Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance

Nature Immunology

Volumn 9, Issue 4, 2008, Pages 432-443

  Oh hora, Masatsugu ^a   Yamashita, Megumi ^b   Hogan, Patrick G ^a   Sharma, Sonia ^a   Lamperti, Ed ^a   Chung, Woo ^b   Prakriya, Murali ^b   Feske, Stefan ^a,c   Rao, Anjana ^a  

^a CENTER FOR BLOOD RESEARCH   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CYTOKINE; MEMBRANE PROTEIN; PROTEIN STIM1; PROTEIN STIM2; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MATURATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOPLASMIC RETICULUM; FIBROBLAST; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CALCIUM; CELL LINE; CELL LINE, TRANSFORMED; CELLS, CULTURED; ENDOPLASMIC RETICULUM; HUMANS; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; T-LYMPHOCYTES, REGULATORY;

EID: 40949123088     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1574     Document Type: Article

References (67)

1. Carafoli, E. The calcium-signalling saga: Tap water and protein crystals. Nat. Rev. Mol. Cell Biol. 4, 326-332 (2003).
2. 2+ entry. J. Cell Sci. 120, 1959-1965 (2007).
3. Lewis, R.S. The molecular choreography of a store-operated calcium channel. Nature 446, 284-287 (2007).
4. Hogan, P.G. & Rao, A. Dissecting ICRAC, a store-operated calcium current. Trends Biochem. Sci. 32, 235-245 (2007).
5. Feske, S. Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 7, 690-702 (2007).
6. Parekh, A.B. & Putney, J.W., Jr. Store-operated calcium channels. Physiol. Rev. 85, 757-810 (2005).
7. Prakriya, M. & Lewis, R.S. CRAC channels: Activation, permeation, and the search for a molecular identity. Cell Calcium 33, 311-321 (2003).
8. Hogan, P.G., Chen, L., Nardone, J. & Rao, A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17, 2205-2232 (2003).
9. 2+ channel function. J. Cell Biol. 169, 435-445 (2005).
10. 2+ influx. Curr. Biol. 15 1235-1241 (2005).
11. Feske, S. et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441, 179-185 (2006).
12. 2+ entry. Science 312, 1220-1223 (2006).
13. 2+ channel activity. Proc. Natl. Acad. Sci. USA 103, 9357-9362 (2006).
14. Gwack, Y. et al. Biochemical and functional characterization of Orai proteins. J. Biol. Chem. 282, 16232-16243 (2007).
15. Prakriya, M. et al. Orai1 is an essential pore subunit of the CRAC channel. Nature 443, 230-233 (2006).
16. Yeromin, A.V. et al. Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443, 226-229 (2006).
17. Vig, M. et al. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr. Biol. 16, 2073-2079 (2006).
18. Feske, S. et al. Severe combined immunodeficiency due to defective binding of the nuclear factor of activated T cells in T lymphocytes of two male siblings. Eur. J. Immunol. 26, 2119-2126 (1996).
19. Le Deist, F. et al. A primay T-cell immunodeficiency associated with defective transmembrane calcium influx. Blood 85, 1053-1062 (1995).
20. Partiseti, M. et al. The calcium current activated by T cell receptor and store depletion in human lymphocytes is absent in a primary immunodeficiency. J. Biol. Chem. 269, 32327-32335 (1994).
21. Feske, S., Giltnane, J., Dolmetsch, R., Staudt, L.M. & Rao, A. Gene regulation mediated by calcium signals in T lymphocytes. Nat. Immunol. 2, 316-324 (2001).
22. 2+/calcineurin signalling in cells of the immune system. Biochem. Biophys. Res. Commun. 311, 1117-1132 (2003).
23. Feske, S., Draeger, R., Peter, H.H., Eichmann, K. & Rao, A. The duration of nuclear residence of NFAT determines the pattern of cytokine expression in human SCID T cells. J. Immunol. 165, 297-305 (2000).
24. 2+ levels. Cell 131, 1327-1339 (2007).
25. 2+ entry. J. Biol. Chem. 281, 35855-35862 (2006).
26. 2+ sensory region of STIM1 and STIM2. Biochem. Biophys. Res. Commun. published online 31 December 2007 (doi:10.1016/j.bbrc.2007.12.129).
27. 2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J. Cell Biol. 174, 803-813 (2006).
28. 2+ store depletion. Proc. Natl. Acad. Sci. USA 104, 9301-9306 (2007).
29. Xu, P. et al. Aggregation of STIM1 underneath the plasma membrane induces clustering of Orai1. Biochem. Biophys. Res. Commun. 350 969-976 (2006).
30. 2+ entry: Local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J. Cell Biol. 174, 815-825 (2006).
31. 2+ store to the plasma membrane. Nature 437, 902-905 (2005).
32. + regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J. Exp. Med. 201, 723-735 (2005).
33. Fontenot, J.D., Rasmussen, J.P., Gavin, M.A. & Rudensky, A.Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6, 1142-1151 (2005).
34. + regulatory T cells in the absence of interleukin 2 signaling. Nat. Immunol. 6, 1152-1159 (2005).
35. Tone, Y. et al. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat. Immunol. 9, 194-202 (2007).
36. Bettelli, E., Dastrange, M. & Oukka, M. Foxp3 interacts with nuclear factor of activated T cells and NF-KB to repress cytokine gene expression and effector functions of T helper cells. Proc. Natl. Acad. Sci. USA 102, 5138-5143 (2005).
37. Wu, Y. et al. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 126, 375-387 (2006).
38. Marson, A. et al. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445, 931-935 (2007).
39. Williams, R.T. et al. Identification and characterization ofthe STIM (stromal interaction molecule) gene family: Coding for a novel class of transmembrane proteins. Biochem. J. 357, 673-685 (2001).
40. Schwenk, F., Baron, U. & Rajewsky, K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23, 5080-5081 (1995).
41. Lee, P.P. et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15, 763-774 (2001).
42. 2+ entry. Curr. Biol. 16, 1465-1470 (2006).
43. Vorndran, C., Minta, A. & Poenie, M. New fluorescent calcium indicators designed for cytosolic retention or measuring calcium near membranes. Biophys. J. 69, 2112-2124 (1995).
44. 3 receptors. J. Physiol. (Lond.) 536 3-19 (2001).
45. Sommers, C.L. et al. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 296, 2040-2043 (2002).
46. Aguado, E. et al. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science 296, 2036-2040 (2002).
47. Sommers, C,L. et al. Mutation of the phospholipase C-γ1-binding site of LAT affects both positive and negative thymocyte selection. J. Exp. Med. 201, 1125-1134 (2005).
48. + regulatory T cell development. J. Exp. Med. 203 119-129 (2006).
49. Baba, Y. et al. Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat. Immunol. 9, 81-88 (2008).
50. Macian, F. NFAT proteins: Key regulators of T-cell development and function. Nat. Rev. Immunol. 5, 472-484 (2005).
51. Fisher, G.H. et al. Dominant interfering Fas gene mutationis impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 81, 935-946 (1995).
52. Sayos, J. et al. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395, 462-469 (1998).
53. Marie, J.C., Liggitt, D. & Rudensky, A.Y. Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-beta receptor. Immunity 25, 441-454 (2006).
54. U, M.O., Sanjabi, S. & Flavell, R.A. Transforming growth factor-β controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 25, 455-471 (2006).
55. Sakaguchi, S. & Sakaguchi, N. Thymus and autoimmunity. Transplantation of the thymus from cyclosporin A-treated mice causes organ-specific autoimmune disease in athymic nude mice. J. Exp. Med. 167, 1479-1485 (1988).
56. Schmidt-Supprian, M. et al. Differential dependence of CD4+CD25+ regulatory and natural killer-like T cells on signals leading to NF-kappaB activation. Proc. Natt. Acad. Sci. USA 101, 4566-4571 (2004).
57. Zhang, W. et al. Association of Grb2, Gads, and phospholipase C-γ1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell angigen receptor-mediated signaling. J. Biol. Chem. 275, 23355-23361 (2000).
58. Lin, J. & Weiss, A. Identification of the minimal tyrosine residues required for linker for activation of T cell function. J. Biol. Chem. 276, 29588-29595 (2001).
59. Paz, P.E. et al. Mapping the Zap-70 phosphorylation sites on LAT (linker for activation of T cells) required for recruitment and activation of signalling proteins in T cells. Biochem. J. 356 461-471 (2001).
60. Ranger, A.M., Oukka, M., Rengarajan, J. & Glimcher, L.H. Inhibitory function of two NFAT family meMbers in lymphoid homeostasis and Th2 development. Immunity 9, 627-635 (1998).
61. + regulatory T cells. J. Exp. Med. 201, 181-187 (2005).
62. Neilson, J.R., Winslow, M.M., Hur, E.M. & Crabtree, G.R. Calcineurin B1 is essential for positive but not negative selection during thymocyte development. Immunity 20, 255-266 (2004).
63. Muljo, S.A. et al. Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 202, 261-269 (2005).
64. Rodriguez, C.I. et al. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet. 25, 139-140 (2000).
65. Ansel, K.M. et al. Deletion of a conserved II4 silencer impairs T helper type 1-mediated immunity. Nat. Immunol. 5, 1251-1259 (2004).
66. Ho, A.M., Jain, J., Rao, A. & Hogan, P.G. Expression of the transcription factor NFATp in a neuronal cell line and in the murine nervous system. J. Biol. Chem. 269, 28181-28186 (1994).
67. Prakriya, M. & Lewis, R.S. Regulation of CRAC channel activity by recruitment of silent channels to a high open-probability gating mode. J. Gen. Physiol. 128, 373-386 (2006).