Utilization of a photoactivatable antigen system to examine B-cell probing termination and the B-cell receptor sorting mechanisms during B-cell activation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 5, 2016, Pages E558-E567

  Wang, Jing ^a   Tang, Shan ^b   Wan, Zhengpeng ^a   Gao, Yiren ^a   Cao, Yiyun ^a   Yi, Junyang ^a   Si, Yanyan ^b   Zhang, Haowen ^a   Liu, Lei ^b   Liu, Wanli ^a  

^a Tsinghua University   (China)

^b Tsinghua University   (China)

Author keywords

B cell activation; B cell receptor; Caged NP; Photoactivatable antigen; Single molecule imaging

Indexed keywords

ANTIGEN; B LYMPHOCYTE RECEPTOR; F ACTIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL FUNCTION; CONTROLLED STUDY; IMAGING; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMBRANE; MOUSE; NONHUMAN; PHOTOACTIVATION; PRIORITY JOURNAL; TRIGGER POINT; ANIMAL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS; B-LYMPHOCYTES; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, B-CELL;

EID: 84956620678     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1517612113     Document Type: Article

References (43)

1. Pierce SK, Liu W (2010) The tipping points in the initiation of B cell signalling: How small changes make big differences. Nat Rev Immunol 10(11):767-777.
2. Dustin ML, Groves JT (2012) Receptor signaling clusters in the immune synapse. Annu Rev Biophys 41:543-556.
3. Davis MM, et al. (2007) T cells as a self-referential, sensory organ. Annu Rev Immunol 25:681-695.
4. Harwood NE, Batista FD (2010) Early events in B cell activation. Annu Rev Immunol 28:185-210.
5. Xu Y, et al. (2014) No receptor stands alone: IgG B-cell receptor intrinsic and extrinsic mechanisms contribute to antibody memory. Cell Res 24(6):651-664.
6. Liu W, Meckel T, Tolar P, Sohn HW, Pierce SK (2010) Antigen affinity discrimination is an intrinsic function of the B cell receptor. J Exp Med 207(5):1095-1111.
7. Fleire SJ, et al. (2006) B cell ligand discrimination through a spreading and contraction response. Science 312(5774):738-741.
8. Bachmann MF, et al. (1993) The influence of antigen organization on B cell responsiveness. Science 262(5138):1448-1451.
9. Liu W, Chen YH (2005) High epitope density in a single protein molecule significantly enhances antigenicity as well as immunogenicity: A novel strategy for modern vaccine development and a preliminary investigation about B cell discrimination of monomeric proteins. Eur J Immunol 35(2):505-514.
10. Liu W, et al. (2004) High epitope density in a single recombinant protein molecule of the extracellular domain of influenza A virus M2 protein significantly enhances protective immunity. Vaccine 23(3):366-371.
11. Avalos AM, et al. (2014) Monovalent engagement of the BCR activates ovalbuminspecific transnuclear B cells. J Exp Med 211(2):365-379.
12. Kim YM, et al. (2006) Monovalent ligation of the B cell receptor induces receptor activation but fails to promote antigen presentation. Proc Natl Acad Sci USA 103(9):3327-3332.
13. Mukherjee S, et al. (2013) Monovalent and multivalent ligation of the B cell receptor exhibit differential dependence upon Syk and Src family kinases. Sci Signal 6(256):ra1.
14. Wan Z, Liu W (2012) The growth of B cell receptor microcluster is a universal response of B cells encountering antigens with different motion features. Protein Cell 3(7):545-558.
15. Liu C, et al. (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.
16. Liu C, et al. (2012) 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.
17. Ketchum C, Miller H, Song W, Upadhyaya A (2014) Ligand mobility regulates B cell receptor clustering and signaling activation. Biophys J 106(1):26-36.
18. Wan Z, et al. (2013) B cell activation is regulated by the stiffness properties of the substrate presenting the antigens. J Immunol 190(9):4661-4675.
19. Zeng Y, et al. (2015) Substrate stiffness regulates B-cell activation, proliferation, class switch, and T-cell-independent antibody responses in vivo. Eur J Immunol 45(6):1621-1634.
20. Natkanski E, et al. (2013) B cells use mechanical energy to discriminate antigen affinities. Science 340(6140):1587-1590.
21. Wan Z, et al. (2015) The activation of IgM- or isotype-switched IgG- and IgE-BCR exhibits distinct mechanical force sensitivity and threshold. eLife 4:4.
22. Ellis-Davies GC, Kaplan JH (1994) Nitrophenyl-EGTA, a photolabile chelator that selectively binds Ca2+ with high affinity and releases it rapidly upon photolysis. Proc Natl Acad Sci USA 91(1):187-191.
23. Nerbonne JM, Richard S, Nargeot J, Lester HA (1984) New photoactivatable cyclic nucleotides produce intracellular jumps in cyclic AMP and cyclic GMP concentrations. Nature 310(5972):74-76.
24. Huse M, et al. (2007) Spatial and temporal dynamics of T cell receptor signaling with a photoactivatable agonist. Immunity 27(1):76-88.
25. De Mond AL, Starr T, Dustin ML, Groves JT (2006) Control of antigen presentation with a photoreleasable agonist peptide. J Am Chem Soc 128(48):15354-15355.
26. Sonoda E, et al. (1997) B cell development under the condition of allelic inclusion. Immunity 6(3):225-233.
27. Hauser AE, et al. (2007) Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity 26(5):655-667.
28. Treanor B, Depoil D, Bruckbauer A, Batista FD (2011) Dynamic cortical actin remodeling by ERM proteins controls BCR microcluster organization and integrity. J Exp Med 208(5):1055-1068.
29. Treanor B, et al. (2010) The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity 32(2):187-199.
30. Liu W, Meckel T, Tolar P, Sohn HW, Pierce SK (2010) Intrinsic properties of immunoglobulin IgG1 isotype-switched B cell receptors promote microclustering and the initiation of signaling. Immunity 32(6):778-789.
31. Tolar P, Hanna J, Krueger PD, Pierce SK (2009) The constant region of the membrane immunoglobulin mediates B cell-receptor clustering and signaling in response to membrane antigens. Immunity 30(1):44-55.
32. Depoil D, et al. (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.
33. Mattila PK, et al. (2013) The actin and tetraspanin networks organize receptor nanoclusters to regulate B cell receptor-mediated signaling. Immunity 38(3):461-474.
34. Liu C, et al. (2013) N-wasp is essential for the negative regulation of B cell receptor signaling. PLoS Biol 11(11):e1001704.
35. Shih TA, Roederer M, Nussenzweig MC (2002) Role of antigen receptor affinity in T cell-independent antibody responses in vivo. Nat Immunol 3(4):399-406.
36. Brodovitch A, Limozin L, Bongrand P, Pierres A (2015) Use of TIRF to Monitor T-Lymphocyte Membrane Dynamics with Submicrometer and Subsecond Resolution. Cell Mol Bioeng 8(1):178-186.
37. Suzuki K, Grigorova I, Phan TG, Kelly LM, Cyster JG (2009) Visualizing B cell capture of cognate antigen from follicular dendritic cells. J Exp Med 206(7):1485-1493.
38. Phan TG, Green JA, Gray EE, Xu Y, Cyster JG (2009) Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat Immunol 10(7):786-793.
39. Choudhuri K, et al. (2014) Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature 507(7490):118-123.
40. Kusumi A, et al. (2012) 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 28:215-250.
41. Kusumi A, et al. (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: High-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34:351-378.
42. Kusumi A, Shirai YM, Koyama-Honda I, Suzuki KG, Fujiwara TK (2010) Hierarchical organization of the plasma membrane: Investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. FEBS Lett 584(9):1814-1823.
43. Xu L, et al. (2014) Through an ITIM-independent mechanism the Fc+RIIB blocks B cell activation by disrupting the colocalized microclustering of the B cell receptor and CD19. J Immunol 192(11):5179-5191.