Polarized Secretion of Lysosomes at the B Cell Synapse Couples Antigen Extraction to Processing and Presentation

Immunity

Volumn 35, Issue 3, 2011, Pages 361-374

  Yuseff, Maria Isabel ^a   Reversat, Anne ^a   Lankar, Danielle ^a   Diaz, Jheimmy ^a   Fanget, Isabelle ^b   Pierobon, Paolo ^a   Randrian, Violaine ^a   Larochette, Nathanael ^b   Vascotto, Fulvia ^a   Desdouets, Chantal ^b   Jauffred, Bertrand ^c   Bellaiche, Yohanns ^c   Gasman, Stéphane ^d   Darchen, François ^b   Desnos, Claire ^b   Lennon Duménil, Ana Maria ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b CNRS   (France)

^c INSTITUT CURIE   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN CDC42;

ANIMAL CELL; ANTIGEN FUNCTION; ARTICLE; B LYMPHOCYTE; CELL SECRETION; LYSOSOME; MICROTUBULE ORGANIZING CENTER; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC POTENTIAL;

ANIMALS; ANTIGEN PRESENTATION; B-LYMPHOCYTES; CDC42 GTP-BINDING PROTEIN; CELL POLARITY; IMMUNOLOGICAL SYNAPSES; LYSOSOMES; MICE; PROTEIN KINASE C; RECEPTORS, ANTIGEN, B-CELL;

EID: 80053130049     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.07.008     Document Type: Article

References (44)

1. Arana E., Vehlow A., Harwood N.E., Vigorito E., Henderson R., Turner M., Tybulewicz V.L., Batista F.D. Activation of the small GTPase Rac2 via the B cell receptor regulates B cell adhesion and immunological-synapse formation. Immunity 2008, 28:88-99.
2. Basto R., Brunk K., Vinadogrova T., Peel N., Franz A., Khodjakov A., Raff J.W. Centrosome amplification can initiate tumorigenesis in flies. Cell 2008, 133:1032-1042.
3. Batista F.D., Harwood N.E. The who, how and where of antigen presentation to B cells. Nat. Rev. Immunol. 2009, 9:15-27.
4. Batista F.D., Neuberger M.S. B cells extract and present immobilized antigen: Implications for affinity discrimination. EMBO J. 2000, 19:513-520.
5. Batista F.D., Iber D., Neuberger M.S. B cells acquire antigen from target cells after synapse formation. Nature 2001, 411:489-494.
6. Boes M., Cerny J., Massol R., Op den Brouw M., Kirchhausen T., Chen J., Ploegh H.L. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 2002, 418:983-988.
7. Boulanger J., Kervrann C., Bouthemy P., Elbau P., Sibarita J.B., Salamero J. Patch-based nonlocal functional for denoising fluorescence microscopy image sequences. IEEE Trans. Med. Imaging 2010, 29:442-454.
8. Brezski R.J., Monroe J.G. B cell antigen receptor-induced Rac1 activation and Rac1-dependent spreading are impaired in transitional immature B cells due to levels of membrane cholesterol. J. Immunol. 2007, 179:4464-4472.
9. Cambier J.C., Pleiman C.M., Clark M.R. Signal transduction by the B cell antigen receptor and its coreceptors. Annu. Rev. Immunol. 1994, 12:457-486.
10. Carrasco Y.R., Batista F.D. 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, 27:160-171.
11. Desnos C., Huet S., Fanget I., Chapuis C., Böttiger C., Racine V., Sibarita J.B., Henry J.P., Darchen F. Myosin va mediates docking of secretory granules at the plasma membrane. J. Neurosci. 2007, 27:10636-10645.
12. Fleire S.J., Goldman J.P., Carrasco Y.R., Weber M., Bray D., Batista F.D. B cell ligand discrimination through a spreading and contraction response. Science 2006, 312:738-741.
13. Goldstein B., Macara I.G. The PAR proteins: Fundamental players in animal cell polarization. Dev. Cell 2007, 13:609-622.
14. Gomes E.R., Jani S., Gundersen G.G. Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 2005, 121:451-463.
15. Goodnow C.C., Crosbie J., Adelstein S., Lavoie T.B., Smith-Gill S.J., Brink R.A., Pritchard-Briscoe H., Wotherspoon J.S., Loblay R.H., Raphael K., et al. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 1988, 334:676-682.
16. Grakoui A., Bromley S.K., Sumen C., Davis M.M., Shaw A.S., Allen P.M., Dustin M.L. The immunological synapse: A molecular machine controlling T cell activation. Science 1999, 285:221-227.
17. Griffiths G.M., Tsun A., Stinchcombe J.C. The immunological synapse: A focal point for endocytosis and exocytosis. J. Cell Biol. 2010, 189:399-406.
18. Guo F., Velu C.S., Grimes H.L., Zheng Y. Rho GTPase Cdc42 is essential for B-lymphocyte development and activation. Blood 2009, 114:2909-2916.
19. Haka A.S., Grosheva I., Chiang E., Buxbaum A.R., Baird B.A., Pierini L.M., Maxfield F.R. Macrophages create an acidic extracellular hydrolytic compartment to digest aggregated lipoproteins. Mol. Biol. Cell 2009, 20:4932-4940.
20. Harwood N.E., Batista F.D. New insights into the early molecular events underlying B cell activation. Immunity 2008, 28:609-619.
21. Huet S., Karatekin E., Tran V.S., Fanget I., Cribier S., Henry J.P. Analysis of transient behavior in complex trajectories: Application to secretory vesicle dynamics. Biophys. J. 2006, 91:3542-3559.
22. Iden S., Collard J.G. Crosstalk between small GTPases and polarity proteins in cell polarization. Nat. Rev. Mol. Cell Biol. 2008, 9:846-859.
23. Junt T., Moseman E.A., Iannacone M., Massberg S., Lang P.A., Boes M., Fink K., Henrickson S.E., Shayakhmetov D.M., Di Paolo N.C., et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007, 450:110-114.
24. Kupfer A., Swain S.L., Singer S.J. The specific direct interaction of helper T cells and antigen-presenting B cells. II. Reorientation of the microtubule organizing center and reorganization of the membrane-associated cytoskeleton inside the bound helper T cells. J. Exp. Med. 1987, 165:1565-1580.
25. Lankar D., Vincent-Schneider H., Briken V., Yokozeki T., Raposo G., Bonnerot C. Dynamics of major histocompatibility complex class II compartments during B cell receptor-mediated cell activation. J. Exp. Med. 2002, 195:461-472.
26. Le Roux D., Lankar D., Yuseff M.I., Vascotto F., Yokozeki T., Faure-André G., Mougneau E., Glaichenhaus N., Manoury B., Bonnerot C., Lennon-Duménil A.M. Syk-dependent actin dynamics regulate endocytic trafficking and processing of antigens internalized through the B-cell receptor. Mol. Biol. Cell 2007, 18:3451-3462.
27. Lennon-Duménil A.M., Bakker A.H., Maehr R., Fiebiger E., Overkleeft H.S., Rosemblatt M., Ploegh H.L., Lagaudrière-Gesbert C. Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J. Exp. Med. 2002, 196:529-540.
28. Liu D., Bryceson Y.T., Meckel T., Vasiliver-Shamis G., Dustin M.L., Long E.O. Integrin-dependent organization and bidirectional vesicular traffic at cytotoxic immune synapses. Immunity 2009, 31:99-109.
29. Martin P., Duran A., Minguet S., Gaspar M.L., Diaz-Meco M.T., Rennert P., Leitges M., Moscat J. Role of zeta PKC in B-cell signaling and function. EMBO J. 2002, 21:4049-4057.
30. Martín-Cófreces N.B., Robles-Valero J., Cabrero J.R., Mittelbrunn M., Gordón-Alonso M., Sung C.H., Alarcón B., Vázquez J., Sánchez-Madrid F. MTOC translocation modulates IS formation and controls sustained T cell signaling. J. Cell Biol. 2008, 182:951-962.
31. Milasta S., Evans N.A., Ormiston L., Wilson S., Lefkowitz R.J., Milligan G. The sustainability of interactions between the orexin-1 receptor and beta-arrestin-2 is defined by a single C-terminal cluster of hydroxy amino acids and modulates the kinetics of ERK MAPK regulation. Biochem. J. 2005, 387:573-584.
32. Mitchison N.A. T-cell-B-cell cooperation. Nat. Rev. Immunol. 2004, 4:308-312.
33. Moss C.X., Tree T.I., Watts C. Reconstruction of a pathway of antigen processing and class II MHC peptide capture. EMBO J. 2007, 26:2137-2147.
34. Onabajo O.O., Seeley M.K., Kale A., Qualmann B., Kessels M., Han J., Tan T.H., Song W. Actin-binding protein 1 regulates B cell receptor-mediated antigen processing and presentation in response to B cell receptor activation. J. Immunol. 2008, 180:6685-6695.
35. Pulecio J., Petrovic J., Prete F., Chiaruttini G., Lennon-Dumenil A.M., Desdouets C., Gasman S., Burrone O.R., Benvenuti F. Cdc42-mediated MTOC polarization in dendritic cells controls targeted delivery of cytokines at the immune synapse. J. Exp. Med. 2010, 207:2719-2732.
36. Puthenveedu M.A., Lauffer B., Temkin P., Vistein R., Carlton P., Thorn K., Taunton J., Weiner O.D., Parton R.G., von Zastrow M. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 2010, 143:761-773.
37. Reth M., Wienands J. Initiation and processing of signals from the B cell antigen receptor. Annu. Rev. Immunol. 1997, 15:453-479.
38. Sankaranarayanan S., De Angelis D., Rothman J.E., Ryan T.A. The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 2000, 79:2199-2208.
39. Stinchcombe J.C., Griffiths G.M. Secretory mechanisms in cell-mediated cytotoxicity. Annu. Rev. Cell Dev. Biol. 2007, 23:495-517.
40. Stoddart A., Jackson A.P., Brodsky F.M. Plasticity of B cell receptor internalization upon conditional depletion of clathrin. Mol. Biol. Cell 2005, 16:2339-2348.
41. Suzuki K., Grigorova I., Phan T.G., Kelly L.M., Cyster J.G. Visualizing B cell capture of cognate antigen from follicular dendritic cells. J. Exp. Med. 2009, 206:1485-1493.
42. Tolar P., Sohn H.W., Pierce S.K. Viewing the antigen-induced initiation of B-cell activation in living cells. Immunol. Rev. 2008, 221:64-76.
43. Vascotto F., Lankar D., Faure-André G., Vargas P., Diaz J., Le Roux D., Yuseff M.I., Sibarita J.B., Boes M., Raposo G., et al. The actin-based motor protein myosin II regulates MHC class II trafficking and BCR-driven antigen presentation. J. Cell Biol. 2007, 176:1007-1019.
44. Wubbolts R., Fernandez-Borja M., Jordens I., Reits E., Dusseljee S., Echeverri C., Vallee R.B., Neefjes J. Opposing motor activities of dynein and kinesin determine retention and transport of MHC class II-containing compartments. J. Cell Sci. 1999, 112:785-795.