Calcium signaling in immune cells

Nature Immunology

Volumn 10, Issue 1, 2009, Pages 21-27

  Vig, Monika ^a   Kinet, Jean Pierre ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; CELL MEMBRANE PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN STIM1; UNCLASSIFIED DRUG;

CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL TYPE; CONCENTRATION (PARAMETERS); EXTRACELLULAR SPACE; GENETIC MANIPULATION; HUMAN; IMMUNOCOMPETENT CELL; MAST CELL; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SECOND MESSENGER; T LYMPHOCYTE; THYMOCYTE;

ANIMALS; ANTIGEN PRESENTATION; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL DEGRANULATION; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MAST CELLS; MEMBRANE PROTEINS; MICE; NEOPLASM PROTEINS; RECEPTORS, CALCIUM-SENSING; THYMUS GLAND;

EID: 57849148942     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.f.220     Document Type: Review

References (92)

1. Parekh, A.B. & Putney, J.W., Jr. Store-operated calcium channels. Physiol. Rev. 85, 757-810 (2005).
2. 2+ influx. Curr. Biol. 15 1235-1241 (2005).
3. 2+ store to the plasma membrane. Nature 437, 902-905 (2005).
4. 2+ entry. Science 312, 1220-1223 (2006).
5. Feske, S. et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441, 179-185 (2006).
6. 2+ channel activity. Proc. Natl. Acad. Sci. USA 103, 9357-9362 (2006).
7. Philipp, S. et al. TRPC3 mediates T-cell receptor-dependent calcium entry in human T-lymphocytes. J. Biol. Chem. 278, 26629-26638 (2003).
8. Venkatachalam, K., Ma, H.T., Ford, D.L. & Gill, D.L. Expression of functional receptor-coupled TRPC3 channels in DT40 triple receptor InsP3 knockout cells. J. Biol. Chem. 276, 33980-33985 (2001).
9. Putney, J.W., Jr. Capacitative calcium entry: Sensing the calcium stores. J. Cell Biol. 169, 381-382 (2005).
10. Yuan, J.P., Zeng, W., Huang, G.N., Worley, P.F. & Muallem, S. STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat. Cell Biol. 9, 636-645 (2007).
11. Villereal, M.L. Mechanism and functional significance of TRPC channel multimerization. Semin. Cell Dev. Biol. 17, 618-629 (2006).
12. Hardie, R.C. TRP channels and lipids: From Drosophila to mammalian physiology. J. Physiol. 578, 9-24 (2007).
13. Rao, G.K. & Kaminski, N.E. Induction of intracellular calcium elevation by Delta9-tetrahydrocannabinol in T cells involves TRPC1 channels. J. Leukoc. Biol. 79, 202-213 (2006).
14. Lioudyno, M.I. et al. Orai1 and STIM1 move to the immunological synapse and are up-regulated during T cell activation. Proc. Natl. Acad. Sci. USA 105, 2011-2016 (2008).
15. Malek, T.R. The biology of interleukin-2. Annu. Rev. Immunol. 26, 453-479 (2008).
16. Baba, Y. et al. Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat. Immunol. 9, 81-88 (2008).
17. 2+ response amplitude and duration. Nature 386, 855-858 (1997).
18. 2+/calmodulin kinase type IV/Gr. J. Exp. Med. 184, 101-112 (1996).
19. Crabtree, G.R. & Olson, E.N. NFAT signaling: Choreographing the social lives of cells. Cell 109, S67-S79 (2002).
20. Huang, G.N. et al. NFAT binding and regulation of T cell activation by the cytoplasmic scaffolding Homer proteins. Science 319, 476-481 (2008).
21. 2+ entry. J. Biol. Chem. 281, 35855-35862 (2006).
22. 2+ store depletion. Proc. Natl. Acad. Sci. USA 104, 9301-9306 (2007).
23. Stathopulos, P.B., Zheng, L., Li, G.Y., Plevin, M.J. & Ikura, M. Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry. Cell 135, 110-122 (2008).
24. 2+ entry: Local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J. Cell Biol. 174, 815-825 (2006).
25. Luik, R.M., Wang, B., Prakriya, M., Wu, M.M. & Lewis, R.S. Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454, 538-542 (2008).
26. 2+ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 103, 16704-16709 (2006).
27. 2+ entry. Curr. Biol. 16, 1465-1470 (2006).
28. 2+ levels. Cell 131, 1327-1339 (2007).
29. Oh-Hora, M. et al. Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nat. Immunol. 9, 432-443 (2008).
30. Peinelt, C. et al. Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat. Cell Biol. 8, 771-773 (2006).
31. Mercer, J.C. et al. Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J. Biol. Chem. 281, 24979-24990 (2006).
32. Soboloff, J. et al. Orai1 and STIM reconstitute store-operated calcium channel function. J. Biol. Chem. 281, 20661-20665 (2006).
33. Vig, M. et al. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr. Biol. 16, 2073-2079 (2006).
34. 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).
35. Prakriya, M. et al. Orai1 is an essential pore subunit of the CRAC channel. Nature 443, 230-233 (2006).
36. 2+ channels with distinct functional properties. Curr. Biol. 17, 794-800 (2007).
37. Ong, H.L. et al. Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx. Evidence for similarities in store-operated and calcium release-activated calcium channel components. J. Biol. Chem. 282, 9105-9116 (2007).
38. Mignen, O., Thompson, J.L. & Shuttleworth, T.J. Orai1 subunit stoichiometry of the mammalian CRAC channel pore. J. Physiol. 586, 419-425 (2008).
39. Ji, W. et al. Functional stoichiometry of the unitary calcium-release-activated calcium channel. Proc. Natl. Acad. Sci. USA 105, 13668-13673 (2008).
40. 2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J. Cell Biol. 174, 803-813 (2006).
41. crac and TRPC1 channels. Nat. Cell Biol. 8, 1003-1010 (2006).
42. Barr, V.A. et al. Dynamic movement of the calcium sensor STIM1 and the calcium channel Orai1 in activated T-cells: Puncta and distal caps. Mol. Biol. Cell 19, 2802-2817 (2008).
43. Muik, M. et al. Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J. Biol. Chem. 283, 8014-8022 (2008).
44. Gwack, Y. et al. Biochemical and functional characterization of Orai proteins. J. Biol. Chem. 282, 16232-16243 (2007).
45. Varnai, P., Toth, B., Toth, D.J., Hunyady, L. & Balla, T. Visualization and manipulation of plasma membrane-endoplasmic reticulum contact sites indicates the presence of additional molecular components within the STIM1-Orai1 complex. J. Biol. Chem. 282, 29678-29690 (2007).
46. Smani, T. et al. A novel mechanism for the store-operated calcium influx pathway. Nat. Cell Biol. 6, 113-120 (2004).
47. 2+ channel activation. J. Biol. Chem. 282, 29448-29456 (2007).
48. Penna, A. et al. The CRAC channel consists of a tetramer formed by STIM-induced dimerization of Orai dimers. Nature 456, 116-120 (2008).
49. Leslie, M. Mast cells show their might. Science 317, 614-616 (2007).
50. Nadler, M.J. & Kinet, J.P. Uncovering new complexities in mast cell signaling. Nat. Immunol. 3, 707-708 (2002).
51. Vig, M. et al. Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat. Immunol. 9, 89-96 (2008).
52. 2+-activated nonselective cation channel mediating cell membrane depolarization. Cell 109, 397-407 (2002).
53. Launay, P. et al. TRPM4 regulates calcium oscillations after T cell activation. Science 306, 1374-1377 (2004).
54. Vennekens, R. et al. Increased IgE-dependent mast cell activation and anaphylactic responses in mice lacking the calcium-activated nonselective cation channel TRPM4. Nat. Immunol. 8, 312-320 (2007).
55. 2+ (CRAC) channels stimulates production of an intracellular messenger and an intercellular pro-inflammatory signal. J. Biol. Chem. 283, 4622-4631 (2008).
56. ++-triggered exocytosis. Science 298, 781-785 (2002).
57. Kalesnikoff, J. et al. SHIP negatively regulates IgE + antigen-induced IL-6 production in mast cells by inhibiting NF-κB activity. J. Immunol. 168, 4737-4746 (2002).
58. Jenkins, M.K., Schwartz, R.H. & Pardoll, D.M. Effects of cyclosporine A on T cell development and clonal deletion. Science 241, 1655-1658 (1988).
59. Gao, E.K., Lo, D., Cheney, R., Kanagawa, O. & Sprent, J. Abnormal differentiation of thymocytes in mice treated with cyclosporin A. Nature 336, 176-179 (1988).
60. Bueno, O.F., Brandt, E.B., Rothenberg, M.E. & Molkentin, J.D. Defective T cell development and function in calcineurin A β-deficient mice. Proc. Natl. Acad. Sci. USA 99, 9398-9403 (2002).
61. 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).
62. Oukka, M. et al. The transcription factor NFAT4 is involved in the generation and survival of T cells. Immunity 9, 295-304 (1998).
63. Gwack, Y. et al. Hair loss and defective T and B cell function in mice lacking ORAI1. Mol. Cell Biol. (2008).
64. DeHaven, W.I., Smyth, J.T., Boyles, R.R. & Putney, J.W., Jr. Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels. J. Biol. Chem. 282, 17548-17556 (2007).
65. 2+ homeostasis. Science 322, 756-760 (2008).
66. 2+ current in human leukemic T cells. Cell Regul. 1, 99-112 (1989).
67. 2+ stores. Proc. Natl. Acad. Sci. USA 90, 6295-6299 (1993).
68. 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).
69. 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).
70. Peng, S.L., Gerth, A.J., Ranger, A.M. & Glimcher, L.H. NFATc1 and NFATc2 together control both T and B cell activation and differentiation. Immunity 14, 13-20 (2001).
71. Kotturi, M.F., Hunt, S.V. & Jefferies, W.A. Roles of CRAC and Cav-like channels in T cells: More than one gatekeeper? Trends Pharmacol. Sci. 27, 360-367 (2006).
72. Badou, A. et al. Critical role for the β regulatory subunits at Cav channels in T lymphocyte function. Proc. Natl. Acad. Sci. USA 103, 15529-15534 (2006).
73. Gomez-Ospina, N., Tsuruta, F, Barreto-Chang, O., Hu, L. & Dolmetsch, R. The C terminus of the L-type voltage-gated calcium channel Cav1.2 encodes a transcription factor. Cell 127, 591-606 (2006).
74. 2+ endoplasmic reticulum-ATPase inhibitor thapsigargin. Eur. J. Immunol. 20, 2269-2275 (1990).
75. 2+-ATPase activity in mouse T lymphocytes by flow cytometry using fluo-3-loaded vesicles. Cytometry 24, 243-250 (1996).
76. Bautista, D.M., Hoth, M. & Lewis, R.S. Enhancement of calcium signalling dynamics and stability by delayed modulation of the plasma-membrane calcium-ATPase in human T cells. J. Physiol. (Lond. 541, 877-894 (2002).
77. Jayaraman, T., Ondriasova, E., Ondrias, K., Harnick, D.J. & Marks, A.R. The inositol 1,4,5-trisphosphate receptor is essential for T-cell receptor signaling. Proc. Natl. Acad. Sci. USA 92, 6007-6011 (1995).
78. Guse, A.H. et al. Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature 398, 70-73 (1999).
79. Sei, Y., Gallagher, K.L. & Basile, A.S. Skeletal muscle type ryanodine receptor is involved in calcium signaling in human B lymphocytes. J. Biol. Chem. 274, 5995-6002 (1999).
80. Guerini, D., Coletto, L. & Carafoli, E. Exporting calcium from cells. Cell Calcium 38, 281-289 (2005).
81. 2+ exchange-mediated calcium entry in human lymphocytes. J. Clin. Invest. 94, 2002-2008 (1994).
82. Saris, N.E. & Carafoli, E. A historical review of cellular calcium handling, with emphasis on mitochondria. Biochemistry (Mosc.) 70, 187-194 (2005).
83. Hoth, M., Fanger, C.M. & Lewis, R.S. Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J. Cell Biol. 137, 633-648 (1997).
84. Beeton, C. & Chandy, K.G. Potassium channels, memory T cells, and multiple sclerosis. Neuroscientist 11, 550-562 (2005).
85. Cowen, D.S. et al. Extracellular adenosine triphosphate activates calcium mobilization in human phagocytic leukocytes and neutrophil/ monocyte progenitor cells. J. Clin. Invest. 83, 1651-1660 (1989).
86. Cui, J., Bian, J.S., Kagan, A. & McDonald, T.V. CaT1 contributes to the stores-operated calcium current in Jurkat T-lymphocytes. J. Biol. Chem. 277, 47175-47183 (2002).
87. Perraud, A.L. et al. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 411, 595-599 (2001).
88. 2+ influx system mediated by LTRPC2. Science 293, 1327-1330 (2001).
89. Nadler, M.J. et al. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 411, 590-595 (2001).
90. 2+-inhibited cation (MIC) channels. J. Gen. Physiol. 119, 487-507 (2002).
91. 2+]i oscillations?-challenging the capacitative model. Cell Calcium 25, 237-246 (1999).
92. 2+ entry through plasma membrane IP3 receptors. Science 313, 229-233 (2006).