective actin polymerization at immune synapses results in weaker signals, allowing for survival of autoreactive B cells with inherently stronger signals [9, 39, 40].”

    From HEM1 Actin Immunodysregulatory Disorder: Genotypes, Phenotypes, and Future Directions (2022) · cites this paper as [40]

    The sections on immune-synapse formation and B-cell morphology say actin-dependent spreading promotes BCR microclusters and amplifies signaling. But the paper does not link defective actin polymerization to survival of autoreactive B cells during development or receptor editing; its section on actin polymerization also reports increased BCR signaling in WASP-deficient B cells. No page numbers are available in our copy. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 129

  1. [1]Rajewsky K. Clonal selection and learning in the antibody system. Nature (1996) 381: 751– 8. 10.1038/381751a0 8657279 · DOI
  2. [2]Mitchison NA. T-cell-B-cell cooperation. Nat Rev Immunol. (2004) 4: 308– 12. 10.1038/nri1334 15057789 · DOI
  3. [3]Barr TA Gray M Gray D. B cells: programmers of CD4 T cell responses. Infect Disord Drug Targets (2012) 12: 222– 31. 10.2174/187152612800564446 22394172 · DOI
  4. [4]Venkitaraman AR Williams GT Dariavach P Neuberger MS. The B-cell antigen receptor of the five immunoglobulin classes. Nature (1991) 352: 777– 81. 10.1038/352777a0 1881434 · DOI
  5. [5]Reth M. Antigen receptor tail clue. Nature (1989) 338: 383– 4. 10.1038/338383b0 24748635 · DOI
  6. [6]Hombach J Lottspeich F Reth M. Identification of the genes encoding the IgM-alpha and Ig-beta components of the IgM antigen receptor complex by amino-terminal sequencing. Eur J Immunol. (1990) 20: 2795– 9. 10.1002/eji.1830201239 2269334 · DOI
  7. [7]Weiss A Littman DR. Signal transduction by lymphocyte antigen receptors. Cell (1994) 76: 263– 74. 10.1016/0092-8674(94)90334-4 8293463 · DOI
  8. [8]Cambier JC. New nomenclature for the Reth motif (or ARH1/TAM/ARAM/YXXL). Immunol Today (1995) 16: 110. 10.1016/0167-5699(95)80105-7 7888063 · DOI
  9. [9]Tolar P Hanna J Krueger PD Pierce SK. The constant region of the membrane immunoglobulin mediates B cell-receptor clustering and signaling in response to membrane antigens. Immunity (2009) 30: 44– 55. 10.1016/j.immuni.2008.11.007 19135393 PMC2656684 · DOI
  10. [10]Carrasco YR Batista FD. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity (2007) 27: 160– 71. 10.1016/j.immuni.2007.06.007 17658276 · DOI
  11. [11]Gonzalez SF Pitcher LA Mempel T Schuerpf F Carroll MC. B cell acquisition of antigen in vivo. Curr Opin Immunol. (2009) 21: 251– 7. 10.1016/j.coi.2009.05.013 19515546 PMC2717615 · DOI
  12. [12]Avalos AM Bilate AM Witte MD Tai AK He J Frushicheva MP. Monovalent engagement of the BCR activates ovalbumin-specific transnuclear B cells. J Exp Med. (2014) 211: 365– 79. 10.1084/jem.20131603 24493799 PMC3920557 · DOI
  13. [13]Volkmann C Brings N Becker M Hobeika E Yang J. Molecular requirements of the B-cell antigen receptor for sensing monovalent antigens. EMBO J. (2016) 35: 2371– 81. 10.15252/embj.201694177 27634959 PMC5090217 · DOI
  14. [15]Hong JJ Yankee TM Harrison ML Geahlen RL. Regulation of signaling in B cells through the phosphorylation of Syk on linker region tyrosines. A mechanism for negative signaling by the Lyn tyrosine kinase. J Biol Chem. (2002) 277: 31703– 14. 10.1074/jbc.M201362200 12077122 · DOI
  15. [16]Kurosaki T Hikida M. Tyrosine kinases and their substrates in B lymphocytes. Immunol Rev. (2009) 228: 132– 48. 10.1111/j.1600-065X.2008.00748.x 19290925 · DOI
  16. [17]Cheng AM Rowley B Pao W Hayday A Bolen JB Pawson T. Syk tyrosine kinase required for mouse viability and B-cell development. Nature (1995) 378: 303. 10.1038/378303a0 7477353 · DOI
  17. [18]Sohn HW Tolar P Pierce SK. Membrane heterogeneities in the formation of B cell receptor-Lyn kinase microclusters and the immune synapse. J Cell Biol. (2008) 182: 367– 79. 10.1083/jcb.200802007 18644892 PMC2483512 · DOI
  18. [21]Kurosaki T Shinohara H Baba Y. B cell signaling and fate decision. Ann Rev Immunol. (2010) 28: 21– 55. 10.1146/annurev.immunol.021908.132541 19827951 · DOI
  19. [22]Bos JL. Linking rap to cell adhesion. Curr Opin Cell Biol. (2005) 17: 123– 8. 10.1016/j.ceb.2005.02.009 15780587 · DOI
  20. [23]Stewart DM Tian L Nelson DL. Mutations that cause the Wiskott-Aldrich syndrome impair the interaction of Wiskott-Aldrich syndrome protein (WASP) with WASP interacting protein. J Immunol. (1999) 162: 5019– 24. 10202051
  21. [24]Lanzi G Moratto D Vairo D Masneri S Delmonte O Paganini T. A novel primary human immunodeficiency due to deficiency in the WASP-interacting protein WIP. J Exp Med. (2012) 209: 29– 34. 10.1084/jem.20110896 22231303 PMC3260865 · DOI
  22. [25]Thrasher AJ New insights into the biology of Wiskott-Aldrich syndrome (WAS). Hematology. Am Soc Hematol Educ Program (2009) 2009: 132– 8. 10.1182/asheducation-2009.1.132 20008191 · DOI
  23. [26]Pfajfer L Seidel MG Houmadi R Rey-Barroso J Hirschmugl T Salzer E. WIP deficiency severely affects human lymphocyte architecture during migration and synapse assembly. Blood (2017) 130: 1949– 53. 10.1182/blood-2017-04-777383 28903942 · DOI
  24. [27]Pore D Bodo J Danda A Yan D Phillips JG Lindner D. Identification of Ezrin-Radixin-Moesin proteins as novel regulators of pathogenic B-cell receptor signaling and tumor growth in diffuse large B-cell lymphoma. Leukemia (2015) 29: 1857– 67. 10.1038/leu.2015.86 25801911 PMC4558318 · DOI
  25. [28]Chugh P Paluch EK. The actin cortex at a glance. J Cell Sci. (2018) 131: jcs186254. 10.1242/jcs.186254 30026344 PMC6080608 · DOI
  26. [29]Ponuwei GA A glimpse of the ERM proteins. J Biomed Sci. (2016) 23: 35. 10.1186/s12929-016-0246-3 26983550 PMC4794931 · DOI
  27. [30]Chugh P Clark AG Smith MB Cassani AD Dierkes K Ragab A. Actin cortex architecture regulates cell surface tension. Nat Cell Biol. (2017) 19: 689– 97. 10.1038/ncb3525 28530659 PMC5536221 · DOI
  28. [31]Logue JS Cartagena-Rivera AX Baird MA Davidson MW Chadwick RS Waterman CM. Erk regulation of actin capping and bundling by Eps8 promotes cortex tension and leader bleb-based migration. Elife (2015) 4:e08314. 10.7554/eLife.08314 26163656 PMC4522647 · DOI
  29. [32]Biro M Romeo Y Kroschwald S Bovellan M Boden A Tcherkezian J. Cell cortex composition and homeostasis resolved by integrating proteomics and quantitative imaging. Cytoskeleton (2013) 70: 741– 54. 10.1002/cm.21142 24136886 · DOI
  30. [33]Lu Y Zhang Y Pan MH Kim NH Sun SC Cui XS. Daam1 regulates fascin for actin assembly in mouse oocyte meiosis. Cell Cycle (2017) 16: 1350– 6. 10.1080/15384101.2017.1325045 28682694 PMC5539815 · DOI
  31. [34]Bovellan M Romeo Y Biro M Boden A Chugh P Yonis A. Cellular control of cortical actin nucleation. Curr Biol. (2014) 24: 1628– 35. 10.1016/j.cub.2014.05.069 25017211 PMC4110400 · DOI
  32. [35]Fritzsche M Erlenkamper C. Actin kinetics shapes cortical network structure and mechanics. (2016) 2:e1501337. 10.1126/sciadv.1501337 27152338 PMC4846455 · DOI
  33. [36]Ichetovkin I Grant W Condeelis J. Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr Biol. (2002) 12: 79– 84. 10.1016/S0960-9822(01)00629-7 11790308 · DOI
  34. [37]Diz-Munoz A Romanczuk P Yu W Bergert M Ivanovitch K Salbreux G. Steering cell migration by alternating blebs and actin-rich protrusions. BMC Biol. (2016) 14: 74. 10.1186/s12915-016-0294-x 27589901 PMC5010735 · DOI
  35. [38]Paluch EK Raz E. The role and regulation of blebs in cell migration. Curr Opin Cell Biol. (2013) 25: 582– 90. 10.1016/j.ceb.2013.05.005 23786923 PMC3989058 · DOI
  36. [39]Welch MD DePace AH Verma S Iwamatsu A Mitchison TJ. The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J Cell Biol. (1997) 138: 375– 84. 10.1083/jcb.138.2.375 9230079 PMC2138188 · DOI
  37. [40]Peng J Wallar BJ Flanders A Swiatek PJ Alberts AS. Disruption of the diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr Biol. (2003) 13: 534– 45. 10.1016/S0960-9822(03)00170-2 12676083 · DOI
  38. [41]Liu C Miller H Orlowski G Hang H Upadhyaya A Song W. Actin reorganization is required for the formation of polarized B cell receptor signalosomes in response to both soluble and membrane-associated antigens. J Immunol. (2012) 188: 3237– 46. 10.4049/jimmunol.1103065 22387556 PMC3312033 · DOI
  39. [42]Arpin M Chirivino D Naba A Zwaenepoel I. Emerging role for ERM proteins in cell adhesion and migration. Cell Adhesion Migration (2011) 5: 199– 206. 10.4161/cam.5.2.15081 21343695 PMC3084986 · DOI
  40. [43]Arana E Vehlow A Harwood NE Vigorito E Henderson R Turner M. Activation of the small GTPase Rac2 via the B cell receptor regulates B cell adhesion and immunological-synapse formation. Immunity (2008) 28: 88– 99. 10.1016/j.immuni.2007.12.003 18191593 · DOI · Paper page
  41. [44]Ricker E Chowdhury L Yi W Pernis AB. The RhoA-ROCK pathway in the regulation of T and B cell responses. F1000Res. (2016) 5:F1000. 10.12688/f1000research.7522.1 27785353 PMC5022701 · DOI
  42. [45]Kechkar A Nair D Heilemann M Choquet D Sibarita JB. Real-time analysis and visualization for single-molecule based super-resolution microscopy. PLoS ONE (2013) 8:e62918. 10.1371/journal.pone.0062918 23646160 PMC3639901 · DOI
  43. [46]Gasparrini F Feest C Bruckbauer A Mattila PK Müller J Nitschke L. Nanoscale organization and dynamics of the siglec CD22 cooperate with the cytoskeleton in restraining BCR signalling. EMBO J. (2016) 35: 258– 80. 10.15252/embj.201593027 26671981 PMC4741297 · DOI
  44. [47]Mattila PK Feest C Depoil D Treanor B Montaner B Otipoby KL. The actin and tetraspanin networks organize receptor nanoclusters to regulate B cell receptor-mediated signaling. Immunity (2013) 38: 461– 74. 10.1016/j.immuni.2012.11.019 23499492 · DOI
  45. [48]Davey A Liu W Sohn HW Brzostowski J Pierce SK. Understanding the initiation of B cell signaling through live cell imaging. Method Enzymol. (2012) 506: 265– 90. 10.1016/B978-0-12-391856-7.00038-X 22341229 PMC3761359 · DOI
  46. [49]Liu W Meckel T Tolar P Sohn HW Pierce SK. Antigen affinity discrimination is an intrinsic function of the B cell receptor. J Exp Med. (2010) 207: 1095– 111. 10.1084/jem.20092123 20404102 PMC2867278 · DOI
  47. [50]Wasim L Treanor B. Single-particle tracking of cell surface proteins. Method Molecul Biol. (2018) 1707: 183– 92. 10.1007/978-1-4939-7474-0_13 29388108 · DOI
  48. [51]Treanor B Depoil D Gonzalez-Granja A Barral P Weber M Dushek O. The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity (2010) 32: 187– 199. 10.1016/j.immuni.2009.12.005 20171124 PMC2984614 · DOI
  49. [52]Suzuki K Ritchie K Kajikawa E Fujiwara T Kusumi A Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. Biophys J. (2005) 88: 3659– 80. 10.1529/biophysj.104.048538 15681644 PMC1305513 · DOI
  50. [53]Treanor B Depoil D Bruckbauer A Batista FD. Dynamic cortical actin remodeling by ERM proteins controls BCR microcluster organization and integrity. J Exp Me. (2011) 208: 1055– 68. 10.1084/jem.20101125 21482698 PMC3092358 · DOI
  51. [54]Lee J Sengupta P Brzostowski J Lippincott-Schwartz J Pierce SK. The nanoscale spatial organization of B-cell receptors on immunoglobulin M- and G-expressing human B-cells. Molecul Biol Cell (2017) 28: 511– 23. 10.1091/mbc.e16-06-0452 27974642 PMC5305258 · DOI
  52. [55]Maity PC Blount A Jumaa H Ronneberger O Lillemeier BF Reth M. B cell antigen receptors of the IgM and IgD classes are clustered in different protein islands that are altered during B cell activation. Science Signal. (2015) 8:ra93. 10.1126/scisignal.2005887 26373673 · DOI
  53. [56]Kläsener K Maity PC Hobeika E Yang J Reth M. B cell activation involves nanoscale receptor reorganizations and inside-out signaling by Syk. eLife (2014) 3:e02069. 10.7554/eLife.02069 24963139 PMC4067077 · DOI
  54. [57]Yasuda S Zhou Y Wang Y Yamamura M Wang Y. A model integrating tonic and antigen-triggered BCR signals to predict the survival of primary B cells. Sci Rep. (2017) 7: 14888. 10.1038/s41598-017-13993-x 29097663 PMC5668375 · DOI
  55. [58]Freeman SA Lei V Dang-Lawson M Mizuno K Roskelley CD Gold MR. 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. (2011) 187: 5887– 900. 10.4049/jimmunol.1102233 22068232 · DOI
  56. [59]Fleire SJ Goldman JP Carrasco YR Weber M Bray D Batista FD. B cell ligand discrimination through a spreading and contraction response. Science (2006) 312: 738– 41. 10.1126/science.1123940 16675699 · DOI
  57. [60]Liu C Miller H Hui KL Grooman B Bolland S Upadhyaya A Song W. A balance of Bruton's tyrosine kinase and SHIP activation regulates B cell receptor cluster formation by controlling actin remodeling. J Immunol. (2011) 187: 230– 9. 10.4049/jimmunol.1100157 21622861 PMC3119787 · DOI
  58. [61]Roman-Garcia S Merino-Cortes SV Gardeta SR de Bruijn JW Hendriks RW Carrasco YR. Distinct roles for bruton's tyrosine kinase in b cell immune synapse formation. Front Immunol. (2018) 9: 2027. 10.3389/fimmu.2018.02027 30237801 PMC6136277 · DOI
  59. [62]Carrasco YR Fleire SJ Cameron T Dustin ML Batista FD. LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity (2004) 20: 589– 99. 10.1016/S1074-7613(04)00105-0 15142527 · DOI
  60. [63]Dustin ML Chakraborty AK Shaw AS. Understanding the structure and function of the immunological synapse. Cold Spring Harbor Perspect Biol. (2010) 2: a002311. 10.1101/cshperspect.a002311 20843980 PMC2944359 · DOI
  61. [64]Song W Liu C Upadhyaya A. The pivotal position of the actin cytoskeleton in the initiation and regulation of B cell receptor activation. Biochim Biophys Acta (2014) 1838: 569– 78. 10.1016/j.bbamem.2013.07.016 23886914 PMC3877175 · DOI
  62. [65]Yang J Reth M. The dissociation activation model of B cell antigen receptor triggering. FEBS Lett. (2010) 584: 4872– 7. 10.1016/j.febslet.2010.09.045 20920502 · DOI
  63. [66]Yang J Reth M. Receptor dissociation and B-cell activation. Curr Top Microbiol Immunol. (2016) 393: 27– 43. 10.1007/82_2015_482 26428245 · DOI
  64. [67]Depoil D Fleire S Treanor BL Weber M Harwood NE Marchbank KL. CD19 is essential for B cell activation by promoting B cell receptor-antigen microcluster formation in response to membrane-bound ligand. Nat Immunol. (2008) 9: 63– 72. 10.1038/ni1547 18059271 · DOI
  65. [68]Tolar P Sohn HW Pierce SK. The initiation of antigen-induced B cell antigen receptor signaling viewed in living cells by fluorescence resonance energy transfer. Nat Immunol. (2005) 6: 1168– 76. 10.1038/ni1262 16200067 · DOI
  66. [69]Ketchum C Miller H Song W Upadhyaya A. Ligand mobility regulates B cell receptor clustering and signaling activation. Biophys J. (2014) 106: 26– 36. 10.1016/j.bpj.2013.10.043 24411234 PMC3907214 · DOI
  67. [70]Rostam HM Singh S Vrana NE Alexander MR Ghaemmaghami AM. Impact of surface chemistry and topography on the function of antigen presenting cells. Biomater Sci. (2015) 3: 424– 41. 10.1039/C4BM00375F 26222286 · DOI
  68. [71]Ketchum CM Sun X Suberi A Fourkas JT Song W Upadhyaya A. Subcellular topography modulates actin dynamics and signaling in B-cells. Molecul Biol Cell (2018) 29: 1732– 42. 10.1091/mbc.E17-06-0422 29771636 PMC6080708 · DOI
  69. [72]Hao S August A. Actin depolymerization transduces the strength of B-cell receptor stimulation. Molecul Biol Cell (2005) 16: 2275– 84. 10.1091/mbc.e04-10-0881 15728723 PMC1087234 · DOI
  70. [73]Gupta N Wollscheid B Watts JD Scheer B Aebersold R DeFranco AL. Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nature Immunol. (2006) 7: 625– 33. 10.1038/ni1337 16648854 · DOI
  71. [74]Huang L Zhang Y Xu C Gu X Niu L Wang J. Rictor positively regulates B cell receptor signaling by modulating actin reorganization via ezrin. PLoS Biol. (2017) 15:e2001750. 10.1371/journal.pbio.2001750 28821013 PMC5562439 · DOI
  72. [75]Freeman SA Jaumouillé V Choi K Hsu BE Wong HS Abraham L Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor. Nat Commun. (2015) 6: 6168 10.1038/ncomms7168 25644899 PMC4327415 · DOI
  73. [76]Chaudhuri A Bhattacharya B Gowrishankar K Mayor S Rao M. Spatiotemporal regulation of chemical reactions by active cytoskeletal remodeling. Proc Natl Acad Sci USA (2011) 108: 14825– 30. 10.1073/pnas.1100007108 21873247 PMC3169122 · DOI
  74. [77]Koster DV Husain K Iljazi E Bhat A Bieling P Mullins RD. Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer. Proc Natl Acad Sci USA (2016) 113: E1645– 54. 10.1073/pnas.1514030113 26929326 PMC4812753 · DOI
  75. [78]Tolar P. Cytoskeletal control of B cell responses to antigens. Nat Rev Immunol. (2017) 17: 621– 34. 10.1038/nri.2017.67 28690317 · DOI
  76. [79]Haviv L Brill-Karniely Y Mahaffy R Backouche F Ben-Shaul A Pollard TD. Reconstitution of the transition from lamellipodium to filopodium in a membrane-free system. Proc Natl Acad Sci USA (2006) 103: 4906– 11. 10.1073/pnas.0508269103 16549794 PMC1458768 · DOI
  77. [80]Mattila PK Batista FD Treanor B. Dynamics of the actin cytoskeleton mediates receptor cross talk: an emerging concept in tuning receptor signaling. J Cell Biol. (2016) 212: 267– 80. 10.1083/jcb.201504137 26833785 PMC4748574 · DOI
  78. [81]Keppler SJ Burbage M Gasparrini F Hartjes L Aggarwal S Massaad MJ. The Lack of WIP binding to actin results in impaired B cell migration and altered humoral immune responses. Cell Rep. (2018) 24: 619– 29. 10.1016/j.celrep.2018.06.051 30021160 PMC6077251 · DOI
  79. [83]Schnyder T Castello A Feest C Harwood NE Oellerich T Urlaub H. B cell receptor-mediated antigen gathering requires ubiquitin ligase Cbl and adaptors Grb2 and Dok-3 to recruit dynein to the signaling microcluster. Immunity (2011) 34: 905– 18. 10.1016/j.immuni.2011.06.001 21703542 · DOI
  80. [84]Wang JC Bolger-Munro M Gold MR. Visualizing the actin and microtubule cytoskeletons at the B-cell immune synapse using stimulated emission depletion (STED) microscopy. J Visual Exp. (2018) 134. 10.3791/57028 29683438 PMC5933440 · DOI
  81. [85]Wang JC Lee JY Christian S Dang-Lawson M Pritchard C Freeman SA Gold MR The Rap1-cofilin-1 pathway coordinates actin reorganization and MTOC polarization at the B cell immune synapse. (2017) 130: 1094– 1109. 28167682
  82. [86]Schulte RJ Campbell MA Fischer WH Sefton BM. Tyrosine phosphorylation of CD22 during B cell activation. Science (1992) 258: 1001– 4. 10.1126/science.1279802 1279802 · DOI
  83. [87]Leprince C Draves KE Geahlen RL Ledbetter JA Clark EA. CD22 associates with the human surface IgM-B-cell antigen receptor complex. Proc Natl Acad Sci USA (1993) 90: 3236– 40. 10.1073/pnas.90.8.3236 8475064 PMC46274 · DOI
  84. [88]She HY Rockow S Tang J Nishimura R Skolnik EY Chen M. Wiskott-Aldrich syndrome protein is associated with the adapter protein Grb2 and the epidermal growth factor receptor in living cells. Molecul Biol Cell (1997) 8: 1709– 21. 10.1091/mbc.8.9.1709 9307968 PMC305731 · DOI
  85. [89]Le Bras S Foucault I Foussat A Brignone C Acuto O Deckert M Recruitment of the actin-binding protein HIP-55 to the immunological synapse regulates T cell receptor signaling and endocytosis. J Biol Chem. (2004) 279: 15550– 60. 10.1074/jbc.M312659200 14729663 · DOI
  86. [90]McNulty S Powell K Erneux C Kalman D. The host phosphoinositide 5-phosphatase SHIP2 regulates dissemination of vaccinia virus. J Virol. (2011) 85: 7402– 10. 10.1128/JVI.02391-10 21543482 PMC3126556 · DOI
  87. [91]Pore D Gupta N. The ezrin-radixin-moesin family of proteins in the regulation of B-cell immune response. Crit Rev Immunol. (2015) 35: 15– 31. 10.1615/CritRevImmunol.2015012327 25746045 PMC4548853 · DOI
  88. [92]Turunen O Wahlström T Vaheri A Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J Cell Biol. (1994) 126: 1445. 10.1083/jcb.126.6.1445 8089177 PMC2290954 · DOI
  89. [93]Fehon RG McClatchey AI Bretscher A. Organizing the cell cortex: the role of ERM proteins. Nat Rev. (2010) 11: 276– 87. 10.1038/nrm2866 20308985 PMC2871950 · DOI · Paper page
  90. [94]Fievet BT Gautreau A Roy C Del Maestro L Mangeat P Louvard D. Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J Cell Biol. (2004) 164: 653– 9. 10.1083/jcb.200307032 14993232 PMC2172172 · DOI
  91. [95]Pietromonaco SF Simons PC Altman A Elias L. Protein kinase C-theta phosphorylation of moesin in the actin-binding sequence. J Biol Chem. (1998) 273: 7594– 603. 10.1074/jbc.273.13.7594 9516463 · DOI
  92. [96]Yonemura S Matsui T Tsukita S Tsukita S. Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J Cell Sci. (2002) 115: 2569– 80. 10.1155/2012/125295 12045227 · DOI
  93. [97]Belkina NV Liu Y Hao JJ Karasuyama H Shaw S. LOK is a major ERM kinase in resting lymphocytes and regulates cytoskeletal rearrangement through ERM phosphorylation. Proc Natl Acad Sci USA. (2009) 106: 4707– 12. 10.1073/pnas.0805963106 19255442 PMC2660762 · DOI
  94. [98]Nakamura N Oshiro N Fukata Y Amano M Fukata M Kuroda S. Phosphorylation of ERM proteins at filopodia induced by Cdc42. Genes Cells (2000) 5: 571– 81. 10.1046/j.1365-2443.2000.00348.x 10947843 · DOI
  95. [99]Baumgartner M Sillman AL Blackwood EM Srivastava J Madson N Schilling JW. The Nck-interacting kinase phosphorylates ERM proteins for formation of lamellipodium by growth factors. Proc Natl Acad Sci USA. (2006) 103: 13391– 6. 10.1073/pnas.0605950103 16938849 PMC1569174 · DOI
  96. [100]Oshiro N Fukata Y Kaibuchi K. Phosphorylation of moesin by rho-associated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J Biol Chem. (1998) 273: 34663– 6. 10.1074/jbc.273.52.34663 9856983 · DOI
  97. [101]Niggli V Andreoli C Roy C Mangeat P. Identification of a phosphatidylinositol-4,5-bisphosphate-binding domain in the N-terminal region of ezrin. FEBS Lett. (1995) 376: 172– 6. 10.1016/0014-5793(95)01270-1 7498535 · DOI
  98. [103]Nishita M Tomizawa C Yamamoto M Horita Y Ohashi K Mizuno K. Spatial and temporal regulation of cofilin activity by LIM kinase and Slingshot is critical for directional cell migration. J Cell Biol. (2005) 171: 349– 59. 10.1083/jcb.200504029 16230460 PMC2171197 · DOI
  99. [104]Maekawa M Ishizaki T Boku S Watanabe N Fujita A Iwamatsu A. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science (1999) 285: 895– 8. 10.1126/science.285.5429.895 10436159 · DOI
  100. [105]Oser M Condeelis J. The cofilin activity cycle in lamellipodia and invadopodia. J Cell Biochem (2009) 108: 1252– 62. 10.1002/jcb.22372 19862699 PMC3718474 · DOI
  101. [106]Maus M Medgyesi D Kiss E Schneider AE Enyedi A Szilagyi N. B cell receptor-induced Ca2+ mobilization mediates F-actin rearrangements and is indispensable for adhesion and spreading of B lymphocytes. J Leukocyte Biol. (2013) 93: 537– 47. 10.1189/jlb.0312169 23362305 · DOI
  102. [107]Hartzell CA Jankowska KI Burkhardt JK Lewis RS. Calcium influx through CRAC channels controls actin organization and dynamics at the immune synapse. eLife (2016) 5:e14850. 10.7554/eLife.14850 27440222 PMC4956410 · DOI
  103. [108]Lin KB Freeman SA Zabetian S Brugger H Weber M Lei V. The rap GTPases regulate B cell morphology, immune-synapse formation, and signaling by particulate B cell receptor ligands. Immunity (2008) 28: 75– 87. 10.1016/j.immuni.2007.11.019 18191594 · DOI · Paper page
  104. [109]Heasman SJ Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Molecul Cell Biol. (2008) 9: 690– 701. 10.1038/nrm2476 18719708 · DOI · Paper page
  105. [110]Padrick SB Rosen MK. Physical mechanisms of signal integration by WASP family proteins. Ann Rev Biochem. (2010) 79: 707– 35. 10.1146/annurev.biochem.77.060407.135452 20533885 PMC3017724 · DOI
  106. [111]Miki H Miura K Takenawa T. N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J. (1996) 15: 5326– 35. 10.1002/j.1460-2075.1996.tb00917.x 8895577 PMC452276 · DOI
  107. [112]Westerberg LS Dahlberg C Baptista M Moran CJ Detre C Keszei M. Wiskott-Aldrich syndrome protein (WASP) and N-WASP are critical for peripheral B-cell development and function. Blood (2012) 119: 3966– 74. 10.1182/blood-2010-09-308197 22411869 PMC3350364 · DOI
  108. [113]Liu C Bai X Wu J Sharma S Upadhyaya A Dahlberg IM. N-wasp is essential for the negative regulation of B cell receptor signaling. PLoS Biol. (2013) 11:e1001704. 10.1371/journal.pbio.1001704 24223520 PMC3818172 · DOI
  109. [114]Volpi S Santori E Abernethy K Mizui M Dahlberg CI. N-WASP is required for B-cell-mediated autoimmunity in Wiskott-Aldrich syndrome. Blood (2016) 127: 216– 20. 10.1182/blood-2015-05-643817 26468226 PMC4713162 · DOI
  110. [115]Martinez-Quiles N Rohatgi R Anton IM Medina M Saville SP Miki H. WIP regulates N-WASP-mediated actin polymerization and filopodium formation. Nat Cell Biol. (2001) 3: 484– 91. 10.1038/35074551 11331876 · DOI
  111. [116]Sun X Wang J Qin T Zhang Y Huang L Niu L. Dock8 regulates BCR signaling and activation of memory B cells via WASP and CD19. Blood Adv. (2018) 2: 401– 13. 29472447 PMC5858470
  112. [117]Keppler SJ Gasparrini F Burbage M Aggarwal S Frederico B Geha RS. Wiskott-aldrich syndrome interacting protein deficiency uncovers the role of the co-receptor CD19 as a generic hub for PI3 kinase signaling in B cells. Immunity (2015) 43: 660– 73. 10.1016/j.immuni.2015.09.004 26453379 PMC4622935 · DOI
  113. [118]Janssen E Tohme M Hedayat M Leick M Kumari S Ramesh N. A DOCK8-WIP-WASp complex links T cell receptors to the actin cytoskeleton. J Clin Invest. (2016) 126: 3837– 51. 10.1172/JCI85774 27599296 PMC5096816 · DOI
  114. [119]Saito K Scharenberg AM Kinet JP. Interaction between the Btk PH domain and phosphatidylinositol-3,4,5-trisphosphate directly regulates Btk. J Biol Chem. (2001) 276: 16201– 6. 10.1074/jbc.M100873200 11279148 · DOI
  115. [120]Scharenberg AM El-Hillal O Fruman DA Beitz LO Li Z Lin S Phosphatidylinositol-3,4,5-trisphosphate (PtdIns-3,4,5-P<sub>3</sub>)/Tec kinase-dependent calcium signaling pathway: a target for SHIP-mediated inhibitory signals. EMBO J. (1998) 17: 1961. 9524119 PMC1170542
  116. [121]OCorneth BJ, Klein R, Wolterink GJ, Hendriks RW. BTK Signaling in B cell differentiation and autoimmunity. Curr Top Microbiol Immunol. (2016) 393: 67– 105. 10.1007/82_2015_478 26341110 · DOI
  117. [122]Saito K Tolias KF Saci A Koon HB Humphries LA Scharenberg et al. BTK regulates PtdIns-4,5-P2 synthesis: importance for calcium signaling and PI3K activity. Immunity (2003) 19: 669– 78. 10.1016/S1074-7613(03)00297-8 14614854 · DOI
  118. [123]Sharma S Orlowski G Song W. Btk regulates B cell receptor-mediated antigen processing and presentation by controlling actin cytoskeleton dynamics in B cells. J Immunol. (2009) 182: 329– 39. 10.4049/jimmunol.182.1.329 19109164 PMC2855895 · DOI
  119. [124]Baba Y Nonoyama S Matsushita M Yamadori T Hashimoto S Imai K. Involvement of wiskott-aldrich syndrome protein in B-cell cytoplasmic tyrosine kinase pathway. Blood (1999) 93: 2003– 12. 10068673
  120. [125]Bolland S Pearse RN Kurosaki T Ravetch JV. SHIP modulates immune receptor responses by regulating membrane association of Btk. Immunity (1998) 8: 509– 16. 10.1016/S1074-7613(00)80555-5 9586640 · DOI
  121. [126]Bai X Zhang Y Huang L Wang J Li W Niu L. The early activation of memory B cells from Wiskott-Aldrichsyndrome patients is suppressed by CD19 downregulation. Blood (2016) 128: 1723– 34. 10.1182/blood-2016-03-703579 27330000 PMC5043127 · DOI
  122. [127]Bai X Huang L Niu L Zhang Y Wang J Sun X. Mst1 positively regulates B-cell receptor signaling via CD19 transcriptional levels. Blood Adv. (2016) 1: 219– 30. 10.1182/bloodadvances.2016000588 29296937 PMC5737167 · DOI
  123. [128]Alsufyani F Mattoo H Zhou D Cariappa A Van Buren D Hock H. The Mst1 kinase is required for follicular B cell homing and B-1 B cell development. Front Immunol. (2018) 9: 2393. 10.3389/fimmu.2018.02393 30386341 PMC6199389 · DOI
  124. [129]Campellone KG Welch MD. A nucleator arms race: cellular control of actin assembly. Nat Rev Molecul Cell Biol. (2010) 11: 237– 51. 10.1038/nrm2867 20237478 PMC2929822 · DOI
  125. [130]Park H Chan MM Iritani BM. Hem-1: putting the “WAVE” into actin polymerization during an immune response. FEBS Lett. (2010) 584: 4923– 32. 10.1016/j.febslet.2010.10.018 20969869 PMC3363972 · DOI
  126. [131]Suetsugu S Kurisu S Oikawa T Yamazaki D Oda A Takenawa T. Optimization of WAVE2 complex-induced actin polymerization by membrane-bound IRSp53, PIP(3), and Rac. J Cell Biol. (2006) 173: 571– 85. 10.1083/jcb.200509067 16702231 PMC2063866 · DOI
  127. [132]Walmsley MJ Ooi SK Reynolds LF Smith SH Ruf S Mathiot A. Critical roles for Rac1 and Rac2 GTPases in B cell development and signaling. Science (2003) 302: 459– 62. 10.1126/science.1089709 14564011 · DOI
  128. [133]Kuhn S Geyer M. Formins as effector proteins of Rho GTPases. Small GTPases (2014) 5:e29513. 10.4161/sgtp.29513 24914801 PMC4111664 · DOI
  129. [134]Vascotto F Lankar D Faure-Andre G Vargas P Diaz J Le Roux D. The actin-based motor protein myosin II regulates MHC class II trafficking and BCR-driven antigen presentation. J Cell Biol. (2007) 176: 1007– 19. 10.1083/jcb.200611147 17389233 PMC2064085 · DOI

Cited by

Sorted by citations

Authors
Li, J., Yin, W., Jing, Y., Kang, D., Yang, L., Cheng, J., Yu, Z., Peng, Z., Li, X., Wen, Y., Sun, X., Ren, B., & Liu, C.
Affiliations
  • Huazhong University of Science and Technology (CN)
  • Wuhan Children's Hospital (CN)
  • Yangtze University (CN)
Corresponding author
  • Ren, Boxu
  • Liu, Chaohong
ORCID
Venue
Frontiers in Immunology
Publisher
Frontiers Media SA
Published
2019-01-09
Volume
9
Pages
3096-3096
ISSN
1664-3224 (ISSN-L)
DOI
10.3389/fimmu.2018.03096
PMC
PMC6333714
OpenAlex
W2910414574
Cited by
70
References
5
Citations by year
2026: 4 · 2025: 8 · 2024: 10 · 2023: 10 · 2022: 12 · 2021: 15 · 2020: 10 · 2019: 1
FWCI
0.83
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Immunology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Natural Science Foundation of China
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
Keywords
B cell activation, B cell receptor signaling, actin cytoskeleton, antigen recognition, lymphoma, autoimmune disease
MeSH terms
Animals, B-Lymphocytes, Cell Membrane, Humans, Lymphocyte Activation, Actin Cytoskeleton, Protein Binding, Receptors, Antigen, B-Cell, Signal Transduction, Biomarkers, Immunological Synapses

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review