Canonical transient receptor potential 5 channel in conjunction with orai1 and STIM1 allows Sr2+ entry, optimal influx of Ca2+, and degranulation in a rat mast cell line

Journal of Immunology

Volumn 180, Issue 4, 2008, Pages 2233-2239

  Ma, Hong Tao ^a   Peng, Ze ^a,c   Hiragun, Takaaki ^a,d   Iwaki, Shoko ^b   Gilfillan, Alasdair M ^b   Beaven, Michael A ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^d HIROSHIMA UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; PROTEIN; PROTEIN STIM1; RNA; STRONTIUM; TRANSIENT RECEPTOR POTENTIAL CHANNEL 5; UNCLASSIFIED DRUG; CALCIUM CHANNEL; MEMBRANE PROTEIN; SMALL INTERFERING RNA; STIM1 PROTEIN, RAT; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC5 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CANCER CELL CULTURE; DEGRANULATION; MAST CELL LEUKEMIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STOICHIOMETRY; ANIMAL; BIOSYNTHESIS; CELL MEMBRANE; GENETICS; IMMUNOLOGY; MAST CELL; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CELL DEGRANULATION; CELL LINE, TUMOR; CELL MEMBRANE; MAST CELLS; MEMBRANE GLYCOPROTEINS; RATS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STRONTIUM; TRPC CATION CHANNELS;

EID: 42149127676     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.4.2233     Document Type: Article

References (68)

1. 2+ and purified isozymes in washed permeabilized cells. J. Biol. Chem. 268: 1749-1756.
2. 2+ stores. Biochem. J. 304: 431-440.
3. Beaven, M. A., J. Rogers, J. P. Moore, T. R. Hesketh, G. A. Smith, and J. C. Metcalfe. 1984. The mechanism of the calcium signal and correlation with histamine release in 2H3 cells. J. Biol. Chem. 259: 7129-7136.
4. Millard, P. J., T. A. Ryan, W. W. Webb, and C. Fewtrell. 1989. Immunoglobulin E receptor cross-linking induces oscillations in intracellular free ionized calcium in individual tumor mast cells. J. Biol. Chem. 264: 19730-19739.
5. Berridge, M. J. 1995. Capacitative calcium entry. Biochem. J. 312: 1-11.
6. Putney, J. W., Jr. 1990. Capacitative calcium entry revisited. Cell Calcium. 11: 611-624.
7. Hoth, M., and R. Penner. 1993. Calcium release-activated calcium current in rat mast cells. J. Physiol. 465: 359-386.
8. Parekh, A. B., and R. Penner. 1996. Regulation of store-operated calcium currents in mast cells. Soc. Gen. Physiol. Ser. 51: 231-239.
9. Zweifach, A., and R. S. Lewis. 1996. Calcium-dependent potentiation of store-operated calcium channels in T lymphocytes. J. Gen. Physiol. 107: 597-610.
10. Christian, E. P., K. T. Spence, J. A. Togo, P. G. Dargis, and J. Patel. 1996. Calcium-dependent enhancement of depletion-activated calcium current in Jurkat T lymphocytes. J. Membr. Biol. 150: 63-71.
11. Foreman, J. C., and J. L. Mongar. 1972. The role of the alkaline earth ions in anaphylactic histamine secretion. J. Physiol. 224: 753-769.
12. Foreman, J. C., M. B. Hallett, and J. L. Mongar. 1977. Movement of strontium ions into mast cells and its relationship to the secretory response. J. Physiol. 271: 233-251.
13. Hide, M., and M. A. Beaven. 1991. Calcium influx in a rat mast cell (RBL-2H3) line: Use of multivalent metal ions to define its characteristics and role in exocytosis. J. Biol. Chem. 266: 15221-15229.
14. Philipp, S., A. Cavalié, M. Freichel, U. Wissenbach, S. Zimmer, C. Trost, A. Marquart, M. Murakami, and V. Flockerzi. 1996. A mammalian capacitative calcium entry channel homologous to Drosophila TRP and TRPL. EMBO J. 15: 6166-6171.
15. 2+-permeable cation channel activated by calcium store depletion. Neuron 16: 1189-1196.
16. -/- mice. Nat. Cell Biol. 3: 121-127.
17. 2+. J. Physiol. 518: 631-638.
18. 2+ influx mechanism in salivary gland cells. J. Biol. Chem. 275: 3403-3411.
19. Freichel, M., R. Vennekens, J. Olausson, S. Stolz, S. E. Philipp, P. Weissgerber, and V. Flockerzi. 2005. Functional role of TRPC proteins in native systems: implications from knockout and knock-down studies. J. Physiol. 567: 59-66.
20. 2+ through TRP-R, a rat homolog of TRP, expressed in Xenopus oocytes. Neurosci. Lett. 248: 195-198.
21. 2+ entry in HEK-293 cells. Am. J. Physiol. 278: C526-C536.
22. 2+ entry pathway. FASEB J. 15: 1727-1738.
23. 2+ entry and attenuates pulmonary artery smooth muscle cell proliferation. Am. J. Physiol. 283: L144-L155.
24. Yang, H., S. Mergler, X. Sun, Z. Wang, L. Lu, J. A. Bonanno, U. Pleyer, and P. S. Reinach. 2005. TRPC4 knockdown suppresses epidermal growth factor-induced store-operated channel activation and growth in human corneal epithelial cells. J. Biol. Chem. 280: 32230-32237.
25. 2+ entry in vascular smooth muscle cells. J. Pharmacol. Exp. Ther. 317: 488-499.
26. Zeng, F., S. Z. Xu, P. K. Jackson, D. McHugh, B. Kumar, S. J. Fountain, and D. J. Beech. 2004. Human TRPC5 channel activated by a multiplicity of signals in a single cell. J. Physiol. 559: 739-750.
27. 2+-permeable nonselective cation channels. Cell Calcium 33: 441-450.
28. Schaefer, M., T. D. Plant, A. G. Obukhov, T. Hofmann, T. Gudermann, and G. Schultz. 2000. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J. Biol. Chem. 275: 17517-17526.
29. Birnbaumer, L., E. Yildirim, and J. Abramowitz. 2003. A comparison of the genes coding for canonical TRP channels and their M, V and P relatives. Cell Calcium 33: 419-432.
30. Hofmann, T., A. G. Obukhov, M. Schaefer, C. Harteneck, T. Gudermann, and G. Schultz. 1999. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397: 259-263.
31. 2+-permeable cation channel that is constitutively activated and enhanced by stimulation of G protein-coupled receptor. J. Biol. Chem. 274: 27359-27370.
32. 2+ entry: roles of Orai, Stim and TRP. Biochim. Biophys. Acta 1763: 1147-1160.
33. 2+ channel function. J. Cell Biol. 169: 435-445.
34. 2+ influx. Curr. Biol. 15: 1235-1241.
35. 2+ channels. Proc. Natl. Acad. Sci. USA 103: 4040-4045.
36. 2+ store to the plasma membrane. Nature 437: 902-905.
37. 2+ entry. J. Biol. Chem. 281: 35855-35862.
38. Feske, S., Y. Gwack, M. Prakriya, S. Srikanth, S. H. Puppel, B. Tanasa, P. G. Hogan, R. S. Lewis, M. Daly, and A. Rao. 2006. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441: 179-185.
39. 2+ entry. Science 312: 1220-1223.
40. + channel gating in T cells from immunodeficient patients. J. Exp. Med. 202: 651-662.
41. Mercer, J. C., W. I. Dehaven, J. T. Smyth, B. Wedel, R. R. Boyles, G. S. Bird, and J. W. Putney, Jr. 2006. 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.
42. Peinelt, C., M. Vig, D. L. Koomoa, A. Beck, M. J. Nadler, M. Koblan-Huberson, A. Lis, A. Fleig, R. Penner, and J. P. Kinet. 2006. Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat. Cell Biol. 8: 771-773.
43. Soboloff, J., M. A. Spassova, X. D. Tang, T. Hewavitharana, W. Xu, and D. L. Gill. 2006. Orai1 and STIM reconstitute store-operated calcium channel function. J. Biol. Chem. 281: 20661-20665.
44. Ong, H. L., K. T. Cheng, X. Liu, B. C. Bandyopadhyay, B. C. Paria, J. Soboloff, B. Pani, Y. Gwack, S. Srikanth, B. B. Singh, et al. 2007. 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.
45. Liao, Y., C. Erxleben, E. Yildirim, J. Abramowitz, D. L. Armstrong, and L. Birnbaumer. 2007. Orai proteins interact with TRPC channels and confer responsiveness to store depletion. Proc. Natl. Acad. Sci. USA 104: 4682-4687.
46. Yuan, J. P., W. Zeng, G. N. Huang, P. F. Worley, and S. Muallem. 2007. STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat. Cell Biol. 9: 636-645.
47. Iwaki, S., C. Tkaczyk, A. B. Satterthwaite, K. Halcomb, M. A. Beaven, D. D. Metcalfe, and A. M. Gilfillan. 2005. Btk plays a crucial role in the amplification of FcεRI-mediated mast cell activation by Kit. J. Biol. Chem. 280: 40261-40270.
48. Babich, L. G., C. Y. Ku, H. W. Young, H. Huang, M. R. Blackburn, and B. M. Sanborn. 2004. Expression of capacitative calcium TrpC proteins in rat myometrium during pregnancy. Biol. Reprod. 70: 919-924.
49. Jones, S. V., O. H. Choi, and M. A. Beaven. 1991. Carbachol induces secretion in a mast cell line (RBL-2H3) transfected with the m1 muscarinic receptor gene. FEBS Lett. 289: 47-50.
50. Choi, O. H., J. H. Lee, T. Kassessinoff, J. R. Cunha-Melo, S. Jones, V., and M. A. Beaven. 1993. Carbachol and antigen mobilize calcium by similar mechanisms in a transfected mast cell line (RBL-2H3 cells) that expresses m1 muscarinic receptors. J. Immunol. 151: 5586-5595.
51. Andrade, M. V., T. Hiragun, and M. A. Beaven. 2004. Dexamethasone suppresses antigen-induced activation of phosphatidylinositol 3-kinase and downstream responses in mast cells. J. Immunol. 172: 7254-7262.
52. 3 knockout cells. J. Biol. Chem. 276: 33980-33985.
53. Schilling, W. P., L. Rajan, and E. Strobl-Jager. 1989. Characterization of the bradykinin-stimulated calcium influx pathway of cultured vascular endothelial cells: saturability, selectivity, and kinetics. J. Biol. Chem. 264: 12838-12848.
54. Mironov, S. L., and M. U. Juri. 1990. Sr and Ba transients in isolated snail neurones studied with fura-2: the recovery from depolarization induced load and modulation of Ca release from intracellular stores. Neurosci. Lett. 112: 184-189.
55. Kwan, C. Y., and J. W. Putney. 1990. Uptake and intracellular sequestration of divalent cations in resting and methacholine-stimulated mouse lacrimal acinar cells. J. Biol. Chem. 265: 678-684.
56. Cissel, D. S., P. F. Fraundorfer, and M. A. Beaven. 1998. Thapsigargin-induced secretion is dependent on activation of a cholera toxin-sensitive and a phosphatidylinositol-3-kinase-regulated phospholipase D in a mast cell line. J. Pharmacol. Exp. Ther. 285: 110-118.
57. Park, D. J., H. K. Min, and S. G. Rhee. 1991. IgE-induced tyrosine phosphorylation of phospholipase C-γ1 in rat basophilic leukemia cells. J. Biol. Chem. 266: 24237-24240.
58. 1 signaling. J. Neurosci. 20: 2774-2782.
59. Zufall, F. 2005. The TRPC2 ion channel and pheromone sensing in the accessory olfactory system. Naunyn Schmiedebergs Arch. Pharmacol. 371: 245-250.
60. Zufall, F., K. Ukhanov, P. Lucas, and T. Leinders-Zufall. 2005. Neurobiology of TRPC2: from gene to behavior. Pflugers Arch. 451: 61-71.
61. Venkatachalam, K., F. Zheng, and D. L. Gill. 2003. Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J. Biol. Chem. 278: 29031-29040.
62. 2+-ATPase inhibitors. J. Immunol. 152: 5226-5240.
63. 2+ stores. Proc. Natl. Acad. Sci. USA 90: 6295-6299.
64. Yeromin, A. V., S. L. Zhang, W. Jiang, Y. Yu, O. Safrina, and M. D. Cahalan. 2006. Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443: 226-229.
65. Vig, M., A. Beck, J. M. Billingsley, A. Lis, S. Parvez, C. Peinelt, D. L. Koomoa, J. Soboloff, D. L. Gill, A. Fleig, et al. 2006. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr. Biol. 16: 2073-2079.
66. 2+ channels. Science 287: 1647-1605.
67. Forsythe, P., and M. Ennis. 2000. Clinical consequences of mast cell heterogeniety. Inflam. Res. 49: 147-154.
68. Welle, M. 1997. Development, significance, and heterogeneity of mast cells with particular regard to the mast cell-specific proteases chymase and tryptase. J. Leukocyte Biol. 61: 233-245.