DOI QR코드

DOI QR Code

Actin Engine in Immunological Synapse

  • Piragyte, Indre (Immune Synapse Research Center and Cell Dynamics Research Center, School of Life Sciences, Gwangju Institute of Science and Technology) ;
  • Jun, Chang-Duk (Immune Synapse Research Center and Cell Dynamics Research Center, School of Life Sciences, Gwangju Institute of Science and Technology)
  • 투고 : 2012.04.19
  • 심사 : 2012.05.19
  • 발행 : 2012.06.30

초록

T cell activation and function require physical contact with antigen presenting cells at a specialized junctional structure known as the immunological synapse. Once formed, the immunological synapse leads to sustained T cell receptor-mediated signalling and stabilized adhesion. High resolution microscopy indeed had a great impact in understanding the function and dynamic structure of immunological synapse. Trends of recent research are now moving towards understanding the mechanical part of immune system, expanding our knowledge in mechanosensitivity, force generation, and biophysics of cell-cell interaction. Actin cytoskeleton plays inevitable role in adaptive immune system, allowing it to bear dynamic and precise characteristics at the same time. The regulation of mechanical engine seems very complicated and overlapping, but it enables cells to be very sensitive to external signals such as surface rigidity. In this review, we focus on actin regulators and how immune cells regulate dynamic actin rearrangement process to drive the formation of immunological synapse.

키워드

참고문헌

  1. Huppa, J. B., and M. M. Davis. 2003. T-cell-antigen recognition and the immunological synapse. Nat. Rev. Immunol.3: 973-983. https://doi.org/10.1038/nri1245
  2. Grakoui, A., S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285: 221-227. https://doi.org/10.1126/science.285.5425.221
  3. Monks, C. R., B. A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395: 82-86. https://doi.org/10.1038/25764
  4. Cemerski, S., and A. Shaw. 2006. Immune synapses in T-cell activation. Curr. Opin. Immunol. 18: 298-304. https://doi.org/10.1016/j.coi.2006.03.011
  5. Saito, T., and T. Yokosuka. 2006. Immunological synapse and microclusters: the site for recognition and activation of T cells. Curr. Opin. Immunol. 18: 305-313. https://doi.org/10.1016/j.coi.2006.03.014
  6. Hill, T. L., and M. W. Kirschner. 1982. Bioenergetics and kinetics of microtubule and actin filament assembly-disassembly. Int. Rev. Cytol. 78: 1-125.
  7. Hamon, M., H. Bierne, and P. Cossart. 2006. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4:423-434. https://doi.org/10.1038/nrmicro1413
  8. Veiga, E., and P. Cossart. 2005. Listeria hijacks the clathrin- dependent endocytic machinery to invade mammalian cells. Nat. Cell Biol. 7: 894-900. https://doi.org/10.1038/ncb1292
  9. Dustin, M. L. 2007. Cell adhesion molecules and actin cytoskeleton at immune synapses and kinapses. Curr. Opin. Cell Biol. 19: 529-533. https://doi.org/10.1016/j.ceb.2007.08.003
  10. Irvine. D. J., M. A. Purbhoo, M. Krogsgaard, and M. M. Davis. 2002. Direct observation of ligand recognition by T cells. Nature 419: 845-849. https://doi.org/10.1038/nature01076
  11. Iezzi, G., K. Karjalainen, and A. Lanzavecchia. 1998. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8: 89-95. https://doi.org/10.1016/S1074-7613(00)80461-6
  12. Mempel, T. R., S. E. Henrickson, and U. H. Von Andrian. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427: 154-159. https://doi.org/10.1038/nature02238
  13. Delon, J., N. Bercovici, R. Liblau, and A. Trautmann. 1998. Imaging antigen recognition by naive CD4+ T cells: compulsory cytoskeletal alterations for the triggering of an intracellular calcium response. Eur. J. Immunol. 28: 716-729. https://doi.org/10.1002/(SICI)1521-4141(199802)28:02<716::AID-IMMU716>3.0.CO;2-E
  14. Wulfing, C., M. D. Sjaastad, and M. M. Davis. 1998. Visualizing the dynamics of T cell activation: intracellular adhesion molecule 1 migrates rapidly to the T cell/B cell interface and acts to sustain calcium levels. Proc. Natl. Acad. Sci. U. S. A. 95: 6302-6307. https://doi.org/10.1073/pnas.95.11.6302
  15. Wulfing, C., and M. M. Davis. 1998. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282: 2266-2269. https://doi.org/10.1126/science.282.5397.2266
  16. Valitutti, S., M. Dessing, K. Aktories, H. Gallati, and A. Lanzavecchia. 1995. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J. Exp. Med. 181: 577-584. https://doi.org/10.1084/jem.181.2.577
  17. Setterblad, N., S. Becart, D. Charron, and N. Mooney. 2004. B cell lipid rafts regulate both peptide-dependent and peptide- independent APC-T cell interaction. J. Immunol. 173:1876-1886. https://doi.org/10.4049/jimmunol.173.3.1876
  18. Vascotto, F., D. Lankar, G. Faure-Andre, P. Vargas, J. Diaz, D. Le Roux, M. I. Yuseff, J. B. Sibarita, M. Boes, G. Raposo, E. Mougneau, N. Glaichenhaus, C. Bonnerot, B. Manoury, and A. M. Lennon-Dumenil. 2007. The actin-based motor protein myosin II regulates MHC class II trafficking and BCR-driven antigen presentation. J. Cell Biol. 176: 1007-1019. https://doi.org/10.1083/jcb.200611147
  19. Harwood, N. E., and F. D. Batista. 2011. The cytoskeleton coordinates the early events of B-cell activation. Cold Spring Harb. Perspect. Biol. 3.
  20. Maravillas-Montero, J. L., P. G. Gillespie, G. Patino-Lopez, S. Shaw, and L. Santos-Argumedo. 2011. Myosin 1c participates in B cell cytoskeleton rearrangements, is recruited to the immunologic synapse, and contributes to antigen presentation. J. Immunol. 187: 3053-3063. https://doi.org/10.4049/jimmunol.1004018
  21. Al-Alwan, M. M., G, Rowden, T. D. Lee, and K. A. West. 2001. The dendritic cell cytoskeleton is critical for the formation of the immunological synapse. J. Immunol. 166:1452-1456. https://doi.org/10.4049/jimmunol.166.3.1452
  22. Metlay, J. P., E. Pure, and R. M. Steinman. 1989. Distinct features of dendritic cells and anti-Ig activated B cells as stimulators of the primary mixed leukocyte reaction. J. Exp. Med. 169: 239-254. https://doi.org/10.1084/jem.169.1.239
  23. Cyster, J. G., D. M. Shotton, and A. F. Williams. 1991. The dimensions of the T lymphocyte glycoprotein leukosialin and identification of linear protein epitopes that can be modified by glycosylation. EMBO J. 10: 893-902.
  24. van der Merwe, P. A., and A. N. Barclay. 1994. Transient intercellular adhesion: the importance of weak protein-protein interactions. Trends. Biochem. Sci. 19: 354-358. https://doi.org/10.1016/0968-0004(94)90109-0
  25. Garboczi, D. N., P. Ghosh, U. Utz, Q. R. Fan, W. E. Biddison, and D. C. Wiley. 2010. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 1996. 384: 134-141. J. Immunol. 185: 6394-6401.
  26. Garcia, K. C., M. Degano, R. L. Stanfield, A. Brunmark, M. R. Jackson, P. A. Peterson, L. Teyton, I., and A. Wilson. 1996. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 274: 209-219. https://doi.org/10.1126/science.274.5285.209
  27. Springer, T. A., M. L. Dustin, T. K. Kishimoto, and S. D. Marlin. 1987. The lymphocyte function-associated LFA-1, CD2, and LFA-3 molecules: cell adhesion receptors of the immune system. Annu. Rev. Immunol. 5: 223-252. https://doi.org/10.1146/annurev.iy.05.040187.001255
  28. Ueda, H., M. K. Morphew, J. R. McIntosh, and M. M. Davis. 2011. CD4+ T-cell synapses involve multiple distinct stages. Proc. Natl. Acad. Sci. U. S. A. 108: 17099-17104. https://doi.org/10.1073/pnas.1113703108
  29. Husson, J., K. Chemin, A. Bohineust, C. Hivroz, and N. Henry. 2011. Force generation upon T cell receptor engagement. PLoS One 6: e19680. https://doi.org/10.1371/journal.pone.0019680
  30. Kandula, S, and C. Abraham. 2004. LFA-1 on CD4+ T cells is required for optimal antigen-dependent activation in vivo. J. Immunol. 173: 4443-4451. https://doi.org/10.4049/jimmunol.173.7.4443
  31. Scholer, A., S. Hugues, A. Boissonnas, L. Fetler, and S. Amigorena. 2008. Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity 28: 258-270. https://doi.org/10.1016/j.immuni.2007.12.016
  32. Hosseini, B. H., I. Louban, D. Djandji, G. H. Wabnitz, J. Deeg, N. Bulbuc, Y. Samstag, M. Gunzer, J. P. Spatz, and G. J. Hämmerling. 2009. Immune synapse formation determines interaction forces between T cells and antigen- presenting cells measured by atomic force microscopy. Proc. Natl. Acad. Sci. U. S. A. 106: 17852-17857. https://doi.org/10.1073/pnas.0905384106
  33. Kim, S. T., K. Takeuchi, Z. Y. Sun, M. Touma, C. E. Castro, A. Fahmy, M. J. Lang, G. Wagner, and E. L. Reinherz. 2009. The alphabeta T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284: 31028-31037. https://doi.org/10.1074/jbc.M109.052712
  34. Li, Y. C., B. M. Chen, P. C. Wu, T. L. Cheng, L. S. Kao, M. H. Tao, A. Lieber, and S. R. Roffler. 2010. Cutting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J. Immunol. 184:5959-5963. https://doi.org/10.4049/jimmunol.0900775
  35. Judokusumo, E., E. Tabdanov, S. Kumari, M. L. Dustin, and L. C. Kam. 2012. Mechanosensing in T lymphocyte activation. Biophys. J. 102: L5-7. https://doi.org/10.1016/j.bpj.2011.12.011
  36. Sloan-Lancaster, J., A. S. Shaw, J. B. Rothbard, and P. M. Allen. 1994. Partial T cell signaling: altered phospho-zeta and lack of zap70 recruitment in APL-induced T cell anergy.Cell 79: 913-922. https://doi.org/10.1016/0092-8674(94)90080-9
  37. Madrenas, J., R. L. Wange, J. L. Wang, N. Isakov, L. E. Samelson, and R. N. Germain. 1995. Zeta phosphorylation without ZAP-70 activation induced by TCR antagonists or partial agonists. Science 267: 515-518. https://doi.org/10.1126/science.7824949
  38. Dittel, B. N., I. Stefanova, R. N. Germain, and C. A. Jr. Janeway. 1999. Cross-antagonism of a T cell clone expressing two distinct T cell receptors. Immunity 11: 289-298. https://doi.org/10.1016/S1074-7613(00)80104-1
  39. La Face, D. M., C. Couture, K. Anderson, G. Shih, J. Alexander, A. Sette, T. Mustelin, A. Altman, and H. M. Grey. 1997. Differential T cell signaling induced by antagonist peptide-MHC complexes and the associated phenotypic responses. J. Immunol. 158: 2057-2064.
  40. Lucas, B., I. Stefanová, K. Yasutomo, N. Dautigny, and R. N. Germain. 1999. Divergent changes in the sensitivity of maturing T cells to structurally related ligands underlies formation of a useful T cell repertoire. Immunity 10: 367-376. https://doi.org/10.1016/S1074-7613(00)80036-9
  41. Lee, K. H., A. D. Holdorf, M. L. Dustin, A. C. Chan, P. M. Allen, and A. S. Shaw. 2002. T cell receptor signaling precedes immunological synapse formation. Science 295:1539-1542. https://doi.org/10.1126/science.1067710
  42. Groves, T., P. Smiley, M. P. Cooke, K. Forbush, R. M. Perlmutter, and C. J. Guidos. 1996. Fyn can partially substitute for Lck in T lymphocyte development. Immunity 5:417-428. https://doi.org/10.1016/S1074-7613(00)80498-7
  43. Palacios, E. H., and A. Weiss. 2004. Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene. 23: 7990-8000. https://doi.org/10.1038/sj.onc.1208074
  44. Finco, T. S., T. Kadlecek, W. Zhang, L. E. Samelson, and A. Weiss. 1998. LAT is required for TCR-mediated activation of PLCgamma1 and the Ras pathway. Immunity 9: 617-626. https://doi.org/10.1016/S1074-7613(00)80659-7
  45. Gomez, T. S., S. D. McCarney, E. Carrizosa, C. M. Labno, E. O. Comiskey, J. C. Nolz, P. Zhu, B. D. Freedman, M. R. Clark, D. J. Rawlings, D. D. Billadeau, and J. K. Burkhardt. 2006. HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse. Immunity 24:741-752. https://doi.org/10.1016/j.immuni.2006.03.022
  46. Carrizosa, E., T. S. Gomez, C. M. Labno, D. A. Klos Dehring, X. Liu, B. D. Freedman, D. D. Billadeau, and J. K. Burkhardt. 2009. Hematopoietic lineage cell-specific protein 1 is recruited to the immunological synapse by IL-2-inducible T cell kinase and regulates phospholipase Cgamma1 Microcluster dynamics during T cell spreading. J. Immunol.183: 7352-7361. https://doi.org/10.4049/jimmunol.0900973
  47. Bunnell, S. C., V. Kapoor, R. P. Trible, W. Zhang, and L. E. Samelson. 2001. Dynamic actin polymerization drives T cell receptor-induced spreading: a role for the signal transduction adaptor LAT. Immunity 14: 315-329. https://doi.org/10.1016/S1074-7613(01)00112-1
  48. Zhang, W., J. Sloan-Lancaster, J. Kitchen, R. P. Trible, and L. E. Samelson. 1998. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92:83-92. https://doi.org/10.1016/S0092-8674(00)80901-0
  49. Liu, S. K., N. Fang, G. A. Koretzky, and C. J. McGlade. 1999. The hematopoietic-specific adaptor protein gads functions in T-cell signaling via interactions with the SLP-76 and LAT adaptors. Curr. Biol. 9: 67-75. https://doi.org/10.1016/S0960-9822(99)80017-7
  50. Bubeck Wardenburg, J., R. Pappu, J. Y. Bu, B. Mayer, J. Chernoff, D. Straus, and A. C. Chan. 1998. Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity 9: 607-616. https://doi.org/10.1016/S1074-7613(00)80658-5
  51. Bunnell, S. C., M. Diehn, M. B. Yaffe, P. R. Findell, L. C. Cantley, and L. J. Berg. 2000. Biochemical interactions integrating Itk with the T cell receptor-initiated signaling cascade. J. Biol. Chem. 275: 2219-2230. https://doi.org/10.1074/jbc.275.3.2219
  52. Yablonski, D., T. Kadlecek, and A. Weiss. 2001. Identification of a phospholipase C-gamma1 (PLC-gamma1) SH3 domain-binding site in SLP-76 required for T-cell receptor- mediated activation of PLC-gamma1 and NFAT. Mol. Cell Biol. 21: 4208-4218. https://doi.org/10.1128/MCB.21.13.4208-4218.2001
  53. Wu, J., D. G. Motto, G. A. Koretzky, and A. Weiss. 1996. Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 4: 593-602. https://doi.org/10.1016/S1074-7613(00)80485-9
  54. Tominaga, T., K. Sugie, M. Hirata, N. Morii, J. Fukata, A. Uchida, H, Imura, and S. Narumiya. 1993. Inhibition of PMA-induced, LFA-1-dependent lymphocyte aggregation by ADP ribosylation of the small molecular weight GTP binding protein, rho. J. Cell Biol. 120: 1529-1537. https://doi.org/10.1083/jcb.120.6.1529
  55. Watanabe, N., P. Madaule, T. Reid, T. Ishizaki, G. Watanabe, A. Kakizuka, Y. Saito, K. Nakao, B. M. Jockusch, and S. Narumiya. 1997. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16: 3044-3056. https://doi.org/10.1093/emboj/16.11.3044
  56. Higashida, C., T. Miyoshi, A. Fujita, F. Oceguera-Yanez, J. Monypenny, Y. Andou, S. Narumiya, and N. Watanabe. 2004. Actin polymerization-driven molecular movement of mDia1 in living cells. Science 303: 2007-2010. https://doi.org/10.1126/science.1093923
  57. Faix, J., and R. Grosse. 2006. Staying in shape with formins. Dev. Cell 10: 693-706. https://doi.org/10.1016/j.devcel.2006.05.001
  58. Campellone, K. G., and M. D. Welch. 2010. A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 11: 237-251. https://doi.org/10.1038/nrm2867
  59. Gomez, T. S., K. Kumar, R. B. Medeiros, Y. Shimizu, P. J. Leibson, and D. D. Billadeau. 2007. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity26: 177-190. https://doi.org/10.1016/j.immuni.2007.01.008
  60. Lammers, M., R. Rose, A. Scrima, and A. Wittinghofer. 2005. The regulation of mDia1 by autoinhibition and its release by Rho*GTP. EMBO J. 24: 4176-4187. https://doi.org/10.1038/sj.emboj.7600879
  61. Eisenmann, K. M., R. A. West, D. Hildebrand, S. M. Kitchen, J. Peng, R. Sigler, J. Zhang, K. A. Siminovitch, and A. S. Alberts. 2007. T cell responses in mammalian diaphanous- related formin mDia1 knock-out mice. J. Biol. Chem.282: 25152-25158. https://doi.org/10.1074/jbc.M703243200
  62. Sakata, D., H. Taniguchi, S. Yasuda, A. Adachi-Morishima, Y. Hamazaki, R. Nakayama, T. Miki, N. Minato, and S. Narumiya. 2007. Impaired T lymphocyte trafficking in mice deficient in an actin-nucleating protein, mDia1. J. Exp. Med.204: 2031-2038. https://doi.org/10.1084/jem.20062647
  63. Ruzzene, M., A. M. Brunati, O. Marin, A. Donella-Deana, and L. A. Pinna. 1996. SH2 domains mediate the sequential phosphorylation of HS1 protein by p72syk and Src-related protein tyrosine kinases. Biochemistry 35: 5327-5332. https://doi.org/10.1021/bi9528614
  64. Takemoto, Y., M. Sato, M. Furuta, and Y. Hashimoto. 1996. Distinct binding patterns of HS1 to the Src SH2 and SH3 domains reflect possible mechanisms of recruitment and activation of downstream molecules. Int. Immunol. 8: 1699-1705. https://doi.org/10.1093/intimm/8.11.1699
  65. Kitamura, D., H. Kaneko, Y. Miyagoe, T. Ariyasu, and T. Watanabe. 1989. Isolation and characterization of a novel human gene expressed specifically in the cells of hematopoietic lineage. Nucleic Acids Res. 17: 9367-9379.
  66. Daly, R. J. 2004. Cortactin signalling and dynamic actin networks. Biochem. J. 382: 13-25. https://doi.org/10.1042/BJ20040737
  67. Hao, J. J., J. Zhu, K. Zhou, N. Smith, and X. Zhan. 2005. The coiled-coil domain is required for HS1 to bind to F-actin and activate Arp2/3 complex. J. Biol. Chem. 280: 37988-37994. https://doi.org/10.1074/jbc.M504552200
  68. Huang, Y., E. O. Comiskey, R. S. Dupree, S. Li, A. J. Koleske, and J. K. Burkhardt. 2008. The c-Abl tyrosine kinase regulates actin remodeling at the immune synapse. Blood 112: 111-119. https://doi.org/10.1182/blood-2007-10-118232
  69. Uruno, T., P. Zhang, J. Liu, J. J. Hao, X. Zhan. 2003. Haematopoietic lineage cell-specific protein 1 (HS1) promotes actin-related protein (Arp) 2/3 complex-mediated actin polymerization. Biochem. J. 371: 485-493. https://doi.org/10.1042/BJ20021791
  70. Yamanashi, Y., M. Okada, T. Semba, T. Yamori, H. Umemori, S. Tsunasawa, K. Toyoshima, D. Kitamura, T. Watanabe, and T. Yamamoto. 1993. Identification of HS1 protein as a major substrate of protein-tyrosine kinase(s) upon B-cell antigen receptor-mediated signaling. Proc. Natl. Acad. Sci. U. S. A. 90: 3631-3635. https://doi.org/10.1073/pnas.90.8.3631
  71. Yamanashi, Y., T. Fukuda, H. Nishizumi, T. Inazu, K. Higashi, D. Kitamura, T. Ishida, H. Yamamura, T. Watanabe, and T. Yamamoto. 1997. Role of tyrosine phosphorylation of HS1 in B cell antigen receptor-mediated apoptosis. J. Exp. Med. 185: 1387-1392. https://doi.org/10.1084/jem.185.7.1387
  72. Scielzo, C., M. T. Bertilaccio, G. Simonetti, A. Dagklis, E. ten Hacken, C. Fazi, M. Muzio, V. Caiolfa, D. Kitamura, U. Restuccia, A. Bachi, M. Rocchi, M. Ponzoni, P. Ghia, and F. Caligaris-Cappio. 2010. HS1 has a central role in the trafficking and homing of leukemic B cells. Blood 116: 3537-3546. https://doi.org/10.1182/blood-2009-12-258814
  73. Butrym, A., M. Majewski, J. Dzietczenia, K. Kuliczkowski, and G. Mazur. 2012. High expression of hematopoietic cell specific Lyn substrate-1 (HS1) predicts poor survival of B-cell chronic lymphocytic leukemia patients. Leuk. Res. 36:876-880. https://doi.org/10.1016/j.leukres.2012.01.017
  74. Dehring, D. A., F. Clarke, B. G. Ricart, Y. Huang, T. S. Gomez, E. K. Williamson, D. A. Hammer, D. D. Billadeau, Y. Argon, and J. K. Burkhardt. 2011. Hematopoietic lineage cell-specific protein 1 functions in concert with the Wiskott- Aldrich syndrome protein to promote podosome array organization and chemotaxis in dendritic cells. J. Immunol.186: 4805-4818. https://doi.org/10.4049/jimmunol.1003102
  75. Huang, Y., C. Biswas, D. A. Klos Dehring, U. Sriram, E. K. Williamson, S. Li, F. Clarke, S. Gallucci, Y. Argon, and J. K. Burkhardt. 2011. The actin regulatory protein HS1 is required for antigen uptake and presentation by dendritic cells. J. Immunol. 187: 5952-5963. https://doi.org/10.4049/jimmunol.1100870
  76. Derry, J. M., H. D. Ochs, and U. Francke. 1994. Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell79: following 922.
  77. Sullivan, K. E., C. A. Mullen, R. M. Blaese, and J. A. Winkelstein. 1994. A multiinstitutional survey of the Wiskott- Aldrich syndrome. J. Pediatr. 125: 876-885. https://doi.org/10.1016/S0022-3476(05)82002-5
  78. Imai, K., T. Morio, Y. Zhu, Y. Jin, S. Itoh, M. Kajiwara, J. Yata, S. Mizutani, H. D. Ochs, and S. Nonoyama. 2004. Clinical course of patients with WASP gene mutations. Blood103: 456-464. https://doi.org/10.1182/blood-2003-05-1480
  79. Thrasher, A. J., and S. O. Burns. 2010. WASP: a key immunological multitasker. Nat. Rev. Immunol. 10: 182-192. https://doi.org/10.1038/nri2724
  80. Linardopoulou, E. V., S. S. Parghi, C. Friedman, G. E. Osborn, S. M. Parkhurst, and B. J. Trask. 2007. Human subtelomeric WASH genes encode a new subclass of the WASP family. PLoS Genet. 3: e237. https://doi.org/10.1371/journal.pgen.0030237
  81. Campellone, K. G., N. J. Webb, E. A. Znameroski, and M. D. Welch. 2008. WHAMM is an Arp2/3 complex activator that binds microtubules and functions in ER to Golgi transport. Cell 134: 148-161. https://doi.org/10.1016/j.cell.2008.05.032
  82. Blanchoin, L., K. J. Amann, H. N. Higgs, J. B. Marchand, D. A. Kaiser, and T. D. Pollard. 2000. Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature 404: 1007-1011. https://doi.org/10.1038/35010008
  83. Miki, H., and T. Takenawa. 2003. Regulation of actin dynamics by WASP family proteins. J. Biochem. 134: 309-313. https://doi.org/10.1093/jb/mvg146
  84. Takenawa, T., and S. Suetsugu. 2007. The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8: 37-48. https://doi.org/10.1038/nrm2069
  85. Kim, A. S., L. T. Kakalis, N. Abdul-Manan, G. A. Liu, and M. K. Rosen. 2000. Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404:151-158. https://doi.org/10.1038/35004513
  86. Chou, H. C., I. M. Antón, M. R. Holt, C. Curcio, S. Lanzardo, A. Worth, S. Burns, A. J. Thrasher, G. E. Jones, and Y. Calle. 2006. WIP regulates the stability and localization of WASP to podosomes in migrating dendritic cells. Curr. Biol. 16: 2337-2344. https://doi.org/10.1016/j.cub.2006.10.037
  87. de la Fuente, M. A., Y. Sasahara, M. Calamito, I. M. Antón, A. Elkhal, M. D. Gallego, K. Suresh, K. Siminovitch, H. D. Ochs, K. C. Anderson, F. S. Rosen, R. S. Geha, and N. Ramesh. 2007. WIP is a chaperone for Wiskott-Aldrich syndrome protein (WASP). Proc. Natl. Acad. Sci. U. S. A. 104:926-931. https://doi.org/10.1073/pnas.0610275104
  88. Ramesh, N., and R. Geha. 2009. Recent advances in the biology of WASP and WIP. Immunol. Res. 44: 99-111. https://doi.org/10.1007/s12026-008-8086-1
  89. Le Bras, S., M. Massaad, S. Koduru, L. Kumar, M. K. Oyoshi, J. Hartwig, and R. S. Geha. 2008. WIP is critical for T cell responsiveness to IL-2. Proc Natl. Acad. Sci. U. S. A. 106:7519-7524.
  90. Abdul-Manan, N., B. Aghazadeh, G. A. Liu, A. Majumdar, O. Ouerfelli, K. A. Siminovitch, and M. K. Rosen. 1999. Structure of Cdc42 in complex with the GTPase-binding domain of the 'Wiskott-Aldrich syndrome' protein. Nature 399:379-383. https://doi.org/10.1038/20726
  91. Tomasevic, N., Z. Jia, A. Russell, T. Fujii, J. J. Hartman, S. Clancy, M. Wang, C. Beraud, K. W. Wood, and R. Sakowicz. 2007. Differential regulation of WASP and NWASP by Cdc42, Rac1, Nck, and PI(4,5)P2. Biochemistry 46:3494-3502. https://doi.org/10.1021/bi062152y
  92. Pauker, M. H., B. Reicher, S. Fried, O. Perl, and M. Barda-Saad. 2011. Functional cooperation between the proteins Nck and ADAP is fundamental for actin reorganization. Mol. Cell Biol. 31: 2653-2666. https://doi.org/10.1128/MCB.01358-10
  93. Padrick, S. B., H. C. Cheng, A. M. Ismail, S. C. Panchal, L. K. Doolittle, S. Kim, B. M. Skehan, J. Umetani, C. A. Brautigam, J. M. Leong, and M. K. Rosen. 2008. Hierarchical regulation of WASP/WAVE proteins. Mol. Cell 32: 426-438. https://doi.org/10.1016/j.molcel.2008.10.012
  94. Badour, K., J. Zhang, F. Shi, Y. Leng, M. Collins, and K. A. Siminovitch. 2004. Fyn and PTP-PEST-mediated regulation of Wiskott-Aldrich syndrome protein (WASp) tyrosine phosphorylation is required for coupling T cell antigen receptor engagement to WASp effector function and T cell activation. J. Exp. Med. 199: 99-112. https://doi.org/10.1084/jem.20030976
  95. Snapper, S. B., F. S. Rosen, E. Mizoguchi, P. Cohen, W. Khan, C. H. Liu, T. L. Hagemann, S. P. Kwan, R. Ferrini, L. Davidson, A. K. Bhan, and F. W. Alt. 1998. Wiskott- Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity 9: 81-91. https://doi.org/10.1016/S1074-7613(00)80590-7
  96. Zhang, J., A. Shehabeldin, L. A. da Cruz, J. Butler, A. K. Somani, M. McGavin, I. Kozieradzki, A. O. dos Santos, A. Nagy, S. Grinstein, J. M. Penninger, and K. A. Siminovitch. 1999. Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J. Exp. Med. 190: 1329-1342. https://doi.org/10.1084/jem.190.9.1329
  97. Westerberg, L., M. Larsson, S. J. Hardy, C. Fernández, A. J. Thrasher, and E. Severinson. 2005. Wiskott-Aldrich syndrome protein deficiency leads to reduced B-cell adhesion, migration, and homing, and a delayed humoral immune response. Blood 105: 1144-1152.
  98. Maillard, M. H., V. Cotta-de-Almeida, F. Takeshima, D. D. Nguyen, P. Michetti, C. Nagler, A. K. Bhan, and S. B. Snapper. 2007. The Wiskott-Aldrich syndrome protein is required for the function of CD4(+)CD25(+)Foxp3(+) regulatory T cells. J. Exp. Med. 204: 381-391. https://doi.org/10.1084/jem.20061338
  99. Gallego, M. D., M. Santamaría, J. Peña, and I. J. Molina. 1997. Defective actin reorganization and polymerization of Wiskott-Aldrich T cells in response to CD3-mediated stimulation. Blood 90: 3089-3097.
  100. Becker-Herman, S., A. Meyer-Bahlburg, M. A. Schwartz, S. W. Jackson, K. L. Hudkins, C. Liu, B. D. Sather, S. Khim, D. Liggitt, W. Song, G. J. Silverman, C. E. Alpers, and D. J. Rawlings. 2011. WASp-deficient B cells play a critical, cell-intrinsic role in triggering autoimmunity. J. Exp. Med.208: 2033-2042. https://doi.org/10.1084/jem.20110200
  101. Bouma, G., A. Mendoza-Naranjo, M. P. Blundell, E. de Falco, K. L. Parsley, S. O. Burns, and A. J. Thrasher. 2011. Cytoskeletal remodeling mediated by WASp in dendritic cells is necessary for normal immune synapse formation and T-cell priming. Blood 118: 2492-2501. https://doi.org/10.1182/blood-2011-03-340265
  102. Suetsugu, S., H. Miki, and T. Takenawa. 1999. Identification of two human WAVE/SCAR homologues as general actin regulatory molecules which associate with the Arp2/3 complex. Biochem. Biophys. Res. Commun. 260: 296-302. https://doi.org/10.1006/bbrc.1999.0894
  103. Ridley, A. J. 2011. Life at the leading edge. Cell 145: 1012-1022. https://doi.org/10.1016/j.cell.2011.06.010
  104. Takenawa, T., and H. Miki. 2001. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114: 1801-1809.
  105. Eden, S., R. Rohatgi, A. V. Podtelejnikov, M. Mann, and M. W. Kirschner. 2002. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418: 790-793. https://doi.org/10.1038/nature00859
  106. Steffen, A., K. Rottner, J. Ehinger, M. Innocenti, G. Scita, J. Wehland, and T. E. Stradal. 2004. Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBOJ. 23: 749-759. https://doi.org/10.1038/sj.emboj.7600084
  107. Leng, Y., J. Zhang, K. Badour, E. Arpaia, S. Freeman, P. Cheung, M. Siu, and K. Siminovitch. 2005. Abelson-interactor- 1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc. Natl. Acad. Sci. U. S. A. 102: 1098-1103. https://doi.org/10.1073/pnas.0409120102
  108. Nolz, J. C., T. S. Gomez, P. Zhu, S. Li, R. B. Medeiros, Y. Shimizu, J. K. Burkhardt, B. D. Freedman, and D. D. Billadeau. 2006. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr. Biol. 16: 24-34. https://doi.org/10.1016/j.cub.2005.11.036
  109. Orange, J. S., S. Roy-Ghanta, E. M. Mace, S. Maru, G. D. Rak, K. B. Sanborn, A. Fasth, R. Saltzman, A. Paisley, L. Monaco-Shawver, P. P. Banerjee, and R. Pandey. 2011. IL-2 induces a WAVE2-dependent pathway for actin reorganization that enables WASp-independent human NK cell function. J. Clin. Invest. 121: 1535-1548. https://doi.org/10.1172/JCI44862
  110. Yan, C., N. Martinez-Quiles, S. Eden, T. Shibata, F. Takeshima, R. Shinkura, Y. Fujiwara, R. Bronson, S. B. Snapper, M. W. Kirschner, R. Geha, F. S. Rosen, and F. W. Alt. 2003. WAVE2 deficiency reveals distinct roles in embryogenesis and Rac-mediated actin-based motility. EMBO J.22: 3602-3612. https://doi.org/10.1093/emboj/cdg350
  111. Yamazaki, D., S. Suetsugu, H. Miki, Y. Kataoka, S. Nishikawa, T. Fujiwara, N. Yoshida, and T. Takenawa. 2003. WAVE2 is required for directed cell migration and cardiovascular development. Nature 424: 452-456. https://doi.org/10.1038/nature01770
  112. Gomez, T. S., and D. D. Billadeau. 2009. A FAM21-containing WASH complex regulates retromer-dependent sorting.Dev. Cell 17: 699-711.
  113. Duleh, S. N., and M. D. Welch. 2010. WASH and the Arp2/3 complex regulate endosome shape and trafficking. Cytoskeleton (Hoboken) 67: 193-206.
  114. Liu, R., M. T. Abreu-Blanco, K. C. Barry, E. V. Linardopoulou, G. E. Osborn, and S. M. Parkhurst. 2009. Wash functions downstream of Rho and links linear and branched actin nucleation factors. Development 136: 2849-2860. https://doi.org/10.1242/dev.035246
  115. Jia, D., T. S. Gomez, Z. Metlagel, J. Umetani, Z. Otwinowski, M. K. Rosen, and D. D. Billadeau. 2010. WASH and WAVE actin regulators of the Wiskott-Aldrich syndrome protein (WASP) family are controlled by analogous structurally related complexes. Proc. Natl. Acad. Sci. U. S. A. 107: 10442-10447. https://doi.org/10.1073/pnas.0913293107
  116. Kelleher, J. F., S. J. Atkinson, T. D. Pollard. 1995. Sequences, structural models, and cellular localization of the actin-related proteins Arp2 and Arp3 from Acanthamoeba. J. Cell Biol. 131: 385-397. https://doi.org/10.1083/jcb.131.2.385
  117. Goley, E. D., and M. D. Welch. 2006. The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol.7: 713-726. https://doi.org/10.1038/nrm2026
  118. Reicher, B., and M. Barda-Saad. 2010. Multiple pathways leading from the T-cell antigen receptor to the actin cytoskeleton network. FEBS Lett. 584: 4858-4864. https://doi.org/10.1016/j.febslet.2010.09.002
  119. Hotulainen, P., E. Paunola, M. K. Vartiainen, P. Lappalainen. 2005. Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells. Mol. Biol. Cell 16: 649-664.
  120. Lee, K. H., S. C. Meuer, and Y. Samstag. 2000. Cofilin: a missing link between T cell co-stimulation and rearrangement of the actin cytoskeleton. Eur. J. Immunol. 30: 892-899. https://doi.org/10.1002/1521-4141(200003)30:3<892::AID-IMMU892>3.0.CO;2-U
  121. Gomez, T. S., M. J. Hamann, S. McCarney, D. N. Savoy, C. M. Lubking, M. P. Heldebrant, C. M. Labno, D. J. McKean, M. A. McNiven, J. K. Burkhardt, and D. D. Billadeau. 2005. Dynamin 2 regulates T cell activation by controlling actin polymerization at the immunological synapse. Nat. Immunol. 6: 261-270. https://doi.org/10.1038/ni1168
  122. Dustin, M. L., M. W. Olszowy, A. D. Holdorf, J. Li, S. Bromley, N. Desai, P. Widder, F. Rosenberger, P. A. van der Merwe, P. M. Allen, and A. S. Shaw. 1998. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell 94: 667-677 https://doi.org/10.1016/S0092-8674(00)81608-6
  123. Hogg, N., I. Patzak, and F. Willenbrock. 2011. The insider's guide to leukocyte integrin signalling and function. Nat. Rev. Immunol. 11: 416-426. https://doi.org/10.1038/nri2986
  124. Calabia-Linares, C., J. Robles-Valero, H. de la Fuente, M. Perez-Martinez, N. Martín-Cofreces, M. Alfonso-Perez, C. Gutierrez-Vazquez, M. Mittelbrunn, S. Ibiza, F. R. Urbano- Olmos, C. Aguado-Ballano, C. O. Sanchez-Sorzano, F. Sanchez-Madrid, and E. Veiga. 2011. Endosomal clathrin drives actin accumulation at the immunological synapse. J. Cell Sci. 124: 820-830. https://doi.org/10.1242/jcs.078832
  125. Wang, C., S. C. Morley, D. Donermeyer, I. Peng, W. P. Lee, J. Devoss, D. M. Danilenko, Z. Lin, J. Zhang, J. Zhou, P. M. Allen, and E. J. Brown. 2010. Actin-bundling protein L-plastin regulates T cell activation. J. Immunol. 185: 7487-7497. https://doi.org/10.4049/jimmunol.1001424
  126. Wabnitz, G. H., P. Lohneis, H. Kirchgessner, B. Jahraus, S. Gottwald, M. Konstandin, M. Klemke, and Y. Samstag. 2010. Sustained LFA-1 cluster formation in the immune synapse requires the combined activities of L-plastin and calmodulin. Eur. J. Immunol. 40: 2437-2449. https://doi.org/10.1002/eji.201040345
  127. Faroudi, M., R. Zaru, P. Paulet, S. Müller, and S. Valitutti. 2003. Cutting edge: T lymphocyte activation by repeated immunological synapse formation and intermittent signaling. J. Immunol. 171: 1128-1132. https://doi.org/10.4049/jimmunol.171.3.1128
  128. Cernuda-Morollón, E., J. Millán, M. Shipman, F. M. Marelli- Berg, and A. J. Ridley. 2010. Rac activation by the T-cell receptor inhibits T cell migration. PLoS One 5: e12393. https://doi.org/10.1371/journal.pone.0012393
  129. Alarcón, B., D. Mestre, and N. Martínez-Martín. 2011. The immunological synapse: a cause or consequence of T-cell receptor triggering? Immunology 133: 420-425. https://doi.org/10.1111/j.1365-2567.2011.03458.x
  130. Hashimoto-Tane, A., T. Yokosuka, K. Sakata-Sogawa, M. Sakuma, C. Ishihara, M. Tokunaga, and T. Saito. 2011. Dynein-driven transport of T cell receptor microclusters regulates immune synapse formation and T cell activation. Immunity 34: 919-931. https://doi.org/10.1016/j.immuni.2011.05.012
  131. Varma, R., G. Campi, T. Yokosuka, T. Saito, and M. L. Dustin. 2006. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25: 117-127. https://doi.org/10.1016/j.immuni.2006.04.010
  132. Dustin, M. L. 2008. T-cell activation through immunological synapses and kinapses. Immunol. Rev. 221: 77-89. https://doi.org/10.1111/j.1600-065X.2008.00589.x

피인용 문헌

  1. Technical Advance: Actin CytoFRET, a novel FRET flow cytometry method for detection of actin dynamics in resting and activated T cell vol.94, pp.3, 2012, https://doi.org/10.1189/jlb.0113022
  2. LZTFL1 Upregulated by All-Trans Retinoic Acid during CD4+ T Cell Activation Enhances IL-5 Production vol.196, pp.3, 2012, https://doi.org/10.4049/jimmunol.1500719
  3. Transgelin-2 in B-Cells Controls T-Cell Activation by Stabilizing T Cell - B Cell Conjugates vol.11, pp.5, 2016, https://doi.org/10.1371/journal.pone.0156429
  4. Actin stabilizer TAGLN2 potentiates adoptive T cell therapy by boosting the inside-out costimulation via lymphocyte function-associated antigen-1 vol.7, pp.12, 2018, https://doi.org/10.1080/2162402x.2018.1500674
  5. The actin remodeling protein cofilin is crucial for thymic αβ but not γδ T-cell development vol.16, pp.7, 2012, https://doi.org/10.1371/journal.pbio.2005380
  6. TAGLN2 polymerizes G-actin in a low ionic state but blocks Arp2/3-nucleated actin branching in physiological conditions vol.8, pp.None, 2018, https://doi.org/10.1038/s41598-018-23816-2
  7. Actin Cytoskeleton Straddling the Immunological Synapse between Cytotoxic Lymphocytes and Cancer Cells vol.8, pp.5, 2019, https://doi.org/10.3390/cells8050463
  8. Transgelin-2: A Double-Edged Sword in Immunity and Cancer Metastasis vol.9, pp.None, 2012, https://doi.org/10.3389/fcell.2021.606149