Control of type I interferon-induced cell death by orai1-mediated calcium entry in T cells

Journal of Biological Chemistry

Volumn 287, Issue 5, 2012, Pages 3207-3216

  Yue, Chanyu ^a   Soboloff, Jonathan ^a   Gamero, Ana M ^a,b  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Kresge Hall ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC; APOPTOTIC EFFECTS; DOMINANT NEGATIVE; GENE TRANSCRIPTIONS; HUMAN T CELLS; INDUCED APOPTOSIS; INHIBITORY EFFECT; IONOMYCIN; JURKAT CELL; OVER-EXPRESSION; PHARMACOLOGICAL INHIBITION; REGULATORY EFFECTS; RESPONSE PATHWAYS; SIGNALING PATHWAYS; T CELL ACTIVATION; T CELLS; THAPSIGARGINS; TRANSCRIPTIONAL RESPONSE; TYPE I INTERFERONS;

ANTIBIOTICS; CELL CULTURE; CELL DEATH; CELL MEMBRANES; GENES; GLYCOPROTEINS; INTERFERONS; TISSUE; TRANSCRIPTION;

CALCIUM;

ALPHA INTERFERON; BETA INTERFERON; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IONOMYCIN; STROMAL INTERACTION MOLECULE 1; THAPSIGARGIN;

APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; WESTERN BLOTTING;

AMINO ACID SUBSTITUTION; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL DEATH; CELL LINE, TUMOR; HUMANS; INTERFERON-ALPHA; INTERFERON-BETA; MUTATION, MISSENSE; NF-KAPPA B; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 84856291077     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.269068     Document Type: Article

References (46)

1. Gimeno, R., Lee, C. K., Schindler, C., and Levy, D. E. (2005) Stat1 and Stat2 but not Stat3 arbitrate contradictory growth signals elicited by αβ interferon in T lymphocytes. Mol. Cell Biol. 25, 5456-5465 (Pubitemid 40853581)
2. Erickson, S., Sangfelt, O., Castro, J., Heyman, M., Einhorn, S., and Grandér, D. (1999) Interferon-α inhibits proliferation in human T lymphocytes by abrogation of interleukin 2-induced changes in cell cycle-regulatory proteins. Cell Growth Differ. 10, 575-582 (Pubitemid 29399065)
3. Dondi, E., Rogge, L., Lutfalla, G., Uzé, G., and Pellegrini, S. (2003) Down-modulation of responses to type I IFN upon T cell activation. J. Immunol. 170, 749-756 (Pubitemid 36070525)
4. Curtsinger, J. M., Valenzuela, J. O., Agarwal, P., Lins, D., and Mescher, M. F. (2005) Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174, 4465-4469
5. Dondi, E., Roué, G., Yuste, V. J., Susin, S. A., and Pellegrini, S. (2004)Adual role of IFN-α in the balance between proliferation and death of human CD4+ T lymphocytes during primary response. J. Immunol. 173, 3740-3747 (Pubitemid 39280735)
6. Rodriguez, B., Lederman, M. M., Jiang, W., Bazdar, D. A., Gàrate, K., Harding, C. V., and Sieg, S. F. (2006) Interferon-α differentially rescues CD4 and CD8 T cells from apoptosis in HIV infection. AIDS 20, 1379-1389 (Pubitemid 43948244)
7. Petricoin, E. F., 3rd, Ito, S., Williams, B. L., Audet, S., Stancato, L. F., Gamero, A., Clouse, K., Grimley, P., Weiss, A., Beeler, J., Finbloom, D. S., Shores, E. W., Abraham, R., and Larner, A. C. (1997) Antiproliferative action of interferon-α requires components of T-cell-receptor signaling. Nature 390, 629-632 (Pubitemid 28016200)
8. Gamero, A. M., Potla, R., Sakamoto, S., Baker, D. P., Abraham, R., and Larner, A. C. (2006) Type I interferons activate apoptosis in a Jurkat cell variant by caspase-dependent and independent mechanisms. Cell. Signal. 18, 1299-1308 (Pubitemid 43674033)
9. Williams, B. L., Schreiber, K. L., Zhang, W., Wange, R. L., Samelson, L. E., Leibson, P. J., and Abraham, R. T. (1998) Genetic evidence for differential coupling of Syk family kinases to the T-cell receptor: reconstitution studies in a ZAP-70-deficient Jurkat T-cell line. Mol. Cell Biol. 18, 1388-1399 (Pubitemid 28100903)
10. Hewavitharana, T., Deng, X., Soboloff, J., and Gill, D. L. (2007) Role of STIM and Orai proteins in the store-operated calcium signaling pathway. Cell Calcium 42, 173-182 (Pubitemid 47029604)
11. Deng, X., Wang, Y., Zhou, Y., Soboloff, J., and Gill, D. L. (2009) STIM and Orai: dynamic intermembrane coupling to control cellular calcium signals. J. Biol. Chem. 284, 22501-22505
12. 2+ influx. Curr. Biol. 15, 1235-1241
13. Stathopulos, P. B., Zheng, L., Li, G. Y., Plevin, M. J., and Ikura, M. (2008) Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry. Cell 135, 110-122
14. Feske, S., Gwack, Y., Prakriya, M., Srikanth, S., Puppel, S. H., Tanasa, B., Hogan, P. G., Lewis, R. S., Daly, M., and Rao, A. (2006)Amutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441, 179-185
15. Prakriya, M., Feske, S., Gwack, Y., Srikanth, S., Rao, A., and Hogan, P. G. (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443, 230-233 (Pubitemid 44387613)
16. Soboloff, J., Spassova, M. A., Tang, X. D., Hewavitharana, T., Xu, W., and Gill, D. L. (2006) Orai1 and STIM reconstitute store-operated calcium channel function. J. Biol. Chem. 281, 20661-20665 (Pubitemid 44115407)
17. Vig, M., Beck, A., Billingsley, J. M., Lis, A., Parvez, S., Peinelt, C., Koomoa, D. L., Soboloff, J., Gill, D. L., Fleig, A., Kinet, J. P., and Penner, R. (2006) CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr. Biol. 16, 2073-2079 (Pubitemid 44573821)
18. Vig, M., Peinelt, C., Beck, A., Koomoa, D. L., Rabah, D., Koblan-Huberson, M., Kraft, S., Turner, H., Fleig, A., Penner, R., and Kinet, J. P. (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312, 1220-1223 (Pubitemid 43801149)
19. Yeromin, A. V., Zhang, S. L., Jiang, W., Yu, Y., Safrina, O., and Cahalan, M. D. (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443, 226-229 (Pubitemid 44387612)
20. 2+ entry signals. J. Biol. Chem. 283, 26252-26262
21. Zhou, Y., Mancarella, S., Wang, Y., Yue, C., Ritchie, M., Gill, D. L., and Soboloff, J. (2009) The short N-terminal domains of STIM1 and STIM2 control the activation kinetics of Orai1 channels. J. Biol. Chem. 284, 19164-19168
22. Abraham, R. T. (2000) Mutant T cell lines as model systems for the dissection of T cell antigen receptor signaling pathways. Immunol. Res. 22, 95-117
23. 2+ store to the plasma membrane. Nature 437, 902-905
24. Liang, S. H., Zhang, W., McGrath, B. C., Zhang, P., and Cavener, D. R. (2006) PERK (eIF2α kinase) is required to activate the stress-activated MAPKs and induce the expression of immediate-early genes upon disruption of ER calcium homoeostasis. Biochem. J. 393, 201-209 (Pubitemid 43049316)
25. Soboloff, J., and Berger, S. A. (2002) Sustained ER Ca2+ depletion suppresses protein synthesis and induces activation-enhanced cell death in mast cells. J. Biol. Chem. 277, 13812-13820 (Pubitemid 34967985)
26. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., and Mori, K. (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891 (Pubitemid 34084979)
27. Wang, C. Y., Mayo, M. W., and Baldwin, A. S., Jr. (1996) TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-κB. Science 274, 784-787 (Pubitemid 26398259)
28. Chang, J. W., Kim, C. S., Kim, S. B., Park, S. K., Park, J. S., and Lee, S. K. (2006) Proinflammatory cytokine-induced NF-κB activation in human mesangial cells is mediated through intracellular calcium but not ROS: effects of silymarin. Nephron Exp. Nephrol 103, e156-165
29. Li, S. Y., Sun, W. G., Jia, Y. H., Wu, G. S., An, G. S., Ni, J. H., and Jia, H. T. (2010) Calcium signal-initiated early activation of NF-κB in neurons is a neuroprotective event in response to kainic acid-induced excitotoxicity. Biochemistry 75, 101-109
30. 2+-dependent phosphatase calcineurin controls the formation of the Carma1-Bcl10-Malt1 complex during T cell receptor-induced NF-κB activation. J. Biol. Chem. 286, 7522-7534
31. Valdés, J. A., Hidalgo, J., Galaz, J. L., Puentes, N., Silva, M., Jaimovich, E., and Carrasco, M. A. (2007) NF-κB activation by depolarization of skeletal muscle cells depends on ryanodine and IP3 receptor-mediated calcium signals. Am. J. Physiol. Cell Physiol. 292, C1960-C1970 (Pubitemid 47080555)
32. Wei, L., Sandbulte, M. R., Thomas, P. G., Webby, R. J., Homayouni, R., and Pfeffer, L. M. (2006) NFκB negatively regulates interferon-induced gene expression and anti-influenza activity. J. Biol. Chem. 281, 11678-11684 (Pubitemid 43855425)
33. May, M. J., D'Acquisto, F., Madge, L. A., Glöckner, J., Pober, J. S., and Ghosh, S. (2000) Selective inhibition of NF-κB activation by a peptide that blocks the interaction of NEMO with the IκB kinase complex. Science 289, 1550-1554
34. Feske, S. (2007) Calcium signaling in lymphocyte activation and disease. Nat. Rev. Immunol. 7, 690-702
35. Lewis, R. S. (2001) Calcium signaling mechanisms in T lymphocytes. Annu. Rev. Immunol. 19, 497-521
36. Hogan, P. G., Chen, L., Nardone, J., and Rao, A. (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes. Dev. 17, 2205-2232 (Pubitemid 37128637)
37. Le Bon, A., and Tough, D. F. (2008) Type I interferon as a stimulus for cross-priming. Cytokine Growth Factor Reviews 19, 33-40
38. Hervas-Stubbs, S., Perez-Gracia, J. L., Rouzaut, A., Sanmamed, M. F., Le Bon, A., and Melero, I. (2011) Direct effects of type I interferons on cells of the immune system. Clin. Canc. Res. 17, 2619-2627
39. Jayaraman, T., and Marks, A. R. (1997) T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol. Cell Biol. 17, 3005-3012 (Pubitemid 27215014)
40. Roifman, C. M., Dadi, H., Somech, R., Nahum, A., and Sharfe, N. (2010) Characterization of zeta-associated protein, 70 kd (ZAP70)-deficient human lymphocytes. J. Allergy Clin. Immunol. 126, 1226-1233.e1221
41. Belka, C., Gruber, C., Jendrossek, V., Wesselborg, S., and Budach, W. (2003) The tyrosine kinase Lck is involved in regulation of mitochondrial apoptosis pathways. Oncogene 22, 176-185 (Pubitemid 36174175)
42. 2+ channels and T-lymphocyte activation by the pyrazole derivative BTP2. J. Biol. Chem. 279, 12427-12437
43. Dellis, O., Gangloff, S. C., Paulais, M., Tondelier, D., Rona, J. P., Brouillard, F., Bouteau, F., Guenounou, M., and Teulon, J. (2002) Inhibition of the calcium release-activated calcium (CRAC) current in Jurkat T cells by the HIV-1 envelope protein gp160. J. Biol. Chem. 277, 6044-6050 (Pubitemid 34968389)
44. Borden, E. C., and Williams, B. R. (2011) Interferon-stimulated genes and their protein products: what and how? J. Interferon Cytokine Res. 31, 1-4
45. Yang, C. H., Murti, A., Pfeffer, S. R., Kim, J. G., Donner, D. B., and Pfeffer, L. M. (2001) Interferon αβ promotes cell survival by activating nuclear factor κB through phosphatidylinositol 3-kinase and Akt. J. Biol. Chem. 276, 13756-13761
46. Yang, C. H., Murti, A., Pfeffer, S. R., Basu, L., Kim, J. G., and Pfeffer, L. M. (2000) IFNαβ promotes cell survival by activating NF-κB. Proc. Natl. Acad. Sci. U.S.A. 97, 13631-13636