Independent and cooperative roles of adaptor molecules in proximal signaling during FcεRI-mediated mast cell activation

Molecular and Cellular Biology

Volumn 30, Issue 17, 2010, Pages 4188-4196

  Kambayashi, Taku ^a,b   Okumura, Mariko ^a,b   Baker, Rebecca G ^a   Hsu, Chih Jung ^b   Baumgart, Tobias ^b   Zhang, Weiguo ^c   Koretzky, Gary A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC EPSILON RECEPTOR I; IMMUNOGLOBULIN E RECEPTOR; LAT PROTEIN; LAT1 PROTEIN; LAT2 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEIN; SRC HOMOLOGY 2 DOMAIN CONTAINING LEUKOCYTE PHOSPHOPROTEIN OF 76; UNCLASSIFIED DRUG; AMINO ACID TRANSPORTER; CALCIUM; CD98 ANTIGEN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SLC7A7 PROTEIN, MOUSE; SLC7A8 PROTEIN, MOUSE; SLP 76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; SLP-76 SIGNAL TRANSDUCING ADAPTOR PROTEINS;

ALLERGY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CALCIUM TRANSPORT; CELL ACTIVATION; CONTROLLED STUDY; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; GENE DELETION; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; ANTIGENS, CD98 LIGHT CHAINS; CALCIUM; CELLS, CULTURED; GENE DELETION; MAST CELLS; MICE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTORS, IGE;

EID: 77956645610     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00305-10     Document Type: Article

References (48)

1. Abraham, R. T., and A. Weiss. 2004. Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat. Rev. Immunol. 4:301-308.
2. Baker, R. G., C. J. Hsu, D. Lee, M. S. Jordan, J. S. Maltzman, D. A. Hammer, T. Baumgart, and G. A. Koretzky. 2009. The adapter protein SLP-76 mediates "outside-in" integrin signaling and function in T cells. Mol. Cell. Biol. 29:5578-5589.
3. Boerth, N. J., J. J. Sadler, D. E. Bauer, J. L. Clements, S. M. Gheith, and G. A. Koretzky. 2000. Recruitment of SLP-76 to the membrane and glycolipid-enriched membrane microdomains replaces the requirement for linker for activation of T cells in T cell receptor signaling. J. Exp. Med. 192:1047-1058.
4. Brdicka, T., M. Imrich, P. Angelisova, N. Brdickova, O. Horvath, J. Spicka, I. Hilgert, P. Luskova, P. Draber, P. Novak, N. Engels, J. Wienands, L. Simeoni, J. Osterreicher, E. Aguado, M. Malissen, B. Schraven, and V. Horejsi. 2002. Non-T cell activation linker (NTAL): a transmembrane adaptor protein involved in immunoreceptor signaling. J. Exp. Med. 196:1617-1626.
5. Bubeck Wardenburg, J., C. Fu, J. K. Jackman, H. Flotow, S. E. Wilkinson, D. H. Williams, R. Johnson, G. Kong, A. C. Chan, and P. R. Findell. 1996. Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J. Biol. Chem. 271:19641-19644.
6. Chiesa, S., M. Mingueneau, N. Fuseri, B. Malissen, D. H. Raulet, M. Malissen, E. Vivier, and E. Tomasello. 2006. Multiplicity and plasticity of natural killer cell signaling pathways. Blood 107:2364-2372. (Pubitemid 43345556)
7. Clements, J. L., S. E. Ross-Barta, L. T. Tygrett, T. J. Waldschmidt, and G. A. Koretzky. 1998. SLP-76 expression is restricted to hemopoietic cells of monocyte, granulocyte, and T lymphocyte lineage and is regulated during T cell maturation and activation. J. Immunol. 161:3880-3889.
8. Ebinu, J. O., S. L. Stang, C. Teixeira, D. A. Bottorff, J. Hooton, P. M. Blumberg, M. Barry, R. C. Bleakley, H. L. Ostergaard, and J. C. Stone. 2000. RasGRP links T-cell receptor signaling to Ras. Blood 95:3199-3203.
9. El-Hillal, O., T. Kurosaki, H. Yamamura, J. P. Kinet, and A. M. Scharenberg. 1997. syk kinase activation by a src kinase-initiated activation loop phosphorylation chain reaction. Proc. Natl. Acad. Sci. U. S. A. 94:1919-1924.
10. Finco, T. S., T. Kadlecek, W. Zhang, L. E. Samelson, and A. Weiss. 1998. LAT1 is required for TCR-mediated activation of PLCgamma1 and the Ras pathway. Immunity 9:617-626.
11. Gomez, G., C. Gonzalez-Espinosa, S. Odom, G. Baez, M. E. Cid, J. J. Ryan, and J. Rivera. 2005. Impaired FcepsilonRI-dependent gene expression and defective eicosanoid and cytokine production as a consequence of Fyn deficiency in mast cells. J. Immunol. 175:7602-7610. (Pubitemid 41713460)
12. Gonzalez-Espinosa, C., S. Odom, A. Olivera, J. P. Hobson, M. E. Martinez, A. Oliveira-Dos-Santos, L. Barra, S. Spiegel, J. M. Penninger, and J. Rivera. 2003. Preferential signaling and induction of allergy-promoting lymphokines upon weak stimulation of the high affinity IgE receptor on mast cells. J. Exp. Med. 197:1453-1465.
13. Gould, H. J., and B. J. Sutton. 2008. IgE in allergy and asthma today. Nat. Rev. Immunol. 8:205-217.
14. Hines, C. 2002. The diverse effects of mast cell mediators. Clin. Rev. Allergy Immunol. 22:149-160.
15. Iwaki, S., B. M. Jensen, and A. M. Gilfillan. 2007. Ntal/Lab/LAT2. Int. J. Biochem. Cell Biol. 39:868-873.
16. Iwaki, S., J. Spicka, C. Tkaczyk, B. M. Jensen, Y. Furumoto, N. Charles, M. Kovarova, J. Rivera, V. Horejsi, D. D. Metcalfe, and A. M. Gilfillan. 2008. Kit- and Fc epsilonRI-induced differential phosphorylation of the transmembrane adaptor molecule NTAL/LAB/LAT2 allows flexibility in its scaffolding function in mast cells. Cell Signal. 20:195-205.
17. Jabril-Cuenod, B., C. Zhang, A. M. Scharenberg, R. Paolini, R. Numerof, M. A. Beaven, and J. P. Kinet. 1996. Syk-dependent phosphorylation of Shc. A potential link between FcepsilonRI and the Ras/mitogen-activated protein kinase signaling pathway through SOS and Grb2. J. Biol. Chem. 271:16268-16272.
18. Janssen, E., M. Zhu, B. Craven, and W. Zhang. 2004. Linker for activation of B cells: a functional equivalent of a mutant linker for activation of T cells deficient in phospholipase C-gamma1 binding. J. Immunol. 172:6810-6819. (Pubitemid 38669119)
19. Jouvin, M. H., M. Adamczewski, R. Numerof, O. Letourneur, A. Valle, and J. P. Kinet. 1994. Differential control of the tyrosine kinases Lyn and Syk by the two signaling chains of the high affinity immunoglobulin E receptor. J. Biol. Chem. 269:5918-5925.
20. Kambayashi, T., J. D. Baranski, R. G. Baker, T. Zou, E. J. Allenspach, J. E. Shoag, P. L. Jones, and G. A. Koretzky. 2008. Indirect involvement of allergen-captured mast cells in antigen presentation. Blood 111:1489-1496.
21. Kambayashi, T., D. F. Larosa, M. A. Silverman, and G. A. Koretzky. 2009. Cooperation of adapter molecules in proximal signaling cascades during allergic inflammation. Immunol. Rev. 232:99-114.
22. Kettner, A., V. Pivniouk, L. Kumar, H. Falet, J. S. Lee, R. Mulligan, and R. S. Geha. 2003. Structural requirements of SLP-76 in signaling via the high-affinity immunoglobulin E receptor (Fc epsilon RI) in mast cells. Mol. Cell. Biol. 23:2395-2406.
23. Koonpaew, S., E. Janssen, M. Zhu, and W. Zhang. 2004. The importance of three membrane-distal tyrosines in the adaptor protein NTAL/LAB. J. Biol. Chem. 279:11229-11235.
24. 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 LAT1 adaptors. Curr. Biol. 9:67-75.
25. Malbec, O., M. Malissen, I. Isnardi, R. Lesourne, A. M. Mura, W. H. Fridman, B. Malissen, and M. Daeron. 2004. Linker for activation of T cells integrates positive and negative signaling in mast cells. J. Immunol. 173:5086-5094. (Pubitemid 39387791)
26. Maltzman, J. S., L. Kovoor, J. L. Clements, and G. A. Koretzky. 2005. Conditional deletion reveals a cell-autonomous requirement of SLP-76 for thymocyte selection. J. Exp. Med. 202:893-900.
27. Myung, P. S., G. S. Derimanov, M. S. Jordan, J. A. Punt, Q. H. Liu, B. A. Judd, E. E. Meyers, C. D. Sigmund, B. D. Freedman, and G. A. Koretzky. 2001. Differential requirement for SLP-76 domains in T cell development and function. Immunity 15:1011-1026.
28. Parravicini, V., M. Gadina, M. Kovarova, S. Odom, C. Gonzalez-Espinosa, Y. Furumoto, S. Saitoh, L. E. Samelson, J. J. O'Shea, and J. Rivera. 2002. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3:741-748.
29. Pivniouk, V. I., T. R. Martin, J. M. Lu-Kuo, H. R. Katz, H. C. Oettgen, and R. S. Geha. 1999. SLP-76 deficiency impairs signaling via the high-affinity IgE receptor in mast cells. J. Clin. Invest. 103:1737-1743.
30. Pribluda, V. S., C. Pribluda, and H. Metzger. 1994. Transphosphorylation as the mechanism by which the high-affinity receptor for IgE is phosphorylated upon aggregation. Proc. Natl. Acad. Sci. U. S. A. 91:11246-11250.
31. Saitoh, S., R. Arudchandran, T. S. Manetz, W. Zhang, C. L. Sommers, P. E. Love, J. Rivera, and L. E. Samelson. 2000. LAT1 is essential for Fc(epsilon) RI-mediated mast cell activation. Immunity 12:525-535.
32. Saitoh, S., S. Odom, G. Gomez, C. L. Sommers, H. A. Young, J. Rivera, and L. E. Samelson. 2003. The four distal tyrosines are required for LAT1- dependent signaling in FcepsilonRI-mediated mast cell activation. J. Exp. Med. 198:831-843.
33. Samelson, L. E. 2002. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu. Rev. Immunol. 20:371-394.
34. Shiue, L., J. Green, O. M. Green, J. L. Karas, J. P. Morgenstern, M. K. Ram, M. K. Taylor, M. J. Zoller, L. D. Zydowsky, J. B. Bolen, et al. 1995. Interaction of p72syk with the gamma and beta subunits of the high-affinity receptor for immunoglobulin E, Fc epsilon RI. Mol. Cell. Biol. 15:272-281.
35. Silverman, M. A., J. Shoag, J. Wu, and G. A. Koretzky. 2006. Disruption of SLP-76 interaction with Gads inhibits dynamic clustering of SLP-76 and FcepsilonRI signaling in mast cells. Mol. Cell. Biol. 26:1826-1838.
36. Singer, A. L., S. C. Bunnell, A. E. Obstfeld, M. S. Jordan, J. N. Wu, P. S. Myung, L. E. Samelson, and G. A. Koretzky. 2004. Roles of the proline-rich domain in SLP-76 subcellular localization and T cell function. J. Biol. Chem. 279:15481-15490.
37. Turner, H., and J. P. Kinet. 1999. Signalling through the high-affinity IgE receptor Fc epsilonRI. Nature 402:B24-B30.
38. Utting, O., B. J. Sedgmen, T. H. Watts, X. Shi, R. Rottapel, A. Iulianella, D. Lohnes, and A. Veillette. 2004. Immune functions in mice lacking Clnk, an SLP-76-related adaptor expressed in a subset of immune cells. Mol. Cell. Biol. 24:6067-6075.
39. Vig, M., and J. P. Kinet. 2007. The long and arduous road to CRAC. Cell Calcium 42:157-162.
40. Volna, P., P. Lebduska, L. Draberova, S. Simova, P. Heneberg, M. Boubelik, V. Bugajev, B. Malissen, B. S. Wilson, V. Horejsi, M. Malissen, and P. Draber. 2004. Negative regulation of mast cell signaling and function by the adaptor LAB/NTAL. J. Exp. Med. 200:1001-1013.
41. Wu, J. N., M. S. Jordan, M. A. Silverman, E. J. Peterson, and G. A. Koretzky. 2004. Differential requirement for adapter proteins Src homology 2 domain-containing leukocyte phosphoprotein of 76 kDa and adhesion- and degranulation- promoting adapter protein in FcepsilonRI signaling and mast cell function. J. Immunol. 172:6768-6774.
42. Yablonski, D., M. R. Kuhne, T. Kadlecek, and A. Weiss. 1998. Uncoupling of nonreceptor tyrosine kinases from PLC-gamma1 in an SLP-76-deficient T cell. Science 281:413-416. (Pubitemid 28340785)
43. Zhang, W., J. Sloan-Lancaster, J. Kitchen, R. P. Trible, and L. E. Samelson. 1998. LAT1: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92:83-92.
44. Zhang, W., C. L. Sommers, D. N. Burshtyn, C. C. Stebbins, J. B. DeJarnette, R. P. Trible, A. Grinberg, H. C. Tsay, H. M. Jacobs, C. M. Kessler, E. O. Long, P. E. Love, and L. E. Samelson. 1999. Essential role of LAT1 in T cell development. Immunity 10:323-332.
45. Zhang, W., R. P. Trible, M. Zhu, S. K. Liu, C. J. McGlade, and L. E. Samelson. 2000. Association of Grb2, Gads, and phospholipase C-gamma 1 with phosphorylated LAT1 tyrosine residues. Effect of LAT1 tyrosine mutations on T cell antigen receptor-mediated signaling. J. Biol. Chem. 275:23355-23361.
46. Zhu, M., S. Koonpaew, Y. Liu, S. Shen, T. Denning, I. Dzhagalov, I. Rhee, and W. Zhang. 2006. Negative regulation of T cell activation and autoimmunity by the transmembrane adaptor protein LAB. Immunity 25:757-768. (Pubitemid 46107283)
47. Zhu, M., Y. Liu, S. Koonpaew, O. Granillo, and W. Zhang. 2004. Positive and negative regulation of FcepsilonRI-mediated signaling by the adaptor protein LAB/NTAL. J. Exp. Med. 200:991-1000.
48. Zhu, M., I. Rhee, Y. Liu, and W. Zhang. 2006. Negative regulation of Fc epsilonRI-mediated signaling and mast cell function by the adaptor protein LAX. J. Biol. Chem. 281:18408-18413.